ISSN 00124966, Doklady Biological Sciences, 2014, Vol. 456, pp. 188–190. © Pleiades Publishing, Ltd., 2014. Original Russian Text © O.N. Lukyanova, V.Yu. Tsygankov, M.D. Boyarova, N.K. Khristoforova, 2014, published in Doklady Akademii Nauk, 2014, Vol. 456, No. 3, pp. 363–365.
GENERAL BIOLOGY
Pesticide Biotransport by Pacific Salmon in the Northwestern Pacific Ocean O. N. Lukyanovaa, b, V. Yu. Tsygankovb, M. D. Boyarovab, and N. K. Khristoforovab Presented by Academician A.V. Andrianov November 25, 2013 Received January 23, 2014
DOI: 10.1134/S0012496614030089
Persistent organic pollutants (POPs) are toxic xenobiotics that circulate in the biosphere over decades. At present, the global background of POPs has been formed on the planet. The pollutants are transported by wind from the regions of their use (tropical and subtropical latitudes) over long distances to middle and polar latitudes. During the last third of the 20th century, hexachlorocyclohexane (HCH) and dichlorodiphenyltrichloroethane (DDT) have been the most actively used among organochlorine pesti cides OCPs. Along with the atmospheric transport, POPs are dispersed in the world ocean by marine organisms that migrate over long distances. Primarily, the biotransport of POPs is performed by salmon, the amount of which has increased recently and is now 1.0–1.5 million tons in the subarctic region of the Pacific Ocean [1]. Along with biogenic elements, salmon, which die after spawning in rivers and lakes, contaminate their habitats with pollutants accumu lated during their feeding and growing period in the ocean; the amount of pollutants may be high. The aim of our study was to estimate the role of Pacific salmon in global transport of OCPs during their biotransport from the open ocean to the Russian coast of the Far Eastern seas. Salmon (6 specimens of pink salmon Oncorhynchus gorbusha and 6 specimens of chum salmon O. keta) were caught in marine cruise of the Pacific Fisheries Research Center (Vladivostok, Russia) in the region of the Kuril Islands in the Pacific Ocean in June–July 2013. Frozen samples (–20°C) were transported to lab oratory. Before the analysis, whole specimens of pink salmon and chum salmon were homogenized. After extraction into organic solvents, the concentrations of α, β, and γhexachlorocyclohexane (HCH), DDT,
dichlorodiphenyldichloromethylmethane (DDD) and dichlorodiphenyldichloroethylene (DDE) were determined by the method of gas chromatography [2]. Chlororganic pesticides were detected in all samples of Pacific salmon under study. The total concentration of OCPs as the sum HCH + DDT in chum salmon was significantly higher than in pink salmon (Table 1), which may be the result of different fat content in fish and duration of their stay in sea. After downstream migration of juveniles to the sea, pink salmon returns to spawn in freshwaters in a year, whereas chum salmon may spend two to five years in the sea and accumulate different pollutants in organs. The total concentration of HCH isomers was higher than DDT in all samples. It is known that some pesticides evaporate in tropical and subtropical lati tudes, are transported by wind and deposited at higher latitudes. Because of the high volatility of HCH, its concentrations in salt water of the Pacific Ocean increases when moving from subtropics northwards. DDT is less volatile, and its high concentrations are detected in the sites of its use [3, 4]. In salmon, α and β isomers prevail over HCH isomers and DDE prevail over DDT metabolites, which testifies to decay of ini tial compounds, i.e., of “prolonged” contamination and circulation of pesticides in the environment. The number of salmon migrating to the Russian coast varies from year to year, but the structure of Table 1. Average values of the total concentration (ng/g wet weight) of HCH isomers (αHCH + βHCH + γHCH) and DDT and metabolites (DDT + DDD + DDE) in Pa cific salmon bodies; M ± m, n = 6 Species
