Dietary exposure of mink to carp from Saginaw Bay, Michigan. 1. Effects on reproduction and survival, and the potential risks to wild mink populations

  • S. N. Heaton
  • S. J. Bursian
  • J. P. Giesy
  • D. E. Tillitt
  • J. A. Render
  • P. D. Jones
  • D. A. Verbrugge
  • T. J. Kubiak
  • R. J. Aulerich
Article

Abstract

Carp (Cyprinus carpio) collected from Saginaw Bay, Michigan, containing 8.4 mg total polychlorinated biphenyls (PCBs)/kg and 194 ng of 2,3,7,8-tetrachloro-dibenzo-p-dioxin equivalents (TEQs)/kg, were substituted for marine fish at levels of 0, 10, 20, or 40% in the diets of adult ranch mink (Mustela vison). The diets, containing 0.015, 0.72, 1.53, and 2.56 mg PCBs/kg diet, or 1.03, 19.41, 40.02, and 80.76 ng TEQs/kg diet, respectively, were fed to mink prior to and throughout the reproductive period to evaluate the effects of a naturally-contaminated prey species on their survival and reproductive performance. The total quantities of PCBs ingested by the mink fed 0, 10, 20, or 40% carp over the 85-day treatment period were 0.34, 13.2, 25.3, and 32.3 mg PCBs/mink, respectively. The corresponding quantities of TEQs ingested by the mink over the same treatment period were 23, 356, 661, and 1,019 ng TEQs/mink, respectively. Consumption of feed by mink was inversely proportional to the PCB and TEQ content of the diet. The diets containing Saginaw Bay carp caused impaired reproduction and/or reduced survival of the kits. Compared to controls, body weights of kits at birth were significantly reduced in the 20 and 40% carp groups, and kit body weights and survival in the 10 and 20% carp groups were significantly reduced at three and six weeks of age. The females fed 40% carp whelped the fewest number of kits, all of which were stillborn or died within 24 hours. Lowest observable adverse effect levels (LOAEL) of 0.134 mg PCBs/kg body weight/day or 3.6 ng TEQs/kg body weight/day for adult female mink were determined. The potential effects of exposure of wild mink to contaminated Great Lakes fish were assessed by calculating “maximum allowable daily intakes” and “hazard indices” based on total concentrations of PCB residues in several species of Great Lakes fish and mink toxicity data derived from the study.

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References

  1. Allen JR, Abrahamson LJ (1979) Responses of rats exposed to polychlorinated biphenyls for fifty-two weeks. II. Compositional and enzymatic changes in the liver. Arch Environ Contam Toxicol 8:191–200Google Scholar
  2. Allen JR, Barsotti DA (1976) The effects of transplacental and mammary movement of PCBs on infant rhesus monkeys. Toxicology 6:331–340Google Scholar
  3. Ando M (1978) Transfer of 2,4,5,2′,4′,5′-hexachlorobiphenyl and 2,2′-bis(p-chlorophenyl) 1,1,1-trichloroethane (p,p′DDT) from maternal to newborn and suckling rats. Arch Toxicol 41:179–186Google Scholar
  4. Anglesea JD, Jackson AJ (1985) Thiaminase activity in fish silage and moist fish feed. Anim Feed Sci Tech 13:39–46Google Scholar
  5. Aulerich RJ, Bleavins MR (1981) Potential of mink as an animal model in testing in area of toxicology. In: Lamb B (ed). 1981 Blue Book of Fur Farming. Comm Marketing Inc, Eden Prairie, MN. pp 30, 32Google Scholar
