Trace Element Concentrations and Bioindicator Responses in Tree Swallows from Northwestern Minnesota

  • Christine M. Custer
  • Thomas W. Custer
  • David Warburton
  • David J. Hoffman
  • John W. Bickham
  • Cole W. Matson


Extremely high concentrations of cadmium (3.5 μg/g dry wgt.) and elevated concentrations of chromium (>10 μg/g dry wgt.) and mercury (1.6 μg/g dry wgt.) were reported in waterbird tissues at Agassiz National Wildlife Refuge in northwestern Minnesota in 1994. Tree swallows (Tachycineta bicolor) were studied during 1998–2001 at three drainages into the Refuge, two pools on the Refuge, and at a nearby reference location to document whether high levels of contaminants were still present, and if so to quantify the source and severity of the contamination. Trace elements were measured in tree swallow eggs, livers, and diet. Reproductive success and bioindicator responses were monitored. In 2000, water was drawn down on Agassiz Pool, one of the main pools on the Refuge. This presented an opportunity to evaluate the response of trace element concentrations in the diet and tissues of tree swallows after reflooding. High concentrations of trace elements were not detected in swallow tissues, nor were there differences among locations. Less than 20% of swallow samples had detectable concentrations of cadmium or chromium. Mercury concentrations were low and averaged <0.25 μg/g dry wgt. in swallow tissues. Trace elements, including mercury, did not increase in tree swallows following the 2000 drawdown at Agassiz Pool. Hatching success and survival of nestlings to 12 days-of-age for tree swallows on the Refuge were similar to the national average and consistent with background trace element concentrations. Bioindicator measurements were within the normal ranges as well.


Agassiz National Wildlife Refuge mercury Minnesota Tachycineta bicolor trace elements tree swallows 


