Trace elements levels in muscle and liver of a rarely investigated large pelagic fish: The Mediterranean spearfish Tetrapturus belone (Rafinesque, 1810)

Marine Pollution Bulletin 151 (2020) 110878

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Baseline

Trace elements levels in muscle and liver of a rarely investigated large pelagic fish: The Mediterranean spearfish Tetrapturus belone (Rafinesque, 1810)

T

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Stefania Ancora , Giacomo Mariotti, Rosetta Ponchia, Maria Cristina Fossi, Claudio Leonzio, Nicola Bianchi Department of Earth, Environmental and Physical Sciences, University of Siena, Italy

A R T I C LE I N FO

A B S T R A C T

Keywords: Tetrapturus belone Mediterranean spearfish Trace elements Large pelagic fish Mediterranean Sea Selenium protective effects

We determined levels of mercury, cadmium, lead and selenium in muscle and liver of 29 specimens of a large pelagic fish rarely investigated, the Mediterranean spearfish Tetrapturus belone (Raf., 1810). The following element concentration ranking (mean ± S.D.; espressed in mg/kg dry weight) was recorded in muscle: Hg (3.401 ± 1.908) > Se (1.727 ± 0.232) > Pb (0.532 ± 0.322) > Cd (0.019 ± 0.015), and Se (6.577 ± 1.789) > Cd (5.815 ± 3.038) > Hg (2.698 ± 2.214) > Pb (0.661 ± 1.334) in liver. Levels of Hg, Se and Cd were compared to those reported for other Istiophoridae from oceanic areas and for other large predators of Mediterranean Sea, like swordfish and tuna. Organotropism of trace elements and their relation to size was discussed. Ecophysiological considerations regarding the Se-Hg relationship as well as Se-Cd indicate a possible detoxification mechanism. The implications for human consumption are briefly discussed.

Marine top predators are particularly exposed to high levels of trace elements through their food. Some organisms have high metabolic rates requiring high food intake rates (Dickson, 1995), leading to accentuated exposure to trace elements (Rainbow and Phillips, 1993; Andersen and Depledge, 1997; Kojadinovic et al., 2007). Like marine mammals and birds, large pelagic fish of the Mediterranean show higher concentrations of mercury and other trace elements than populations from other areas (Renzoni et al., 1978; Renzoni et al., 1986; Andre et al., 1991; Lahaye et al., 2006; Damiano et al., 2011), even though, some comparisons have been made without considering a possible source of bias as different growth rate in different areas (Lahaye et al., 2006). Several studies have been carried out in the Mediterranean Sea to assess levels of trace elements in large pelagic fish of commercial interest, especially tuna or swordfish (Storelli and Marcotrigiano, 2001; Licata et al., 2005; Storelli et al., 2005; Vizzini et al., 2010; Damiano et al., 2011), whereas little data is available on the Mediterranean spearfish Tetrapturus belone (Raf., 1810). This large pelagic predator belongs to the Istiophoridae family and its distribution is mainly limited to the Mediterranean Sea, in particular around the Strait of Messina (De Sylva, 1975; Nakamura, 1985; Arocha and Ortiz, 2006; Castriota et al., 2008; Romeo et al., 2009).

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Based on examination of stomach contents, the first studies indicated that T. belone probably feeds on pelagic fish (Bini, 1968; De Sylva, 1975; Tortonese, 1975; Nakamura, 1985). Further diet studies conducted around the Strait of Messina, Italy, showed that T. belone feeds on a large variety of marine organisms, including cephalopods which it hunts at night when these molluscs move towards the surface (Castriota et al., 2008). However, fish have been identified as the main prey (Castriota et al., 2008; Romeo et al., 2009). Due to its position in the food web at Trophic Level 4.4 (Fishbase, 2019), its Mediterranean distribution, large size and high metabolic rate, this species may be subject to bioaccumulation and/or biomagnification of toxic metals. However, the biology, ecology and ecotoxicology of the T. belone is still unclear (Fossi et al., 2002; Arocha and Ortiz, 2006; Castriota et al., 2008). The Mediterranean Sea, a semi-closed basin surrounded by some of the most industrialized countries of the world, has reached alarming levels of contamination (Gabrielides, 1995; UNEP, 1996; UNEP, 2002; Danovaro, 2003; EEA, 2006) and has required strong regulatory measures in recent decades. The catchment also contains abundant natural mercury deposits (Nriagu, 1979; Lindberg et al., 1987; Bacci, 1989). Most mercury released into the marine environment is inorganic then converted by microorganisms into the organic form (methylmercury,

Corresponding author. E-mail address: [email protected] (S. Ancora).

https://doi.org/10.1016/j.marpolbul.2019.110878 Received 15 July 2019; Received in revised form 22 December 2019; Accepted 31 December 2019 Available online 29 January 2020 0025-326X/ © 2020 Elsevier Ltd. All rights reserved.