a
Pacific Fisheries Research Center (TINROCenter), Vladivostok, 690950 Russia b Far Eastern Federal University, Vladivostok, 690091 Russia email: [email protected]; olga.lukyanova@tinrocenter.ru
HCH
58.7 ± 12.4 Pink salmon O. gorbusha Chum salmon 167.5 ± 51.1 O. keta 188
DDT + DDD + DDE
COPs
10.2 ± 2.1
68.85 ± 14.55
15.0 ± 11.8
182.5 ± 60.2
PESTICIDE BIOTRANSPORT BY PACIFIC SALMON
189
Table 2. Escapement of Pacific salmon (thousand specimens) to spawning areas [5] and the amount of OCPs (g) transport ed by fish to the Pacific coast of Russia in 2009 Region
Pink salmon
Amount of OCPs
Chum salmon
Amount of COPs
Total of OCPs
Western Bering Sea Eastern Kamchatka Western Kamchatka Continental coast of the Sea of Okhotsk Southern Kuril Islands Eastern Island Amur River basin Total
170 94497 3 67
15.2 8500 0.2 6.0
1943 2954 716 8828
120 1900 457 5600
1215 10400 457 5606
7 18479 2927 116147
0.6 1600 262 10384
73 513 20079 26278
46 327 12800 21250
47 1927 13062 31634
migratory fish remains the same: pink salmon consti tute 60–65%, chum salmon constitute 20–25%, and redfish constitute 10–12%. The proportion of silver salmon and Chinook salmon is small. Chum salmon and pink salmon are the main migratory fish in the eastern part of Kamchatka, eastern Island, the conti nental coast of the Sea of Okhotsk, and in the Amur River basin. The maximum catches of salmon (542 000 t) were recorded in 2009. The number of fish that performed spawning migrations to some regions of the Far East in 2009 [5] is shown in Table 2. The average mass of one specimen of pink salmon is 1.3 kg, and the average mass of one specimen of spawning chum salmon is 3.5 kg. Our calculations show that one specimen of pink salmon contains as much as 90 µg of pesticides, and one specimen of chum salmon, as much as 640 µg of pesticides.
caught fish. In recent years, the catches of salmon in Russian waters are high: 542 000 t in 2009, 325 000 t in 2010, 504 000 t in 2011, 438 000 t in 2012, and about 400 000 t in 2013. The amount of pesticides in salmon that are caught during a year is from 40 to 67 kg. Finally, the pesticides are spread on land. According to some evaluations, the transfer of pollutants to coastal ecosystems by salmon two to six times exceeds the atmospheric transfer [8, 9].
The amount of OCPs transported by these salmon species to eastern Kamchatka is 10.4 kg; to the Amur River basin, more than 13 kg; to the continental coast of the Sea of Okhotsk, 5.6 kg; and the total amount of OCPs transported to the Pacific coast of Russia is more than 30 kg. The amount of pesticides varies from year to year, but the total concentration of pesticides in a particular habitat increases. These compounds are rather persistent and can circulate in the ecosystem for a long time. They may enter the food web and affect the terrestrial organisms of a higher trophic level [6, 7], primarily, predators. According to expert evaluation, the catches of salmon by brown bear and sea mammals amount from 50 000 to 100 000 t, which is rather much compared to commercial catches in the past years (300 000–540 000 t) [1]. It is assumed that bears con sume from 10 000 to 30 000 t of salmon; i.e., they transfer from 1.5 to 4 kg of pesticides to the Pacific coast of Russia.
In the past years, the pollution of coastal waters with pesticides has decreased as a result of measures on prohibition of their use. However, in the open ocean, water pollution by contaminants is still rather high. The ocean is a reservoir that receives persistent toxi cants, and bioaccumulation of pesticides in the ocean continues in food chains. Salmon provide biotransport of POPs in the biosphere and their global transport from sea to land.