  6. Aulerich RJ, Bursian SJ, Breslin WJ, Olson BA, Ringer RK (1985) Toxicological manifestations of 2,4,5,2′,4′,5′-, 2,3,6,2′,3′,6′-, and 3,4,5,3′,4′,5′-hexachlorobiphenyl and Aroclor® 1254 in mink. J Toxicol Environ Health 15:63–79Google Scholar
  7. Aulerich RJ, Bursian SJ, Evans MG, Hochstein JR, Koudele KA, Olson BA, Napolitano AC (1987) Toxicity of 3,4,5,3′,4′,5′-hexachlorobiphenyl to mink. Arch Environ Contam Toxicol 16:53–60Google Scholar
  8. Aulerich RJ, Ringer RK, Iwamoto S (1973) Reproductive failure and mortality in mink fed on Great Lakes fish. J Reprod Fert (Supplement) 19:365–376Google Scholar
  9. Aulerich RJ, Ringer RK (1977) Current status of PCB toxicity to mink and effect on their reproduction. Arch Environ Contam Toxicol 6:279–292Google Scholar
  10. Aulerich RJ, Ringer RK, Safronoff J (1986) Assessment of primary vs secondary toxicology of Aroclor® 1254 to mink. Arch Environ Contam Toxicol 15:393–399Google Scholar
  11. Aulerich RJ, Ringer RK, Seagran HL, Youatt WG (1971) Effects of feeding Coho salmon and other Great Lakes fish on mink reproduction. Canadian J Zool 49(5):611–616Google Scholar
  12. Barsotti DA, Marlor RJ, Allen JR (1976) Reproductive dysfunction in rhesus monkeys exposed to low levels of polychlorinated biphenyls (Aroclor® 1248). Fd Cosmet Toxicol 149:99–103Google Scholar
  13. Birnbaum LS, Weber H, Harris MW, Lamb JC, McKinney JD (1985) Toxic interaction of specific polychlorinated biphenyls and 2,3,7,8-tetrachlorodibenzo-p-dioxin: Increased incidence of cleft palate in mice. Toxicol Appl Pharmacol 77:292–302Google Scholar
  14. Bleavins MR, Aulerich RJ, Ringer RK (1980) Polychlorinated biphenyls (Aroclors® 1016 and 1242): Effects on survival and reproduction in mink and ferrets. Arch Environ Contam Toxicol 9:627–635Google Scholar
  15. Bleavins MR, Aulerich RJ, Ringer RK (1982) Placental and mammary transfer of polychlorinated and polybrominated biphenyls in the mink and ferret. In: Lamb DW, Kenaga EE (eds). Avian and Mammalian Wildlife Toxicology, Second Conference, ASTM STP 757. Amer Soc Testing and Materials, Philadelphia, PA. pp 121–131Google Scholar
  16. Brezner S, Terkel J, Perry AS (1984) The effect of Aroclor® 1254 (PCB) on the physiology of reproduction in the female rat — I. Comp Biochem Physiol 77C(1):65–70Google Scholar
  17. Burkhard LP, Weininger D (1987) Determination of polychlorinated biphenyls using multiple regression with outlier detection and elimination. Anal Chem 59:1187–1190Google Scholar
  18. Calabrese EJ, Aulerich RJ, Padgett GA (1992) Mink as a predictive model in toxicology. Drug Metab Rev 24(4):559–578Google Scholar
  19. Courtney KD, Putnam JP, Andrews JE (1978) Metabolic studies with TCDD (dioxin) treated rats. Arch Environ Contam Toxicol 7:385–396Google Scholar
  20. Erlinge S (1967) Food habits of the fish otter Lutra lutra L., in southern Swedish habitats. Viltrevy 4:371–447Google Scholar
  21. Fein CG, Jacobsen JL, Jacobsen SW, Schwartz PM, Dowler JK (1984) Prenatal exposure to polychlorinated biphenyls: Effects on birth size and gestational age. J Ped 105(2):315–320Google Scholar
  22. Fox GA, Collins B, Hayakawa E, Weseloh DV, Ludwig JP, Kubiak TJ, Erdman TC (1991) Reproductive outcomes in colonial fisheating birds: A biomarker for developmental toxins in Great Lakes food chains. II. Spatial variation in the occurrence and prevalence of bill defects in young double-crested cormorants in the Great Lakes, 1979–1987. J Great Lakes Res 17(2):158–167Google Scholar