Marine Pollution Bulletin 151 (2020) 110878

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MeHg) in the upper layers of sediment (Duran et al., 2008) or in the open ocean water (Heimbürger et al., 2010). MeHg is the most toxic Hg species able to efficiently bioaccumulate and biomagnify especially in marine food webs (Riisgård and Hansen, 1990; Futter, 1994; Jarman et al., 1996; Hansen and Danscher, 1997). Cd is relatively mobile in the marine environment, exchangeable and potentially bioavailable. Cd is considered a modern toxic metal as its industrial use was minor until about 80 years ago. Cd is accumulated mainly through the gills especially in digestive gland, liver and kidney probably sequestered in insoluble granules or bound to tissue proteins such as metallothioneins (Roesijadi, 1996; Canli and Atli, 2003). Lead is present in marine ecosystems at lower concentrations in clean open ocean waters than in coastal waters. It is mainly derived from land-based natural and anthropogenic sources (Neff, 2002). However, most lead enters the oceans from atmosphere in large part from burning gasoline and from metal smelters (Pacyna and Pacyna, 2001). Se is a semimetal essential for the functioning of all organisms. However, the difference between the dose necessary for the proper functioning of the organism and a harmful dose is small. The biological importance of this element is associated with its occurrence in proteins and enzymes. It is known to have a protective role against Hg (CuvinAralar and Furness, 1991; Wang et al., 2001; Wang and Wang, 2017) or against Cd toxicity (Zwolak and Zaporowska, 2012; Siscar et al., 2014). Probably due also to its more limited commercial interest in comparison with fish such as tuna and swordfish, no extensive studies on environmental contaminant in the Mediterranean spearfish have been conducted yet. Indeed, traditionally this species is mainly eaten by inhabitants of north-eastern Sicily, where it is caught accidentally in saury nets or by special harpoons from boats called “passerelle” used for hunting swordfish. Since stocks of large pelagic predators such as tuna and swordfish are diminishing (Myers and Worm, 2003) as a result of high demand on the global fish market and consequent overfishing (FAO, 2011), some species currently of low commercial interest, such as the Mediterranean spearfish, may be an important alternative fish resource for human consumption in the years to come. The Mediterranean spearfish may also be extremely useful in the assessment of the quality of the pelagic marine ecosystem. Large pelagic fish, are suitable for monitoring short- to medium-term changes compared to cetaceans that provide an integrated view of long-term changes (Fossi et al., 2012). The aim of the present study was to fill some of the gaps in the knowledge of trace elements in T. belone by providing data on total trace elements in muscle and liver of 29 specimens caught in the southern Tyrrhenian Sea, Strait of Messina and Ionian Sea (Fig. 1) in the summers 2008 and 2009. On the boat, after catching specimens, lower jaw fork length (LJFL) was measured to the nearest 1.0 cm and, when possible, sex was

Fig. 2. Length frequency distribution of T. belone specimens (length was lower jaw fork length, LJFL).

determined by macroscopic examination after dissection of gonads. Samples of muscle and liver were immediately obtained, stored in polyethylene containers in a freezer at −20 °C and sent to the laboratory. The specimens ranged from 6 to 22 kg in weight and from 128 to 190 cm in length (Fig. 2); the catch included 15 females, 4 males and 10 specimens which sex was not determined. Analytical procedures were carried out on dry material after lyophilisation; water content (%) was calculated. Trace element levels were quantified by atomic absorption spectrometry after microwaveassisted acid decomposition of tissues with 4:1 v/v HNO3 and H2O2 and dilution to a final volume of 40 mL with ultrapure water. Graphite furnace atomic absorption spectrometry (GFAAS) was used for Cd and Pb (Analytik Jena ContrAA 700), cold vapour (CVAAS) flow injection (Perkin Elmer FIAS 400) for total Hg, and graphite furnace atomic absorption coupled with hydride generation (GFAAS–HGAAS) spectrometry for Se (Analytik Jena ContrAA 700, HydrEA). Quality assurance procedures included instrument calibration using certified standards, analyses of matrix spikes, reagent blank and Standard Reference Materials (SRM) namely Dorm-4 (Institute of Environmental Chemistry, Ottawa, Canada) and Oyster Tissue n. 1566b (National Institute of Standards and Technology, Gaithersburg, MD, USA). Element concentrations (mean of three replicates) were expressed in mg/kg dry weight (d.w.). Values below the LOD (limit of detection) were replaced with the value LOD/2. To calculate Se:Hg, Se:Cd and Se:(Hg + Cd) molar ratios, element concentrations were converted to mol/g. Statistical analysis was performed with Stat Soft for Windows version 7.0. KolmogorovSmirnov test was used to verify the normal distribution. Correlations were verified by the Spearman correlation coefficient rs and differences between variables by the Mann-Whitney test. The results were considered significant for values of p < 0.05. Results on concentrations of Cd, Pb, Hg and Se (mg/kg d.w.) in liver and muscle of T. belone are shown in Table 1. Liver showed the following mean concentration ranking: Se > Cd > Hg > Pb; the ranking for muscle was Hg > Se > Pb > Cd. The calculated muscle/ liver ratios, which emphasized the element tissue organotropism, are reported in Table 2. Significant differences were found between liver and muscle for all four elements, with Cd, Pb and Se levels higher in liver than muscle (p < 0.01), which conversely showed higher Hg levels (p < 0.05). However, the differences in Hg content between the two tissues were not significant when moisture was considered. No significant differences in element concentration were found between males, females and/or specimens of undetermined sex or in relation to year of capture.

