Abstract
As part of a larger investigation, northern pike (n = 158; Esox lucius) were collected from ten sites in the Yukon River Basin (YRB), Alaska, to document biomarkers and their correlations with organochlorine pesticide (total p,p’-DDT, total chlordane, dieldrin, and toxaphene), total polychlorinated biphenyls (PCBs), and elemental contaminant (arsenic, cadmium, copper, lead, total mercury, selenium, and zinc) concentrations. A suite of biomarkers including somatic indices, hepatic 7-ethoxyresorufin O-deethylase (EROD) activity, vitellogenin concentrations, steroid hormone (17B- ustradiol and 16-kebtestosteront) concentrations, splenic macrophage aggregates (MAs), oocyte atresia, and other microscopic anomalies in various tissues were documented in YRB pike. Mean condition factor (0.50 to 0.68), hepatosomatic index (1.00% to 3.56%), and splenosomatic index (0.09% to 0.18%) were not anomalous at any site nor correlated with any contaminant concentration. Mean EROD activity (0.71 to 17.51 pmol/min/mg protein) was similar to basal activity levels previously measured in pike and was positively correlated with selenium concentrations (r = 0.88, P < 0.01). Vitellogenin concentrations in female (0.09 to 5.32 mg/mL) and male (<0.0005 to 0.097 mg/mL) pike were not correlated with any contaminant, but vitellogenin concentrations >0.01 mg/mL in male pike from multiple sites indicated exposure to estrogenic compounds. Mean steroid hormone concentrations and percent oocyte atresia were not anomalous in pike from any YRB site. Few site differences were significant for mean MA density (1.86 to 6.42 MA/mm2), size (812 to 1481 μm2), and tissue occupied (MA-%; 0.24% to 0.75%). A linear regression between MA-% and total PCBs was significant, although PCB concentrations were generally low in YRB pike (≤63 ng/g), and MA-% values in female pike (0.24% to 0.54%) were lower than in male pike (0.32% to 0.75%) at similar PCB concentrations. Greater numbers of MAs were found as zinc concentrations increased in YRB female pike, but it is unlikely that this is a causative relationship. Histological abnormalities observed in gill, liver, spleen, and kidney tissues were not likely a result of contaminant exposure but provide information on the general health of YRB pike. The most common histologic anomalies were parasitic infestations in various organs and developing nephrons and nephrocalcinosis in posterior kidney tissues. Overall, few biomarker responses in YRB pike were correlated with chemical contaminant concentrations, and YRB pike generally appeared to be healthy with no site having multiple anomalous biomarker responses.
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References
Adams SM, Bevelhimer MS, Greeley Jr MS, Levine DA, Teh SJ (1999) Ecologic risk assessment in a large river-reservoir. 6. Bioindicators of fish population health. Environ Toxicol Chem 18:628–640
Agius C, Roberts RJ (2003) Melano-macrophage centres and their role in fish pathology. J Fish Dis 26:499–509
American Fisheries Society, American Institute of Fishery Research Biologists, and American Society of Ichthyologists and Herpetologists (2004) Guidelines for the use of fishes in research. American Fisheries Society, Bethesda, MD
Blazer VS (2002) Histopathological assessment of gonadal tissue in wild fishes. Fish Physiol Biochem 26:85–101
Blazer VS, Wolke RE, Brown J, Powell CA (1987) Piscine macrophage aggregate parameters as health monitors: Effect of age, sex, relative weight, season and site quality in largemouth bass (Micropterus salmoides). Aquat Toxicol 10:199–215
Blazer VS, Facey DE, Fournie JW, Courtney LA, Summers JK (1994) Macrophage aggregates as indicators of environmental stress. In: Stolen JS, Fletcher TC (eds) Modulators of fish immune responses. Volume one. Models for environmental toxicology, biomarkers, immunostimulators. SOS Publications, Fair Haven, NJ, p 169–185
Blazer VS, Dethloff GM, Wright B (2002) Fish health indicators. In: Schmitt CJ (ed) Biomonitoring Environmental Status and Trends (BEST) Program: Environmental contaminants and their effects on fish in the Mississippi River basin. United States Geological Survey, Biologic Resources Division, Biologic Science Report 2002–0004, pp 89–134
