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Bioaccumulation of Mercury in the Pelagic Food Chain of the Lake Baikal

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Bioaccumulation of Mercury in the Pelagic Food Chain of the Lake Baikal Chemosphere 78 (2010) 1378–1384 Contents lists available at ScienceDirect Chemosphere journal homepage: www.elsevier.com/locate/chemosphere Bioaccumulation of mercury in the pelagic food chain of the Lake Baikal T. Ciesielski a,*, M.V. Pastukhov b, P. Szefer c, B.M. Jenssen a a Department of Biology, Norwegian University of Science and Technology, NO-7491 Trondheim, Norway b Institute of Geochemistry, Siberian Branch of the Russian Academy of Science, Irkutsk 664033, Russia c Department of Food Sciences, Medical University of Gdan´sk, al. Gen. J. Hallera 107, 80-416 Gdan´sk, Poland article info abstract Article history: Mercury (Hg) concentrations were analyzed in the livers of Baikal seals and in plankton, zoobenthos and Received 23 May 2009 fish which constitute food items for the seals. Concentrations of Hg in the liver of Baikal seals were up to Received in revised form 26 December 2009 two orders of magnitude lower than those in seals inhabiting other lakes. The low levels of Hg are due to Accepted 28 December 2009 the low levels of the Hg in the fish from the family Comephoride, which reflect the very low concentra- Available online 1 February 2010 tions of Hg in Baikal water. The development stage (pups and adults) and the sex of the seals have sig- nificant influence on their hepatic Hg concentrations. The differences between Hg accumulation in Keywords: adult males, adult females and pups could be attributed to the reproductive cycle of the Baikal seals. Mercury In spite of low concentrations, Hg is characterized by high values of the concentration factor (CF) for Lake Baikal Trophic transfer the livers of for Baikal seals. Biomagnification factors (BMFs) suggest biomagnifications of Hg in the Fish fish-seal trophic link. Plankton Ó 2010 Elsevier Ltd. All rights reserved. Baikal seal 1. Introduction tion. Other sources include thermal energy and power plants as well as urban activity and gold production (Koval et al., 1999). Anthropogenic factors have increased the geochemical cycling The Lake Baikal consists of three separate basins: southern, cen- of Hg to a significant extent, on both regional and global scales. tral and northern. The distance from and occurrence of Hg pollu- Two to three times more Hg is presently being cycled through tion sources are different for each of the basins (Vetrov and the atmosphere and upper ocean water than before the rise of Kuznetsova, 1997). Additionally, hydrothermal vents found in the industry (Macdonald et al., 2005). The UN Environment Program sediment floor of the northeastern area of the lake could also be ‘‘Global Mercury Assessment” reported Hg to be a growing and potential sources of natural Hg emissions (Meuleman et al., worldwide problem. Chemical elements, like heavy metals can be 1995). However, in spite of different atmospherics and natural transported along the successive links of the food chain and their sources, the levels of Hg in the Lake Baikal are very low and com- concentrations rise at each higher trophic level. This phenomenon parable to those in open ocean waters and even lower than the is known as biomagnification. Mercury in the form of monomethyl concentrations reported for other remote and unpolluted freshwa- mercury bioaccumulates and biomagnifies along marine and fresh- ter systems (Meuleman et al., 1995). water food chains and this leads to high levels in the top predators. The only species of seal living exclusively in fresh water, the Finally this can result in severe toxicological effects in aquatic top Baikal seal (Phoca sibirica), is the top predator in the Lake Baikal pe- predators (Booth and Zeller, 2005; McIntyre and Beauchamp, lagic food chain. Marine mammals can accumulate substantial lev- 2007). els of organochlorine compounds and heavy metals (Das et al., Several previous studies have focused on the influence of local 2003). This has led to speculation about the possible involvement industrial emission sources on the Hg levels in the Lake Baikal eco- of environmental pollutants in immunosuppression associated ef- system and adjacent areas (Grachev, 1999; Koval et al., 1999). fects (Bennett et al., 2001; Kannan et al., 2006). Severity of lesions Important sources of the potential Lake Baikal pollution have been and high Hg levels were associated with a relatively poor health described by Ciesielski et al. (2006a). The main anthropogenic Hg status of marine mammals from German waters of the North Sea sources in the vicinity of the Lake Baikal are concentrated primarily and the Baltic Sea (Siebert et al., 1999). in the Irkutsk-Cheremkhovo industrial zone where Hg is used in Concentrations of different elements in tissues and organs of the chemical industries such as chemical pulp and paper produc- Baikal seals have been reported previously by Watanabe et al. (1996, 1998), Beim and Renzoni (2000), Ikemoto et al. (2004) and * Corresponding author. Tel.: +47 73551289; fax: +47 73596100. Ciesielski