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Compromised immune competence in free-living tree swallows exposed to mercury

Ecotoxicology volume 18, pages 499–503 (2009)Cite this article

Abstract

Mercury is a pervasive environmental contaminant and a well-documented immunosuppressor. However, little is known about the effects of mercury contamination on health of free-living vertebrate populations. The South River in Virginia, USA was heavily contaminated with industrial mercury from 1929 to 1950, and recent studies have documented high levels of circulating mercury in riparian songbirds breeding below the site of contamination. Here we used two standardized immune assays, mitogen-induced swelling in response to phytohaemagglutinin (PHA) and antibody response to sheep red blood cells (SRBCs), to test for effects of mercury toxicity on the immune system of female tree swallows (Tachycineta bicolor) which feed on terrestrial and aquatic insects along the contaminated waterway. We found that females breeding at mercury-contaminated sites mounted significantly weaker PHA-induced swelling responses than those at reference sites in both years of study. However, among females on the contaminated sites, individual bloodstream mercury concentration did not predict the extent of mitogen-induced swelling. We did not detect any differences between reference and contaminated females in the strength of antibody responses to SRBCs, but sample sizes for this assay were significantly smaller. Overall, our results suggest that mercury toxicity can exert sub-lethal immunosuppression in free-living, insectivorous songbirds. The potential fitness consequences of the detected differences in immunocompetence caused by mercury toxicity warrant further study.

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References

  • Brasso RL, Cristol DA (2008) Effects of mercury exposure on the reproductive success of tree swallows (Tachycineta bicolor). Ecotoxicol 17:133–141. doi:10.1007/s10646-007-0163-z

    Article  CAS  Google Scholar 

  • Carter LJ (1977) Chemical plants leave unexpected legacy for two Virginia rivers. Science 198:1015–1020. doi:10.1126/science.198.4321.1015

    Article  Google Scholar 

  • Cristol DA, Brasso RL, Condon AM, Fovargue RE, Friedman SL, Hallinger KK et al (2008) The movement of aquatic mercury through terrestrial food webs. Science 320:335. doi:10.1126/science.1154082

    Article  CAS  Google Scholar 

  • Day RD, Segars AL, Arendt MD, Lee AM, Peden-Adams MM (2007) Relationship of blood mercury levels to health parameters in the loggerhead sea turtle (Caretta caretta). Environ Health Perspect 115:1421–1428

    CAS  Google Scholar 

  • Deerenberg C, Apanius V, Daan S, Bos N (1997) Reproductive effort decreases antibody responsiveness. Proc R Soc Lond B Biol Sci 264:1021–1029. doi:10.1098/rspb.1997.0141

    Article  Google Scholar 

  • Evers DC, Burgess NM, Champoux L, Hoskins B, Major A, Goodale WM et al (2005) Patterns and interpretation of mercury exposure in freshwater avian communities in northeastern North America. Ecotoxicol 14:193–221. doi:10.1007/s10646-004-6269-7

    Article  CAS  Google Scholar 

  • Friedman SL, Brasso RL, Condon AM (2008) An improved simple nest-box trap. J Field Ornithol 79:99–101. doi:10.1111/j.1557-9263.2008.00150.x

    Article  Google Scholar 

  • Gorissen L, Snoeijs T, Van Duyse E, Eens M (2005) Heavy metal pollution affects dawn singing behaviour in a small passerine bird. Oecologia 145:504–509. doi:10.1007/s00442-005-0091-7

    Article  Google Scholar 

  • Haggqvist B, Havarinasab S, Bjorn E, Hultman P (2005) The immunosuppressive effect of methylmercury does not preclude development of autoimmunity in genetically susceptible mice. Toxicol 208:149–164. doi:10.1016/j.tox.2004.11.020

    Article  Google Scholar 

  • Henny CJ, Kaiser JL, Packard HA, Grove RA, Taft MR (2005) Assessing mercury exposure and effects to American dippers in headwater streams near mining sites. Ecotoxicol 14:709–725. doi:10.1007/s10646-005-0023-7

    Article  CAS  Google Scholar 

  • Hill CH (1979) Dietary influences on resistance to Salmonella infection in chicks. Fed Proc 38:2129–2133

    CAS  Google Scholar 

  • Janssens E, Dauwe T, Pinxten R, Bervoets L, Blust R, Eens M (2003) Effects of heavy metal exposure on the condition and health of nestlings of the great tit (Parus major), a small songbird species. Environ Pollut 126:267–274. doi:10.1016/S0269-7491(03)00185-4

    Article  CAS  Google Scholar 

  • Kennedy MW, Nager RG (2006) The perils and prospects of using phytohaemagglutinin in evolutionary ecology. Trends Ecol Evol 21:653–655. doi:10.1016/j.tree.2006.09.017

    Article  Google Scholar 

  • Kenow KP, Grasman KA, Hines RK, Meyer MW, Gendron-Fitzpatrick A, Spalding MG et al (2007) Effects of methylmercury exposure on the immune function of juvenile common loons (Gavia immer). Environ Toxicol Chem 26:1460–1469. doi:10.1897/06-442R.1