  23. Gerell R (1967) Food selection in relation to habitat in mink (Mustela vison Schreber) in Sweden. Oikos 18:233–246Google Scholar
  24. Giesy JP, Ludwig JP, Tillitt DE (1994a) Dioxins, dibenzofurans, PCBs, and similar chlorinated diaromatic hydrocarbons in and their effects on birds: Wildlife biomonitoring for hazards of complex environmental mixtures in the Laurentian Great Lakes. In: Schecter A (ed) Dioxin and Health (in press)Google Scholar
  25. Giesy JP, Ludwig JP, Tillitt DE (1994b) Embryolethality and deformities in colonial, fish-eating, water birds of the Great Lakes region; Assessing causality. Environ Sci Technol 28:128A-137AGoogle Scholar
  26. Giesy JP, Verbrugge DA, Othoudt RA, Bowerman WW, Mora MA, Jones PD, Newsted JL, Vandervoot C, Heaton SN, Aulerich RJ, Bursian SJ, Ludwig JP, Dawson GA, Kubiak TJ, Best DA, Tillitt DE (1994c) 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 27:213–223Google Scholar
  27. Gilbert FF, Nacekivell EG (1982) Food habits of mink (Mustela vison) and otter (Lutra canadensis) in northeastern Alberta. Canad J Zool 60:1282–1288Google Scholar
  28. Gilbertson M (1983) Etiology of chick-edema disease in herring gulls in the lower Great Lakes. Chemosphere 12:357–370Google Scholar
  29. Gilbertson M, Kubiak T, Ludwig J, Fox G (1991) Great Lakes embryo mortality, edema, and deformities syndrome (GLEMEDS) in colonial fish-eating birds: Similarity to chick edema disease. J Toxicol Environ Health 33:455–520Google Scholar
  30. Gill JL (1978) Design and Analysis of Experiments in the Animal and Medical Sciences. Vol. 1. Iowa State Univ Press, Ames, IA. 410 ppGoogle Scholar
  31. Gillette DM, Corey RD, Helferich WG, McFarland JM, Lowenstein LJ, Moody DE, Hammock BD, Shull LR (1987a) Comparative toxicology of tetrachlorobiphenyls in mink and rats. I. Changes in hepatic enzyme activity and smooth endoplasmic reticulum volume. Funda Appl Toxicol 8:5–14Google Scholar
  32. Gillette DM, Corey RD, Lowenstein LJ, Shull LR (1987b) Comparative toxicology of tetrachlorobiphenyls in mink and rats. II. Pathology. Funda Appl Toxicol 8:15–22Google Scholar
  33. Gnaedinger RH, Krzeczkowski RA (1966) Heat inactivation of thiaminase in whole fish. Comm Fisheries Rev 28(8):11–14Google Scholar
  34. Hamilton WJ (1940) The summer food of minks and raccoons on the Montezuma Marsh, NY. J Wildl Manage 4:80–84Google Scholar
  35. Hartsough GR (1965) Great Lakes fish now suspect as mink food. Amer Fur Breeder 38:25–27Google Scholar
  36. Hochstein JR, Aulerich RJ, Bursian SJ (1987) Toxicity of dioxin to mink confirmed. In: Smith B (ed). 1987 Blue Book of Fur Farming. Comm Marketing Inc, Eden Prairie, MN. pp 76–77Google Scholar
  37. Hochstein JR, Aulerich RJ, Bursian SJ (1988) Acute toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to mink. Arch Environ Contam Toxicol 17:33–37Google Scholar
  38. Hoffman DJ, Rattner BA, Sileo L, Docherty D, Kubiak TJ (1987) Embryotoxicity, teratogenicity, and aryl hydrocarbon hydroxylase activity in Forster's terns on Green Bay, Lake Michigan. Environ Res 42:176–184Google Scholar
  39. Hornshaw TC, Aulerich RJ, Johnson HE (1983) Feeding Great Lakes fish to mink: Effects on mink and accumulation and elimination of PCBs by mink. J Toxicol Environ Health 11:933–946Google Scholar
