CONCENTRATIONS and INTERACTIONS of SELECTED ESSENTIAL and NON-ESSENTIAL ELEMENTS in BOWHEAD and BELUGA WHALES of ARCTIC ALASKA Author(S): Victoria M
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CONCENTRATIONS AND INTERACTIONS OF SELECTED ESSENTIAL AND NON-ESSENTIAL ELEMENTS IN BOWHEAD AND BELUGA WHALES OF ARCTIC ALASKA Author(s): Victoria M. Woshner, Todd M. O'Hara, Gerald R. Bratton, Robert S. Suydam, and Val R. Beasley Source: Journal of Wildlife Diseases, 37(4):693-710. Published By: Wildlife Disease Association DOI: http://dx.doi.org/10.7589/0090-3558-37.4.693 URL: http://www.bioone.org/doi/full/10.7589/0090-3558-37.4.693 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Wildlife Diseases, 37(4), 2001, pp. 693–710 ᭧ Wildlife Disease Association 2001 CONCENTRATIONS AND INTERACTIONS OF SELECTED ESSENTIAL AND NON-ESSENTIAL ELEMENTS IN BOWHEAD AND BELUGA WHALES OF ARCTIC ALASKA Victoria M. Woshner,1,2 Todd M. O’Hara,2,4 Gerald R. Bratton,3 Robert S. Suydam,2 and Val R. Beasley1 1 Department of Veterinary Biosciences, University of Illinois, Urbana, Illinois 61802, USA 2 Department of Wildlife Management, North Slope Borough, Barrow, Alaska 99723, USA 3 Department of Veterinary Anatomy and Public Health, Texas A&M University, College Station, Texas 77843, USA 4 Corresponding author (e-mail: [email protected]) ABSTRACT: In this study, we evaluated concentrations of twelve essential and non-essential ele- ments (As, Cd, Co, Cu, Pb, Mg, Mn, Hg, Mo, Se, Ag, and Zn) in tissues of bowhead (Balaena mysticetus) and beluga (Delphinapterus leucas) whales from arctic Alaska (USA) and northwestern Canada. Tissue samples were collected between 1983 and 1997, mostly in 1995–97. The essential elements are reported to develop reference ranges for health status determination, and to help assess known or suspected interactions affecting toxicoses of cadmium (Cd) and mercury (Hg). In some tissues, Cd, Hg, and selenium (Se) were present at concentrations that have been as- sociated with toxicoses in some domestic animals. Nevertheless, tissue levels of all elements were within ranges that have been reported previously in marine mammals. While mean Ag concen- trations in beluga whale liver were relatively high (15.91 g/g ww), Ag was not associated with hepatic Se levels or age, contrary to previous findings. Significant associations included: Cd with age, Zn, or Cu; Cu with age, Zn or Ag; and Hg with age, Se, Zn, or Cu. This study found hepatic Hg:Se molar ratios to be consistently lower than unity and different between species. Possible explanations for observed elemental correlations (i.e., interactions) and ancillary mechanisms of Cd and Hg detoxification are discussed. Key words: Balaena mysticetus, Beluga whale, bowhead whale, cadmium, cetaceans, Delphi- napterus leucas, elements, marine mammals, mercury, molar ratio, selenium, silver. INTRODUCTION mammals off the coast of the Netherlands that were consistent with experimental In general, the Arctic is sparsely popu- monomethylmercury (MHg) toxicosis in lated by humans and has comparatively lit- various laboratory and domestic species. tle industry or agricultural enterprise. Koeman et al. (1973) indicated that prey Consequently, detection of anthropogenic of piscivorous marine mammals contain contaminants in the arctic food chain has approximately 16-fold greater molar Se incited public apprehension, especially than molar Hg, and concluded that the 1:1 among native people who consume marine Hg:Se ratio in liver, kidney and brain, is mammals (Wheatley and Paradis, 1995). established in the marine mammal (Koe- Of particular concern are persistent toxi- man et al., 1975). cants, including some metals, which have Koeman’s theory (Koeman et al., 1975) the potential to accumulate in biotic and of equimolar Hg:Se ratios has been cor- abiotic components of the environment roborated by data on tissues of various ma- (Pacyna and Winchester, 1990). Cadmium rine mammal species, including ringed (Cd) and mercury (Hg) occur naturally; (Phoca hispida) and bearded seals (Erig- however, there is no doubt that recent hu- nathus barbatus) (Smith and Armstrong, man activities have increased the rate at 1978); polar bears (Ursus maritimus) which they and other elements are mobi- (Braune et al., 1991; Dietz et al., 1995); lized to and within the biosphere (Pacyna and harbor porpoises (Phocoena phocoena) and Keeler, 1995). (Paludan-Mu¨ ller et al., 1993) with some Koeman et al. (1973, 1975) examined variation from a 1:1 molar ratio noted (Wa- relationships between levels of Hg and se- gemann et al., 1983; Hansen et al., 1990; lenium (Se) in liver and brain of marine Braune et al., 