- Email: [email protected]
Evidence of Strong Lake Trout Recruitment Despite High PCB (Total Aroclors) Concentrations
J. Great Lakes Res. 24(4):974-979 Internat. Assoc. Great Lakes Res., 1998
NOTE Evidence of Strong Lake Trout Recruitment Despite High PCB (Total Aroclors) Concentrations Daniel W. Smith*
Conestoga Rovers & Associates 559 W Uwchlan Ave., Suite 120 Exton, Pennsylvania 19341 ABSTRACT. Lake trout in New York's Canadice Lake have exhibited strong natural recruitment despite total PCB concentrations four to seven times those recently found in lake trout from the Great Lakes. In contrast, lake trout recruitment has been significantly impacted in Lakes Ontario, Michigan, and Huron. This evidence is inconsistent with the hypothesis that PCBs caused the failure of lake trout recruitment in the Great Lakes over the last two decades. A limitation of this conclusion is that PCBs in Canadice Lake lake trout were quantitated only as total Aroclors. It is possible that Canadice Lake PCBs have a relatively low toxicity per unit PCB. On the other hand, in contrast to most data suggesting impacts of PCBs on recruitment, the Canadice Lake data are from a natural population in a natural system, and include the suite of natural biotic and abiotic factors, lethal and sub-lethal, affecting lake trout recruitment throughout the fish's life-cycle. INDEX WORDS:
Lake trout, recruitment, PCB, dioxin, Great Lakes
INTRODUCTION
tario) where trout have high PCB concentrations, and early life stage mortality sometimes correlates significantly with high PCB concentrations (Mac et al. 1993.) In addition, PCBs exert dioxin-like toxicity, and lake trout are very sensitive to this kind of toxicity (Walker et al. 1991). PCBs are also thought to pose the primary toxicity to other fish and wildlife (Giesy et al. 1994, 1995). However, in a detailed review, Fitzsimons (l995a) concluded that PCBs were not likely to be the causal agent behind recruitment failure in the Great Lakes. Critical evaluation of the chemical-causation hypothesis is complicated for the following reasons. PCBs were used in a wide variety of industrial processes and products; consequently, high concentrations of PCBs in Great Lakes fish tend to cooccur with high levels of industry and human population density in a Great Lake's watershed. High human population densities, in turn, tend to correlate with other anthropogenic stressors also important to lake trout populations. Thus, Great Lakes with higher concentrations of PCBs also tend to have higher levels of eutrophication, fishing
Attempts over the last two decades to rehabilitate the lake trout (Salvelinus namaycush) populations of Lakes Ontario, Michigan, Huron, and Erie remain largely unsuccessful. Despite excellent growth of stocked adults and the production of viable eggs and fry by feral fish in the laboratory and in the field, little to no natural recruitment currently occurs in any of these lakes (Schneider et al. 1990, 1991; Holey et al. 1995), although significant numbers of naturally recruited fingerlings have been observed in Lake Ontario in the last 5 years. A predominant explanation for recruitment failure is that organochlorines are precluding recruitment due to mortality in early life stages (Mac and Edsal 1991, EPA 1993, Mac et al. 1993, Zint et al. 1995, Colborn et al. 1996). Of potential causal chemicals, PCBs are often cited as most likely. Recruitment failure tends to occur in Great Lakes (Huron, Michigan, and On-
'Corresponding author. E-mail: [email protected]
974
Strong Lake Trout Recruitment Despite High PCB-Levels pressure, and inputs of other industrial chemicals and conventional pollutants such as nutrients and suspended sediments. Since these other stressors are jointly and sometimes solely sufficient to cause recruitment failure in the absence of high PCBs (Environment Canada 1991a,b; Evans et ai. 1991; Sly 1991; Schneider et ai. 1991), the relationship between high concentrations of PCBs and failure of lake trout recruitment in the Great Lakes is confounded by multiple alternative hypotheses. Canadice Lake, the smallest of New York's Finger Lakes, offers a test of the impacts of moderately high concentrations of PCBs in the absence of most other confounding factors. Canadice Lake has native lake trout populations whose population dynamics have been routinely monitored by the New York Department of Environmental Conservation (NYDEC) since 1970. Despite being remote and unaffected by agriculture, industry, or municipal waste, routine monitoring by NYDEC in the early 1980s led to the discovery of high concentrations of PCBs (10 mg/kg and higher) in adult lake trout from Canadice Lake. The lake was apparently contaminated with PCB-containing transformer oil by an individual who was dismantling transformers in the watershed (personal communication, Bruce Finster, NYDEC). The transformer oil containing the PCBs was apparently dumped into a nearby tributary from which it ran into Canadice Lake. NYDEC has not been able to determine exactly when the contamination occurred, although they believe it occurred sometime in the late 1970s. NYDEC sampling of Canadice Lake lake trout in 1975 showed very low concentrations of PCBs (Spagnoli and Skinner 1977). The objective of the following analysis is to compare PCB concentrations and recruitment success in Canadice Lake to that observed for lake trout from the Great Lakes.
METHODS AND DATA SOURCES PCBs in lake trout from Canadice Lake have been monitored since 1984 by NYDEC. Data on chemicals in lake trout were kindly supplied by NYDEC (personal communication, Ron Sloan, NYDEC). As per usual NYDEC methods (Spagnoli and Skinner 1977), PCBs were quantitated as total Aroclors in fillets with skin. The PCBs found in Canadice Lake lake trout are primarily Aroclors 1254 and 1260. PCB concentrations in Lake Ontario lake trout were obtained from NYDEC's sampling of Lake Ontario (NYDEC 1994). The Lake Ontario data are for composites of same age fish.
975
PCB concentrations in lake trout from Lakes Michigan and Huron were obtained from the Michigan Department of Natural Resources (MDNR), kindly supplied by Robert Day. Both MDNR and NYDEC analyze lake trout fillets with skins, controlling for tissue types across lakes.
