Chemical contaminants in gray whales (Eschrichtius robustus) stranded in Alaska, Washington, and California, U.S.A.
Varanasi, U. J.E. Sein, K.L. Tilbury, J.P. Meador, C.A. Sloan, D.W. Brown, J. Calambokidis, and S-L. Chan. 1993. Chemical contaminants in gray whales (Eschrichtius robustus) stranded in Alaska, Washington, and California, U.S.A. U.S. Department of Commerce, NOAA Technical Memorandum NMFS-NWFSC-11. 115pp.
Gray whale (Eschrichtius robustus) populations in the eastern North Pacific have increased at an annual rate of close to 3% since cessation of commercial exploitation and now number over 20,000 (Buckland et al. 1993, Reilly 1992), which is close to their historical population size. These marine mammals make an annual round-trip migration between their breeding grounds in Mexican waters (along Baja California) and their feeding grounds in more northern waters which range from northern California to Alaska (Rice and Wolman 1971). The southbound migration to the breeding grounds occurs in December and January along the West Coast and the northbound migration from February through May (Pike 1962). Gray whales generally fast during the breeding season in Mexico and during their migrations (Rice and Wolman 1971). Their body mass, overall fat content, girth, and blubber thickness are significantly lower during the northbound migration than during the southbound migration (Rice and Wolman 1971). Though the majority of gray whales feed in the Bering and Chukchi Seas in Alaska (Rice and Wolman 1971), some animals spend extended periods in the spring and summer feeding in coastal waters of California, Oregon, Washington, and British Columbia (Nerini 1984; Rice and Wolman 1971; Sumich 1984; Mallonee 1991; Patten and Samaras 1977; Darling 1984; Calambokidis et al. 1991, 1992). Up to 17 gray whales have been documented entering Puget Sound, Washington, in a year and some have spent up to 4 months in the area (Calambokidis et al. 1991, 1992, 1993). Some of these whales return in multiple years with two whales seen in Puget Sound in three consecutive years (Calambokidis et al. 1993). Further, between 1986 and 1991, 5 of 23 gray whales individually identified while alive in Puget Sound were subsequently found dead (Calambokidis et al. 1991, 1992). This high proportion of gray whale deaths may be due either to the whales entering Puget Sound in poor health or to the exposure to contaminants affecting the whales' health. There has not been adequate information to determine which factor explains the apparent high rate of gray whales deaths in Puget Sound.
Gray whales feed primarily on benthic prey, though feeding on pelagic prey has also been documented (Nerini 1984). The whales use suction to engulf sediments and prey from the bottom, then filter out water and sediment through their baleen plates and then ingest the remaining prey (Nerini 1984). This feeding method often results in the ingestion of sand and other bottom materials (Rice and Wolman 1971). The dominant prey of gray whales in feeding grounds in Alaska are ampeliscid amphipods (Ampelisca macrocephala) though a variety of other benthic prey items are also consumed (Rice and Wolman 1971, Nerini 1984). Recent studies of gray whale feeding in northern Puget Sound have revealed predation on ghost shrimp (Callianassa californiensis) (Weitkamp et al. 1992). Thus, the potential exists for exposure to sediment associated contaminants if gray whales feed in urban embayments.
There is increasing evidence that chemical pollution in coastal areas near urban centers may be responsible for a variety of deleterious biological effects in aquatic species, from liver tumors and reproductive dysfunction (infertility, spawning failure) in bottomfish that reside on contaminated sediments (Varanasi et al. 1992a) and altered immune function in juvenile salmon after only a brief residency in waters of polluted estuaries (Arkoosh et al. 1991) to reproductive dysfunction in marine mammals (DeLong et al. 1973, Duinker et al. 1979, Reijnders 1986). In Puget Sound, sediments in several urban and industrialized bays have elevated concentrations of anthropogenic chemicals (Krahn et al. 1986). Several field and laboratory studies have provided considerable evidence that anthropogenic compounds present in contaminated sediments are probable causative agents for hepatic tumors, related lesions, and reproductive dysfunction (Myers et al. 1987, Johnson et al. 1989, Casillas et al. 1991). Thus, the stranding of a gray whale near Port Angeles, Washington, on the Strait of Juan de Fuca in 1984 heightened public concern that chemical contaminants in sediments may have been responsible for its death. Chemical analyses, conducted in our laboratory, of tissues (liver, blubber, kidney, brain) and stomach contents of this whale revealed that the concentrations of chlorinated hydrocarbons (CHs) such as polychlorinated biphenyls (PCBs), 1,1,1-trichloro-2,2-bis (p-chlorophenyl) ethanes (DDTs), and a number of toxic elements (e.g., mercury and lead) were at levels well below toxicological concern and also well below the concentrations reported in most cetaceans and pinnipeds (Wagemann and Muir 1984). The only exception was that the concentrations of aluminum were relatively high in both the liver and brain of this gray whale. It was not possible, however, to compare the results with published values. There is little information on a broad spectrum of contaminants in gray whale tissues. Wolman and Wilson (1970) reported the presence of DDT and its metabolites in 6 of 23 gray whales taken off of San Francisco, California, during their northern and southern migrations. The concentrations of DDTs, 1,1-dichloro-2,2-bis (p-chlorophenyl) ethanes (DDDs), and 1,1-dichloro-2,2-bis (p-chlorophenyl) ethenes (DDEs) in blubber of these whales ranged from 22 to 360 ng/g wet weight, whereas it was reported that liver did not contain any of these chlorinated pesticides. Schaffer et al. (1984) reported concentrations of DDTs of 470 ng/g wet weight in blubber of a gray whale sampled in southern California in 1976. Total PCBs were not detected in the blubber (<230 ng/g wet weight).