Fig. 1. Sampling area. 2

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Table 1 Trace element concentrations (mg/kg d.w.) and water content (%) in liver and muscle of specimens of T. belone. Tissue Liver

Muscle

a

Cd Range Mean ± S.D. CV % n Range Mean ± SD CV % n

Hg

1.227–13.254 5.815 ± 3.038 52.2 26 < LODa–0.06 0.019 ± 0.015 80.7 25

0.508–7.508 2.698 ± 2.214 82.1 26 0.786–8.565 3.401 ± 1.908 56.1 25

Se

Pb

Water content

3.488–11.141 6.577 ± 1.789 27.2 26 1.240–2.113 1.727 ± 0.232 13.5 25

< LOD –6.282 0.661 ± 1.344 203.5 26 0.107–1.525 0.532 ± 0.322 60.6 25

74.2–79.1 76 ± 2 2.7 26 63.9–72.6 68 ± 2.4 3.5 25

a

LODs were 0.45 μg/L for Pb and 0.02 μg/L for Cd.

Se (rs = 0.458, p < 0.05). The muscle/liver ratio for Cd showed an inverse correlation with specimen size (LJFL) (rs = −0.700, p < 0.005). Unlike levels of Hg, Se and Cd, those of Pb are not directly related to diet (Suedel et al., 1994). Indeed, since T. belone feeds on fish and cephalopods, it belongs to a high level of the food web. Fish ingestion is considered the main dietary input of Hg (Bloom, 1992) and Se (Yang et al., 2008) and cephalopod consumption is a vector of Cd in the food web (Bustamante et al., 1998; Das et al., 2003). Both are major dietary items of T. belone (Castriota et al., 2008; Romeo et al., 2009). Due to extremely limited knowledge on Mediterranean spearfish, our data on trace elements in muscle and liver of T. belone was compared with that of other Istiophoridae species found in recent literature (Table 3). Comparisons are seldom straightforward due to differences in species-specific features, size of specimens, methodology etc., nevertheless it can be useful to highlight the main differences. Within the Mediterranean Sea, only muscle Hg levels have been reported on this species (Di Bella et al., 2018) with values slightly higher than those of the present research. This is probably related to a slight differences in specimens size even though a proper comparison is not possible as the type of length Di Bella et al. (2018) measured is not

Table 2 Mean ( ± S.D.) muscle/liver ratios in T. belone, calculate from element concentration expressed on dry weight basis (d.w.) and wet weight basis (w.w.). Element Cd Hg Se Pb

Muscle/liver ratio (d. w.) 0.004 1.754 0.283 4.839

± ± ± ±

0.004 1.128 0.078 6.224

Muscle/liver ratio (w. w.) 0.003 1.316 0.212 3.632

± ± ± ±

0.003 0.847 0.059 4.672

Significant positive correlations were found between element concentrations and size (LJFL) (Fig. 3) for Hg in liver (rs = 0.713, p < 0.01) and muscle (rs = 0.452, p < 0.05). Cd levels showed a significant positive correlation with size in liver (rs = 0.395, p < 0.05) and a significant negative correlation in muscle (rs = −0.430, p < 0.05). Relationships among elements were found. Cd and Se concentrations were correlated with those of Hg (rs = 0.546, p < 0.01 and rs = 0.396, p < 0.05, respectively) in liver. A negative correlation was found between Pb and Se in muscle (rs = −0.618, p < 0.01). A significant correlation was found between muscle/liver ratios for Hg and

Fig. 3. Correlations between length (LJFL) and levels of Hg and Cd in muscle and liver of T. belone. 3

4

a

M. nigricans K. audax M. nigricans M. nigricans M. nigricans

M. nigricans

platypterus platypterus platypterus platypterus platypterus platypterus K. audax K. audax K. audax K. audax K. audax M. mazara M. mazara T. angustirostris T. angustirostris M. nigricans M. nigricans M. nigricans M. nigricans

I. I. I. I. I. I.

T. belone T. belone T. belone

Species

Muscle Muscle Muscle Muscle Muscle

Muscle

Muscle Liver Muscle Muscle Muscle Liver Muscle Muscle Muscle Muscle Liver Muscle Muscle Muscle Muscle Muscle Liver Muscle Liver

Muscle Liver Muscle

Tissue

265–311 – – 50–545 kg –

219 ± 14

192.7 ± 1.7 192.7 ± 1.7 166–246 217–265 163–240 163–240 159–254 – 192–222 140–183 (post orbital 140–183 (post orbital 212–225 – – 81 ± 32 kg 196–237 196–237 134–261 (post orbital 134–261 (post orbital length) length)

length) length)

128–190 128–190 142–179 (unspecified length)

LJFL (cm)

9 7 7 4 3

3

67 67 17 22 67 67 13 30 5 57 57 5 50 20 19 99 99 21 21

25 26 14

N.