RESULTS AND DISCUSSION Since the first sample in 1984, PCB concentrations in Canadice Lake trout have fallen at a rate of about 15% per year, attesting to the efficacy of NYDEC's investigation and clean-up of the source areas (Fig. 1). However, concentrations in large adult lake trout fillets were very high in 1984 and remained above 3 mg/kg in 1990. As mean length at maturation is about 60 cm (Abraham 1993), first maturing females from Canadice Lake averaged about 6.0, 3.5, and 2.5 mglkg PCBs in fillets with skins in 1984, 1988, and 1990, respectively. In 1984, fillets of large trout had PCB concentrations above 10 mg/kg (Fig. 1). According to data presented in NYDEC (1994), the "standard fillet" with skins analyzed by NYDEC has about 60% of the PCB concentrations of whole fish. Whole fish concentrations were, therefore, likely about 167% of those depicted in Figure 1. PCB concentrations in Canadice Lake trout in 1984 were generally higher, on a lipid normalized basis, than PCB concentrations found in similar sized lake trout from the Great Lakes throughout the 1980s and 1990s (DeVault et ai. 1996). Recent concentrations of PCBs in fillets from similar-sized lake trout from Lakes Michigan, Huron, and Ontario are considerably lower than those found in Canadice Lake. Data reported for Lake Ontario in 1989 indicate that 60 cm lake trout would have had an estimated 1.5 mg/kg total PCBs in fillets with skins (NYDEC 1994). More recent data from Lake Michigan (1995) and Lake Huron (1996) indicate that 60 cm lake trout had 1 mg/kg and 0.8 mg/kg, respectively, in fillets. In 1984, PCB concentrations in Canadice Lake trout were about 4, 6, and 7.5 times concentrations recently observed in trout from Lakes Ontario, Michigan, and Huron, respectively (Fig. 2). The Great Lakes concentrations depicted in Figure 2 are most recent PCB concentrations co-incident with widespread recruitment failure. Despite these relatively high concentrations of PCBs in Canadice Lake, recruitment of naturally spawned fish continued throughout the 1970s and 1980s (Abraham 1993, 1994), and natural recruitment was described
Daniel W; Smith
976
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FIG. 1. PCBs in lake trout fillets from Canadice Lake versus fish length for 1984, 1987, and 1990. Also included are best-fit log-linear regressions for each year.
as "strong" during the early 1980s when PCB concentrations were highest (Abraham 1994). This assessment of strong natural recruitment was based on the following information. From 1981 onward, about 7.9 spring yearlings and 15.0 fall fingerling lake trout per hectare were stocked into Canadice Lake. Subsequent sampling suggested that fall fingerling were about 7.5 times less likely to survive than fish stocked as yearlings, probably due to predation by adult salmonids (Abraham 1993, 1994); thus, the stocking rate was equivalent to about 10 yearlings per hectare. This rate of stocking was estimated to be sufficient to sustain the stocks in the absence of natural recruitment. Despite this stocking, naturally recruited lake trout were about three times more common than stocked fish in a 1987 gillnetting (Table 1). Observed nat-
45
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Length, em
FIG. 2. PCBs vs. length, in lake trout fillets from Canadice Lake and Lakes Ontario, Michigan, and Huron. Canadice data are from 1984, Lake Ontario data are from 1989, and Lake Michigan and Lake Huron data are from 1996. Also, included are best-fit log-linear regressions. Data from Great Lakes are most recent data corresponding to periods ofgeneral recruitment failure, while Canadice Lake concentrations are the highest concentrations, from 1984, corresponding with strong natural recruitment.
ural recruitment in the early 1980s was equivalent to a stocking of about 30 yearling lake trout per ha. Consequently, Canadice Lake presents a seminatural experiment whose results are inconsistent with the hypothesis that high levels of PCBs and dioxin-like chemicals have noticeably impacted lake trout in the Great Lakes, as suggested by other works (Fitzsimons 1995a). A potential limitation of the Canadice Lake information is that the pattern of PCB congeners may vary from site to site. Although the PCBs in Lake Michigan and Lake Ontario, as with Canadice Lake, are identified as
Strong Lake Trout Recruitment Despite High PCB-Levels TABLE l. Origin of Lake Trout sampled from Canadice Lake in 1987. Data from NYDEC sampling (Abraham 1993). Age 1 2 3 4 5 6 7 8 9 10 11
12
Year Class
Hatchery Fish
Wild Recruits
1986 1985 1984 1983 1982 1981 1980 1979 1978 1977 1976 1975
2 3 4 18 6 4
0 3 31 27 24 20 12 5 3 3 3 1
* * * * * *
* No fish were stocked in 1975 to
1980.
primarily Aroclors 1254 and 1260 (Williams et ai. 1989, NYDEC 1994), the PCBs in Canadice Lake might have a different toxicological potential than the PCBs in the Great Lakes. It is also important to note that PCBs contribute only about one fifth of the total dioxin toxicity in Lake Ontario, with the rest posed by dioxin and furans (Guiney et ai. 1996). Dioxins and furans may also pose significant additional toxicity to trout from Lakes Huron and Michigan (Cook et ai. 1997). Because of these limitations, the Canadice Lake data set cannot be seen as conclusive disproof of the importance of dioxinlike molecules to recruitment failure. However, dioxin toxicity is probably not a good explanation for recruitment failure (Fitzsimons 1995a). Total dioxin equivalents in Great Lakes lake trout eggs have generally been below concentrations that cause mortality in laboratory experiments (Smith 1994, Fitzsimons 1995a, Guiney et ai. 1996). Consistent with this, blue-sac disease, the lesion specific to dioxin-like toxicity, has not been detected in ecologically significant levels in fry spawned from Great Lakes fish for about two decades (Symula et ai. 1990, Fitzsimons 1995a). Moreover, in the only instance in which ecologically significant levels of blue sac did occur-a brief period in the 1970s associated with eggs spawned from feral Lake Ontario trout-the mortality due to blue-sac was suppressed at low water temperatures (Symula et ai. 1990). In contrast, mortality due to blue-sac syndrome induced by dioxin in laboratory experiments (Guiney et ai. 1996) was not affected by water temperature.
