Environ. Sci. Technol. 2007, 41, 2216-2222
Bioaccumulation, Temporal Trend, and Geographical Distribution of Synthetic Musks in the Marine Environment H A R U H I K O N A K A T A , * ,† H I R O S H I S A S A K I , † AKIRA TAKEMURA,‡ MOTOI YOSHIOKA,§ SHINSUKE TANABE,| AND KURUNTHACHALAM KANNAN⊥ Graduate School of Science and Technology, Kumamoto University, 2-39-1 Kurokami, Kumamoto 860-8555 Japan, Faculty of Fishery, Nagasaki University, Bunkyo-machi, Nagasaki, 852-8521 Japan, Graduate School of Bioresources, Mie University, 1577 Kurimamachiya-cho, Tsu, 514-8507 Japan, Center for Marine Environmental Studies (CMES), Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japan, and Wadsworth Center, New York State Department of Health and Department of Environmental Health Sciences, School of Public Health, State University of New York at Albany, Empire State Plaza, PO Box 509, Albany, New York 12201-0509
Bioaccumulation of synthetic musks in a marine food chain was investigated by analyzing marine organisms at various trophic levels, including lugworm, clam, crustacean, fish, marine mammal, and bird samples collected from tidal flat and shallow water areas of the Ariake Sea, Japan. Two of the polycyclic musks, HHCB and AHTN, were the dominant compounds found in most of the samples analyzed, whereas nitro musks were not detected in any of the organisms, suggesting greater usage of polycyclic musks relative to the nitro musks in Japan. The highest concentrations of HHCB were detected in clams (2582730 ng/g lipid wt.), whereas HHCB concentrations in mallard and black-headed gull were low, and comparable with concentrations in fish and crab. These results are in contrast to the bioaccumulation pattern of polychlorinated biphenyls; for which a positive correlation between the concentration and the trophic status of organisms was found. Such a difference in the bioaccumulation is probably due to the metabolism and elimination of HHCB in higher trophic organisms. Temporal trends in concentrations of synthetic musks were examined by analyzing tissues of marine mammals from Japanese coastal waters collected during 1977-2005. HHCB concentrations in marine mammals have shown significant increase since the early 1990s, suggesting a continuous input of this compound into the marine environment. Comparison of the time trend for HHCB with those for PCBs and PBDEs suggested that the rates of increase in HHCB concentrations were higher than the other classes of pollutants. To examine the geographical distribution of HHCB, we have analyzed tissues of fish, marine * Corresponding author phone/fax: +81-96-342-3380; e-mail:
[email protected]. † Kumamoto University. ‡ Nagasaki University. § Mie University. | Ehime University. ⊥ State University of New York at Albany. 2216
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mammals, and birds collected from several locations. Synthetic musks were not detected in a sperm whale (pelagic species) from Japanese coastal water and in eggs of south polar skua from Antarctica. While the number of samples analyzed is limited, these results imply a lack of long-range transportation potential of synthetic musks in the environment.
Introduction Musk fragrances have been synthesized for more than 100 years; the “Musk Baur” [2-(1,1-dimethylethyl)-4-methyl-1,3,5trinitro-benzene] was the first artificial compound with fragrance odor (1). The market for the fragrance industry developed through the 20th century, and now large quantities of synthetic musks are manufactured and used in a wide variety of personal care products, such as perfumes, skin cream, deodorants, soaps, and detergents. Among the various classes of synthetic fragrances, polycyclic musks and nitro musks are dominant in terms of production volume; they comprised 61% and 35%, respectively, of the total amount of synthetic musk compounds produced in the world (7000 t) in 1987 (1). In particular, high production and usage of HHCB (1,3,4,6,7,8-hexahydro-4,6,6,7,8,8-hexamethylcyclopenta[g]-2-benzopyrane) and AHTN (7-acetyl-1,1,3,4,4,6hexamethyltetrahydronaphthalene) were reported in Europe and the United States in the 1990s. The industrial usage of polycyclic musks (HHCB and AHTN) and nitro musks (musk xylene and nitro ketone) in 2000 were 3285 and 298 t, respectively (2). The United States Environmental Protection Agency lists HHCB as a high-production-volume chemical; more than 400 t of HHCB is produced in or imported into the United States every year (3). Since the first report of detection of synthetic musks in the environment (4), the concentrations and distribution of these compounds have been investigated in various matrices and locations. High concentrations of synthetic musks (mg/L range) were found in sewage effluent and sludge from a wastewater treatment plant (WWTP), and in freshwater fish around the WWTP facility (5, 6). These results indicated that the major source of synthetic musks to the environment is WWTPs. The occurrence of musk fragrances has been reported in air (7, 8), freshwater (9), seawater (10), and sediment (11, 12), suggesting that these compounds are widespread contaminants in the environment. Because of their highly lipophilic nature, synthetic musks have been found in a number of aquatic organisms, such as mussels, crustaceans, and fish from the freshwater and marine environments. Concentrations of musk fragrances in eel and pikeperch from the Elbe River ranged from 30 to 3840 ng/g (lipid wt.) for HHCB, and from 40 to 990 ng/g for AHTN (9). High concentrations of musk ketone were found in clams and mussels from Canadian coastal waters, ranging from 2200 to 17 700 ng/g on a lipid wt. basis (13). Recently, polycyclic musks have been shown to accumulate in higher trophic organisms, such as sharks and mammals from marine ecosystems. HHCB and AHTN were detected in tissues of finless porpoises from the Ariake Sea, Japan (14), and in other aquatic mammals from U.S. inland and coastal waters (15). In addition, musk xylene and polycyclic musks were found in coastal bird species and in otters, respectively (16). These reports suggest food chain transfer of synthetic musks in aquatic ecosystems. The bioaccumulation factor, on a wet weight basis (BAFw), in fish was 4200-5100 for musk xylene (17), 1584 for HHCB, 10.1021/es0623818 CCC: $37.00
2007 American Chemical Society Published on Web 03/03/2007
and 597 for AHTN (18), under laboratory exposure conditions. The BAFw values of musks in four fish species from a pond that received WWTP were 20-580 for HHCB, 40-670 for AHTN, 60-1300 for musk ketone, and 290-40 000 for musk xylene (6). The wide range of BAFw determined in these earlier studies suggested species-dependent accumulation and metabolism of synthetic musks in fish (6). However, most of the earlier studies focused on bioconcentration between water and fish, with little attempt to assess accumulation and food chain transfer to top predators of marine ecosystems. Because synthetic musks have been shown to exert potential effects in organisms at various trophic levels, such as mussels (19), fish (20), rats (21), and humans (22), based on in vivo and/or in vitro assays, it is important to understand the biomagnification potential of these compounds and to identify those species that accumulate high concentrations of musks through their diet and habitat. Accordingly, we measured three nitro musks (nitro ketone, nitro xylene, and nitro ambrette) and two polycyclic musks (HHCB and AHTN) in lugworm, mussel, crustacean, fish, marine mammal, and bird samples collected from tidal flat and shallow water areas of the Ariake Sea, Japan. Time trends in the concentrations of synthetic musks have been examined in Germany and the United States. Concentrations of musk xylene in eel from the Elbe River decreased during 1994-1999, with a mean concentration of 127 ng/g (lipid wt.) in 1994 to