10.52 ± 5.03 0.51 ± 0.08 0.56 ± 0.05 5.13 ± 4.01 3.1 ± 0.17

0.747 ± 0.865

– – 1.48 ± 0.93 0.4 ± 0.95 0.56 ± 0.04 0.57 ± 0.07 1.72 ± 0.61 0.47 ± 0.37 0.14 ± 0.13 – – 0.36 ± 0.48 2.38 ± 3.00 0.21 ± 0.13 1.616 ± 1.14 1.91 5.5 – –

0.816 ± 0.458 0.862 ± 0.707 1.082

Hg

– – – – –

0.018 ± 0.017

0.434 ± 0.089 95.1 ± 11 0.55 ± 0.37 – – – 0.37 ± 0.40 – – 0.15 ± 0.16 139.1 ± 161.2a – – – – – – 0.06 ± 0.04 62.71 ± 37.66a

0.005 ± 0.004 1.858 ± 0.971 –

Cd

– – – – 2.1 ± 0.35

1.126 ± 0.550

– – – – 0.67 ± 0.03 11.4 ± 2.5 – 0.72 ± 0.20 – – – – 1.59 ± 0.17 0.58 ± 0.12 – – – – –

0.413 ± 0.0556 2.10 ± 0.575 –

Se

Data originally expressed on a dry weight basis was converted to wet weight using the moisture content of 76% found in the present study for T. belone.

Gulf of Mexico unspecified unspecified North Atlantic Bermuda

Atlantic Ocean

Seychelles

Indian Ocean

Gulf of California Gulf of California Golf of California Gulf of California Gulf of California Gulf of California Gulf of California Honolulu, Hawaii Gulf of California Gulf of California Gulf of California Gulf of California Honolulu, Hawaii Honolulu, Hawaii Honolulu, Hawaii Southern Gulf of California Southern Gulf of California Gulf of California Gulf of California

Pacific Ocean

Strait of Messina Strait of Messina Strait of Messina

Mediterranean Sea

Area

Table 3 Levels of Cd, Pb, Hg and Se (mean ± S.D. or range; mg/kg w.w.) in the present study and in the recent literature for Istiophoridae.

– – – – –

0.009 ± 0.001

0.025 ± 0.009 0.047 ± 0.004 0.36 ± 0.29 – – – 0.35 ± 0.08 – – – – – – – – – – – –

0.128 ± 0.077 0.211 ± 0.431 –

Pb

Cai et al., 2007 Yamashita et al., 2005 Yamashita et al., 2005 Luckhurst et al., 2006 Dewailly et al., 2008

Bodin et al., 2017

Moreno-Sierra et al., 2016 Moreno-Sierra et al., 2016 Soto-Jiménez et al., 2010 García-Hernández et al., 2007 Bergés-Tiznado et al., 2015 Bergés-Tiznado et al., 2015 Soto-Jiménez et al., 2010 Kaneko and Ralston, 2007 García-Hernández et al., 2007 Ordiano-Flores et al., 2019 Ordiano-Flores et al., 2019 García-Hernández et al., 2007 Kaneko and Ralston, 2007 Kaneko and Ralston, 2007 Brooks, 2004 Vega-Sánchez et al., 2017 Vega-Sánchez et al., 2017 Ordiano-Flores et al., 2019 Ordiano-Flores et al., 2019