The biotransport of OCPs to spawning grounds depends on the number of migrating spawners, whereas the input of toxicants to the human body with consumed salmon is determined by the amount of
1. Shuntov, V.P. and Temnykh, O.S., Tikhookeanskie lososi v morskikh i okeanicheskikh ekosistemakh (Pacific Salmon in Marine and Ocean Ecosystems), Vladivos tok: TINROTsentr, 2011, vol. 2.
DOKLADY BIOLOGICAL SCIENCES
Vol. 456
2014
Now, salmon as a mass fish in the upper layer of epipelagial of the northern Pacific Ocean dominate at depths from 0 to 50 m [1]. Precisely in this layer, atmo spheric precipitations, pollutants deposited on sus pended particles, and toxic products of decomposed plastic may concentrate and be accumulated by salmon [10].
ACKNOWLEDGMENTS This study was partly supported by the program “Scientific Foundation” of the Far Eastern Federal University, project no. 12041300033/13. REFERENCES
190
LUKYANOVA et al.
2. Klisenko, M.A., Mel’tser, F.R., Novikova, K.F., et al., Assays for Microscopic Amounts of Pesticides in Foods, Forage, and Environment, Moscow: Kolos, 1983. 3. Wania, F., Mackay, D., Environ. Sci. Technol., 1996, vol. 30, pp. 390A–396A. 4. Tanabe, S., Dev. Environ. Sci., 2007, vol. 7, pp. 773– 817. 5. www.npafc.org. 6. O’Toole, S., Metcalfe, C., Craine, I., and Gross, M., Environm. Pollut., 2006, vol. 140, pp. 102–113.
7. Veldhoen, N., Ikonomou, M., Dubetz, C., et al., Aquat. Toxicol., 2010, vol. 97, pp. 212–225. 8. Ewald, G., Larsson, P., Linge, H., et al., Arctic, 1998, vol. 51, no. 1, pp. 40–47. 9. Krummel, E.M., Macdonald, R.W., Kimpe, L.E., et al., Nature, 2003, vol. 425, pp. 255–256. 10. Choy, C.A. and Drazen, J.C., Mar. Ecol.: Proc. Ser., 2013, vol. 485, pp. 155–163.
Translated by N. Ruban
DOKLADY BIOLOGICAL SCIENCES
Vol. 456
2014
GENERAL BIOLOGY
Pesticide Biotransport by Pacific Salmon in the Northwestern Pacific Ocean O. N. Lukyanovaa, b, V. Yu. Tsygankovb, M. D. Boyarovab, and N. K. Khristoforovab Presented by Academician A.V. Andrianov November 25, 2013 Received January 23, 2014
DOI: 10.1134/S0012496614030089
Persistent organic pollutants (POPs) are toxic xenobiotics that circulate in the biosphere over decades. At present, the global background of POPs has been formed on the planet. The pollutants are transported by wind from the regions of their use (tropical and subtropical latitudes) over long distances to middle and polar latitudes. During the last third of the 20th century, hexachlorocyclohexane (HCH) and dichlorodiphenyltrichloroethane (DDT) have been the most actively used among organochlorine pesti cides OCPs. Along with the atmospheric transport, POPs are dispersed in the world ocean by marine organisms that migrate over long distances. Primarily, the biotransport of POPs is performed by salmon, the amount of which has increased recently and is now 1.0–1.5 million tons in the subarctic region of the Pacific Ocean [1]. Along with biogenic elements, salmon, which die after spawning in rivers and lakes, contaminate their habitats with pollutants accumu lated during their feeding and growing period in the ocean; the amount of pollutants may be high. The aim of our study was to estimate the role of Pacific salmon in global transport of OCPs during their biotransport from the open ocean to the Russian coast of the Far Eastern seas. Salmon (6 specimens of pink salmon Oncorhynchus gorbusha and 6 specimens of chum salmon O. keta) were caught in marine cruise of the Pacific Fisheries Research Center (Vladivostok, Russia) in the region of the Kuril Islands in the Pacific Ocean in June–July 2013. Frozen samples (–20°C) were transported to lab oratory. Before the analysis, whole specimens of pink salmon and chum salmon were homogenized. After extraction into organic solvents, the concentrations of α, β, and γhexachlorocyclohexane (HCH), DDT,
