Organochlorine pesticides are persistent toxic substances of anthropogenic origin that affect biota. Hexachlorocyclohexane (HCH) isomers (α-, β-, and γ-), DDT and its metabolites (DDD and DDE) were detected in five individuals of fulmars Fulmarus glacialis Linnaeus, 1761 from the coast of Eastern Kamchatka and the Kuril Islands. The average amount of HCH isomers in the organs of fulmars ranged from 608 ± 177 ng/g lipids in the total homogenate of the organs to 2093 ± 264 ng/g lipids in the feathers with skin. The average range of the amounts of DDT and its metabolites was from 3606 ± 333 ng/g lipids in the feathers with skin to 4076 ± 1624 ng/g lipids in the feathers. The results are discussed.


HCH ; DDT ; Eastern Kamchatka ; Kuril Islands ; Fulmar Fulmarus glacialis


The 1960s and 1970s were marked by the mass death of wild bird populations in various parts of the world. The reason for this phenomenon turned out to be the use of organochlorine pesticides (OCPs). As a result of endrin intoxication, partridges and pheasants died; dieldrin killed bald eagles and geese. DDT (dichlorodiphenyltrichloroethane) caused the death of cormorants, pelicans, and seagulls; lindane caused the death of starlings (Tanabe et al ., 1984  ;  Rovinskii et al ., 1990 ).

After the ban on the use of pesticides was imposed, bird deaths decreased significantly, but deaths caused by OCPs poisoning continued. It is important that in areas contaminated by OCPs, birds are particularly sensitive to other groups of chemical toxicants. Thus, the presence of DDE (dichlorodiphenyldichloroethylene) disguises the effect of the negative effects of mercury on reproduction of birds (Rovinskii et al ., 1990  ;  Jorundsdottir et al ., 2010 ).

A number of experiments managed to identify critical concentrations of OCPs in the brain of birds. Lethal doses of pesticides are specific for each species and fall within the range from 4 (for the Japanese quail and yellow cres) to 65 mg/kg (for sparrows) (Tanabe, 2007 ).

For the first time, a correlation between eggshell thinning and the deterioration of breeding populations of peregrine falcons and sparrow hawk in the field of persistent organochlorine insecticides was revealed in the UK.

Compared with the eggshell thickness in 1940, by the end of 1960s, the eggshell thickness of nine out of the 17 studied species was found to decrease by 5 to 19%. Studies in the U.S. and Canada also revealed a certain degree of thinning of the shell; the shell thickness and the weight of many bird species decreased by 20% (Kunisue et al ., 2003  ; Tanabe and Subramanian, 2006  ;  Tanabe, 2007 ).

Birds are useful bioindicators for organochlorine pollutants monitoring because they often are at the apex of the food pyramid. Non-migrating birds can reflect the background contamination of their habitat places. If there are no local pollution sources, birds reflect the global pollution resulting from the trans-boundary transfer of pollutants (Kunisue et al ., 2003  ;  Knudsen et al ., 2007 ).

The purpose of this study is to determine the concentration of HCH isomers (hexachlorocyclohexane) (α-, β-, γ-HCH), DDT and its metabolites (DDD (dichlorodiphenyldichloroethane), DDE (dichlorodiphenyldichloroethylene)) in fulmars Fulmarus glacialis Linnaeus, 1761, collected in the coastal waters in the Sea of Okhotsk, West Kamchatka and the Kuril Islands.

Materials and Methods

Five studied samples of fulmars F. glacialis were collected from the coast of western Kamchatka and the Kuril Islands in June and October 2012 during the TINRO centre expeditions ( Fig. 1 ).

Map of the work area: A — fulmar sampling locations.

Fig. 1.

Map of the work area: A — fulmar sampling locations.

Various organs were scrutinised, depending on the size of birds: feather, feather with skin, and whole carcass (internal organs with feathers). Lipids were extracted from homogenised organs by means of n -hexane extraction, with subsequent disintegration of the fat components by concentrated sulphuric acid ( Klisenko et al., 1983 ).

Detection of the mass content of organochlorine pesticides in the biomaterial was performed on a gas chromatograph Shimadzu GC- 16A with an ECD electron capture detector (capillary column Shimadzu HiCap CBP5). Column temperature: 210 °C, injector: − 250 °C, and detector: − 280 °C. Carrier gas: argon, inlet pressure: 2 kg/cm2 , 1:60 flow divider, and flow rate of carrier gas through the column: 0.5 ml/min. To identify individual substances, standard working solutions of OCPs in the concentration range of 1–100 mg/ml were applied.

Results and Discussion

Pesticides were detected in all of the studied birds samples (Table 1 ). The average amount of HCH isomers in the bodies of fulmars ranged from 608 ± 177 ng/g lipids in the general organ homogenates to 2093 ± 264 ng/g lipids in feathers with skin. α-HCH was found in all the samples of feathers with a maximum value of 1450 ± 186 ng/g lipids. β-Isomer was not detected. γ-HCH was present in samples of feathers and feathers with skin, corresponding to 371 ± 87 and 305 ± 55 ng/g lipids, respectively.

Table 1. Average values of isomers of HCH, DDT and its metabolites in the organs of fulmars Fulmarus glacialis (M + m, n = 5).
Samples Detected OCP, ng/g lipids
HCH isomers DDT and metabolites ΣOCP
Feathers 1450 ± 186 - 371 ± 87 1821 ± 273 1471 ± 502 - 2605 ± 1122 4076 ± 1624 5898 ± 1897
Feathers and skin 1788 ± 209 - 305 ± 55 2093 ± 264 - - 3606 ± 333 3606 ± 333 5699 ± 597
Organ homogenates 608 ± 177 - 0 608 ± 177 - - 4005 ± 406 4005 ± 406 4613 ± 583

“-” denotes not found.

