Acta Oceanol. Sin., 2015, Vol. 34, No. 6, P. 21–25 DOI: 10.1007/s13131-015-0683-y http://www.hyxb.org.cn E-mail: [email protected] The level and bioaccumulation of Cd, Cu, Cr and Zn in benthopelagic species from the Bering Sea SHI Ronggui1, 2, LIN Jing1, 3, YE Yi1, MA Yifan1, CAI Minggang1, 4* 1 College of Ocean and Earth Sciences, Xiamen University, Xiamen 361005, China 2 South China Sea Environmental Monitor Center, State Ocean Administration, Guangzhou 501300, China 3 Third Institution of Oceanography, State Oceanic Administration, Xiamen 361005, China 4 State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361005, China Received 30 May 2014; accepted 11 September 2014

©The Chinese Society of Oceanography and Springer-Verlag Berlin Heidelberg 2015

Abstract The Bering Sea is an area of high biological productivity, with large populations of sea-birds, demersal and pelagic fishes, so it seemed desirable to assess the bioaccumulation of trace metals in the marine organisms from this area. However, few data on trace metal concentrations are available for the benthopelagic organisms from the Bering Sea till now. Ten specimens of benthos (including 120 biological samples) were collected in the western Bering Sea in August 2008 during the 3rd Chinese National Arctic Research Expeditions, and the concentration of Cd, Cu, Cr and Zn determined using atomic absorption spectrometry. Zn, Cr and Cd concentrations in muscle tissues of the crab species were much higher than those from fish and cephalopod species, and the highest concentration of Cu was observed in the muscle tissues ofCylichna nucleoli. The results showed a similar hierarchy for Zn, Cr, Cd and Cu concentrations among different tissues as follows: hepatopancreas>muscle tissue>gonad. Bioconcentration factors indicated that benthic organisms had high accumulation abilities for Zn and Cu. Key words: trace metal, benthopelagic species, bioconcentration, Bering Sea, Arctic Citation: Shi Ronggui, Lin Jing, Ye Yi, Ma Yifan, Cai Minggang. 2015. The level and bioaccumulation of Cd, Cu, Cr and Zn in benthopelagic species from the Bering. Acta Oceanologica Sinica, 34(6): 21–25, doi: 10.1007/s13131-015-0683-y

1 Introduction marine pollution (Jabeen and Chaudhry, 2010). Because of their toxicity, nonbiodegradability and bioaccu- High-latitude regions are regarded as the ultimate reservoir mulation capacity in the marine environment, heavy metals are for semivolatile organic pollutants and trace metals (Alexeeva et always regarded as one of the most severe pollutants (Sinex and al., 2001). The Bering Sea is an area of high biological productiv- Wright, 1988; Dragun et al., 2010). Some metals, such as copper, ity, with large populations of sea-birds, demersal and pelagic zinc, iron, and manganese, are essential metals for aquatic or- fishes (Jewett and Naidu, 2000). For this reason, it seemed desir- ganisms at a low concentration, while if their concentrations are able to assess the bioaccumulation of trace metals in the marine increased above the natural baseline level, they may become tox- organisms from this area. Considerable attention has been given ic for marine organisms (Sandor et al., 2001; Tüzen, 2003; Bu- to metal contamination in waters, organisms, and sediments suioc et al., 2011). On the other hand, some other metals, such as from high-latitude regions (Fujishima et al., 2001; Trefry et al., cadmium, lead and mercury, which are not essential for organ- 2003; McMeans et al., 2007). However, few data on trace metal isms, have toxic effects (Lai et al., 2008; Anim et al., 2011). concentrations are available for the benthopelagic organisms Because of their obvious bioaccumulation, once discharged from the Bering Sea (Jewett and Naidu, 2000). The objective of into the marine environment, these metals tend to be accumu- our work was to study the distribution of trace metals in various lated in sediments and marine organisms and subsequently tissues of the benthos from the pelagic Bering Sea, and to calcu- transferred along the food chain, which may finally influence the late the bioconcentration factors of trace metals in benthic tis- local marine ecosystem and the health of humans (Sivaperumal sues compared with the levels in the surface sediments from the et al., 2007; Wang and Wang, 2007; Maanan, 2008; Polak- study area, and to compare the relative concentrations of trace Juszczak, 2009). Trace metals are taken up by different organs of metals here to those from other areas. the organism and many are concentrated at different levels in these different organs (Karadede et al., 2004). It is important, 2 Materials and methods therefore, to determine the concentrations of trace metals in The Bering Sea, a semi-enclosed high-latitude sea, is one of marine organisms to understand their physiological and toxico- the largest marginal seas in the world (Okazaki et al., 2005). It has logical effects. The distribution of metals in the tissues of differ- an area of approximately 2.29×106 km2 and a volume of 3.75×106 ent organisms is extensively used as an indicator of the degree of km3. The eastern continental shelf is wide and extends from the