dichlorodiphenyldichloromethylmethane (DDD) and dichlorodiphenyldichloroethylene (DDE) were determined by the method of gas chromatography [2]. Chlororganic pesticides were detected in all samples of Pacific salmon under study. The total concentration of OCPs as the sum HCH + DDT in chum salmon was significantly higher than in pink salmon (Table 1), which may be the result of different fat content in fish and duration of their stay in sea. After downstream migration of juveniles to the sea, pink salmon returns to spawn in freshwaters in a year, whereas chum salmon may spend two to five years in the sea and accumulate different pollutants in organs. The total concentration of HCH isomers was higher than DDT in all samples. It is known that some pesticides evaporate in tropical and subtropical lati tudes, are transported by wind and deposited at higher latitudes. Because of the high volatility of HCH, its concentrations in salt water of the Pacific Ocean increases when moving from subtropics northwards. DDT is less volatile, and its high concentrations are detected in the sites of its use [3, 4]. In salmon, α and β isomers prevail over HCH isomers and DDE prevail over DDT metabolites, which testifies to decay of ini tial compounds, i.e., of “prolonged” contamination and circulation of pesticides in the environment. The number of salmon migrating to the Russian coast varies from year to year, but the structure of Table 1. Average values of the total concentration (ng/g wet weight) of HCH isomers (αHCH + βHCH + γHCH) and DDT and metabolites (DDT + DDD + DDE) in Pa cific salmon bodies; M ± m, n = 6 Species
a
Pacific Fisheries Research Center (TINROCenter), Vladivostok, 690950 Russia b Far Eastern Federal University, Vladivostok, 690091 Russia email: [email protected]; olga.lukyanova@tinrocenter.ru
HCH
58.7 ± 12.4 Pink salmon O. gorbusha Chum salmon 167.5 ± 51.1 O. keta 188
DDT + DDD + DDE
COPs
10.2 ± 2.1
68.85 ± 14.55
15.0 ± 11.8
182.5 ± 60.2
PESTICIDE BIOTRANSPORT BY PACIFIC SALMON
189
Table 2. Escapement of Pacific salmon (thousand specimens) to spawning areas [5] and the amount of OCPs (g) transport ed by fish to the Pacific coast of Russia in 2009 Region
Pink salmon
Amount of OCPs
Chum salmon
Amount of COPs
Total of OCPs
Western Bering Sea Eastern Kamchatka Western Kamchatka Continental coast of the Sea of Okhotsk Southern Kuril Islands Eastern Island Amur River basin Total
170 94497 3 67
15.2 8500 0.2 6.0
1943 2954 716 8828
120 1900 457 5600
1215 10400 457 5606
7 18479 2927 116147
0.6 1600 262 10384
73 513 20079 26278
46 327 12800 21250
47 1927 13062 31634
migratory fish remains the same: pink salmon consti tute 60–65%, chum salmon constitute 20–25%, and redfish constitute 10–12%. The proportion of silver salmon and Chinook salmon is small. Chum salmon and pink salmon are the main migratory fish in the eastern part of Kamchatka, eastern Island, the conti nental coast of the Sea of Okhotsk, and in the Amur River basin. The maximum catches of salmon (542 000 t) were recorded in 2009. The number of fish that performed spawning migrations to some regions of the Far East in 2009 [5] is shown in Table 2. The average mass of one specimen of pink salmon is 1.3 kg, and the average mass of one specimen of spawning chum salmon is 3.5 kg. Our calculations show that one specimen of pink salmon contains as much as 90 µg of pesticides, and one specimen of chum salmon, as much as 640 µg of pesticides.
caught fish. In recent years, the catches of salmon in Russian waters are high: 542 000 t in 2009, 325 000 t in 2010, 504 000 t in 2011, 438 000 t in 2012, and about 400 000 t in 2013. The amount of pesticides in salmon that are caught during a year is from 40 to 67 kg. Finally, the pesticides are spread on land. According to some evaluations, the transfer of pollutants to coastal ecosystems by salmon two to six times exceeds the atmospheric transfer [8, 9].