  1. Annual Water Plan: 2001, Agassiz National Wildlife Refuge, Middle River, MN, USA. Station Files.Google Scholar
  2. Aust, S. D.: 1985, ‘Lipid peroxidation’, in: R. A. Greenwald (ed), Handbook of Methods for Oxygen Radical Research, CRC, Boca Raton, FL, USA, pp. 203–207.Google Scholar
  3. Blancher, P. J. and McNicol, D. K.: 1991, ‘Tree swallow diet in relation to wetland acidity’, Can. J. Zool. 69, 2629–2637.Google Scholar
  4. Blus, L. J., Henny, C. J., Hoffman, D. J. and Grove, R. A.: 1995, ‘Accumulation in and effects of lead and cadmium on waterfowl and passerines in northern Idaho’, Environ. Pollut. 89, 311–318.CrossRefGoogle Scholar
  5. Burger, J. and Gochfeld, M.: 1994, ‘Franklin's gull (Larus pipixcan)’, in: A. Poole and F. Gill (eds), The Birds of North America, No. 116, Academy of Natural Sciences, Philadelphia, PA, USA, pp. 28.Google Scholar
  6. Burger, J. and Gochfeld, M.: 1996a, ‘Heavy metal and selenium levels in birds at AgassizNational Wildlife Refuge, Minnesota: Food chain differences’, Environ. Monit. Assess. 43, 267–282.CrossRefGoogle Scholar
  7. Burger, J. and Gochfeld, M.: 1996b, ‘Heavy metal and selenium levels in Franklin's gull (Larus pipixcan) parents and their eggs’, Arch. Environ. Contam. Toxicol. 30, 487–491.CrossRefGoogle Scholar
  8. Burger, J. and Gochfeld, M.: 1999, ‘Heavy metals in Franklin's gull tissues: Age and tissue differences’, Environ. Toxicol. Chem. 18, 673–678.CrossRefGoogle Scholar
  9. Clarke, K. R. and Warwick, R. M.: 1994, Change in Marine Communities: An Approach to Statistical Analysis and Interpretation, 2nd edn, Plymouth Marine Laboratories, Plymouth, United Kingdom.Google Scholar
  10. Custer, T. W., Hines, R. H., Melancon, M. J., Hoffman, D. J., Bickham, J. W., Martin, J. W. and Henshel, D.: 1997, ‘Contaminant concentrations and biomarker response in great blue heron eggs from 10 colonies on the upper Mississippi River, USA’, Environ. Toxicol. Chem. 16, 260–271.CrossRefGoogle Scholar
  11. Custer, T. W., Custer, C. M., Hines, R. H., Sparks, D. W., Melancon, M. J., Hoffman, D. J., Bickham, J. W. and Wickliffe, J. K.: 2000, ‘Mixed-function oxygenases, oxidative stress, and chromosomal damage measured in lesser scaup wintering on the Indiana Harbor Canal’, Arch. Environ. Toxicol. Chem. 38, 522–529.CrossRefGoogle Scholar
  12. Custer, T. W., Custer, C. M., Dickerson, K., Allen, K., Melancon, M. J. and Schmidt, L. J.: 2001, ‘Polycyclic aromatic hydrocarbons, aliphatic hydrocarbons, trace elements and monooxygenase activity in birds nesting on the North Platte River, Casper, Wyoming, USA’, Environ. Toxicol. Chem. 20, 624–631.CrossRefGoogle Scholar
  13. Custer, C. M., Custer, T. W., Archuleta, A. S., Coppock, L. C., Swartz, C. D. and Bickham, J.W: 2003a, ‘A mining impacted stream: Exposure and effects of lead and other trace elements on tree swallows (Tachycineta bicolor) nesting in the upper Arkansas River basin, Colorado’, in: Hoffman et al. (eds), Handbook of Ecotoxicology, Volume 2, Lewis Publishers, Boca Raton, FL, USA, pp. 787–812.Google Scholar
  14. Custer, C. M., Custer, T. W., Dummer, P. M. and Munney, K. L.: 2003b, ‘Exposure and effects of chemical contamination on tree swallows nesting along the Housatonic River, Berkshire County, MA, USA, 1998–2000’, Environ. Toxicol. Chem. 22, 1605–1621.CrossRefGoogle Scholar
  15. Custer, C. M., Custer, T. W., Rosiu, C. J., Melancon, M. J., Bickham, J. W. and Matson, C. W.: 2005, ‘Exposure and effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin in tree swallows (Tachycineta bicolor) nesting along the Woonasquatucket River, Rhode Island’, Environ. Toxicol. Chem. 93–109.Google Scholar
  16. Dunn, P. O., Thusius, K. J., Kimber, K. and Winkler, D. W.: 2000, ‘Geographic and ecological variation in clutch size of tree swallows’, Auk 117, 215–221.CrossRefGoogle Scholar
  17. Eisler, R.: 1985, ‘Cadmium hazards to fish, wildlife, and invertebrates: A synoptic review’, U S. Fish Wildl. Serv. Biol. Rep. 85(1.2), 60.Google Scholar
  18. Eisler, R.: 1986, ‘Chromium hazards to fish, wildlife, and invertebrates: A synoptic review’, U.S. Fish Wildl. Serv. Biol. Rep. 85(1.6), 60.Google Scholar
  19. Eisler, R.: 1987, ‘Mercury hazards to fish, wildlife, and invertebrates: A synoptic review’, U.S. Fish Wildl. Serv. Biol. Rep. 85(1.10), 63.Google Scholar
  20. Fairchild, W. L., Muir, D. C.G., Currie, R. S. and Yarechewski, A. L.: 1992, ‘Emerging insects as a biotic pathway for movement of 2,3,7,8-tetrachlorodibenzofuran from lake sediments’, Environ. Toxicol. Chem. 11, 867–872.Google Scholar
  21. Furness, R. W.: 1996, ‘Cadmium in birds’, in: W. N. Beyer, G. H. Heinz, and A. W. Redmon-Norwood (eds), Environmental Contaminants in Wildlife, Interpreting Tissue Concentrations, CRC Press/Lewis Publishers, Boca Raton, FL, USA, pp. 389–404.Google Scholar
  22. Gerrard, P. M. and St. Louis, V. L.: 2001, ‘The effects of experimental reservoir creation on the bioaccumulation of methylmercury and reproductive success of tree swallows (Tachycineta bicolor)’, Environ. Sci. Technol. 35, 1329–1338.Google Scholar