Brabets TP, Wang B, Meade RH (2000) Environmental and hydrologic overview of the Yukon River Basin, Alaska and Canada. United States Geological Survey, Water Resources Discipline, WRIR 99–4204, Anchorage, AK
Braune B, Muir D, DeMarch B, Gamberg M, Poole K, Currie R, et al. (1999) Spatial and temporal trends in contaminants in Canadian Arctic freshwater and terrestrial ecosystems: A review. Sci Total Environ 230:145–207
Buhl KJ, Hamilton SJ (1990) Comparative toxicity of inorganic contaminants released by placer mining to early life stages of salmonids. Ecotoxicol Environ Safety 20:325–342
Bury NR, Walker PA, Glover CN (2003) Nutritive metal uptake in teleost fish. J Exp Biol 206:11–23
Carlander KD (1969) Handbook of freshwater fishery biology. Iowa State University Press, Ames, IA
Cordone AJ, Kelley DW (1961) The influences of inorganic sediment on the aquatic life of streams. Cal Fish Game 47:189–228
Couillard CM, Hodson PV (1996) Pigmented macrophage aggregates: A toxic response in fish exposed to bleached-kraft mill effluent? Environ Toxicol Chem 15:1844–1854
Cross JN, Hose JE (1988) Evidence for impaired reproduction in white croaker (Genyonemus lineatus) from contaminated areas off southern California. Mar Environ Res 24:185–188
Denslow ND, Chow MC, Kroll KJ, Green L (1999) Vitellogenin as a biomarker of exposure for estrogen or estrogen mimics. Ecotoxicol 8:385–398
Drevnick PE, Sandheinrich MB (2003) Effects of dietary methylmercury on reproductive endocrinology of fathead minnows. Environ Sci Technol 37:4390–4396
Duffy LK, Scofield E, Rodgers T, Patton M, Bowyer RT (1999) Comparative baseline levels of mercury, Hsp 70 and Hsp 60 in subsistence fish from the Yukon-Kuskokwim delta region of Alaska. Comp Biochem Physiol C 124:181–186
Dusel-Bacon C, Bressler JR, Takaoka H, Mortensen JK, Oliver DH, Leventhal JS, et al. (1998) Stratiform zinc-lead mineralization in Nasina assemblage rocks of the Yukon-Tanana Upland in east-central Alaska. United States Geological Survey, OFR 98–340, Menlo Park, CA
Eiler JH, Spencer TR, Pella JJ, Masuda MM, Holder RR (2004) Distribution and movement patterns of Chinook salmon returning to the Yukon River basin in 2000–2002. National Oceanic and Atmospheric Administration Technical Memo, NMFS-AFSC-148, Seattle, WA
Evans MS, Muir D, Lockhart WL, Stern G, Roach P (2005) Persistent organic pollutants and metals in the freshwater biota of the Canadian Subarctic and Arctic: An overview. Sci Total Environ 351–352:94–147
Ferguson HW (1989) Systemic pathology of fish: A text and atlas of comparative tissue responses in disease of teleosts. Iowa State University Press, Ames, IA
Fournie JW, Summers JK, Courtney LA, Engle VD, Blazer VS (2001) Utility of splenic macrophage aggregates as an indicator of fish exposure to degraded environments. J Aquat Animal Health 13:105–116
Friedmann AS, Watzin MC, Leiter JC, Brinck-Johnsen T (1996) Effects of environmental mercury on gonadal function in Lake Champlain northern pike (Esox lucius). Bull Environ Contam Toxicol 56:486–492
Gingerich WH (1982) Hepatic toxicology of fishes. In: Weber LJ (ed) Aquatic toxicology. Raven, New York, NY, pp 55–105
Goodbred SL, Gilliom RJ, Gross TS, Denslow NP, Bryant WL, Schoeb TR (1997) Reconnaissance of 17β-estradiol, 11-ketotestosterone, vitellogenin, and gonad histopathology in common carp of United States streams: Potential for contaminant-induced endocrine disruption. United States Geological Survey, Open-File Report 96–627, Sacramento, CA
Gunderson DT, Miller R, Mischler A, Elpers K, Mims SD, Millar JG, et al. (2000) Biomarker response and health of polychlorinated biphenyl- and chlordane-contaminated paddlefish from the Ohio River Basin, United States. Environ Toxicol Chem 19:2275–2285
Haaparanta A, Valtonen ET, Hoffmann R, Holmes J (1996) Do macrophage centres in freshwater fishes reflect the differences in water quality? Aquat Toxicol 34:253–272
Hinck JE, Bartish TM, Blazer VS, Denslow ND, Gross TS, Myers MS, et al. (2004) Biomonitoring Environmental Status and Trends (BEST) Program: Environmental contaminants and their effect on fish in the Yukon River basin. United States Geological Survey, Biologic Resources Division, SIR 2004–5285, Columbia, MO