Present study Present study Di Bella et al., 2018

Reference

S. Ancora, et al.

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2006; Fishbase, 2019). Moreover, we had no information on the body condition (e.g. somatic index) and on metabolic activity of our specimens, therefore these factors should be further investigated on this specie to explain the variability. Indeed, some elements vary with age and may accumulate over a lifetime. Since size, whether LJFL or weight, is usually assumed to be directly related to age or a proxy for age (Canli and Atli, 2003; Barghigiani et al., 2000; Monteiro and Lopes, 1990), size is the most important parameter to consider. Results on T. belone, in line with a number of previous studies on fish (Walker, 1976; Monteiro and Lopes, 1990; Andersen and Depledge, 1997; Storelli et al., 2002; Adams, 2004; Licata et al., 2005; Kojadinovic et al., 2006; Endo et al., 2008; Hajeb et al., 2009; Damiano et al., 2011), showed that specimen size significantly correlated with certain element concentrations, namely Hg and Cd (Fig. 3). In muscle, a significant positive correlation between Hg and size has been widely reported in Istiophoridae (Mackay et al., 1975; Shultz and Crear, 1976; Shultz et al., 1976; Barber and Whaling, 1983; Luckhurst et al., 2006; García-Hernández et al., 2007). However, no information on this relationship was indicated for M. nigricans from the Gulf of Mexico by Cai et al. (2007) or for M. nigricans and T. audax from Japan by Yamashita et al. (2005) and no relationship could be deduced from data on I. platypterus and M. audax from the Gulf of California by SotoJiménez et al. (2010). The positive relationship between Hg concentrations and size depends on the slow rate of elimination of MeHg relative to its rapid rate of uptake, as elsewhere indicated (Trudel and Rasmussen, 1997). MeHg forms covalent bonds with proteins in muscle (Carty and Malone, 1979; Georgieva et al., 2004). Almost all MeHg in muscle of T. thynnus and X. gladius has been reported in myofibrilar and sarcoplasmic proteins (Arima and Umemoto, 1976) and covalent binding of MeHg to cysteine residues has been showed by X-ray absorption spectroscopy (Harris et al., 2003). In addition, since protein assimilation in carnivorous fish is generally 80% of total assimilation from food (Brett and Groves, 1979), the positive correlation between Hg concentration and body mass observed here is in line with expected patterns of accumulation. In liver, the significant positive correlation between Hg concentrations and size (LJFL) found in T. belone is in line with findings on other Istiophoridae (Moreno-Sierra et al., 2016; Bergés-Tiznado et al., 2015; Vega-Sánchez et al., 2017). Excluding one study indicating uncommon negative correlations in tuna (Licata et al., 2005) and one other with similar levels in these two tissues reported for I. platypterus (BergésTiznado et al., 2015), positive relationships have been extensively reported in the literature on fish (Kojadinovic et al., 2007; Branco et al., 2007; Endo et al., 2008), as well as for marine mammals (Honda et al., 1983; Monaci et al., 1998). In particular, as in the case of muscle, the increase in hepatic concentrations of Hg with size, and therefore age, is a true case of accumulation with little or no elimination process (McFarlane and Franzin, 1980). Conversely, the negative correlations between fish size and Cd concentrations in muscle may be due to growth being faster than metal accumulation in this tissue, whereas in liver we see an opposite trend (Fig. 3). Interestingly, the opposite relationship found between the Cd muscle-liver ratio and the specimens size indicates that in the muscle of younger specimens, the accumulation rate of this element is slightly higher than in older ones. There could be increasing induction of Cdbinding metallothioneins in liver with exposure to Cd (Cornelis and Nordberg, 2007), leading to higher Cd levels with specimen size and thus specimen age. Also, different diets at different ages, with younger fish presumably feeding mainly on cephalopods, a diet richer in Cd than that of adults, as well as a differences in Cd detoxification and excretion at different ages, with adult being more efficient than younger fish, may be involved. Data in the literature concerning Cd levels in muscle and specimen size, indicates inconsistent correlations: positive for example in swordfish and skipjack tuna (Kojadinovic et al., 2007; Damiano et al.,

specified. Mean levels of Hg in muscle and liver of T. belone specimens from the Mediterranean Sea were generally in the range of literature data on other Istiophoridae from the Pacific and Atlantic Oceans (Table 3). However, levels up to three times higher have been reported in muscle of I. platypterus, K. audax (Soto-Jiménez et al., 2010) and M. mazara (Kaneko and Ralston, 2007) from the Pacific Ocean compared to those of T. belone from the Mediterranean. Concentrations of Hg in M. nigricans from the Atlantic Ocean (Luckhurst et al., 2006; Dewailly et al., 2008; Cai et al., 2007) appear to be up to one order of magnitude higher than mean levels found by us in T. belone. Indeed, intrinsic factors such as different physiological processes or high uptake rates due to feeding rates, and larger size of specimens or longer lifespan can determine major interspecies concentration differences. Scanty literature is available for Cd, nevertheless, T. belone showed extremely low levels compared to those reported for muscle and especially for liver of Istiophoridae from the Pacific Ocean which were up to 70 times higher (Soto-Jiménez et al., 2010; Moreno-Sierra et al., 2016; Ordiano-Flores et al., 2019). These higher Cd levels may be due to a higher contribution of cephalopods in the diet of these species with respect to T. belone or to emissions from industrialized countries and volcanic activity along the eastern Pacific seaboard (Stamatis et al., 2019). Lower Pb concentrations were found by Moreno-Sierra et al. (2016) in I. platypterus and by Bodin et al. (2017) in M. nigricans; contrarily, Soto-Jiménez et al. (2010) found higher mean levels of Pb in I. platypterus and K. audax compared to those found in T. belone. Selenium levels recorded in the present study were lower than those reported in liver and muscle of specimens from other areas (Table 3). Comparisons with the trace element concentration in muscle and liver of other large pelagic fish with similar trophic levels from the Mediterranean Sea, namely X. gladius and T. thynnus,are available in Supplemental material. The overall results on trace elements in T. belone indicated variations in concentrations between tissues and between specimens of different sizes. High variations were expected since trace elements in top predators are likely to be influenced by factors such as sex, age, growth rate, longevity, body condition, metabolic activity, reproductive status, feeding preferences, migrations, and so forth (Barghigiani et al., 2000; Monteiro and Lopes, 1990; Hornung et al., 1993; Kojadinovic et al., 2006; Lahaye et al., 2006; Branco et al., 2007; Cai et al., 2007; Pethybridge et al., 2010; Damiano et al., 2011; Bergés-Tiznado et al., 2015). Concerning the influence of gender, the lack of differences in liver and muscle element levels, as well as in size (LJFL), between males, females and specimens of unknown sex was in line with results of studies on other Istiophoridae (Bergés-Tiznado et al., 2015; MorenoSierra et al., 2016; Ordiano-Flores et al., 2019). For species which show sexual size dimorphism, such as X. gladius, significant differences in Hg concentrations between males and females have been reported for specimens larger than 125 cm LJFL (Monteiro and Lopes, 1990). Indeed, mercury net accumulation is age-dependent and the faster growing sex (females in the case of swordfish) shows lower concentrations due to greater dilution by tissue growth (Monteiro and Lopes, 1990; Mendez et al., 2001). Similarly to X. gladius, a different Hg accumulation between male and female may not be excluded in T. belone: studies on other Istiophoridae indicate that they initially grow rapidly and exhibit sexual dimorphism, with females growing to larger maximum sizes than males (Hoolihan, 2006). The relationships between element tissue concentrations and the length differences between sexes need further investigation for this species with studies on large number of sexed specimens. Information regarding the age and growth of T. belone is limited and unreliable and it was impossible to calculate specimen age with the von Bertalanffy model without growth parameters specific for this species. No studies on tagging experiments have been found (Arocha and Ortiz, 5