In recent years, a number of gray whales have stranded in Puget Sound, as noted above, raising, once again, the concern that chemical pollution may have played a role in their deaths. However, demonstrating a causal link between pollution and strandings of marine mammals is particularly difficult because of inherent problems of availability of a sufficient number of tissue samples from both healthy and stranded animals and the inability to conduct controlled laboratory studies with live animals, particularly the large marine mammals. In addition to these sampling and experimental difficulties, the lack of detailed information on the biology and migration patterns of gray whales makes it very difficult to make a definitive assessment of the role of chemical pollution in their mortality. Nevertheless, the stranding of marine mammals and the increased public and scientific awareness of the potential impact of anthropogenic chemicals make it imperative that this issue be evaluated using the best possible strategy and state-of-the-art methodologies.
There has been considerable controversy around the role of pollutants in the deaths of gray whales in Puget Sound (Calambokidis 1992). Primary factors that have been cited to support a link to pollutants in these deaths has been the poor condition of the liver in some of these animals, the bottom-feeding behavior of this species, and the presence of contaminants in stomach contents and tissues (Fouty 1984). The basis for most of these conclusions has been challenged (Calambokidis 1992), but in the absence of better information, the question of the role of contaminants has largely been unresolved.
In the case of the recent gray whale strandings, tissue samples were collected from a total of 22 animals stranded at locations in Puget Sound, along the Strait of Juan de Fuca and Strait of Georgia, along the outer Washington Coast, on Kodiak Island, Alaska, and in San Francisco Bay, California, from 1988 through 1991. These sites represent a wide range of chemical contamination in bottom sediment, from the relatively pristine Alaskan waters to the urbanized areas of Puget Sound and San Francisco Bay (Varanasi et al. 1989a). We obtained stomach contents, liver, and blubber tissues from many of these animals with the assumption that the chemical profiles of CHs and essential and toxic elements in the stomach contents would reflect the most recent exposure, and the profiles in liver and blubber would reflect longer-term bioaccumulation of contaminants. The results from analyses of these samples should provide some insight into the relationship, if any, between chemical contamination at the site of stranding and concentrations and profiles of selected contaminants in various tissues. Moreover, to determine whether a particular group of contaminants preferentially accumulated in specific organs such as brain or kidney, these organs were also analyzed.
In the present study, we included measurements of CHs, selected toxic and essential elements (e.g., mercury, lead, zinc, copper) and polycyclic aromatic contaminants (PACs), which consisted primarily of polycyclic aromatic hydrocarbons and the dibenzothiophenes (Table 1). Because CHs such as PCBs, DDTs and chlordanes are among the most widespread and persistent chemical contaminants in the near coastal environment (Varanasi et al. 1992b) and because of their lipophilicity and resistance to metabolism, these pollutants tend to bioaccumulate in aquatic organisms, particularly in lipid-rich tissues of marine mammals. Several toxic and essential elements were measured because of their toxicological significance and their possible accumulation in certain tissues of marine mammals. For example, mercury is nephrotoxic in mammals and it has been suggested that aluminum may alter brain function (Goyer 1986). Additionally, because gray whales feed on benthic organisms, a feeding strategy unique among baleen whales, stomach contents were analyzed for CHs, selected toxic and essential elements, and PACs to provide insight into sources and levels of these compounds available through diet. Further, because of the extensive metabolism by mammals and fish of contaminants such as the polycyclic aromatic hydrocarbons (Varanasi et al. 1992b and 1989b, Lee et al. 1972, Stegeman et al. 1981), the parent compounds generally are not detected in tissues, but may be present in the stomach contents of bottom feeding gray whales. Stomach contents consist of benthic invertebrates that do not efficiently biotransform PACs, as well as incidentally ingested sediment; the sediments from many urban areas contain elevated levels of parent PACs (Varanasi et al. 1989a).
Overall, the findings from this study showed that the concentrations of chemical contaminants in tissues of bottom feeding gray whales were substantially lower than the concentrations measured in certain pinnipeds and toothed cetaceans (Odontoceti) whose diets consist largely of fish. The findings also showed that there were no statistically significant region-specific differences in tissue concentrations or profiles of CHs and selected elements.