ISSN 10630740, Russian Journal of Marine Biology, 2015, Vol. 41, No. 6, pp. 479–484. © Pleiades Publishing, Ltd., 2015. Original Russian Text © N.K. Khristoforova, V.Yu. Tsygankov, M.D. Boyarova, O.N. Lukyanova, 2015, published in Biologiya Morya.
ECOLOGY
Heavy Metal Contents in the Pink Salmon Oncorhynchus gorbuscha Walbaum, 1792 from Kuril Oceanic Waters during Anadromous Migration N. K. Khristoforovaa, b, V. Yu. Tsygankova, M. D. Boyarovaa, and O. N. Lukyanovaa, c aFar
Eastern Federal University, pr. Okeanskii 19, Vladivostok, 690091 Russia Pacific Institute of Geography, Far East Branch, Russian Academy of Sciences, ul. Radio 7, Vladivostok, 690041 Russia c Pacific Research Fisheries Center, per. Shevchenko 4, Vladivostok, 690091 Russia email:
[email protected]
b
Received June 4, 2015
Abstract—The contents of trace elements, viz., Hg, As, Pb, Cd, Zn, and Cu, in a common species of Pacific salmon, viz., the pink salmon, which were caught in early July 2012 and 2013 in the vicinity of Kuril Islands, were examined. It was found that the contents of toxic elements, Cd, Pb, As, and Hg, in the salmon meet humanhealth consumption guidelines for seafood by the sanitary standards and regulations of the Russian Federation. The contents of all of the metals (except zinc) in pink salmon from the geochemically extreme Kuril area were higher than that in pink salmon from the Sea of Japan. The greatest difference was recorded for lead, whose concentrations in organs and tissues (liver, gonads, and muscle) of fish from Kuril oceanic waters was one and a half order of magnitude higher than that of pink salmon from the Sea of Japan. Keywords: Pacific salmon, pink salmon, Kuril oceanic waters, heavy metals DOI: 10.1134/S1063074015060085
INTRODUCTION Pacific salmon is in great demand among pelagic objects that are the basis of fisheries in the Sea of Japan, the Sea of Okhotsk, and the Bering Sea. In this century these highly valuable commercial fish are sec ond and third after pollock and herring according to their catch volume. Of the six welldifferentiated spe cies of Pacific salmon (chum, pink, Chinook, sockeye, Coho, and masu salmon) the pink salmon Oncorhyn chus gorbuscha Walbaum, 1792 is the most numerous, smallest, and fastestgrowing species. Like other spe cies of the genus, it is monocyclic, i.e., it reproduces once in its lifetime and then dies. Three species, viz., the pink, sockeye, and chum salmon provide 90% of the catches of Pacific salmon. Pink salmon in Russian waters, as a rule, has the leading trade value [20]. Among the studied six elements (Zn, Cu, Cd, Pb, As, and Hg), copper and zinc are essential (necessary) or true bioelements, while cadmium, lead, arsenic, and mercury are nonessential, but almost ubiquitous in tissues and organs. In addition to their biological significance, these elements also differ in their geo ecological parameters. Zinc and copper, when they do not enter the environment from mining, metallurgi cal, and machinebuilding industries, are ordinary components of domestic sewage, indicating the inten sity of anthropogenic impacts on the environment. Lead, cadmium, and mercury, which began all of the
“black lists” of heavy metals in the 1960–1970s because of their toxic effects, are indicators of anthro pogenic impacts to the environment [15], or may indi cate natural biogeochemical provinces. We have repeatedly observed the latter when studying the heavymetal contents (Fe, Mn, Zn, Cu, Cd, Pb, Ni, and Cr) in marine benthic organisms, brown algae, gastropods, and bivalves that live in the Kuril Islands that foul navigational buoys along the coast of the Northwest Pacific [4, 5, 8, 16, 23]. The pacific Ring of Fire, starting from the volcanoes of Kamchatka and continuing with the Kuril volcanoes and the Japanese islands, as well as more southern island arcs of the West Pacific, is a powerful source of geochemical impacts on the marine environment. The sources of chemical elements to the environment are underwater and sur face volcanism [9] and the KurilKamchatka Trench due to upwelling outflows of nutrients [11, 13] and other elements [8] to the surface, which form a geochemical zone of impact in the Northwest Pacific. At the same time, data on heavymetal contents in actively moving organisms such as fish, in particular, the Pacific salmon, during their feeding and migration in Kuril waters are not available. The information on the traceelement composition of Asian salmon is extremely scarce. Most of it is found in the works of researchers of the TINRO Center [6, 7] to evaluate the contents of trace elements in commercial fish of the Far East seas from the MPC standpoint.
