U.S. Dept Commerce/NOAA/NMFS/NWFSC/Tech Memos
NOAA-NMFS-NWFSC TM-29: Estuarine and Ocean Survival of Northeastern Pacific Salmon


ESTUARINE POLLUTION AND JUVENILE SALMON HEALTH:
POTENTIAL IMPACT ON SURVIVAL

E. Casillas, B. B. McCain, M. Arkoosh, and J. E. Stein

Environmental Conservation Division

Northwest Fisheries Science Center
2725 Montlake Blvd. E.
Seattle, WA 98112-2097

The marked declines in several Pacific Northwest salmon stocks are attributed to the cumulative effects of natural and anthropogenic factors. Although the relative contributions of these factors to changes in individual runs are not well understood, human impacts on the environment have contributed significantly to stock declines in many river systems. Human impacts on various life history stages of salmon in freshwater habitats include certain forest and agricultural practices, dams, water diversions, and urbanization. The addition of hatcheries to mitigate the human-induced losses of habitat has also been recently recognized as another potentially important factor affecting the survival of wild stocks of salmon. In the ocean, an important anthropogenic factor is harvesting, whereas natural environmental factors, including climatic changes, reduced food availability, and predation are the other forces thought to influence survival of juvenile and subadult salmon.

Estuaries serve as the natural linkage for salmon migrating between freshwater and ocean environments, providing the necessary habitat for their transition. Because of the urbanization of many coastal regions, estuaries located near urban centers are known to receive both point and nonpoint inputs of chemical contaminants from municipal and industrial activities. Many of the chemicals from these sources are known to accumulate in estuarine sediments (McCain et al. 1988), and a large number of these chemicals are bioaccumulated by sediment-dwelling organisms, including amphipods and copepods, which are important prey organisms for downstream migrant juveniles of certain salmonid species (McCain et al. 1990). As a result, pollution in urban estuaries is one anthropogenic factor that may influence the survival of juvenile salmon, whether directly in the estuary or subsequently in the nearshore ocean.

Recent studies in several urban estuaries, including San Francisco Bay, Elliott Bay and Commencement Bay in Puget Sound, and the Fraser River estuary in Vancouver, British Columbia, have shown that juvenile fall chinook salmon (Oncorhynchus tshawytscha) accumulate significant concentrations of chemical contaminants during their relatively short residence time. In studies conducted in urban estuaries in Puget Sound by our laboratory, we found evidence of exposure to high levels of polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs) (McCain et al. 1990, Stein et al. 1995). For example, we consistently found significantly elevated concentrations of fluorescent aromatic compounds (FACs) in bile of juvenile salmon from urbanized estuaries compared to concentrations in fish from nonurban estuaries (Fig. 1). Because fish extensively metabolize PAHs, the parent compounds do not accumulate in tissues but are found in the bile as metabolites (Varanasi et al. 1989). Measurement of these metabolites, quantified as FACs, provides an estimate of exposure of fish to PAHs (Krahn et al. 1986). Concentrations of PCBs in the liver of juvenile salmon were also significantly higher in fish from the urban estuaries compared to fish from hatcheries and nonurban estuaries. No significant differences in tissue levels of selected toxic metals were found in this study.

We have also demonstrated in field and laboratory studies that juvenile salmon from polluted environments exhibit abnormalities ranging from subcellular effects to changes in immune function and growth. In many cases the effects alter physiological processes, such that the potential for survival is reduced. As an example, chemically induced immunosuppression and the subsequent increased susceptibility to disease represent a serious problem to exposed animals. Immune dysfunction in mammals and fish has been recognized as a sublethal effect of chemical contaminant exposure affecting both cellular and humoral aspects of the immune system (McLeay and Gordon 1977, Dean et al. 1986, Arkoosh and Kaattari 1987, Rice and Weeks 1989, Thuvander 1989).

In our studies with juvenile salmon, immunocompetence was evaluated by analyzing the functional ability of leukocytes to produce an in vitro primary and secondary plaque-forming cell (PFC) response to a foreign antigen. This has been shown to be a very sensitive approach to evaluating the long-term chronic effects of exposure to chemical contaminants for short time periods (Arkoosh and Kattari 1987). We showed that leukocytes of juvenile salmon collected from hatcheries and from a nonurban estuary were able to generate a significantly higher secondary PFC response to a foreign antigen than that produced during the primary PFC response, which is the normal and expected response (Arkoosh et al. 1991). However, an enhanced secondary PFC response did not occur with leukocytes of juvenile salmon exposed to pollution from an urban estuary (Arkoosh et al. 1991) (Fig. 2).