1991). Departures from uni- 693 694 JOURNAL OF WILDLIFE DISEASES, VOL. 37, NO. 4, OCTOBER 2001 ty have been interpreted as evidence that differ with age, tissue type, gender, spe- the mechanism for Hg detoxification has cies, etc.; (3) evaluate elemental interac- been overwhelmed or is not Se-depen- tions; and (4) report ‘‘normal ranges’’ of dent. Arima and Gakura (1979) found a essential elements. linear increase in muscle total Hg with age MATERIALS AND METHODS in odontocetes, in conjunction with a Hg: Se molar ratio of approximately 1.5:1, Sample collection and processing which they construed as an excess of Hg. From 1983 through 1997, tissues were col- Zeisler et al. (1993) noted a positive cor- lected from bowhead and beluga whales relation of Se with both silver (Ag) and to- through the cooperation of Alaskan Eskimo (Inuit) subsistence hunters. Forty-one bowhead tal Hg (THg) in liver of beluga whales whales were sampled from 1983 through 1990 (Delphinapterus leucas). Becker et al. near Barrow (71.33ЊN, 156.00ЊW) (n ϭ 31), (1995) further investigated relationships Kaktovik (70.10ЊN, 143.23ЊW) (n ϭ 3), and among Ag, Se, and Hg in beluga whales. Wainwright (70.55ЊN, 159.95ЊW) (n ϭ 7), Alas- Hepatic total Hg concentrations were sim- ka. From 1995–97, 21 bowhead whales were sampled near Barrow, Alaska. Between 1992 ilar between Alaskan belugas and Atlantic and 1996 beluga whales were sampled in late pilot whales. In contrast, hepatic Ag con- June/early July at Pt Lay, Alaska (69.66ЊN, centrations in belugas were one to three 162.83ЊW) (1992, n ϭ 9; 1995, n ϭ 10; 1996, orders of magnitude greater than in pilot n ϭ 10); in spring (May, 1997) at Point Hope Њ Њ ϭ whales (5.93–107.4 vs. 0.13–0.33 g/g (68.30 N, 166.63 W), Alaska (n 9); in August of 1996 (n ϭ 1) and July of 1997 (n ϭ 3) at ww). Becker et al. (1995) further specu- Barrow, Alaska; summer of 1993 at the North- lated that Ag at these concentrations might west Territories (Inuvik) of Canada (68.32ЊN, adversely affect the Se status of Alaskan 133.50ЊW) (n ϭ 7); and in July at Kaktovik, belugas through competitive binding, ren- Alaska (1997, n ϭ 1). Tissues collected included dering them more vulnerable to Hg toxi- liver, kidney, muscle, blubber and epidermis. Tissues were either frozen or chilled and sub- cosis. sequently processed under clean conditions fol- Major concerns regarding element lev- lowing a strict protocol (Becker, 1995) to min- els in these species include potential toxic imize contamination from handling. This in- effects to wildlife and human consumers. cluded rinsing tissue with HPLC grade water We present what may be considered ‘‘nor- (Sigma Chemical Co., St. Louis, Missouri, USA) prior to sub-sampling and cutting with mal’’ or reference ranges of essential ele- titanium knives on a clean, Teflon-covered sur- ments in apparently healthy (as deter- face. Subsamples of tissues were placed in acid- mined by gross and histologic examination; washed scintillation vials (Fisher Scientific, Woshner et al., 2000b) subsistence-har- Pittsburgh, Pennsylvania, USA) in preparation vested bowhead and beluga whales that for heavy metals analysis. All tissues were fro- zen (Ϫ20 C) immediately after processing. Fro- may be used when a mineral deficiency is zen samples were express delivered (24–48 hr) suspected, for comparison to other spe- to College Station, Texas (USA) for archiving cies, to identify interactions that may and analyses under appropriate National Ma- counter toxicoses (i.e., Se and Hg), or to rine Fisheries Service permits. Teeth were col- establish guidelines for human consump- lected from belugas for age determination us- ing counts of dentinal growth layer groups tion. A better understanding of essential (GLGs), which have been estimated to deposit elements in arctic marine mammals will at a rate of two GLGs annually (Goren et al., help to improve health assessments and 1987). Total GLGs were used in all analyses. disease investigations. Body length was used as a surrogate for age in The objectives of this study were to (1) bowhead whales (George et al., 1999). evaluate concentrations of selected essen- Metals analysis tial and non-essential elements in tissues In preparation for elemental analysis, tissue of bowhead and beluga whales harvested samples were weighed (wet weight or ww), by Alaskan Native subsistence hunters; (2) dried to constant weight, and digested in a wet to determine whether these element levels ash procedure using concentrated (70%) nitric WOSHNER ET AL.—ESSENTIAL AND NON-ESSENTIAL ELEMENTS IN BOWHEAD AND BELUGA WHALES 695 acid and microwave processing at 120 C for 60 Washington, USA; Bloom and Crecelius, 1983; min.