  40. Hornshaw TC, Safronoff J, Ringer RK, Aulerich RJ (1986) LC50 test results in polychlorinated biphenyl-fed mink: Age, season, and diet comparisons. Arch Environ Contam Toxicol 15:717–723Google Scholar
  41. Jones PD, Giesy JP, Kubiak TJ, Verbrugge DA, Newsted JC, Ludwig JP, Tillitt DE, Crawford R, De Galan N, Ankley GT (1993) Biomagnification of bioassay-derived 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents. Chemosphere 26:1203–1212Google Scholar
  42. Kihlström JE, Olsson M, Jensen S, Johansson A, Ahlbom J, Bergman A (1992) Effects of PCB and different fractions of PCB on the reproduction of the mink (Mustela vison). Ambio 21:563–569Google Scholar
  43. Korschgen L (1958) December food habits of mink in Missouri. J Mamm 39:521–527Google Scholar
  44. Kubiak TJ, Harris HJ, Smith LM, Schwartz TR, Stalling DL, Trick JA, Sileo L, Docherty DE, Erdman TC (1989) Microcontaminants and reproductive impairment of the Forster's tern on Green Bay, Lake Michigan-1983. Arch Environ Contam Toxicol 18:706–727Google Scholar
  45. Langford HD (1979) Looking at polychlorinated biphenyls as environmental object lesson. News Rept 29(9):1–5Google Scholar
  46. Mac MJ, Edsall CD, Seelye JG (1985) Survival of lake trout eggs and fry reared in water from the Upper Great Lakes. J Great Lakes Res 11:520–529Google Scholar
  47. Masuda Y, Kagawa R, Kuroki H (1978) Transfer of polychlorinated biphenyls from mothers to foetuses and infants. Fd Cosmet Toxicol 16:543–546Google Scholar
  48. MDNR (Michigan Dept Natural Resources) (1991) Michigan fish contaminant monitoring program. 1991 Annual Report. Surface Water Quality Division, Mich Dept Nat Res Rept #MI/DNR/SWQ-91/273Google Scholar
  49. Melquist WE, Whitman JS, Hornocker MG (1981) Resource partitioning and coexistence of sympathic mink and river otter populations. In: Chapman JA and Pursley D (eds). Worldwide Furbearer Conf Proc, August 3–11, 1980, Vol 1. Worldwide Furbearer Conference Inc, Frostberg, MD pp 187–220Google Scholar
  50. Mora MA, Verbrugge D (1991) Standard operating procedure. Analysis of organochlorine pesticides and PCBs in muscle tissues of fish and birds. Michigan State University, Pesticide Research Center, Aquatic Toxicology Laboratory. 12 ppGoogle Scholar
  51. O'Brien DJ, Kaneene JB, Poppenga RH (1993) The use of mammals as sentinels for human exposure to toxic contaminants in the environment. Environ Health Perspect 99:351–368Google Scholar
  52. Platonow NS, Karstad LH (1973) Dietary effects of polychlorinated biphenyls on mink. Canadian J Comp Med 37(4):391–400Google Scholar
  53. Pohl RJ, Fouts JR (1980) A rapid method for assaying the metabolism of 7-ethoxyresorufin by microsomal subcellular fractions. Analy Biochem 107:150–155Google Scholar
  54. Ringer RK, Aulerich RJ, Zabik M (1972) Effect of dietary polychlorinated biphenyls on growth and reproduction of mink. 164th Natl Meeting, Amer Chem Soc 12:149–154Google Scholar
  55. Ringer RK, Aulerich RJ, Bleavins MR (1981) Biological effects of PCBs and PBBs on mink and ferrets — A review. In: Khan MAQ (ed). Halogenated Hydrocarbons: Health and Ecological Effects. Pergamen Press Inc, Elmsford, NY. pp 329–343Google Scholar
  56. Rogan WJ, Gladen BC, Hung KL, Koong SL, Shih LY, Taylor JS, Wu YC, Yang D, Ragan NB, Hsu CC (1988) Congenital poisoning by polychlorinated biphenyls and their contaminants. Science 241:334–336Google Scholar