977
The Canadice Lake analyses are more applicable to hypotheses concerning non-dioxin toxicity of total PCBs. Analyses of lake trout eggs spawned in the laboratory sometime shows significant correlation between concentrations of PCBs and egg and fry mortality due to factors other than the dioxinspecific lesion, blue-sac disease (Mac and Edsall 1991, Mac and Scwartz 1992, Mac et ai. 1993). The Canadice Lake data set offers evidence that nondioxin toxicity of PCBs is not the cause of recruitment failure in the Great Lakes. At the least, the Canadice Lake data set demonstrates that any correlation between recruitment failure and moderately high body burdens of total Aroclors is not strong evidence of impacts of PCBs. Despite the limitations of the PCB quantitation technique, the Canadice Lake data set has important advantages over much other work on potential chemical impacts on lake trout recruitment. The Canadice Lake data are from a natural system and include the panoply of natural factors-predation, competition, and abiotic factors that cause lethal and non-lethal effects-that affect recruitment of all life-stages. As such, the real world data from Canadice Lake have advantages over work studying small intervals of the lake trout life-cycle conducted in the artificial environments of egg trays in cold rooms (Mac et ai. 1993, Walker et ai. 1991). Similarly, in contrast to the situation in Lakes Michigan, Huron, and Ontario, the observation of strong lake trout recruitment with moderately high PCB concentrations is generally consistent with analyses on eggs spawned in the laboratory from those Great Lakes (Fitzsimons 1995a). These experiments have rather consistently shown that maternal PCB levels less than about 6 to 10 mglkg (= egg burdens less than about 2 to 3 mg/kg = fillet with skin concentrations of about 4 to 6 mg/kg) have no discernible effect on egg or fry mortality (Stauffer 1979, Berlin et ai. 1981, Mac et ai. 1981, Mac and Schwartz 1992, Mac et ai. 1993, Fitzsimons 1995a). In his detailed review of early life stage mortality, Fitzsimons (l995a) concluded that laboratory data would suggest even higher no adverse effect levels, about 25 mg/kg of PCBs in eggs, suggesting safe adult female concentrations three to four times that concentration. In addition to impacts of chemicals like PCBs, numerous alternative hypotheses exist to explain recruitment failure of lake trout in the Great Lakes: lamprey predation (Schneider et ai. 1991), overfishing (Holey et al. 1995), vitamin deficiencies associated with alewife consumption (Fitzsimons 1995b),
978
Daniellv. Smith
incompatibility of stocked strains with local conditions (Burnham-Curtis et al. 1995), and predation on emerging fry by exotic bait fish such as alewives (Krueger et al. 1995) and smelt (Abraham 1993). Besides providing evidence contrary to the chemical causation hypothesis, the Canadice Lake information supports the hypothesis that predation on lake trout fry by exotic bait fish is suppressing recruitment. Although natural recruitment was "strong" throughout the 1980s, there was suppression of natural recruitment in the late 1970s. NYDEC attributed this reduced recruitment to predation of young lake trout by high numbers of forage fish-smelt and alewives-which had invaded the lake and reached high levels during the late 1970s (Abraham 1993). Based on their working hypothesis, NYDEC stocked the lake with brown, rainbow, and lake trout in the early 1980s specifically to reduce the densities of forage fish. Subsequent to this stocking, and arguably because of the resulting predation pressure on the smelt, "strong" natural recruitment of lake trout resumed by the mid 1980s. In summary, Canadice Lake has had strong natural recruitment of lake trout despite PCB (total Aroclors) body burdens generally higher than those found in Great Lakes lake trout since 1980, and 4 to 7 times body burdens found more recently in Great Lakes trout during periods of general recruitment failure. While the observation of strong natural recruitment does not preclude the existence of any PCB effect on recruitment, the data indicate that moderately high body burdens of total Aroclors are not a sufficient explanation for the failure of lake trout recruitment in the Great Lakes. ACKNOWLEDGMENTS I thank members of the NYDEC, especially Bill Abraham, Ron Sloan, Bruce Finster, and Cliff Schneider who were so generous with their time and information. I also thank Ruth Anderson, Steve Jones, Randy Eshenroder, and three external peer reviewers (Carol Edsall, Dave De Vault, and an anonymous reviewer) for providing additional helpful review. REFERENCES Abraham, W. J. 1993. Results of the 1987 lake trout assessment netting in Canadice Lake. Unpublished report of NY Department of Environmental Conservation, Region 8 Fisheries Management Unit, June 1993.
___ . 1994. 1990 lake trout assessment report for Canadice Lake, Ontario County. Unpublished report of NY Department of Environmental Conservation, Region 8 Fisheries Management Unit. Berlin, W. H., Hesselberg, R. J., and Mac, M. P. 1981. Growth and mortality of fry of Lake Michigan lake trout during chronic exposure to PCBs and DDE. In Chlorinated hydrocarbons as a factor in the reproduction and survival of lake trout in Lake Michigan, US Fish and Wildlife Service Technical paper #105. Burnham-Curtis, M. K., Kreuger, C. c., Schreiner, D. R., Johnson, J. E., Stewart, T. J., Horral, R. M., MacCallum, W. R., Kenyon, R., and Lange. R. E. 1995. Genetic strategies for lake trout rehabilitation: A synthesis. 1995. J. Great Lakes. Res. 21 (Supplement 1): 477-486. Colborn, T., Dumanoski, D., and Myers, J. P. 1996. Our Stolen Future: Are We Threatening our Fertility, Intelligence, and Survival-A Scientific Detective Story. New York, New York: Penguin Group. Cook, P. M., Zabel, E. W., and Peterson, R. E. 1997. The TCDD toxicity equivalence approach for characterizing risks for early life-stage mortality in trout. In Chemically Induced Alterations in Functional Development and Reproduction in Fishes, eds. R. M. Rolland, M. Gilberson, and R. E. Peterson, pp. 9-27. SETAC Technical Publications. De Vault, D S., Hesselberg, R., Rodgers, P.W., and Feist, T. J. 1996. Contaminant trends in lake trout and walleye from the Laurentian Great Lakes. J. Great Lakes Res. 22: 884-895. Environment Canada. 1991 a. Toxic Chemicals in the Great Lakes and Associated Effects. Vol. 1. Contaminant Levels and Trends. Environmental Canada, Department of Fisheries and Oceans, Health and Welfare Canada. _ _ . 1991b. Toxic Chemicals in the Great Lakes and Associated Effects: Volume II-Effects. Environmental Canada, Department of Fisheries and Oceans, Health and Welfare Canada. EPA. 1993. The Great Lakes Water Quality Guidance: Proposed Rule. U.S. Federal Register 58: 20800-21046. Evans, D.O., Brisbane, J., Casselman, J. M., Coleman, K. E., Lewis, C. A., Sly, P. G., Wales, D. L., and Wilcox, C. C. 1991. Anthropogenic stressors and diagnosis of their effects on lake trout populations in Ontario lakes. Report of the Lake Trout Synthesis: Response to Stress Working Group. Ontario Ministry of Natural Resources. Fitzsimons, J. D. 1995a. A critical review of the effects of contaminants on early life stage (ELS) mortality of lake trout in the Great Lakes. J. Great Lakes. Res. 21 (Supplement 1): 267-276. _ _ . 1995b. The effect of B-vitamins on swim-up syndrome in Lake Ontario lake trout. J. Great Lakes Res. 21 (Supplement 1): 286-289.