Foundation item: The National Natural Science Foundation of China under contract Nos 40776040 and 41076133; the Ocean Public Welfare Scientific Research Project, State Oceanic Administration of China (SOAC) under contract No. CHINARE2012-03-04; the Marine Science Base Project for Scientific Research Training and Capacity Enhancement—Xiamen University, supported by the National Natural Science Foundation of China under contract No. J1210050. * Corresponding author, E-mail: [email protected] 22 SHI Ronggui et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 6, P. 21–25

Bristol Bay in the south to the Bering Strait in the north along Analytical accuracy was assessed using a Standard Reference Alaska’s west coast. The Aleutian Basin, located in the western Material (GBW 08573, yellow croaker, China). The results were in Bering Sea, is a vast marine plain with a depth of approximately 3 good agreement with the certified values and the recoveries 800 m. There are three main rivers that empty into the Bering ranged from 95% to 105% (Table 1). Sea: the Kuskokwin and Tukon Rivers drain central Alaska, and the Anadyr River drains western Siberia (Takahashi, 2005). Ten specimens of benthos (including 120 biological samples) Table 1. Concentrations (mg/kg, dw) of trace metals in Stand- were collected in the western Bering Sea in August 2008 during ard Reference Material (GBW 08573, yellow croaker, China) the 3rd Chinese National Arctic Research Expeditions. The Metal Measured value Certified value Detection limit benthic samples were captured with a trawl, while the surface Zn 29.11±0.00 27.90±0.90 0.127 sediment was sampled using a grab sampler. After cleaning with Cr 0.66±0.07 0.63±0.08 0.328 milli-Q ultrapure water, samples were transferred carefully to Cd 1.15±0.02 1.14±0.11 0.001 acid-rinsed plastic bags and then were frozen at –18°C until ana- Cu 5.81±0.01 5.01±0.32 0.263 lysis in March 2009.

In the laboratory, samples were unfrozen at 4ºC in the refri- gerator overnight, washed with milli-Q ultrapure water, and then 3 Results and discussion dried naturally in the plastic pallet. Chionoecetes opilio were dis- sected with plastic scissors to separate muscle tissue, hepatopan- 3.1 Concentrations and distribution of trace metals in the benthos creas and gonad. Muscle tissues were collected from other organ- Concentrations of trace metals in the benthos studied varied isms for analysis. from 11.03–31.43, 0.05–0.25, 0.02–0.55, and 0.71–10.88 mg/kg for These organs were dried in an oven at 60ºC to constant mass Zn, Cr, Cd, and Cu, respectively (Table 2). Concentrations of Zn, and then ground with an agate pestle and mortar. (0.2±0.001) g of Cr and Cd were higher in the muscle tissue of Maja sp. than those sample (dry weight, dw) was dissolved in 10 mL of ultrapure nitric acid in an acid-washed Teflon vessel overnight at room in other benthos. High concentrations of trace metals were also temperature and then digested in a microwave oven at 190ºC for found in the muscle tissue of Chionoecetes opilio. With respect to 15 min. After cooling, the solution was heated until almost dry. the shrimp species, the highest concentrations of Zn, Cr and Cu Finally, the digested sample was quantitatively transferred to a were found in the muscle tissue of Pandalus dispar, Argis lar and tube and diluted to 25 mL with 1% nitric acid (v/v). Sample solu- Ceradocus sp., respectively. In addition, for the cephalopod spe- tions were analyzed for Zn using flame atomic absorption spec- cies, highest concentrations of Zn, Cd and Cu were observed in trometry, and for Cu, Cr and Cd using graphite furnace atomic the muscle tissue of Alvania sp., Cryptonatica clausa and Cy- absorption spectrometry (SOLLAAR M6, Thermo Electron). lichna nucleola, respectively. A fish species, Micromesistius pou- All trace metal concentrations in benthos tissues are reported tassou, on the other hand, had concentrations relatively lower in mg/kg of dry weight. The mean water content ranged from than all the other benthos studied. Such significant variation of 62% to 84% in muscle, from 65% to 78% in hepatopancreas and trace metal concentrations in the muscle tissue of different from 66 to 81% in gonad. For the purpose of comparison with benthic organisms could be related to species-specific feeding other studies, dry weight was converted to wet weight (ww) with habits, metallothionein level, the growth stage of the benthos, water content. etc. (Pourang and Dennis, 2005; Sankar et al., 2006).