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Fig. 4. Relationships between length (LJFL) and elements molar ratios in muscle and liver of T. belone.

muscle usually exceeds 80% (Kannan et al., 1998) in contrast to the liver, where accumulation is mostly in inorganic form of Hg. Since Hg turnover rates are, as a general rule, higher in liver than in muscle, muscle concentration reflects elemental intake over a longer period than other tissues (Kojadinovic et al., 2007; Bustamante et al., 2003; Branco et al., 2007). The accumulation levels are species-specific, as indicated by Yamashita et al. (2005) who reported that the proportion of MeHg on the total Hg was 76 ± 6% in T. audax, 43 ± 3% in M. nigricans, 72 ± 8% in X. gladius and 77 ± 11% in T. thynnus. Differences between species may therefore be related to the fact that MeHg is either processed or stored in liver tissue of certain species of fish (Licata et al., 2005). Higher Cd accumulation in liver is consistent with most studies in the literature on fish (Canli and Atli, 2003; Kojadinovic et al., 2007; Endo et al., 2008; Eisler, 2010) and has been reported for other Istiophoridae (Moreno-Sierra et al., 2016; Ordiano-Flores et al., 2019). This can be explained by metal-binding proteins such as metallothioneins in liver (Roesijadi, 1992; Roesijadi, 1996; Ploetz et al., 2007). They play an essential role in the detoxification (Samson and Gedamu, 1997) of various metals, especially Cd and even Hg (Cornelis and Nordberg, 2007). However, no specific studies on these metal-binding proteins have been found in Istiophoridae. Unlike Cd, the significantly higher concentrations of Pb in liver, also reported in I. platypterus (Moreno-Sierra et al., 2016) and in other fish (Canli and Atli, 2003; Storelli et al., 2005), may not be related to induction of metallothioneins, rather to other biochemical or metabolic function, as these do not bind Pb (Ploetz et al., 2007). Pb muscle-liver ratios (about 4.8) seem inconsistent with the element ranking based on mean tissue concentrations (with similar mean concentrations in muscle and liver), presumably due to high variability of tissue levels. In line with our finding on T. belone, higher levels of Se in liver than in muscle have reported also in other Istiophoridae (Bergés-Tiznado et al., 2015) and other large pelagic fish (Branco et al., 2007). As reported for various marine organisms (Wang et al., 2001; Farias et al., 2005; Gajdosechova et al., 2016), the significantly higher levels of Se in liver compared to muscle could be related to liver metabolic activity in counteracting Hg toxicity and in preventing oxidative

2011), absent in yellowfin tuna and dolphinfish (Kojadinovic et al., 2007) and negative in small fish such as grey mullet (Canli and Atli, 2003). Only a few studies on Istiophoridae analysed Cd in muscle: excluding a positive relationship with size reported in K. audax (OrdianoFlores et al., 2019), no significant relationship was reported for other (Ordiano-Flores et al., 2019; Moreno-Sierra et al., 2016). Similarly, no relationship with size can be calculated from the data of Soto-Jiménez et al. (2010). The lack of relationship with size may be due to the low concentrations of Cd in muscle which are probably easier to eliminate than to accumulate. In line with the results of the present research on T. belone (Fig. 3), significant positive correlation between Cd in liver and size was reported in I. platypterus (Moreno-Sierra et al., 2016) and in K. audax (Ordiano-Flores et al., 2019). Excluding Hg, the other elements accumulated in T. belone more in liver than in muscle, in line with previous observations of different authors in other pelagic fish: cadmium in particular showed a mean concentration in liver two orders of magnitude higher than in muscle (Canli and Atli, 2003; Kojadinovic et al., 2007; Licata et al., 2005; Branco et al., 2007; Storelli et al., 2005). In contrast, the organotropism of Hg in T. belone was not well defined: indeed significantly higher mean Hg level was found in muscle than in liver, nevertheless, the difference in Hg content between the two tissues was not significant when the concentration was expressed on wet weight bases. Results for I. platypterus (Bergés-Tiznado et al., 2015) indicate similar values for the two tissues whereas, a recent study on M. nigricans from the southern Gulf of California (Vega-Sánchez et al., 2017) reported Hg higher in liver than in muscle only when Hg in liver was elevated (> 10 mg/kg w.w.). Besides a number of studies showing higher Hg concentrations in liver than muscle (Kojadinovic et al., 2007; Branco et al., 2007; Endo et al., 2008; Hajeb et al., 2009; ), Hg has also been reported occasionally in literature with lower levels in liver than in muscle (Licata et al., 2005; Branco et al., 2007). The liver plays an important role in contaminant storage, redistribution, detoxification and transformation and acts as an active site of pathological effects induced by contaminants (Evans et al., 1993). Mercury accumulation in muscle and in liver, is known to be related to the chemical form of the element. Methylmercury to total Hg ratio in