The range of values of the concentration of DDT and its metabolites sum varied from 3606 ± 333 ng/g lipids in feathers with the skin to 4076 ± 1624 ng/g lipids in feathers. DDT was detected in all of the feather samples, and its average value was 1471 ± 502 ng/g lipids. DDD metabolite was not detected at all. DDE was present in all of the samples, reaching a maximum average value of 4005 ± 406 ng/g lipids in organ homogenates.

The HCH isomers ratio is used to evaluate the prescription of pesticides input in the ecosystem. A value of the coefficient α/γ-HCH above 1 denotes the longstanding presence of OCPs in the environment; a value below 1 denotes the predominance of γ-isomer, which is typical of “fresh” input because HCH comes into the environment mainly in the form of γ-HCH (lindane). The DDTs residence time in the objects is considered by ratio of the DDT concentrations and its degradation product of DDE. High values of the coefficient of DDT/DDE (above 1) indicate the recent DDTs introduction in the environment, while low values indicate the long residence time of DDT in the system and the gradual transformation into DDE.

Detection of γ-HCH and DDT on the feathers of birds enables estimation of the presence of “fresh” contamination. However, there are no local pollution sources of marine environment and the air in the Sea of Okhotsk areas; as a result, the atmospheric transport from areas of application, such as Southeast Asia, appears as the most probable source.

Based on the physicochemical properties of these compounds, it can be concluded that the high values of the coefficient octanol/water distribution Cow (material with a higher Cow exhibits higher hydrophobic properties and binds easier with organic substances, e.g., lipids) and low water solubility of compounds of DDTs and HCH isomers contribute to the fact that in the environment, these compounds bind to soil particles, sediments and suspended particles in water and air as well as fat covering feathers (Rovinskii et al ., 1990  ; Quemerais et al ., 1994  ; Wu et al ., 1997  ;  Zeng et al ., 1999 ).

Another physico-chemical parameter, Henrys constant, is of great importance for the description of the distribution processes in the water–air system. HCHs and DDTs have relatively high values of Henrys constant, indicating a significant volatility of these compounds and the reasons they are detected on the feathers of birds (Rovinskii et al ., 1990  ;  Quemerais et al ., 1994 ).

The predominance of DDT over γ-HCH on the feathers of fulmars can be explained by the pressure ratings of the saturated vapours — the maximum vapour pressure of the compound at its transition to the gas phase from the solid (sublimation) or liquid (water vapour) state at a certain temperature. Canadian and Norwegian research reports (Wania and Mackay, 1996 ) based on the vapour pressure subdivided the compounds into groups according to their behaviour in the atmosphere (redistribution between the gas and aerosolised phases in the atmosphere). According to these reports, the compounds with vapour pressure within the range 10− 2 –10− 4  Pa at 25 °C, i.e., HCHs, can be present in the atmosphere in both gas and aerosolised phases. Compounds with a vapour pressure lower than 10− 4  Pa at 25 °C (DDT compound) may be in the atmosphere only in aerosolised phase (Rovinskii et al ., 1990  ;  Wania and Mackay, 1996 ). Therefore, these substances can be transported in the atmosphere over long distances, including arctic regions, and deposited onto the feathers of the birds.

Birds are good bioindicators of the global pesticide background, even with habitation in places where there are no local contamination sources of organochlorine pollutants. The feathers of fulmar and other birds from the northern regions of the World Ocean were taken for comparison (Fig. 2 ).

Contents of HCH isomers (A) and DDT and its metabolites (B) in northern seabird ...

Fig. 2.

Contents of HCH isomers (A) and DDT and its metabolites (B) in northern seabird feathers from different regions of the World Ocean. 1 — little auk Alle alle (Baffin Bay) ( Buckman et al., 2004 ); 2 — common guillemot Cepphus grylle (Baffin Bay) ( Buckman et al., 2004 ); 3 — thick-billed Murre Uria lomvia (Baffin Bay) ( Buckman et al., 2004 ); 4 — kittiwake Rissa tridactyla (Baffin Bay) ( Buckman et al., 2004 ); 5 — fulmar Fulmarus glacialis (Baffin Bay) ( Buckman et al., 2004 ); 6 — Glaucous Gull Larus hyperboreus (Baffin Bay) ( Buckman et al., 2004 ); 7 — ivory gull Pagophila eburnea (Baffin Bay) ( Buckman et al., 2004 ); 8 — Glaucous Gull Larus hyperboreus (Bear Island, Barents Sea) ( Knudsen et al., 2007 ); 9 — fulmar Fulmarus glacialis (Sea of Okhotsk) (present work).

The total content of HCH isomers in the Sea of Okhotsk of fulmars is higher than of the birds of the northern seas (Baffin Bay and the Barents Sea). The total content of DDT and its metabolites exceeds the same value for little auk Alle alle , guillemot Cepphus grylle , thick-billed murre Uria lomvia , and kittiwake Rissa tridactyla from Baffin Bay and Glaucous Gull Larus hyperboreus from Bear Island in the Barents Sea.

Thus, the bioaccumulation of DDTs by seabirds of Okhotsk Sea is approximately equal to that of birds from other regions of the worlds oceans, while the content of HCHs is significantly higher.

Different levels of accumulation of pesticides by particular species primarily reflect the nutritional characteristics, type of diet, migration, and fat content in individual organs. Hence, the northern species of birds are the model of global contamination by organochlorine pollutants that demonstrate the relevance of the international problem of environmental pollution in the water and air.


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