Strong Lake Trout Recruitment Despite High PCB-Levels Giesy, J.P., Verbrugge, D.A., Othout, R.A., Bowerman, W.W., Mora, M.A., Jones, P.D., Newsted, J.L., Vandervoort, C., Heaton, S.N., Aulerich, R.J., Bursian, S.J., Ludwig, J.P., Dawson, G.A., Kubiak, T.J., Best, D.A., and Tillitt, D.E. 1994. Contaminants in fishes from Great Lakes-influenced sections and above dams of three Michigan rivers. II. Implications for health of mink. Arch. Environ. Contam. Toxicol. 27:213-223. ___ , Bowerman, W.W., Mora, M.A., Verbrugge, D.A., Othoudt, R.A., Newsted, J.L., Summer, e.L., Aulerich, R.J., Bursian, S.J., Ludwig, J.P., Dawson, G.A., Kubiak, T.J., Best, D.A., and TiJlitt, D.E. 1995. Contaminants in fishes from Great Lakes-influenced sections and above dams of three Michigan rivers: III. Implications for health of bald eagles. Arch. Environ. Contam. Toxicol. 29:309-321. Guiney, P.D., Cook, P. M., Casselman, J. M., Fitzsimon, J. F., Simonin, H. A., Zabel, E. W., and Peterson, R. E. 1996. Assessment of 2,3,7,8-tetrachlorodibenzo-pdioxin induced sac fry mortality in lake trout (Salvelinus namaycush) from different regions of the Great Lakes. Can. 1. Fish. Aquat. Sci. 53: 2080-2092. Holey, M., Rybicki, R., Eck, G.W., Brown, E. H., Marsden, J. E., Lavis, D.S., Toneys, M. L., Trudeau, R. N., and Horrall, R. M. 1995. Progress toward lake trout restoration in Lake Michigan. 1. Great Lakes. Res. 21 (Supplement 1): 128-151.. Kreuger, e. e., Perkins, D. L., Mills, E. L., and Marsden, J. E. 1995. Predation by alewives on lake trout fry in Lake Ontario: role of exotic species in preventing restoration. J. Great Lakes. Res. 2 I (Supplement 1): 458-469. Mac, M. J., and Edsall, e.e. 1991. Environmental contaminants and the reproductive success of lake trout in the Great Lakes: An epidemiological approach. J. Tox. Environ. Health, 33:375-394. _ _ , and Schwartz, T. R. 1992. Investigations into the effects of PCB congeners on reproduction in lake trout from the Great Lakes. Chemosphere 1-2: 189-192. _ _ , Berlin, W. H., and Rottiers, D.V. 1981. Comparative hatchability of Lake trout eggs differing in containant burden and incubation conditions. In Chlorinated hydrocarbons as a factor in the reproduction and survival of lake trout in Lake Michigan. US Fish and Wildlife Service Technical paper #105. _ _ , Schwartz, T. R., Edsall, C. e., and Frank, A. M. 1993. Polychlorinated biphenyl in Great Lakes lake trout and their eggs: relations to survival and congener composition 1979-1988. J. Great Lakes. Res. 19:753-765.
979
NYDEC 1994. Niagara River Remedial Action Plan. New York Department of Environmental Conservation, September, 1994. Schneider, e. P., Eckert, T. H., Elrod, J. H., O'Gorman, R., Owens, R. W., Schaner, T., Grewe, P., Perkins D., and Krueger, C. e. 1990. Lake Ontario Committee Report, Lake Trout Rehabilitation in Lake Ontario, 1990. New York State Department of Environmental Conservation. _ _ , Schaner, T., Marsden, J. E., and Busch, W.-D. N. 1991. Lake Ontario Lake Trout Rehabilitation Plan, 1990 Revision. Lake Ontario Committee Great Lakes Fishery Commission. Sly, P. G. 1991. The effects of land use and cultural development on the Lake Ontario ecosystem since 1750. Hydrobiologia 213: 1-75. Smith, D. W. 1994 Dioxin impacts on Great Lakes Ecosystems: A Tale of TCDs. Presentation at 15th annual meeting of SETAC, Denver, 1994. Spagnoli, J. J., and Skinner, L. e. 1977. PCBs in fish from selected waters of New York State. 1. Pest. Monitor. 11: 69-87. Stauffer, T. M. 1979. Effects of DDT and PCBs on the survival of lake trout eggs and fry in a hacthery and in Lake Michigan, 1973-1976. Trans. Am. Fish. Soc. 108: 178-186. Symu1a, 1., Meade, M., Skea, M.e., Cummings, 1., Colquhoun, J.R., Dean, H.J., and Miccoli, J. 1990. Blue sac disease in Lake Ontario lake trout. J. Great Lakes Res. 16: 41-52. Walker, M. K., Spitzbergen, J. M, Olson, J. R., and Peterson, R. E. 1991. 2,3,7,8,-tetrachlordibenzodioxin (TCDD) toxicity during early life stages of lake trout (Salve1inus namaycush). Can. J. Fish. Aquat. Sci. 48: 875-883. Williams, L.L., Giesy, J.P., DeGa1an, N., Verbrugge, D.A., Tillitt, D., and Ankley, G.T. 1989. Size and seasonal variations of PCBs in chinook salmon (Oncorhynchus tshawytscha) fillets from Lake Michigan near Ludington, Michigan, USA. Michigan Sea Grant Publication MICHU-SG-89-202. Zint, M.T., Taylor, W.W., Carl, L., Edsall, C.C., Heinrich, J., Sippel, A., Lavis, D., and Schaner, T. 1995. Do toxic substances pose a threat to rehabilitation of lake trout in the Great Lakes? A review of the literature. J. Great Lakes Res. 21 (Supplement 1):530-546.