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Table 4 Molar ratios of Se:Hg, Se:Cd and Se:(Hg + Cd) in liver and muscle of T. belone specimens with mean and standard deviation. ID specimen

Se:Hg

LIVER Se:Cd

Se:(Cd + Hg)

Se:Hg

MUSCLE Se:Cd

Se:(Cd + Hg)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 Mean ± S.D.

34.56 17.46 21.47 15.16 8.49 12.89 6.35 n.a. 8.10 9.45 9.00 10.55 16.11 8.10 8.35 11.95 10.29 3.53 11.21 2.86 8.44 3.84 3.57 4.97 1.85 n.a. n.a. 4.87 4.38 9.92 6.98

3.16 4.05 1.59 1.29 3.33 2.45 0.99 n.a. 2.98 1.51 2.86 0.84 1.68 2.01 2.27 2.83 2.73 1.24 2.50 1.45 1.22 1.06 1.12 1.72 0.72 n.a. n.a. 1.09 2.88 1.98 0.91

2.89 3.28 1.48 1.19 2.39 2.06 0.85 n.a. 2.18 1.30 2.17 0.78 1.52 1.61 1.79 2.29 2.16 0.92 2.05 0.96 1.07 0.83 0.86 1.28 0.52 n.a. n.a. 0.89 1.74 1.58 0.71

6.01 5.50 1.51 1.11 1.38 1.39 1.59 1.21 n.a. 1.68 n.a. 2.04 2.76 2.01 1.54 0.96 1.66 0.94 1.75 n.a. 2.32 n.a. 0.53 0.77 0.77 0.66 1.02 1.13 2.36 1.78 1.32

44.9 224. 120 36.1 59.7 98.9 165 143 n.a. 171 n.a. 78 283 598 143 1448 92.7 80.6 606 n.a. 148 n.a. 97.5 1085 168 106 261 1368 320 317 422

5.30 5.37 1.49 1.08 1.35 1.37 1.58 1.20 n.a. 1.66 n.a. 1.98 2.74 2.00 1.52 0.96 1.63 0.93 1.75 n.a. 2.28 n.a. 0.52 0.77 0.76 0.66 1.02 1.13 2.34 1.74 1.22

unclear (Cusack et al., 2017). The direct correlation between Hg and Cd in T. belone liver may indicate co-accumulation of the two metals as also observed in studies of arctic marine mammals (Hansen et al., 1990; Paludan-Müller et al., 1993). Indeed, Se seems to also protect from the toxic effects of Cd with Se-Cd molar ratio found in liver of T. belone similar to those reported by Hansen et al. (1990) for minke whale, beluga and narwhal livers. The two elements may form equimolar Cd-Se complexes in liver (Caurant et al., 1994; Seixas et al., 2007) and indeed a significant positive relationship has been observed between the molar concentrations of Se and Cd in liver of various marine mammals (Caurant et al., 1994; Monaci et al., 1998; Meador et al., 1999). The protection mechanism formerly postulated for cephalopods (Barghigiani et al., 1993) and partially investigated with terrestrial mammals, under laboratory conditions, is based on formation of Cd-Se complexes (Zwolak and Zaporowska, 2012). Se first produced a Cd-Se complex, which subsequently bound to a selenoprotein P, reduce Cd availability (Sasakura and Suzuki, 1998). Recent studies provided evidence for a strong defense capacity of Se and metallothioneins against Cd in deep-sea fish from the NW Mediterranean (Siscar et al., 2014; Sørmo et al., 2011) and suggested several mechanisms of metal detoxification in fish liver, some involving both Se and metallothioneins. Interestingly, the Se: (Hg + Cd) molar ratio > 1 found in liver may further indicate that in T. belone the Se levels in liver were likely sufficient to contribute to the detoxification of both Hg and Cd. Since stocks of large pelagic predators such as tuna and swordfish are diminishing due to high demand from global fish markets and overfishing (FAO, 2011), species currently of low commercial interest such as T. belone may become important alternative resources in the near future. In order to protect consumers and especially susceptible subjects such as pregnant women, the elderly and children against the toxic effects associated with excessive consumption of contaminated