    Article  CAS  Google Scholar 

  • Kumar A, Chauhan RS, Singh NP (1999) Immunopathological effect of mercury on humoral immune response in chickens. Indian J Anim Sci 69:550–552

    Google Scholar 

  • Martin LB II, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct Ecol 20:290–299. doi:10.1111/j.1365-2435.2006.01094.x

    Article  Google Scholar 

  • O’Halloran J, Irwin S, Harrison S, Smiddy P, O’Mahony B (2003) Mercury and organochlorine content of dipper Cinclus cinclus eggs in south-west Ireland: trends during 1990–1999. Environ Pollut 123:85–93. doi:10.1016/S0269-7491(02)00336-6

    Article  Google Scholar 

  • Rimmer CC, McFarland KP, Evers DC, Miller EK, Aubry Y, Busby D et al (2005) Mercury concentrations in Bicknell’s thrush and other insectivorous passerines in Montane forests of northeastern North America. Ecotoxicol 14:223–240. doi:10.1007/s10646-004-6270-1

    Article  CAS  Google Scholar 

  • Robertson RJ, Stutchbury BJ, Cohen RR (1992) Tree Swallow (Tachycineta bicolor). In: Poole A, Stettenheim P, Gill F (eds) The birds of North America, No. 11. The Academy of Natural Sciences, Philadelphia PA, and American Ornithologists’ Union, Washington DC

    Google Scholar 

  • Scheuhammer AM, Meyer WM, Sandheinrich MB, Murray MW (2007) Effects of environmental methylmercury on the health of wild birds, mammals, and fish. Ambio 36:12–19. doi:10.1579/0044-7447(2007)36[12:EOEMOT]2.0.CO;2

    Article  CAS  Google Scholar 

  • Shenker BJ, Rooney C, Vitale L, Shapiro IM (1992) Immunotoxic effects of mercuric compounds on human lymphocytes and monocytes: I. Suppression of T-cell activation. Immunopharmacol Immunotoxicol 14:539–553

    Article  CAS  Google Scholar 

  • Shriver WG, Evers DC, Hodgman TP, Macculloch BJ, Taylor RJ (2006) Mercury in sharp-tailed sparrows breeding in coastal wetlands. Environ Bioindic 1:129–135. doi:10.1080/15555270600695734

    Article  CAS  Google Scholar 

  • Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572. doi:10.1046/j.1365-2435.1999.00338.x

    Article  Google Scholar 

  • Spalding MG, Frederick PC, McGill HC, Bouton SN, Richey LJ, Schumacher IM et al (2000) Histologic, neurologic, and immunologic effects of methylmercury in captive great egrets. J Wildl Dis 3:423–435

    Google Scholar 

  • Stutchbury BJ, Robertson RJ (1986) A simple trap for catching birds in nest boxes. J Field Ornithol 57:64–65

    Google Scholar 

  • Wiener J, Krabbenhoft D, Heinz G, Scheuhammer A (2003) Ecotoxicology of mercury. In: Hoffman D, Rattner BA, Burton GA Jr, Cairns J Jr (eds) Handbook of ecotoxiology. CRC Press, Boca Raton, pp 409–463

    Google Scholar 

  • Zelikoff JT, Smialowicz R, Bigazzi PE, Goyer RA, Lawrence DA, Maibach HI et al (1994) Immunomodulation by metals. Fundam Appl Toxicol 22:1–7. doi:10.1006/faat.1994.1001

    Article  CAS  Google Scholar 

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Acknowledgments

Funding was provided by E.I. DuPont de Nemours and Company and the Vice Provost for Research at College of William & Mary and NSF UBM 0436318. We thank the South River Science Team, Rebecka Brasso, Anne Condon, Rachel Fovargue, Adrian Monroe, Robert Taylor and the many cooperative landowners in the Shenandoah Valley. Two anonymous reviewers helped to improve the manuscript.

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Authors and Affiliations

  1. Department of Biological Sciences, Virginia Tech, 4036 Derring Hall, Blacksburg, VA, 24061, USA

    Dana M. Hawley

  2. Institute for Integrative Bird Behavior Studies, Department of Biology, College of William and Mary, P.O. Box 8795, Williamsburg, VA, 23187, USA

    Kelly K. Hallinger & Daniel A. Cristol

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  1. Dana M. Hawley
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  2. Kelly K. Hallinger
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  3. Daniel A. Cristol
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Correspondence to Dana M. Hawley.

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Hawley, D.M., Hallinger, K.K. & Cristol, D.A. Compromised immune competence in free-living tree swallows exposed to mercury. Ecotoxicology 18, 499–503 (2009). https://doi.org/10.1007/s10646-009-0307-4

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  • DOI: https://doi.org/10.1007/s10646-009-0307-4

Keywords

  • Mercury
  • Songbird
  • Immune competence
  • Tree swallow
  • Tachycineta bicolor