The amount of OCPs transported by these salmon species to eastern Kamchatka is 10.4 kg; to the Amur River basin, more than 13 kg; to the continental coast of the Sea of Okhotsk, 5.6 kg; and the total amount of OCPs transported to the Pacific coast of Russia is more than 30 kg. The amount of pesticides varies from year to year, but the total concentration of pesticides in a particular habitat increases. These compounds are rather persistent and can circulate in the ecosystem for a long time. They may enter the food web and affect the terrestrial organisms of a higher trophic level [6, 7], primarily, predators. According to expert evaluation, the catches of salmon by brown bear and sea mammals amount from 50 000 to 100 000 t, which is rather much compared to commercial catches in the past years (300 000–540 000 t) [1]. It is assumed that bears con sume from 10 000 to 30 000 t of salmon; i.e., they transfer from 1.5 to 4 kg of pesticides to the Pacific coast of Russia.
In the past years, the pollution of coastal waters with pesticides has decreased as a result of measures on prohibition of their use. However, in the open ocean, water pollution by contaminants is still rather high. The ocean is a reservoir that receives persistent toxi cants, and bioaccumulation of pesticides in the ocean continues in food chains. Salmon provide biotransport of POPs in the biosphere and their global transport from sea to land.
The biotransport of OCPs to spawning grounds depends on the number of migrating spawners, whereas the input of toxicants to the human body with consumed salmon is determined by the amount of
1. Shuntov, V.P. and Temnykh, O.S., Tikhookeanskie lososi v morskikh i okeanicheskikh ekosistemakh (Pacific Salmon in Marine and Ocean Ecosystems), Vladivos tok: TINROTsentr, 2011, vol. 2.
DOKLADY BIOLOGICAL SCIENCES
Vol. 456
2014
Now, salmon as a mass fish in the upper layer of epipelagial of the northern Pacific Ocean dominate at depths from 0 to 50 m [1]. Precisely in this layer, atmo spheric precipitations, pollutants deposited on sus pended particles, and toxic products of decomposed plastic may concentrate and be accumulated by salmon [10].
ACKNOWLEDGMENTS This study was partly supported by the program “Scientific Foundation” of the Far Eastern Federal University, project no. 12041300033/13. REFERENCES
190
LUKYANOVA et al.
2. Klisenko, M.A., Mel’tser, F.R., Novikova, K.F., et al., Assays for Microscopic Amounts of Pesticides in Foods, Forage, and Environment, Moscow: Kolos, 1983. 3. Wania, F., Mackay, D., Environ. Sci. Technol., 1996, vol. 30, pp. 390A–396A. 4. Tanabe, S., Dev. Environ. Sci., 2007, vol. 7, pp. 773– 817. 5. www.npafc.org. 6. O’Toole, S., Metcalfe, C., Craine, I., and Gross, M., Environm. Pollut., 2006, vol. 140, pp. 102–113.
7. Veldhoen, N., Ikonomou, M., Dubetz, C., et al., Aquat. Toxicol., 2010, vol. 97, pp. 212–225. 8. Ewald, G., Larsson, P., Linge, H., et al., Arctic, 1998, vol. 51, no. 1, pp. 40–47. 9. Krummel, E.M., Macdonald, R.W., Kimpe, L.E., et al., Nature, 2003, vol. 425, pp. 255–256. 10. Choy, C.A. and Drazen, J.C., Mar. Ecol.: Proc. Ser., 2013, vol. 485, pp. 155–163.
Translated by N. Ruban
DOKLADY BIOLOGICAL SCIENCES
Vol. 456
2014