damage, especially through production of enzymes containing Se, such as glutathione peroxidase (Nagai et al., 1999; Belzile et al., 2006; Chatziargyriou and Dailianis, 2010) and formation of Se-complexes with Hg (Cuvin-Aralar and Furness, 1991) or with other metals (Zwolak and Zaporowska, 2012; Sasakura and Suzuki, 1998; Sørmo et al., 2011) discussed below in this article. The Se-element molar ratios in liver and muscle of T. belone are reported in Table 4. The mean molar ratio was close to 1 for Se:Hg in muscle and for Se:Cd in liver. Interestingly, the mean ratio calculated for Se:(Cd + Hg) was in both liver and muscle also close to 1. Specimen size (LJFL) was significantly negatively correlated with all molar ratios in muscle and liver, excluding the case of Se:Cd in muscle (Fig. 4). Se:Hg close to 1 is common in marine mammals and seabirds with high liver concentrations of Hg (> 100 mg/kg w.w.), while ratios close to 1 have even been reported at Hg levels > 2 mg/kg w.w. (Braune et al., 1991; Dietz et al., 2000; Storelli and Marcotrigiano, 2002) and together with a positive correlation between Hg and Se indicate Se protective role against Hg (Cuvin-Aralar and Furness, 1991; Wang et al., 2001). The mechanisms involved in this process are species- and tissue-specific and include the formation of inert Hg-Se complexes (Martoja and Berry, 1980), Hg binding to selenoproteins (Palmisano et al., 1995), action of Se in preventing oxidative damage by Hg (Belzile et al., 2006) and demethylation of MeHg (Wang and Wang, 2017). A Se:Hg molar ratio closed to 1 for liver found in T. belone suggests a protective role of Se against Hg toxicity, although the inverse correlation observed between Se:Hg molar ratio and fish size (Fig. 4) indicates lower protection by Se in larger fish (Santos and Silva, 2017; Wang et al., 2018). It has also been reported that a protective molar ratio would need to be greater than one (Sørmo et al., 2011), because if all selenium in the body does bind mercury in a 1:1 ratio, this leaves insufficient selenium to synthesize enzymes and carry out its essential role. However, there is currently no agreement on the actual Se:Hg molar ratio that confers protection and the mechanisms protecting against Hg toxicity remain

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References

products, the European Community passed Commission Regulation no. 1881/2006 (and subsequent amendments) imposing specific maximum levels of certain contaminants in fish marketed for human consumption. The contaminants include Hg, Pb and Cd due to their high toxicity. The Regulation sets maximum levels of Hg, Cd and Pb of 1.0 mg/kg w.w., 0.05 mg/kg w.w. and 0.30 mg/kg w.w. respectively, for muscle of T. belone, classified as “Makaira species”. The mean mercury level of 0.816 ± 0.458 mg/kg w.w. found in the present study was below the Hg limit of 1 mg/kg w.w. established for the Mediterranean spearfish. However, 28% of samples exceeded the limit. The mean concentration of lead was 0.128 ± 0.077 mg/kg w.w., about one third of the maximum level of 0.30 mg/kg w.w. set for this element by the same EC Regulation and only 4% of samples exceeded the threshold. None of the samples exceeded the maximum level allowed for Cd (0.05 mg/kg w.w.), and the mean concentration of 0.005 ± 0.004 mg/kg w.w. was about one tenth of the regulatory threshold. Regarding selenium, the difference between a dose necessary for the proper functioning of the organism and a harmful dose is small (Kieliszek, 2019) and there is no maximum level in fish marketed for human consumption for Se. The World Health Organization (WHO) recommends a daily dose of selenium (Recommended dietary allowances, RDAs) at a level of 55 μg for adults. A daily dose of 400 μg is considered harmless. The dose that does not show any adverse effect for adults is estimated at 800 μg Se/day, whereas a dose that causes the onset of toxicity ranges from 1540 to 1600 μg Se/day. Indeed the Se:Hg molar ratio in muscle is also a marker of Hg-related risk for human consumption (Burger et al., 2012) and in our samples it exceeded 1, indicating negligible risk for human health (Table 4). In conclusion, this study gathered a first set of data on trace elements in the Mediterranean spearfish drawing a baseline for insights into organotropism and for comparison with levels of other Istiophoridae, of other large pelagic fish and those of future monitoring studies. Combined with biometric parameters, feeding habits and other data they contribute to fill out an ecotoxicological and ecophysiological picture of T. belone. Trophodynamic studies using stable isotopes may provide further knowledge on the ecology of this species and on the contribution of different prey species in Hg and other trace element accumulation. Assessment of other contaminants, such as persistent organic pollutants POPs and emergent contaminants, in tissues of the Mediterranean spearfish will complete the ecotoxicological and ecophysiological picture of this pelagic predator.

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CRediT authorship contribution statement Stefania Ancora: Conceptualization, Writing - review & editing, Writing - original draft. Giacomo Mariotti: Validation, Data curation, Writing - review & editing. Rosetta Ponchia: Methodology, Investigation. Maria Cristina Fossi: Resources, Methodology. Claudio Leonzio: Resources, Methodology. Nicola Bianchi: Conceptualization, Software, Writing - original draft.

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.

Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.marpolbul.2019.110878. 8

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