Submitted: 17 April 1997 Accepted: 21 August 1998 Editorial handling: Thomas J. Murphy
NOTE Evidence of Strong Lake Trout Recruitment Despite High PCB (Total Aroclors) Concentrations Daniel W. Smith*
Conestoga Rovers & Associates 559 W Uwchlan Ave., Suite 120 Exton, Pennsylvania 19341 ABSTRACT. Lake trout in New York's Canadice Lake have exhibited strong natural recruitment despite total PCB concentrations four to seven times those recently found in lake trout from the Great Lakes. In contrast, lake trout recruitment has been significantly impacted in Lakes Ontario, Michigan, and Huron. This evidence is inconsistent with the hypothesis that PCBs caused the failure of lake trout recruitment in the Great Lakes over the last two decades. A limitation of this conclusion is that PCBs in Canadice Lake lake trout were quantitated only as total Aroclors. It is possible that Canadice Lake PCBs have a relatively low toxicity per unit PCB. On the other hand, in contrast to most data suggesting impacts of PCBs on recruitment, the Canadice Lake data are from a natural population in a natural system, and include the suite of natural biotic and abiotic factors, lethal and sub-lethal, affecting lake trout recruitment throughout the fish's life-cycle. INDEX WORDS:
Lake trout, recruitment, PCB, dioxin, Great Lakes
INTRODUCTION
tario) where trout have high PCB concentrations, and early life stage mortality sometimes correlates significantly with high PCB concentrations (Mac et al. 1993.) In addition, PCBs exert dioxin-like toxicity, and lake trout are very sensitive to this kind of toxicity (Walker et al. 1991). PCBs are also thought to pose the primary toxicity to other fish and wildlife (Giesy et al. 1994, 1995). However, in a detailed review, Fitzsimons (l995a) concluded that PCBs were not likely to be the causal agent behind recruitment failure in the Great Lakes. Critical evaluation of the chemical-causation hypothesis is complicated for the following reasons. PCBs were used in a wide variety of industrial processes and products; consequently, high concentrations of PCBs in Great Lakes fish tend to cooccur with high levels of industry and human population density in a Great Lake's watershed. High human population densities, in turn, tend to correlate with other anthropogenic stressors also important to lake trout populations. Thus, Great Lakes with higher concentrations of PCBs also tend to have higher levels of eutrophication, fishing
Attempts over the last two decades to rehabilitate the lake trout (Salvelinus namaycush) populations of Lakes Ontario, Michigan, Huron, and Erie remain largely unsuccessful. Despite excellent growth of stocked adults and the production of viable eggs and fry by feral fish in the laboratory and in the field, little to no natural recruitment currently occurs in any of these lakes (Schneider et al. 1990, 1991; Holey et al. 1995), although significant numbers of naturally recruited fingerlings have been observed in Lake Ontario in the last 5 years. A predominant explanation for recruitment failure is that organochlorines are precluding recruitment due to mortality in early life stages (Mac and Edsal 1991, EPA 1993, Mac et al. 1993, Zint et al. 1995, Colborn et al. 1996). Of potential causal chemicals, PCBs are often cited as most likely. Recruitment failure tends to occur in Great Lakes (Huron, Michigan, and On-
'Corresponding author. E-mail: [email protected]
974
Strong Lake Trout Recruitment Despite High PCB-Levels pressure, and inputs of other industrial chemicals and conventional pollutants such as nutrients and suspended sediments. Since these other stressors are jointly and sometimes solely sufficient to cause recruitment failure in the absence of high PCBs (Environment Canada 1991a,b; Evans et ai. 1991; Sly 1991; Schneider et ai. 1991), the relationship between high concentrations of PCBs and failure of lake trout recruitment in the Great Lakes is confounded by multiple alternative hypotheses. Canadice Lake, the smallest of New York's Finger Lakes, offers a test of the impacts of moderately high concentrations of PCBs in the absence of most other confounding factors. Canadice Lake has native lake trout populations whose population dynamics have been routinely monitored by the New York Department of Environmental Conservation (NYDEC) since 1970. Despite being remote and unaffected by agriculture, industry, or municipal waste, routine monitoring by NYDEC in the early 1980s led to the discovery of high concentrations of PCBs (10 mg/kg and higher) in adult lake trout from Canadice Lake. The lake was apparently contaminated with PCB-containing transformer oil by an individual who was dismantling transformers in the watershed (personal communication, Bruce Finster, NYDEC). The transformer oil containing the PCBs was apparently dumped into a nearby tributary from which it ran into Canadice Lake. NYDEC has not been able to determine exactly when the contamination occurred, although they believe it occurred sometime in the late 1970s. NYDEC sampling of Canadice Lake lake trout in 1975 showed very low concentrations of PCBs (Spagnoli and Skinner 1977). The objective of the following analysis is to compare PCB concentrations and recruitment success in Canadice Lake to that observed for lake trout from the Great Lakes.
METHODS AND DATA SOURCES PCBs in lake trout from Canadice Lake have been monitored since 1984 by NYDEC. Data on chemicals in lake trout were kindly supplied by NYDEC (personal communication, Ron Sloan, NYDEC). As per usual NYDEC methods (Spagnoli and Skinner 1977), PCBs were quantitated as total Aroclors in fillets with skin. The PCBs found in Canadice Lake lake trout are primarily Aroclors 1254 and 1260. PCB concentrations in Lake Ontario lake trout were obtained from NYDEC's sampling of Lake Ontario (NYDEC 1994). The Lake Ontario data are for composites of same age fish.
975
PCB concentrations in lake trout from Lakes Michigan and Huron were obtained from the Michigan Department of Natural Resources (MDNR), kindly supplied by Robert Day. Both MDNR and NYDEC analyze lake trout fillets with skins, controlling for tissue types across lakes.