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Ka mc hat ka
Pe n.
60°
Sea of Okhotsk 55°
50° Sakhalin Isl. e ril u K
45° 135°
140°
145°
Sampling area
s nd a l Is
0 150°
155°
200 400 km 160°
165°
A schematic map of the catch area of the Pacific pink salmon in the Kuril oceanic waters.
The goal of this work was to determine the contents of heavy metals in pink salmon in Kuril oceanic waters during its anadromous migration and to compare the results with the data for this salmon species from other areas of the Pacific. MATERIALS AND METHODS Pink salmon were caught in early July in 2012 and 2013 in the Northwest Pacific in the Kuril Islands area during an expedition of the TINRO Center (see the figure). In Russian practice the catch salmon are processed almost completely with a minimum of waste. There fore, the contents of trace elements was determined in the whole fish, milled to homogeneity, as well as in fil lets (muscles), milt, and roe of salmon that are in great demand. In 2012, the sample was small and we did not differentiate individuals by sex, while attempting to obtain a first overview of the element content in the whole body. In 2013, females and males were analyzed separately. All of the elements except mercury were deter mined in homogenates of fish and their organs that were dried at 85°C after sample mineralization by con centrated nitric acid of high purity according to the State Standard, GOST 2692994 [3] with an AA 6800 Shimadzu atomicabsorption spectrophotometer. The accuracy of element measurement and possible con
tamination of assays during the analysis was controlled by four calibration solutions, including a background (zero) solution. The results were converted to wet weight. Mercury was determined in homogenates of whole fish that were frozen to –20°C after mineraliza tion of assays by nitric acid with the addition of hydro gen peroxide. Data on the mass concentration of mer cury (μg/g wet weight) was prepared by the method of stripping voltammetry with a Tomanalyt analyzer (TA4). The content of this element in mineralized (solutions) assays was determined by addition of certified mix tures with a determined mercury content. The average, standard deviation, and confidence of the differences (using the Mann–Whitney Utest) were calculated in the environment of SPSS Statistics 21 for Mac OS X. To identify differences in the heavy metal contents in the pink salmon from Kuril oceanic waters and from the Sea of Japan the previously pub lished data were used [6]. RESULTS The first notable issue is the difference in the size (mass) of pink salmon that were caught in Kuril waters in different years (Table 1). Thus, in 2013, the mass range of the fish was almost 2 times higher (1168.0– 1458.7 g) than in 2012 (718.5–862.5 g). According to Temnykh [14], on the Asian coast, among pink salmon that were traveling towards the river, individuals that
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Table 1. The weight and the concentration of trace elements in pink salmon (whole fish) caught in the Kuril oceanic waters in 2012 and 2013 Catch time, sex, sample
Concentration, µg/g wet weight
Mass, g Zn
Cu
Cd
Pb
As
Hg
July 2012, n = 4
718.5–862.5
0.53 * 0.02
0.080 0.011
0.080 0.014
0.256 0.057
0.210 0.05
0.045 0.010
July 2013, male, n = 3
1208–1458.7
2.24 0.63
0.118 0.036
0.071 0.012
0.542 0.181
0.917 0.276
0.070 0.01
July 2013, the female, n = 3
1168–1272.4
2.48 0.74
0.113 0.031
0.081 0.012
0.683 0.198
0.933 0.276
0.087 0.018
July 2013, n = 6
1168–1458.7
2.36 0.15
0.115 0.006
0.076 0.008
0.613 0.071
0.925 0.058
0.078 0.009
* The numerator is the mean value, while the denominator is the standard deviation. MPC of toxic elements (µg/g wet weight) in seafood in Russia: Pb, 1.0; As, 5.0; Cd, 0.2; Hg, 0.2 [12]; Canada: Hg, 0.5; US: Cd, 3; Pb, 1.5; As, 86.