  23. Griffith, O. W.: 1980, ‘Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinyl pyridine’, Anal. Biochem. 106, 207–212.CrossRefGoogle Scholar
  24. Henny, C. J., Hill, E. F., Hoffman, D. J., Spalding, M. G. and Grove, R. A.: 2002. ‘Nineteenth century mercury: Hazard to wading birds and cormorants of the Carson River, Nevada’, Ecotoxicology 11, 213–231.CrossRefGoogle Scholar
  25. Hensler, G. L. and Nichols, J. D.: 1981, ‘The Mayfield method of estimating nesting success: A model, estimators and simulation results’, Wilson Bull. 93, 42–53.Google Scholar
  26. Hoffman, D. J., Heinz, G. H. and Krynitsky, A. J.: 1989, ‘Hepatic glutathione metabolism and lipid peroxidation in response to excess dietary selenomethionine and selenite in mallard ducklings’, J. Toxicol. Environ. Health 27, 263–271.CrossRefGoogle Scholar
  27. Hoffman, D. J. and Heinz, G. H.: 1998, ‘Effects of mercury and selenium on glutathione metabolism and oxidative stress in mallard ducks’, Environ. Toxicol. Chem. 17, 161–166.CrossRefGoogle Scholar
  28. Hoffman, D. J., Ohlendorf, H. H., Marn, C. M. and Pendleton, G. W.: 1998, ‘Association of mercury and selenium with altered glutathione metabolism and oxidative stress in diving ducks from the San Francisco Bay region, USA’, Environ. Toxicol. Chem. 17, 167–172.CrossRefGoogle Scholar
  29. Hussell, C. J. T. and Quinney, T. E.: 1987, ‘Food abundance and clutch size of tree swallows Tachycineta bicolor’, Ibis 129, 243–258.Google Scholar
  30. Kelly, C. A. et al.: 1997, ‘Increases in fluxes of greenhouse gases and methyl mercury following flooding of an experimental reservoir’, Environ. Sci. Techol. 31, 1334–1344.CrossRefGoogle Scholar
  31. King, K. A., Custer, T. W. and Weaver, D. A.: 1994, ‘Reproductive success of barn swallows nesting near a selenium-contaminated lake in east Texas, USA’, Environ. Pollut. 84, 53–58.CrossRefGoogle Scholar
  32. Kraus, M. L.: 1989, ‘Bioaccumulation of heavy metals in pre-fledgling tree swallows, Tachycineta bicolor’, Bull. Environ. Contam. Toxicol. 43, 407–414.CrossRefGoogle Scholar
  33. Mayfield, H.: 1961, ‘Nesting success calculated from exposure’, Wilson Bull. 73, 255–261.Google Scholar
  34. Mayfield, H.: 1975, ‘Suggestions for calculating nest success’, Wilson Bull. 87, 456–466.Google Scholar
  35. Mengelkoch, J. M., Niemi, G. J. and Regal, R. R.: 2004, ‘Diet of the nestling tree swallow’, Condor 106, 423–429.CrossRefGoogle Scholar
  36. Quinney, T. E. and Ankney, C. D.: 1985, ‘Prey size selection by tree swallows’, Auk 102, 245–250.Google Scholar
  37. Robertson, R. J., Stutchbury, B. J. and Cohen, R. R.: 1992, ‘Tree swallow (Tachycineta bicolor)’ in: A. Poole, P. Stettenheim and F. Gill (eds), The Birds of North America, No. 11, Academy of Natural Sciences, Philadelphia, PA, USA, pp. 26.Google Scholar
  38. Sanz, J. J.: 1998, ‘Effects of geographic location and habitat on breeding parameters of great tits’, Auk 115, 1034–1051.Google Scholar
  39. Sauer, J. R. and Williams, B. K.: 1989, ‘General procedures for testing hypotheses about survival or recovery rates’, J. Wildl. Manage. 53, 137–142.Google Scholar
  40. Scheuhammer, A. M.: 1987, ‘The chronic toxicity of aluminum, cadmium, mercury, and lead in birds: A review’, Environ. Pollut. 46, 263–295.CrossRefGoogle Scholar
  41. Sedlak, J. and Lindsay, R. H.: 1968, ‘Estimate of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellmans' reagent’, Anal. Biochem. 25, 192–205.CrossRefGoogle Scholar
  42. Tietze, F.: 1969, ‘Enzymic method for quantitiative determination of nanogram amounts of total and oxidized glutathione’, Anal. Biochem. 27, 502–522.CrossRefGoogle Scholar
  43. Vindelov L. L., Christensen, I. J. and Nissen, N. I.: 1983, ‘A detergent-trypsin method for the preparation of nuclei for flow cytometric DNA analysis’, Cytometry 3, 323–327.CrossRefGoogle Scholar
  44. Wiener, J. G., Krabbenhoft, D. F., Heinz, G. F. and Scheuhammer, A. M.: 2003, ‘Ecotoxicology of mercury’, in: D. J. Hoffman, B. A. Rattner, G. A. Burton Jr. and J. Cairns Jr. (eds), Handbook of Ecotoxicology, Volume 2, Lewis Publishers, Boca Raton, FL, USA, pp. 409–463.Google Scholar
  45. Yauk, C. L. and Quinn, J. S.: 1996, ‘Multilocus DNA fingerprinting reveals high rate of heritable genetic mutation in herring gulls nesting in an industrialized urban site’, Proc. Natl. Acad. Sci. 93, 12137–12141.CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2006

Authors and Affiliations

  • Christine M. Custer
    • 1
  • Thomas W. Custer
    • 1
  • David Warburton
    • 2
  • David J. Hoffman
    • 3
  • John W. Bickham
    • 4
  • Cole W. Matson
    • 4
  1. 1.U.S. Geological SurveyUpper Midwest Environmental Sciences CenterLa CrosseUSA
  2. 2.U.S. Fish and Wildlife ServiceBloomingtonUSA
  3. 3.U.S. Geological SurveyPatuxent Wildlife Research CenterBeltsvilleUSA
  4. 4.Department of Wildlife and FisheriesTexas A&M UniversityCollege StationUSA

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