Table 2. Trace metal concentrations (mg/kg, ww) in muscle tissue of benthos Species Zn Cr Cd Cu Cephalopods Cylichna nucleola 15.23±3.13 0.10±0.14 0.15±0.03 10.88±4.51 Solariella varicosa 15.23±5.26 0.05±0.19 0.02±0.03 1.76±0.89 Cryptonatica clausa 15.58±2.47 0.10±0.67 0.30±0.16 1.86±3.13 Alvania sp. 17.44±4.32 0.08±0.25 0.10±0.07 5.92±1.23 Pandalus dispar 15.23±5.26 0.05±0.08 0.14±0.04 3.47±0.11 Argis lar 11.03±7.15 0.14±0.25 0.05±0.26 2.11±0.14 Crustaceans Ceradocus sp. 11.44±6.82 0.10±0.40 0.07±0.23 3.91±0.42 Chionoecetes opilio 26.23±1.24 0.21±0.02 0.40±0.03 3.08±0.02 Maja sp. 31.43±2.43 0.25±0.07 0.55±0.09 2.02±0.05 Fish Micromesistius poutassou 13.60±1.16 0.12±0.05 0.04±0.01 0.71±0.02

Generally speaking, benthosand attaching organism have rel- species-specific feeding habits, metallothionein level and the atively stronger accumulate ability than nektons (Sankar et al., growth stage of the benthos could also affect the trace metal con- 2006; Sivaperumal et al., 2007). Chionoecetes opilio and Maja sp. centrations in benthos (Pourang and Dennis, 2005; Sankar et al., that have direct contact with sediment, could accumulate more 2006). Zn, Cr and Cd than other benthos. Theragra chalcogramma has Concentrations of Zn and Cu in the muscle tissue of the stronger migration capability than other benthos, which could benthos were higher than those of Cd and Cr. It is possible that prevent it from being poisoned by high concentration of trace Zn and Cu are essential metals for aquatic organisms and thus metals in sediment. Cd and Cu concentrations in Pandalus dis- subject to active absorption in marine organisms (Okazaki et al., par were higher than Trochidae Solariella varicosa because of the 2005). Cr is an essential trace element in organisms and plays a higher trophic level. Other than the life habit and trophic level, very important role (in its biologically usable form) during the SHI Ronggui et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 6, P. 21–25 23 metabolic processing of glucose (Sivaperumal et al., 2007). Com- results from the coast of Mexico (Páez-Osuna and Ruiz- pared with Zn and Cu, the quantity of Cr demanded for the or- Fernández, 1995), concentrations of Zn, Cd and Cu in muscle tis- ganisms is low, and thus the levels of Cr in the organisms are rel- sue of shrimp species from our study area were significantly atively lower than those of Zn and Cu. Cd is not essential for or- lower. Cd concentration in muscle tissue of Chionoecetes opilio ganisms and has toxic effects even at low concentration (Soylak and Maja sp. from the Bering Sea were similar to that of red king et al., 2004), therefore, Cd in muscle from different benthos was crab from the coast of Alaska (Jewett and Naidu, 2000). In com- the lowest. parison with the red king crab, concentrations of Cr and Cd were Concentrations of trace metals in organisms from other re- higher in the hepatopancreas of Chionoecetes opilio from the gions are listed in Table 3. Concentrations of Zn, Cd and Cu in study area, while the Cu and Zn concentrations were lower. The the muscle tissue of Micromesistius poutassou are higher than difference of trace metal levels in organisms from different areas those of Bathyraja from the Barents Sea and Nematonurus was likely to be due to the different species, the source of trace armatus, a deep-water fish species, from the Rockall Trough metals, and the degree of contamination. (Mormede and Davies, 2001; Zauke et al., 1999). Compared to the

Table 3. Comparison of trace metals concentration (mg/kg, ww) from various locations Study area Species Tissue Zn Cr Cd Cu Reference Barents Sea Sockeye salmon muscle tissue 6.70 – <0.01 0.30 Zauke et al. (1999) Coast of Alaska Red king crab muscle tissue 31.00 0.21 0.04 12.19 Jewett and Naidu hepatopancreas 37.30 0.22 3.20 39.00 (2000) Coast of Mexico Penaeus muscle tissue 60.60 – 0.57 23.30 Páez-Osuna and vannamei Ruiz-Fernández (1995) Rockall Trough Nematonurus muscle tissue 4.40 – 0.01 0.31 Mormede and armatus Davies (2001) Bering Sea Micromesistius muscle tissue 13.60 0.12 0.04 0.71 present study poutassou Note: – represents data not available.