Table 2. The concentrations of elements in the organs of pink salmon from the Kuril oceanic waters (our data) and the range of their contents in fish from the Sea of Japan, that were caught in 1992, 2001, and 2008, after [6] Concentration, µg/g wet weight
Organ, sex, sample size Zn
Cu
Cd
Pb
As
Hg
2.97 * 0.089
0.165 0.008
0.152 0.015
0.902 0.108
1.118 0.089
0.120 0.021
3.00–4.35**
0.110–0.165
0.080–0.145
0.020–0.025
0.450–0.800
0.010–0.025
Gonads, male, n = 3
2.430 0.029
0.090 0.010
0.017 0.006
0.297 0.029
0.310 0.017
0.053 0.006
Gonads, female, n = 3
2.350 0.076
0.087 0.006
0.023 0.006
0.327 0.025
0.337 0.060
0.070 0.010
0.037–0.090
0.001–0.003
0.007–0.020
0.100–0.320
0.003–0.005
0.108 0.012
0.037 0.005
0.503 0.059
0.930 0.093
0.030 0.009
0.032–0.087
0.005–0.012
0.012–0.013
0.300–1.370
0.007–0.015
Liver, n = 6
2.90–3.90 Muscle, n = 6
1.290 0.079 0.57–3.25
* The numerator is the mean value, while the denominator is the standard deviation. ** The range of element concentrations in the organs of pink salmon from the Sea of Japan.
weighed 1.2–2.3 kg prevailed. Obviously, individuals that were caught in 2013 fall into this cohort. The higher contents of almost all of the elements in the larger fish that were caught in 2013 are also noteworthy (Table 1). While the masses of individuals in 2013 were nearly two times greater, the trace element contents in them as compared to the smaller individuals of the previous year were higher by 4.4 times for arsenic, 4.1 times for zinc, 2.4 times for lead, 1.7 times for mer cury, and 1.5 times for copper. The cadmium content of the individuals did not differ in various years. According to the obtained data the zinc content was the highest, followed by arsenic and lead in whole RUSSIAN JOURNAL OF MARINE BIOLOGY
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pink salmon (Table 1) and its organs (Table 2). Cop per, cadmium, and mercury fall into the group of minor elements; their concentrations were almost one order of magnitude lower. The distribution of trace elements in organs and tissues of pink salmon in gen eral did not differ from that previously described [7]. The liver is the major traceelement depot; therefore, its concentration of all the components was the great est. The gonads of males and females (sperm and eggs) had the lowest Cu, Cd, Pb, and As contents, as the ger minal products in any organism are the most protected from toxic elements. The Hg concentration in muscle was lower than that in sperm and, in particular, in eggs, which contain large amounts of fat. The concentration No. 6
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of Zn as an element that is necessary for the growth and development of offspring was 2 times higher in the gonads of fish of the both sexes than in their muscles. The differences in the traceelement contents of pink salmon from the waters of the Sea of Japan and Kurils was significant with p ≤ 0.05 confidence (Table 1). The Zn content was higher in pink salmon from the Sea of Japan: all of the upper values of the range and lower values for the liver and gonads of fish that were caught in the Sea of Japan were significantly higher than in fish from Kuril waters. The average concentra tions of Cu and As in the muscles, gonads, and liver of pink salmon from Kuril waters approached or was equal to the upper values of the concentration range of these elements in fish from the Sea of Japan. The con tents of the remaining three elements, Cd, Hg, and Pb, were significantly higher in pink salmon from Kuril waters. Thus, the cadmium concentration was 3–8 times higher, that of mercury was 2–4 times higher, and lead was 40 times higher in the muscles of these fish; the lead content was 15–43 times higher in the gonads and 36–45 times in the liver. DISCUSSION We know that size can considerably vary in some local clusters of pink salmon. It depends not only on the specific conditions of growth that are defined by feed and hydrological parameters. The sizes of the odd and even generations significantly differ. In addition, the small size and low maturity of fish may be due to later spawning of some stocks [18]. Thus, in 2008 and 2010, abundant pink salmon, attracted to the South Kuril region, had a low mass (in June it was less than 1 kg) [20]. The salmon that were caught in the same area in 2012 and 2013 once again displayed a signifi cant difference between the actual sizes and weights of the fish in stocks of different years and generations. It has long been known that higher contents of elements are found in larger salmon that spend a longer period of time in the sea. Thus, Kelly et al. [24] observed a sig nificant correlation between the concentration of total mercury and the size of wild Chinook salmon. The Hg content in fish fillets varied from 0.01 μg/g in 2 kg