RESULTS AND DISCUSSION Since the first sample in 1984, PCB concentrations in Canadice Lake trout have fallen at a rate of about 15% per year, attesting to the efficacy of NYDEC's investigation and clean-up of the source areas (Fig. 1). However, concentrations in large adult lake trout fillets were very high in 1984 and remained above 3 mg/kg in 1990. As mean length at maturation is about 60 cm (Abraham 1993), first maturing females from Canadice Lake averaged about 6.0, 3.5, and 2.5 mglkg PCBs in fillets with skins in 1984, 1988, and 1990, respectively. In 1984, fillets of large trout had PCB concentrations above 10 mg/kg (Fig. 1). According to data presented in NYDEC (1994), the "standard fillet" with skins analyzed by NYDEC has about 60% of the PCB concentrations of whole fish. Whole fish concentrations were, therefore, likely about 167% of those depicted in Figure 1. PCB concentrations in Canadice Lake trout in 1984 were generally higher, on a lipid normalized basis, than PCB concentrations found in similar sized lake trout from the Great Lakes throughout the 1980s and 1990s (DeVault et ai. 1996). Recent concentrations of PCBs in fillets from similar-sized lake trout from Lakes Michigan, Huron, and Ontario are considerably lower than those found in Canadice Lake. Data reported for Lake Ontario in 1989 indicate that 60 cm lake trout would have had an estimated 1.5 mg/kg total PCBs in fillets with skins (NYDEC 1994). More recent data from Lake Michigan (1995) and Lake Huron (1996) indicate that 60 cm lake trout had 1 mg/kg and 0.8 mg/kg, respectively, in fillets. In 1984, PCB concentrations in Canadice Lake trout were about 4, 6, and 7.5 times concentrations recently observed in trout from Lakes Ontario, Michigan, and Huron, respectively (Fig. 2). The Great Lakes concentrations depicted in Figure 2 are most recent PCB concentrations co-incident with widespread recruitment failure. Despite these relatively high concentrations of PCBs in Canadice Lake, recruitment of naturally spawned fish continued throughout the 1970s and 1980s (Abraham 1993, 1994), and natural recruitment was described
Daniel W; Smith
976
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FIG. 1. PCBs in lake trout fillets from Canadice Lake versus fish length for 1984, 1987, and 1990. Also included are best-fit log-linear regressions for each year.
as "strong" during the early 1980s when PCB concentrations were highest (Abraham 1994). This assessment of strong natural recruitment was based on the following information. From 1981 onward, about 7.9 spring yearlings and 15.0 fall fingerling lake trout per hectare were stocked into Canadice Lake. Subsequent sampling suggested that fall fingerling were about 7.5 times less likely to survive than fish stocked as yearlings, probably due to predation by adult salmonids (Abraham 1993, 1994); thus, the stocking rate was equivalent to about 10 yearlings per hectare. This rate of stocking was estimated to be sufficient to sustain the stocks in the absence of natural recruitment. Despite this stocking, naturally recruited lake trout were about three times more common than stocked fish in a 1987 gillnetting (Table 1). Observed nat-
45
55
65
75
85
Length, em
FIG. 2. PCBs vs. length, in lake trout fillets from Canadice Lake and Lakes Ontario, Michigan, and Huron. Canadice data are from 1984, Lake Ontario data are from 1989, and Lake Michigan and Lake Huron data are from 1996. Also, included are best-fit log-linear regressions. Data from Great Lakes are most recent data corresponding to periods ofgeneral recruitment failure, while Canadice Lake concentrations are the highest concentrations, from 1984, corresponding with strong natural recruitment.
ural recruitment in the early 1980s was equivalent to a stocking of about 30 yearling lake trout per ha. Consequently, Canadice Lake presents a seminatural experiment whose results are inconsistent with the hypothesis that high levels of PCBs and dioxin-like chemicals have noticeably impacted lake trout in the Great Lakes, as suggested by other works (Fitzsimons 1995a). A potential limitation of the Canadice Lake information is that the pattern of PCB congeners may vary from site to site. Although the PCBs in Lake Michigan and Lake Ontario, as with Canadice Lake, are identified as
Strong Lake Trout Recruitment Despite High PCB-Levels TABLE l. Origin of Lake Trout sampled from Canadice Lake in 1987. Data from NYDEC sampling (Abraham 1993). Age 1 2 3 4 5 6 7 8 9 10 11
12
Year Class
Hatchery Fish
Wild Recruits
1986 1985 1984 1983 1982 1981 1980 1979 1978 1977 1976 1975
2 3 4 18 6 4
0 3 31 27 24 20 12 5 3 3 3 1
* * * * * *
* No fish were stocked in 1975 to
1980.
primarily Aroclors 1254 and 1260 (Williams et ai. 1989, NYDEC 1994), the PCBs in Canadice Lake might have a different toxicological potential than the PCBs in the Great Lakes. It is also important to note that PCBs contribute only about one fifth of the total dioxin toxicity in Lake Ontario, with the rest posed by dioxin and furans (Guiney et ai. 1996). Dioxins and furans may also pose significant additional toxicity to trout from Lakes Huron and Michigan (Cook et ai. 1997). Because of these limitations, the Canadice Lake data set cannot be seen as conclusive disproof of the importance of dioxinlike molecules to recruitment failure. However, dioxin toxicity is probably not a good explanation for recruitment failure (Fitzsimons 1995a). Total dioxin equivalents in Great Lakes lake trout eggs have generally been below concentrations that cause mortality in laboratory experiments (Smith 1994, Fitzsimons 1995a, Guiney et ai. 1996). Consistent with this, blue-sac disease, the lesion specific to dioxin-like toxicity, has not been detected in ecologically significant levels in fry spawned from Great Lakes fish for about two decades (Symula et ai. 1990, Fitzsimons 1995a). Moreover, in the only instance in which ecologically significant levels of blue sac did occur-a brief period in the 1970s associated with eggs spawned from feral Lake Ontario trout-the mortality due to blue-sac was suppressed at low water temperatures (Symula et ai. 1990). In contrast, mortality due to blue-sac syndrome induced by dioxin in laboratory experiments (Guiney et ai. 1996) was not affected by water temperature.