et al. (2006a). The relatively straightforward trophic E-mail address: [email protected] (T. Ciesielski). relationships in the Lake Baikal make it a very good system for 0045-6535/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2009.12.070 T. Ciesielski et al. / Chemosphere 78 (2010) 1378–1384 1379 studying natural biogeochemical fates of Hg in a relatively unpol- of Hg in a predator (consumer, whole body w.b.) and the concen- luted aquatic ecosystem (Gurova and Pastukhov, 1974; Yoshii tration of Hg in the prey (food, whole body w.b.): et al., 1999). Such a study includes work on biological factors that influence bioaccumulation and biomagnification of Hg in low BMF ¼ Cw:b:ðpredatorÞ=Cw:b:ðpreyÞ exposure conditions. The content of Hg differs considerably in various tissues and or- The aim of the present study was to examine trophic transfer of gans of vertebrates. To overcome the problem of using liver con- Hg along sequential trophic levels of the food chain of the Baikal centrations of the seals in the calculation of BMFs we used the seal, and to examine the biological importance of sex and age procedure described by Strand and Jacobsen (2005). Thus, the con- and spatial (geographical) distribution on the bioaccumulation of centration of Hg in whole body of the seals (Cseal) was estimated Hg. In addition, concentrations of other elements previously re- from the concentration in liver Cliv, and the proportion between ported in Baikal seals (Ciesielski et al., 2006a) were included in a the two factors L and P using the equation: meta-analysis to clarify biological processes responsible for Hg accumulation in relation to other elements. Cseal ¼ Cliv: Ã L=P where L is the liver weight/body weight (weights measured during 2. Experimental procedures dissections), and P is the ratio between the liver and total body res- idues of Hg in Baikal seals based on literature values. For the BMF The sample collection and biometry for 27 individuals of Baikal calculation only Hg concentrations in adult seals were used. P data seal (P. sibirica), fish species (Comephorus dybowski, Comephorus were obtained both from Watanabe et al. (1996) and from personal baicalensis, Cottocomephorus inermis, Cottocomephorus grewingki), communication with authors of this publication. zooplankton and zoobenthos species (Acanthogammarus godlew- Two-way analysis of variance (ANOVA) was used to test for the skii) have been described in detail previously (Ciesielski et al., two qualitative biological predictors, sex (males and females), and 2006a). Seals were found dead (n = 11) or were obtained from local age. The seals were grouped into one of three age groups: 1– hunters (who had appropriate permission) during the official cull 2 months, 5–8 years and 9–15 years. In order to assess the signifi- (n = 16). The location of the sampling stations is shown in Fig. 1. cance of the spatial (geographical) distribution of the seals, a ‘re- The mesozooplankton composition was as follows: Epishura baical- gion’ factor (the southern, central and northern basins of Baikal) ensis (50%), Cyclops kolensis (20%), Daphnia galeata (20%) and Bos- and a qualitative predictor reflecting both maturity and the sex mina longirostris (10%). Macrohectopus branickii of the seals (seals were divided into 3 groups-pups [1–2 months], (macrozooplankton) samples were obtained with the use of an adult males [>5 years] and adult females [>5 years]) were also in- appropriate plankton net in 2003. All samples were preserved cluded. ANOVA was applied to test for the differences in Hg con- and transported frozen at À20 °C until analysis. The age of adult centration between seals found dead and those that had been seals was determined in analysis of the dentinal and cemental culled. The Hg concentrations obtained herein were compared to growth layers in the canine teeth. our previous results on other chemical elements for the same seals The details of chemical procedure for Hg determination includ- (Ciesielski et al., 2006a) in a meta-analysis using factor analysis ing sample preparation, microwave digestion and final determina- (FA). The application of multidimensional statistical analysis (FA) tion by atomic absorption spectrometry with cold vapor allows correct interpretation of the results because of the numer- generation (CV-AAS) are given in Ciesielski et al. (2006b). The livers ous interrelationships between the elements in the data set. of the seals were lyophilised and homogenized and subsamples of Mann–Whitney U test and linear correlation analysis (Pearson’s around 0.6 g were subsequently weighed. Because of their high fat r) were used for comparing groups and for examining associations, content, the fish samples were homogenized whole, without prior respectively. Statistical analyses were performed with STATISTICA drying. The plankton and zoobenthos samples were treated in the 6.0 for Windows. For comparison with results on element concen- same way. The final results were calculated as the mean of the con- trations reported in other studies, a factor of 0.3 was applied to centrations determined for three replicate samples.
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