  57. SAS Institute Inc (1987) SAS/STAT Guide for Personal Computers, Version 6 ed. SAS Institute Inc, Cary, NC. pp 1028Google Scholar
  58. Schmitt CJ, Zajicek JL, Ribick MA (1985) National pesticide monitoring program: Residues of organochlorine chemicals in freshwater fish, 1980–1981. Arch Environ Contam Toxicol 14:225–260Google Scholar
  59. Schwartz P (1982) Determination of polychlorinated biphenyls in plant tissue. Bull Environ Contam Toxicol 28:723–727Google Scholar
  60. Sealander JA (1943) Winter food habits of mink in southern Michigan. J Wildl Manage 7:411–417Google Scholar
  61. Somers JD (1985) Pesticide and PCB residues in northeastern Alberta otter. Alberta Environmental Center, Vegreville, Alberta, Canada. AECV85-R4. 35 ppGoogle Scholar
  62. Stalling DL, Norstrom RJ, Smith LM, Simon M (1985) Patterns of PCDD, PCDF, and PCB contamination in Great Lakes fish and birds and their characterization by principal components analysis. Chemosphere 14:627–634Google Scholar
  63. Summer CL (1992) An Avian Ecosystem Health Indicator: The Reproductive Effects Induced by Feeding Great Lakes Fish to White Leghorn Laying Hens. MS Thesis. Dept Animal Science, Michigan State University, E Lansing, MI. 117 ppGoogle Scholar
  64. Tillitt DE, Ankley GT, Giesy JP, Ludwig JP, Kurita-Matsuba H, Weseloh DV, Ross PS, Bishop CH, Sileo L, Stromberg KL, Larson J, Kubiak TJ (1992) Polychlorinated biphenyl residues and egg mortality in double-crested cormorants from the Great Lakes. Environ Toxicol Chem 11:1281–1288Google Scholar
  65. Tillitt DE, Giesy JP, Ankley GT (1991) Characterization of the H4IIE rat hepatoma cell bioassay as a tool for assessing toxic potency of planar halogenated hydrocarbons in environmental samples. Environ Sci Tech 25:87–92Google Scholar
  66. Wren CD, Hunter DB, Leatherland JF, Stokes PM (1987) The effects of PCB and methyl mercury, singly and in combination, on mink. II: Reproduction and kit development. Arch Environ Contam Toxicol 16(4):449–454Google Scholar
  67. Yu ML, Hsu CC, Gladen BC, Rogan WJ (1991) In utero PCB/PCDF exposure: Relation of developmental delay to dysmorphology and dose. Neurotox Teratol 13:195–202Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1995

Authors and Affiliations

  • S. N. Heaton
    • 1
  • S. J. Bursian
    • 1
    • 4
  • J. P. Giesy
    • 2
    • 4
    • 5
  • D. E. Tillitt
    • 6
  • J. A. Render
    • 3
  • P. D. Jones
    • 2
  • D. A. Verbrugge
    • 2
    • 5
  • T. J. Kubiak
    • 7
  • R. J. Aulerich
    • 1
    • 4
  1. 1.Department of Animal ScienceMichigan State UniversityEast Lansing
  2. 2.Department of Fisheries and WildlifeMichigan State UniversityEast Lansing
  3. 3.Department of PathologyMichigan State UniversityEast Lansing
  4. 4.Department of Institute for Environmental ToxicologyMichigan State UniversityEast Lansing
  5. 5.Department of Pesticide Research CenterMichigan State UniversityEast Lansing
  6. 6.National Biological SurveyNational Fisheries Contaminant Research CenterColumbia
  7. 7.U.S. Fish and Wildlife ServiceEast Lansing
  8. 8.Surface Water Quality Division, Michigan Department of Natural ResourcesKnapp CenterLansing
  9. 9.ESR Environmental, Gracefield Rd.Wellington Science CenterLower HuttNew Zealand
  10. 10.U.S. Fish and Wildlife ServiceDivision of Environmental ContaminantsArlington

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