977
The Canadice Lake analyses are more applicable to hypotheses concerning non-dioxin toxicity of total PCBs. Analyses of lake trout eggs spawned in the laboratory sometime shows significant correlation between concentrations of PCBs and egg and fry mortality due to factors other than the dioxinspecific lesion, blue-sac disease (Mac and Edsall 1991, Mac and Scwartz 1992, Mac et ai. 1993). The Canadice Lake data set offers evidence that nondioxin toxicity of PCBs is not the cause of recruitment failure in the Great Lakes. At the least, the Canadice Lake data set demonstrates that any correlation between recruitment failure and moderately high body burdens of total Aroclors is not strong evidence of impacts of PCBs. Despite the limitations of the PCB quantitation technique, the Canadice Lake data set has important advantages over much other work on potential chemical impacts on lake trout recruitment. The Canadice Lake data are from a natural system and include the panoply of natural factors-predation, competition, and abiotic factors that cause lethal and non-lethal effects-that affect recruitment of all life-stages. As such, the real world data from Canadice Lake have advantages over work studying small intervals of the lake trout life-cycle conducted in the artificial environments of egg trays in cold rooms (Mac et ai. 1993, Walker et ai. 1991). Similarly, in contrast to the situation in Lakes Michigan, Huron, and Ontario, the observation of strong lake trout recruitment with moderately high PCB concentrations is generally consistent with analyses on eggs spawned in the laboratory from those Great Lakes (Fitzsimons 1995a). These experiments have rather consistently shown that maternal PCB levels less than about 6 to 10 mglkg (= egg burdens less than about 2 to 3 mg/kg = fillet with skin concentrations of about 4 to 6 mg/kg) have no discernible effect on egg or fry mortality (Stauffer 1979, Berlin et ai. 1981, Mac et ai. 1981, Mac and Schwartz 1992, Mac et ai. 1993, Fitzsimons 1995a). In his detailed review of early life stage mortality, Fitzsimons (l995a) concluded that laboratory data would suggest even higher no adverse effect levels, about 25 mg/kg of PCBs in eggs, suggesting safe adult female concentrations three to four times that concentration. In addition to impacts of chemicals like PCBs, numerous alternative hypotheses exist to explain recruitment failure of lake trout in the Great Lakes: lamprey predation (Schneider et ai. 1991), overfishing (Holey et al. 1995), vitamin deficiencies associated with alewife consumption (Fitzsimons 1995b),
978
Daniellv. Smith
incompatibility of stocked strains with local conditions (Burnham-Curtis et al. 1995), and predation on emerging fry by exotic bait fish such as alewives (Krueger et al. 1995) and smelt (Abraham 1993). Besides providing evidence contrary to the chemical causation hypothesis, the Canadice Lake information supports the hypothesis that predation on lake trout fry by exotic bait fish is suppressing recruitment. Although natural recruitment was "strong" throughout the 1980s, there was suppression of natural recruitment in the late 1970s. NYDEC attributed this reduced recruitment to predation of young lake trout by high numbers of forage fish-smelt and alewives-which had invaded the lake and reached high levels during the late 1970s (Abraham 1993). Based on their working hypothesis, NYDEC stocked the lake with brown, rainbow, and lake trout in the early 1980s specifically to reduce the densities of forage fish. Subsequent to this stocking, and arguably because of the resulting predation pressure on the smelt, "strong" natural recruitment of lake trout resumed by the mid 1980s. In summary, Canadice Lake has had strong natural recruitment of lake trout despite PCB (total Aroclors) body burdens generally higher than those found in Great Lakes lake trout since 1980, and 4 to 7 times body burdens found more recently in Great Lakes trout during periods of general recruitment failure. While the observation of strong natural recruitment does not preclude the existence of any PCB effect on recruitment, the data indicate that moderately high body burdens of total Aroclors are not a sufficient explanation for the failure of lake trout recruitment in the Great Lakes. ACKNOWLEDGMENTS I thank members of the NYDEC, especially Bill Abraham, Ron Sloan, Bruce Finster, and Cliff Schneider who were so generous with their time and information. I also thank Ruth Anderson, Steve Jones, Randy Eshenroder, and three external peer reviewers (Carol Edsall, Dave De Vault, and an anonymous reviewer) for providing additional helpful review. REFERENCES Abraham, W. J. 1993. Results of the 1987 lake trout assessment netting in Canadice Lake. Unpublished report of NY Department of Environmental Conservation, Region 8 Fisheries Management Unit, June 1993.
___ . 1994. 1990 lake trout assessment report for Canadice Lake, Ontario County. Unpublished report of NY Department of Environmental Conservation, Region 8 Fisheries Management Unit. Berlin, W. H., Hesselberg, R. J., and Mac, M. P. 1981. Growth and mortality of fry of Lake Michigan lake trout during chronic exposure to PCBs and DDE. In Chlorinated hydrocarbons as a factor in the reproduction and survival of lake trout in Lake Michigan, US Fish and Wildlife Service Technical paper #105. Burnham-Curtis, M. K., Kreuger, C. c., Schreiner, D. R., Johnson, J. E., Stewart, T. J., Horral, R. M., MacCallum, W. R., Kenyon, R., and Lange. R. E. 1995. Genetic strategies for lake trout rehabilitation: A synthesis. 1995. J. Great Lakes. Res. 21 (Supplement 1): 477-486. Colborn, T., Dumanoski, D., and Myers, J. P. 1996. Our Stolen Future: Are We Threatening our Fertility, Intelligence, and Survival-A Scientific Detective Story. New York, New York: Penguin Group. Cook, P. M., Zabel, E. W., and Peterson, R. E. 1997. The TCDD toxicity equivalence approach for characterizing risks for early life-stage mortality in trout. In Chemically Induced Alterations in Functional Development and Reproduction in Fishes, eds. R. M. Rolland, M. Gilberson, and R. E. Peterson, pp. 9-27. SETAC Technical Publications. De Vault, D S., Hesselberg, R., Rodgers, P.W., and Feist, T. J. 1996. Contaminant trends in lake trout and walleye from the Laurentian Great Lakes. J. Great Lakes Res. 22: 884-895. Environment Canada. 1991 a. Toxic Chemicals in the Great Lakes and Associated Effects. Vol. 1. Contaminant Levels and Trends. Environmental Canada, Department of Fisheries and Oceans, Health and Welfare Canada. _ _ . 1991b. Toxic Chemicals in the Great Lakes and Associated Effects: Volume II-Effects. Environmental Canada, Department of Fisheries and Oceans, Health and Welfare Canada. EPA. 1993. The Great Lakes Water Quality Guidance: Proposed Rule. U.S. Federal Register 58: 20800-21046. Evans, D.O., Brisbane, J., Casselman, J. M., Coleman, K. E., Lewis, C. A., Sly, P. G., Wales, D. L., and Wilcox, C. C. 1991. Anthropogenic stressors and diagnosis of their effects on lake trout populations in Ontario lakes. Report of the Lake Trout Synthesis: Response to Stress Working Group. Ontario Ministry of Natural Resources. Fitzsimons, J. D. 1995a. A critical review of the effects of contaminants on early life stage (ELS) mortality of lake trout in the Great Lakes. J. Great Lakes. Res. 21 (Supplement 1): 267-276. _ _ . 1995b. The effect of B-vitamins on swim-up syndrome in Lake Ontario lake trout. J. Great Lakes Res. 21 (Supplement 1): 286-289.