Hinck JE, Schmitt CJ, Echols KR, May TW, Orazio CE, Tillitt DE (2006a) Environmental contaminants in fish and their associated risk to piscivorous wildlife in the Yukon River Basin, Alaska. Arch Environ Contam Toxicol 51:661–672
Hinck JE, Schmitt CJ, Blazer VS, Denslow ND, Bartish TM, Anderson PJ, et al. (2006b) Environmental contaminants and biomarker responses in fish from the Columbia River and its tributaries: Spatial and temporal trends. Sci Total Environ 366:549–578
Jewett SC, Zhang X, Naidu AS, Kelley JJ, Dasher D, Duffy LK (2003) Comparison of mercury and methylmercury in northern pike and Arctic grayling from western Alaska rivers. Chemosphere 50:383–392
Johnson LL, Casillas E, Collier TK, McCain BB, Varanasi U (1988) Contaminant effects on ovarian development in English sole (Parophyrs vetulus) from Puget Sound, Washington. Can J Fish Aquat Sci 45:2133–2146
June FC (1970) Atresia and year-class abundance of northern pike, Esox lucius, in two Missouri River impoundments. J Fish Res Board Can 27:587–591
June FC (1977) Reproductive patterns in seventeen species of warm water fishes in a Missouri River reservoir. Environ Biol Fish 2:285–296
LaPerriere JD, Wagener SM, Bjerklie DM (1985) Gold-mining effects on heavy metals in streams, Circle Quadrangle, Alaska. Water Res Bull 21:245–252
Lloyd DS, Koenings JP, LaPerriere JD (1987) Effects of turbidity in fresh waters of Alaska. North Am J Fish Manage 7:18–33
Malette MD, Morgan GE (2005) Provincial summary of northern pike life history characteristics based on Ontario’s hall walleye index netting (FWIN) programs 1993 to 2002. Ontario, Canada Report ISBN 0-7794-7573-9
McLeay DJ, Birtwell IK, Hartman GF, Ennis GL (1987) Responses of Arctic grayling (Thymallus arcticus) to acute and prolonged exposure to Yukon placer mining sediment. Can J Fish Aquat Sci 44:658–673
Meinelt T, Krüger R, Pietrock M, Osten R, Steinberg C (1997) Mercury pollution and macrophage centres in pike (Esox lucius) tissues. Environ Sci Pollut Res 4:32–36
Merritt RD, Hawley CC (1986) Map of Alaska’s coal resources. Alaska Department of Natural Resources, Division of Mining and Geological and Geophysical Surveys, Fairbanks, Alaska
Mueller KA, Matz AC (2000) Organochlorine concentrations in burbot (Lota lota) livers from Fairbanks, Alaska, and Kanuti, Tetlin, and Yukon Flats National Wildlife Refuges, Alaska, 1998. United States Fish and Wildlife Service, Northern Alaska Ecologic Services, NAES-TR-00-01, Fairbanks, Alaska
Orlando EF, Binczik GA, Gates J, Gray LE Jr, Horton M, Kolok AS, et al. (2004) Endocrine disrupting effects of cattle feedlot effluent on a sentinel species, the fathead minnow. Environ Health Perspect 112:353–358
Reimschuessel R, Bennet RO, May EB, Lipsky MM (1990) Development of newly formed nephrons in the goldfish kidney following hexachlorobutadiene-induced nephrotoxicity. Toxicol Pathol 8:32–38
Reynolds JB, Simmons RC, Burkholder AR (1989) Effects of placer mining discharge on health and food of Arctic grayling. Water Resources Bull 25:625–635
Roberts RJ (1989) Fish pathology, 2nd ed. Bailliere Tindall, Great Britain
Salomone P, Bergstrom DJ (2004) Yukon River summer chum salmon stocks status and action plan. Alaska Department of Fish and Game Division of Commercial Fisheries, Anchorage, Alaska, Regional Information Report No. 3A04-03
Schmitt CJ, Zajicek JL, May TW, Cowman DF (1999) Organochlorine residues and elemental contaminants in United States freshwater fish, 1976–1986: National Contaminant Biomonitoring Program. Rev Environ Contam Toxicol 162:43–104
Schmitt CJ (2002) Biomonitoring Environmental Status and Trends (BEST) Program: Environmental contaminants and their effects on fish in the Mississippi River basin. United States Geological Survey, Biologic Resources Division, BSR 2002–0004, Columbia, MO
Schmitt CJ, Hinck JE, Blazer VS, Denslow ND, Dethloff GM, Bartish TM, et al. (2005) Environmental contaminants and biomarker responses in fish from the Rio Grande and its United States tributaries: Spatial and temporal trends. Sci Total Environ 250:161–193
Sepúlveda MS, Ruessler DS, Denslow ND, Holm SE, Schoeb TR, Gross TS (2001) Assessment of reproductive effects in largemouth bass (Miropterus salmoides) exposed to bleached/unbleached kraft mill effluents. Arch Environ Contam Toxicol 41:475–482