individuals to 0.1 μg/g in 8 kg fish. The authors also stressed that the level of the concentration of elements in wild salmon may reflect geographical variation of species, especially their biology and ecology. The wild Chinook salmon is a longlived large oily fish with a wide spectrum of feeding (from a variety of crusta ceans to relatively large fish). Its mercury concentra tion was one order of magnitude higher than in the pink salmon, which is smaller and has a shorter lifespan and feeds on plankton and small nekton. However, for the pink salmon, which feeds in the sea for only 1 year, the relationship between mass and the concentrations of elements is less direct. Accord ing to our data, the concentrations of elements in pink salmon of masses that were caught in 2013 practically
did not differ. Only slightly higher contents of Zn, Pb, and Hg was observed in females. Despite the variation in the fish size, the contents of toxic elements in pink salmon that were caught in the ocean were below the humanhealth consumption guidelines set out for sea food in the Russian MPC and lower than the standards that have been adopted in Canada and the United States. Easton et al. [22] provided data on the mercury content in samples of wild and reared salmon, as well as in the commercial production of salmon from Can ada (British Columbia) and Alaska (United States). The content of this element in the wild and caged salmon var ied within 0.025–0.072 and 0.017–0.042 mg/kg of wet weight, respectively. In the pink salmon that we stud ied, the mercury concentration was slightly higher, 0.060–0.090 μg/g. However, it is necessary to note that foreign authors, based on commercial interests, provide data on trace element contents in fish fillets. We analyzed entire fish. For correct comparison of our results with the data of foreign researchers, we also deter mined the element concentrations in the muscles of Pacific salmon. The average mercury content in the mus cle of pink salmon (0.030 ± 0.007 μg/g) was lower than in the wild salmon from Canada and Alaska (Table 2). We know that Asian pink salmon comprises many salmon stocks that spawn in the rivers of the Far East ern seas. In wintering migration the redistribution of pink salmon from the Sea of Okhotsk to the southeast into the Subarctic frontal zone occurs from the south ern and central parts of the Kuril Ridge [19, 20]. Indi viduals of different stocks of pink salmon, viz., Pri morye, Amur, West Sakhalin, East Sakhalin, and North Japan, winter in the Sea of Japan [1, 2], while the Okhotsk Sea pink salmon and its populations from the Amur estuary migrate into the Sea of Japan and back via the La Perouse Strait [10]. Thus, in traveling to feed and then returning to spawn not all Asian stocks of pink salmon pass through the Kuril region, in particular, the Japan Sea pink salmon pass beyond it. The pink salmon is absent along the mainland coast of the Sea of Japan in the area of the cold Primorye Current in the depth of winter. The Primorye stock that prevails in this season in the western part of the Sea of Japan shifts to the south up to the shelf in front of the Korea Strait (about 36° N) and is evenly distrib uted in the waters of the southern trough. In April and May, pink salmon begin to migrate at a broad front at the western side of the sea to the northeast. From the end of April until approximately June 20, the average size of pink salmon in the open waters of Primorye increased to 50.3 cm (males up to 52.1 cm and up to 2170 g in weight and females up to 49.3 cm with a weight up to 1550 g). In terms of fishing (June–July), the Primorye, Amur, and West Sakhalin stocks of Asian pink salmon are the earliest [20]. Therefore, wintering migration routes of pink salmon signifi cantly differ in the Far Eastern seas. While the
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Okhotsk Sea stocks as a rule enter the ocean through the Kuril straits, winter in the western part of the Sub arctic front, and then return in the spring and summer, the Japan Sea stocks spend the winter in the Sea of Japan, do not pass through the Kuril straits and do not feed in the Kuril–Kamchatka waters. The biogeochemical province, which is the Kuril– Kamchatka Region with its surface and underwater volcanism, as well as the addition of trace elements due to the upwelling of the Kuril–Kamchatka Trench into surface Kuril water, causes an excess of trace ele ments in the environment and in animals that living here permanently or fatten here [25]. High contents of cadmium, mercury, and especially lead in pink salmon from the Kuril oceanic waters compared to that in the Sea of Japan are evidence for the influence of the nat ural biogeochemical province on the Okhotsk salmon stocks. However, the prevalence of zinc, which is a marker of