Mercury (Hg) is one of the metals with a large number of studies because of its negative impacts on the environment. It is released from natural and anthropogenic sources and its occurrence in the atmosphere is increased by industrial activity (Sullivan and Krieger 2001). In the terrestrial environment, the extensive use of Hg as a fungicide in agricultural activities has caused several poisoning outbreaks (Clarkson 2002). In aquatic ecosystems, Hg is a relevant issue since it can be biomagnified in top consumers of the food webs. Human exposure to Hg is mainly through dermal contact, inhalation and food. It is recognized that dietary intake is the main contributor of this element to humans; among main food items, fish is the most important. Furthermore, the predominant and most dangerous Hg species in fish muscle is the methylated form (methyl Hg). Consequently, consumption of fish is the primary route of exposure to methylmercury in most human populations (Mergler et al. 2007).

The process of biomagnification enhances a higher Hg accumulation in the elevated levels of food webs. For this reason, in the marine environment top predators like fish are likely to have more Hg concentrations than other organisms. Makaira nigricans (Lacépède 1802), usually known as blue marlin, is a large predator that lives in surface and subsurface waters of tropical and temperate oceans (Abitia-Cárdenas et al. 2010). This fish species has a low diversity of prey, with its main prey being frigate and other related tuna (Auxis spp.) and jumbo squid (Dosidicus gigas). This indicates a high degree of food specialization (Shimose et al. 2010). Besides the food specialization of M. nigricans, its diet is similar among years in the southern Gulf of California (Abitia-Cárdenas and Aguilar-Palomino 1999) but its feeding habits are known to change depending on the size of specimens (Shimose et al. 2010).

The Gulf of California locates in NW Mexico, it is a marginal sea surrounded by desertic areas (Castro et al. 2006), mostly on its west side. The southern part of the Gulf of California connects to the Pacific Ocean in an oceanographical transition zone where diverse water masses intermix. The mixing extent of the water masses varies on a seasonal basis (Torres-Orozco 1993); additionally, inter-annual climatic variations that comprise the Pacific Ocean known as El Niño-Southern Oscillation (ENSO) occur (Lluch-Cota et al. 2001). As a consequence of ENSO, patterns of precipitations and winds in the southern region of the Gulf of California are modified. Similarly, primary production is increased when cold and nutrient rich deep waters go to the surface areas (Thunell 1998); this, in turn, supports other components of the trophic webs. The presence of M. nigricans in the southern Gulf of California seems to be related to warm surface waters that have been registered from May to November (Ortega-García et al. 2006).

Fig. 1
figure 1

Sampling sites of Makaira nigricans in the states of Baja California Sur (1. La Paz; 2. Los Cabos) and Sinaloa (3. Mazatlán), Mexico

Full size image

The objectives of this work were: (a) to determine Hg distribution in muscle and liver of M. nigricans from the southern Gulf of California for the period 2005–2012; (b) to compare Hg levels with specimens of the same species from different areas; and (c) to contrast Hg levels in the edible portion of blue marlin with the maximum permissible limits in the Mexican legislation.

Materials and Methods

Individuals of Makaira nigricans were collected from three areas along the southern Gulf of California between 2005 and 2012 (Fig. 1). Fish were obtained by sport fishermen, trolling with bait (mainly chub mackerel Scomber japonicus). The total fresh weight, sex and size the lower jaw length (LJL), from the tip of the lower jaw to the fork; and the posorbital length (POL), from the post eye part to the caudal fin of each fish were determined in the field. The sampling areas, years of capture, number of specimens, sex, mean weight and length of individuals are presented in Table 1. Muscle and liver samples were taken from each fish, then packed and kept frozen until their laboratory processing. Fish samples were freeze-dried (−52°C and 80 × 10− 3 mBars) for 72 h. Dried samples were ground and homogenized in an agate mortar with pestle.

Table 1 Sampling areas, collection years and biological features of blue marlin Makaira nigricans
Full size table

Aliquots of 0.25 g were predigested in Teflon containers (Savillex, Eden Prairie, MN, USA) with 5 mL of nitric acid (trace metal grade) overnight; sample duplicates were digested using hot plates (Barnstead Thermolyne, Radnor, PA, USA) during 3 h at 120°C (MESL 1997). Digested samples were diluted to 25 mL with milli-Q water; additionally, blanks and reference materials (fish muscle-DORM3, and fish liver-DOLT4) were used. Total mercury was analyzed by cold vapor atomic absorption spectrophotometry (CV-AAS) on a Buck Scientific instrument (East Norwalk, CT, USA). The limit of detection was 0.002 µg g−1; results are reported in µg g−1 on a dry weight basis. Elemental recoveries were estimated as the ratio of measured concentrations with respect to the corresponding value in the certificate of the reference material (DORM 3, fish protein National Research Council Canada; and DOLT4, dogfish liver, National Research Council Canada, 1200 Montreal Road, Building M-58 Ottawa, Ontario K1A 0R6, Canada). Percentage recoveries for mercury were 96.9 and 102.7 for DORM3 and DOLT4 respectively.