Snyder-Conn E (1992) Contaminant investigation of fish in Lake Minchumina, Alaska. United States Fish and Wildlife Service, Northern Alaska Ecologic Services, NAES-TR-92-03, Fairbanks, Alaska
Specker J, Sullivan CV (1994) Vitellogenesis in fishes: Status and perspectives. In: Davey KG, Peter RG, Tobe SS (eds) Perspectives in comparative endocrinology. National Research Council of Canada, Ottawa, Canada, pp 304–315
Spehar RL, (1976) Cadmium and zinc toxicity to flagfish (Jordanella floridae). J Fish Res Board Can 33:1939–1945
Stegeman JJ, Brouwer M, DiGiulio RT, Forlin L, Fowler BA, Sanders BM, et al. (1992) Molecular responses to environmental contamination: Enzyme and protein synthesis as indicators of contaminant exposure and effect. In: Hugget RJ, Kimerle RA, Mehrle PM, Bergman HL (eds) Biomarkers: Biochemical, physiologic, and histologic markers of anthropogenic stress. Lewis, Boca Raton, FL, p 235–335
Stein X, Risso C, Gnassia-Barelli M, Rome M, LaFaurie M (1997) Effect of copper chloride in vitro and in vivo on the hepatic EROD activity in the fish Dicentrarchus labrax. Environ Toxicol Chem 16:214–219
Szumigala DJ, Hughes RA, Harris RH (2003) Alaska’s mineral industry 2003. Division of Geological and Geophysical Survey, Fairbanks, Alaska, Special Report 58
Teh SJ, Adams SM, Hinton DE (1997) Histopathologic biomarkers in feral freshwater fish populations exposed to different types of contaminant stress. Aquat Toxicol 37:51–70
Tillitt DE, Papoulias DM, Buckler DR (2003) Fish reproductive health assessment in PCB contaminated regions of the Housatonic River, Massachusetts, United States: Investigation of causal linkages between PCBs and fish health. Final Report of Phase I Studies, Interagency Agreement 1448-50181-99-H-008. United States Geological Survey, Columbia Environmental Research Center Biochemistry & Physiology Branch Report, FY03-30-09, Columbia, MO
United States Bureau of Land Management (2002) Final environmental impact statement renewal of the federal grant for the trans-Alaska pipeline system right-of-way. United States Bureau of Land Management, BLM/AK/PT-03/005+2880+990
United States Environmental Protection Agency (1998) EPA superfund record of decision amendment: Eielson Air Force Base, EPA ID AK1570028646. Fairbanks, Alaska, EPA/AMD/R10-98/185
United States Fish and Wildlife Service (2005) National wildlife refuges—Alaska region. Available at: http://www.alaska.fws.gov/internettv/nwrtv/maptv.htm. Accessed August 4, 2005
Vine E, Shears J, van Aerle R, Tyler CR, Sumpter JP (2005) Endocrine (sexual) disruption is not a prominent feature in the pike (Esox lucius), a top predator, living in English waters. Environ Toxicol Chem 24:1436–1443
Whyte JJ, Jung RE, Schmitt CJ, Tillitt DE (2000) Ethoxyresorufin O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit Rev Toxicol 30:347–570
Williams TG, Lockhart WL, Metner DA, Harbicht S (1997) Baseline studies in the Slave River, NWT, 1990–1994, Part III. MFO enzyme activity in fish. Sci Total Environ 197:87–109
Wilson HM, Peterson MR, Troy D (2004) Concentrations of metals and trace elements in blood of spectacled and king eiders in northern Alaska, United States. Environ Toxicol Chem 23:408–414
Acknowledgments
This study was conducted as a component of the Large River Monitoring Network of the United States Geological Survey Biomonitoring Environmental Status and Trends (BEST) Program. R. Lipkin created the map. We thank K. Chojnacki, G. Chuiko, A. Matz, K. Mueller, M. Ryan, C. Schmitt, and two anonymous reviewers for providing comments on earlier versions of this manuscript. Although information in this article was developed by the United States Geological Survey, the article may not necessarily reflect the views of this organization, and no official endorsement should be inferred.
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Hinck, J.E., Blazer, V.S., Denslow, N.D. et al. Biomarkers of Contaminant Exposure in Northern Pike (Esox lucius) from the Yukon River Basin, Alaska. Arch Environ Contam Toxicol 52, 549–562 (2007). https://doi.org/10.1007/s00244-006-0134-z
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DOI: https://doi.org/10.1007/s00244-006-0134-z