Both PAHs and PCBs are known to induce immunoaltering effects in mammals (Ward et al. 1985, Dean et al. 1990), suggesting that PCBs or PAHs or both may be responsible for a suppressed PFC response to an antigen in juvenile salmon from the contaminated urban estuary. This hypothesis was supported by the results of our recent laboratory studies (Arkoosh et al. 1994). Juvenile chinook salmon were administered sublethal doses of PAHs and PCBs. The exposed fish exhibited suppression of their secondary PFC responses. Thus, an impaired secondary PFC response has been demonstrated in both field and laboratory studies, supporting the putative causal relationship between impaired immunity and chemical contaminant exposure in juvenile fall chinook salmon from polluted urban estuaries.

These physiological effects have recently been linked to increased susceptibility to disease. Infectious diseases are commonly suspected of contributing to mortality of juvenile salmon in estuarine and nearshore environments (Elliott et al. 1995). We collected juvenile fall chinook salmon from urban and nonurban estuaries, and from the respective releasing hatcheries, and exposed them in the laboratory to the marine pathogen Vibrio anguillarum. We found that juvenile chinook salmon from the contaminated estuary were more susceptible to V. anguillarum-induced mortality than fish from the corresponding hatchery (Fig. 3). In contrast, juvenile fall chinook salmon from the nonurban estuary were not more susceptible to V. anguillarum-induced mortality than the fish from the corresponding hatchery. The results of these initial disease challenges indicate that, in juvenile chinook salmon from an urban estuary, contaminant-associated immunodysfunction appears to lead to increased susceptibility to pathogenesis by a virulent marine bacterium. Similar findings were reported by Servizi et al. (1993) for outmigrating juvenile chinook salmon in the Fraser River estuary. In their laboratory based study evaluating the toxic effects of bleached kraft mill effluents, they observed an increased prevalence of bacterial kidney disease (a chronic bacterial infection of salmonids) in juveniles following a 212-day study simulating exposure to pollutants found in the Fraser River.

Immunosuppression and the subsequent increased susceptibility to disease are not the only potential deadly effects of exposure to chemical contaminants in urban estuaries. Effects on neuronal function and subsequently on behavior have been reported in juvenile salmonids exposed to 2-(thio-cyanomethylthio) benzothiazole (TCMTB), an antisapstain fungicide used to protect freshly cut lumber. Exposure of juvenile chinook salmon to TCMTB at levels comparable to exposures occurring in the Fraser River estuary increased susceptibility to predation by a natural marine predator, yellowtail rockfish (Sebastes flavidus) (Kruzynski and Birtwell 1994). Although the mechanisms and the linkages between exposure and biological effects are not fully delineated, the performance-based assessment on survival potential is ecologically relevant. The implication to survival of juvenile salmon in an environment at times of high predator densities is indicated by the study of Beamish and Neville (1995) showing that the potential impact of predation by lamprey on juvenile chinook salmon in the Fraser River estuary plume may reduce by a large percentage (nearly 50%) the recruitment potential of hatchery fish to harvest. Thus, increasing the chemical contaminant burden in urban estuaries may have even greater implications to the survival of a stock already depressed.

The findings presented here strongly indicate that, in addition to the myriad anthropogenic factors that can affect the survival of outmigrating juvenile fall chinook salmon in fresh water, the biological effects of chemical contaminants on these fish during their residency in certain urban estuaries can also potentially lead to reduced survival. Concomitant with the increased chemical exposure, juvenile chinook salmon inhabiting certain urban estuaries exhibit evidence of impairment of physiological processes such as immune system alterations, impaired growth (not described here), and behavioral changes. The assessment of the long-term effects of physiological changes induced by chemical pollution in urban estuaries on selected salmon stocks can be placed into context by using performance-based evaluations of effects at the level of the organism (Fig. 4). Overall, the findings from these recent studies provide evidence of linkage between the presence of elevated levels of complex mixtures of chemical contaminants in polluted estuaries and effects on health and survival of juvenile chinook salmon. Additional research is clearly needed to address the large gaps in understanding concerning the effects of oceanic factors on salmon survival. However, this recent evidence suggesting that outmigrant juvenile fall chinook salmon are experiencing sublethal effects from toxic chemical exposure during their residence in urbanized estuaries indicates the need to further investigate estuarine pollution as a contributing factor to declines in salmon stocks from urbanized watersheds.

Citations

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Arkoosh, M. R., E. Clemons, M. Myers, and E. Casillas. 1994. Suppression of B-cell mediated immunity in juvenile chinook salmon (Oncorhynchus tshawytscha) after exposure to either a polycyclic aromatic hydrocarbon or to polychlorinated biphenyls. Immunopharmacol. Immunotoxicol. 16:293-314.

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