3.2 Comparison of trace metal levels in different tissues of of metallothionein, which are related to the metabolism, storage Chionoecetes opilio and detoxication of trace metals in the organism (Powers and Out of the three types of Chionoecetes opilio tissues analyzed Bliss, 1983; Moksnes et al., 1995; Anderson et al., 1997). The (muscle tissue, hepatopancreas and gonad) concentrations of metabolic capability of the cells of an organ is strong and, in gen- trace metals were greatest in the hepatopancreas and smallest in eral, levels of trace metals in the gonad are similar to those in the the gonad (Table 4). The concentration of Cd in the hepatopan- hepatopancreas (Beltrame et al., 2010). Whereas, in our study, creas was 12 and 40 times higher than that in muscle tissue and levels of trace metals in the Chionoecetes opilio gonad were lower gonad. Studies also indicate that the level of Cd is higher in the than those in the hepatopancreas and muscle tissue. This could hepatopancreas than that in other tissues of crab species (Bjer- be related to the different embryonic developmental stages of regaard et al., 2005; Chen et al., 2007). High concentrations of Chionoecetes opilio (Beltrame et al., 2010). trace metals in the hepatopancreas may be due to the high levels

Table 4. Trace metals concentrations (mg/kg, ww) in different tissues of Chionoecetes opilio Tissue Zn Cr Cd Cu Muscle tissue 26.23±1.24 0.21±0.02 0.40±0.03 3.08±0.02 Hepatopancreas 26.32±0.08 0.97±0.13 4.78±0.03 10.62±0.05 Gonad 16.74±0.00 0.03±0.02 0.12±0.01 7.96±0.02

3.3 The bioconcentration factor of trace metals Chionoecetes opilio (BF=79.6). This could potentially be due to The bioconcentration factor of trace metals in marine organ- the similar geochemical behavior and ionic radius of Cd and Ca, isms is defined as the ratio of trace metal concentration in the tis- allowing the substitution of Cd for Ca. High concentrations of Cd sue of the organisms to that of the surface sediments (Table 5). In in organisms from the Bering Sea may also be related to high our study, bioconcentration factors were calculated based on the levels of Cd in the surface waters through the upwelling of nutri- trace metal concentrations in surface sediments, where the trace ent-rich waters in the study area (Roméo et al., 1999; De Mora et metal concentrations in mg/kg were 21.06 for Zn, 8.91 for Cr, 0.30 al., 2004; Gao et al., 2004). for Cd, and 3.85 for Cu, respectively (Cai et al., 2011). The biocon- centration factors of the benthos were higher for essential ele- 4 Conclusions ments (Cu and Zn). High bioconcentration factors of Cd were Different metals were present in the bio-samples from the also found in some benthos, especially in the hepatopancreas of Bering Sea at different concentrations. Zn, Cr and Cd concentra- 24 SHI Ronggui et al. Acta Oceanol. Sin., 2015, Vol. 34, No. 6, P. 21–25 tions in the muscle tissue of crab species were much higher than different tissues of Chionoecetes opilio as follows: hepatopan- those for fish and cephalopods, while Cu was present at a high creas>muscles>gonads. High bioconcentration factors for Cu level in the muscle tissue of the cephalopods. A similar hierarchy and Zn were found in all the benthic species studied and for Cd for Zn, Cr, Cd and Cu concentrations was apparent among the in the majority.

Table 5. Bioconcentration factors of trace metals in tissues of benthos from the Bering Sea Species Zn Cr Cd Cu Cephalopods Cylichna nucleola 3.62 0.10 2.5 14.1 Solariella varicosa 3.62 0.03 0.3 2.3 Cryptonatica clausa 3.70 0.05 4.9 2.4 Alvania sp. 4.10 0.05 1.7 7.7 Crustaceans Pandalus dispar 3.60 0.03 2.4 4.5 Argis lar 2.60 0.08 0.8 2.7 Pandalus dispar 2.70 0.06 1.1 5.1 Chionoecetes opilio-muscle tissues 6.30 0.10 6.7 4.0 Chionoecetes opilio-hepatopancreas 6.30 0.10 79.6 13.8 Chionoecetes opilio-gonad 4.00 0.01 2.0 10.2 Maja sp. 7.50 0.10 9.1 2.6 Fish Micromesistius poutassou 3.20 0.10 0.6 0.9

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