Strong Lake Trout Recruitment Despite High PCB-Levels Giesy, J.P., Verbrugge, D.A., Othout, R.A., Bowerman, W.W., Mora, M.A., Jones, P.D., Newsted, J.L., Vandervoort, C., Heaton, S.N., Aulerich, R.J., Bursian, S.J., Ludwig, J.P., Dawson, G.A., Kubiak, T.J., Best, D.A., and Tillitt, D.E. 1994. Contaminants in fishes from Great Lakes-influenced sections and above dams of three Michigan rivers. II. Implications for health of mink. Arch. Environ. Contam. Toxicol. 27:213-223. ___ , Bowerman, W.W., Mora, M.A., Verbrugge, D.A., Othoudt, R.A., Newsted, J.L., Summer, e.L., Aulerich, R.J., Bursian, S.J., Ludwig, J.P., Dawson, G.A., Kubiak, T.J., Best, D.A., and TiJlitt, D.E. 1995. Contaminants in fishes from Great Lakes-influenced sections and above dams of three Michigan rivers: III. Implications for health of bald eagles. Arch. Environ. Contam. Toxicol. 29:309-321. Guiney, P.D., Cook, P. M., Casselman, J. M., Fitzsimon, J. F., Simonin, H. A., Zabel, E. W., and Peterson, R. E. 1996. Assessment of 2,3,7,8-tetrachlorodibenzo-pdioxin induced sac fry mortality in lake trout (Salvelinus namaycush) from different regions of the Great Lakes. Can. 1. Fish. Aquat. Sci. 53: 2080-2092. Holey, M., Rybicki, R., Eck, G.W., Brown, E. H., Marsden, J. E., Lavis, D.S., Toneys, M. L., Trudeau, R. N., and Horrall, R. M. 1995. Progress toward lake trout restoration in Lake Michigan. 1. Great Lakes. Res. 21 (Supplement 1): 128-151.. Kreuger, e. e., Perkins, D. L., Mills, E. L., and Marsden, J. E. 1995. Predation by alewives on lake trout fry in Lake Ontario: role of exotic species in preventing restoration. J. Great Lakes. Res. 2 I (Supplement 1): 458-469. Mac, M. J., and Edsall, e.e. 1991. Environmental contaminants and the reproductive success of lake trout in the Great Lakes: An epidemiological approach. J. Tox. Environ. Health, 33:375-394. _ _ , and Schwartz, T. R. 1992. Investigations into the effects of PCB congeners on reproduction in lake trout from the Great Lakes. Chemosphere 1-2: 189-192. _ _ , Berlin, W. H., and Rottiers, D.V. 1981. Comparative hatchability of Lake trout eggs differing in containant burden and incubation conditions. In Chlorinated hydrocarbons as a factor in the reproduction and survival of lake trout in Lake Michigan. US Fish and Wildlife Service Technical paper #105. _ _ , Schwartz, T. R., Edsall, C. e., and Frank, A. M. 1993. Polychlorinated biphenyl in Great Lakes lake trout and their eggs: relations to survival and congener composition 1979-1988. J. Great Lakes. Res. 19:753-765.
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NYDEC 1994. Niagara River Remedial Action Plan. New York Department of Environmental Conservation, September, 1994. Schneider, e. P., Eckert, T. H., Elrod, J. H., O'Gorman, R., Owens, R. W., Schaner, T., Grewe, P., Perkins D., and Krueger, C. e. 1990. Lake Ontario Committee Report, Lake Trout Rehabilitation in Lake Ontario, 1990. New York State Department of Environmental Conservation. _ _ , Schaner, T., Marsden, J. E., and Busch, W.-D. N. 1991. Lake Ontario Lake Trout Rehabilitation Plan, 1990 Revision. Lake Ontario Committee Great Lakes Fishery Commission. Sly, P. G. 1991. The effects of land use and cultural development on the Lake Ontario ecosystem since 1750. Hydrobiologia 213: 1-75. Smith, D. W. 1994 Dioxin impacts on Great Lakes Ecosystems: A Tale of TCDs. Presentation at 15th annual meeting of SETAC, Denver, 1994. Spagnoli, J. J., and Skinner, L. e. 1977. PCBs in fish from selected waters of New York State. 1. Pest. Monitor. 11: 69-87. Stauffer, T. M. 1979. Effects of DDT and PCBs on the survival of lake trout eggs and fry in a hacthery and in Lake Michigan, 1973-1976. Trans. Am. Fish. Soc. 108: 178-186. Symu1a, 1., Meade, M., Skea, M.e., Cummings, 1., Colquhoun, J.R., Dean, H.J., and Miccoli, J. 1990. Blue sac disease in Lake Ontario lake trout. J. Great Lakes Res. 16: 41-52. Walker, M. K., Spitzbergen, J. M, Olson, J. R., and Peterson, R. E. 1991. 2,3,7,8,-tetrachlordibenzodioxin (TCDD) toxicity during early life stages of lake trout (Salve1inus namaycush). Can. J. Fish. Aquat. Sci. 48: 875-883. Williams, L.L., Giesy, J.P., DeGa1an, N., Verbrugge, D.A., Tillitt, D., and Ankley, G.T. 1989. Size and seasonal variations of PCBs in chinook salmon (Oncorhynchus tshawytscha) fillets from Lake Michigan near Ludington, Michigan, USA. Michigan Sea Grant Publication MICHU-SG-89-202. Zint, M.T., Taylor, W.W., Carl, L., Edsall, C.C., Heinrich, J., Sippel, A., Lavis, D., and Schaner, T. 1995. Do toxic substances pose a threat to rehabilitation of lake trout in the Great Lakes? A review of the literature. J. Great Lakes Res. 21 (Supplement 1):530-546.
Submitted: 17 April 1997 Accepted: 21 August 1998 Editorial handling: Thomas J. Murphy