human impacts on the environment, in pink salmon from the Sea of Japan suggests a marked influ ence of human activities in the water area. In the transition from river water through the mar ginal seas to the oceans, the terrigenous suspension deposits and ocean water is enriched with dissolved forms of elements. Almost all of the elements in the pelagic zone of oceans are in the dissolved form at 80– 90% or higher. Lead and many trace elements in the open ocean are found in trace amounts, from 5 to 150 pmol/kg [21]. However, unlike the other ele ments, lead has a high sorption capacity, i.e., an affin ity to surfaces such as mineral and organic particles [17]. In a rich mineral and organic suspension zone saturated with plankton organisms (from nano and microplankton to macroplankton) and dead organ isms, there are a great number of fine particles that can adsorb lead. The Kuril waters of the Pacific are well known as one of the most productive areas of the World Ocean. The productivity of these waters that are within a spe cific biogeochemical province is second only to the main fishing area of the Far Eastern seas, viz., the Sea of Okhotsk, and it has remained high for many years. Without doubt, with the abundance of macroplank ton, which Shuntov and Temnykh [20] noted, micro and nanoplankton and pellets (different small and fine particles) are even more abundant and can vary by orders of magnitude. Therefore the lead that is adsorbed on the nutrient suspension is probably easily fixed by organisms of higher trophic levels, initially by zooplankton, then by its consumer nekton, including the massive fish of the upper pelagic zone, which include the pink salmon. Thus, the pink salmon that are caught in the Kuril waters meet the sanitary regulations [12] for seafood according to the contents of the normalized toxic ele ments Cd, Pb, As, and Hg. The differences in levels of elements that we revealed in pink salmon from the Sea of Okhotsk and the Sea of Japan, which indicate the RUSSIAN JOURNAL OF MARINE BIOLOGY
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relevance of the environmental geochemical condi tions during the formation of the traceelement com positions of organisms, are of great scientific and prac tical interest. While the increase in the concentration of Zn in pink salmon from the Sea of Japan is appar ently due to human influence on the closed marginal sea, the higher contents of Cd, Hg, and, in particular, Pb in pink salmon from the Kuril oceanic waters occur due to the environment of the biogeochemical prov ince that formed under the effects of natural factors, modern volcanism, and upwelling. ACKNOWLEDGMENTS The authors are highly grateful to Dr. V.P. Shuntov for scientific advice. The work was supported by the Russian Science Foundation, project no. 1450 00034. REFERENCES 1. Atlas rasprostraneniya v more razlichnykh stad tikhookeanskikh lososei v period vesenneletnego nagula i prednerestovyh migracii (Atlas of Sea Distribution of Various Stocks of Pacific Salmon during the Spring and Summer Feeding and Prespawning Migrations), Mos cow: Vseross., NauchnoIssled. Inst. Rybn. Khoz. Okeanogr., 2002. 2. Birman, I.B., Morskoi period zhizni i voprosy dinamiki stad tikhookeanskikh lososei (The Sea Life Period and Problem of the Dynamics of Stocks of Pacific Salmon.), Moscow: Agropromizdat, 1986. 3. GOST (State Standard) 26929_94: Raw materials and food. Sample preparation. Mineralization for determina tion of toxic elements in food, Moscow: Standartinform, 2010. 4. Kavun, V.Ya. and Khristoforova, N.K., The role of modern volcanism and upwellings in development of the impact zones of heavy metals in the coastal waters of the Kuril Islands, in Melkovodnye gazogidrotermy i ekosistema bukhty Kraternoi (vulkan Ushishir, Kuril’skie ostrova (Shallow Water Vents and the Ecosystem of the Craternaya Bay (Ushishir Volcano, Kuril Islands), Vladivostok: Dal’nevost. Otd., Ross. Akad. Nauk, 1991, book 1, part 2, pp. 114–120. 5. Kavun, V.Ya., Khristoforova, N.K., and Shulkin, V.M., Trace element composition in the tissues of blue mus sels from the coastal waters of Kamchatka and northern Kuril Islands, Ekologiya, 1989, no. 3, pp. 53–59. 6. Kovekovdova, L.T., Trace elements in marine fishery objects of the Far East of Russia, Extended Abstract of Doctoral (Biol.) Dissertation, Vladivostok: TINRO Center,, 2011. 7. Kovekovdova, L.T., Simokon’, M.V., and Kiku, D.P., Trace element composition of commercial fish of Far East seas, Probl. Reg. Ekol., 2013, no. 2, pp. 72–75. 8. Malinovskaya, T.M. and Khristoforova, N.K., Charac terization of coastal waters of the south Kuril Islands by the trace element content of indicatory organisms, Russ. J. Mar. Biol., 1997, vol. 23, no. 4, pp. 212–218. No. 6
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