For the comparisons of Hg concentrations in the present study with published information from other areas (mostly reported on wet weight basis), concentrations were converted from dry weight (dw) to wet weight (ww) using the equation Hgww = Hgdw × (100 − % humidity)/100 (Magalhães et al. 2007). Comparisons of Hg levels among the sampled years were made by a Kruskal–Wallis test; variations of Hg levels in muscle and tissue with size and weight of specimens were defined by a Pearson correlation analysis. Statistical analyses were performed by using Graphpad Prism 4.0 (Graph Pad software, San Diego, CA, USA).

Fig. 2
figure 2

Variation of Hg concentrations (µg g− 1 dry weight) in muscle and liver of blue marlins, Makaira nigricans, from the southern Gulf of California (a), Los Cabos, B.C.S. (b), La Paz, B.C.S. (c), and Mazatlán, Sinaloa (d) along the sampling years

Full size image

Results and Discussion

Variations of Hg concentrations in muscle and liver of M. nigricans along the sampled years are presented as the average values from all the specimens (Fig. 2a), and as the average values from fish collected at Los Cabos, B.C.S. (Fig. 2b), La Paz, B.C.S. (Fig. 2c) and Mazatlán, Sinaloa (Fig. 2d). Considering all the studied specimens (from all the areas together), Hg concentrations in muscle along the sampling period and in liver for the sampling years were not significantly (p > 0.05) different; the similar diet composition among several years in M. nigricans from the southern Gulf of California (Abitia-Cárdenas and Aguilar-Palomino 1999) may have a strong influence on this pattern. Besides, mercury content was higher in liver than in muscle, but only when Hg content in liver was elevated (>10 µg g−1). Several authors have pointed out that there is a tendency to accumulate higher mercury levels in liver than in muscle of fish species (Azevedo et al. 2012; Polak-Juszaczak 2015).

Fig. 3
figure 3

Relationship of Hg (µg g−1 dry weight) in muscle and liver with biometric features of M. nigricans; a Hg in muscle with LJL, b Hg in liver with LJL, c Hg in muscle with POL, d Hg in liver with POL, e Hg in muscle with weight, and f Hg in liver with weight

Full size image

This could be due to the Hg forms present in these two tissues, since inorganic and organic mercury forms have higher affinity for liver and muscle, respectively (Soares et al. 2011). On the other hand, modifications of precipitation and wind patterns associated to ENSO may alter the primary production (Thunell 1998) in the southern Gulf of California and eventually result in different Hg levels in prey and subsequently in M. nigricans. However, this was not reflected along the sampling years. In this respect, average temperatures during the period 2005–2012 in the sea surface for the studied areas were higher in 2009. This coincided with the lowest Hg levels in M. nigricans. Colder waters are related to upwelling that carry nutrients and dissolved elements; this might account for the low Hg levels in the blue marlin during 2009.

The relationships of Hg concentrations with fish size and weight are presented in Fig. 3. In all cases (Fig. 3a–f), Hg levels increased significantly (p < 0.05) with fish dimensions; i.e., there is a tendency to accumulate more Hg as length and weight increase. Correlation coefficients were more elevated in the relationships of size and weight with Hg levels in muscle (Fig. 3a, c, e) than the corresponding cases of Hg levels in liver versus LJL, POL and weight (Fig. 3b, d, f). In diverse studies (Shomura and Craig 1972; Shultz and Crear 1976; Shultz and Ito 1979; Luckhurst et al. 2006), it has been reported that Hg concentrations in muscle of M. nigricans increase with fish weight. This observation is important, since considerable amounts of Hg may be accumulated in the edible portion of the blue marlin. In fact, Hg levels (12.7 µg g−1 wet weight) reported in muscle of M. nigricans are among the highest values reported in this species (Luckhurst et al. 2006).

For comparative purposes, Hg concentrations in muscle and liver of specimens of the same species from different areas were considered (Table 2). In liver, the highest Hg concentration (14.84 µg g−1 wet weight) was reported in specimens from Hawaii (Shomura and Craig 1972); in muscle, the highest value (10.52 µg g−1 wet weight) corresponded to specimens from the northern Gulf of Mexico (Cai et al. 2007).

Table 2 Comparison of average Hg levels (µg g−1 wet weight) in muscle and liver of Makaira nigricans from different areas
Full size table

Our results were comparable to Hg levels reported in muscle and liver of specimens from Hawaii (Shultz et al. 1976) but higher than Hg concentrations in muscle of blue marlins from the Atlantic Ocean (Yamashita et al. 2005) and from the northern Pacific (Kaneko and Ralston 2007).

With respect to the maximum permissible limits of Hg in Mexico, a value of 1.0 µg g−1 (wet weight) has been established in fishery products for human consumption. The average concentration of Hg (1.91 µg g−1 wet weight) in the edible portion (muscle) of blue marlin from the southern Gulf of California is almost twice as high as the legal limit. Considering the elevated concentrations of Hg in the edible part of blue marlin, it is important to monitor the occurrence of this element in this fish species; additionally, the rate of consumption of this species and the co-occurrence of selenium in the muscle tissue are key aspects to consider in the toxicology of Hg in the marine biota.