PHA-Stimulated Immune-Responsiveness in Mercury-Dosed Zebra Finches Does Not Match Results from Environmentally Exposed Songbirds

Abstract

Dietary mercury exposure is associated with suppressed immune responsiveness in birds. This study examined the immune-responsiveness of domestic zebra finches (Taeniopygia guttata) experimentally exposed to mercury through their diet. We used the phytohemagglutinin (PHA) skin-swelling test to assay the effect of two modes of mercury exposure. Some finches received exposure to mercury only after reaching sexual maturity, while others were maintained on a mercury-dosed diet throughout life, including development. Each bird received one of five dietary concentrations of methylmercury cysteine (0.0, 0.3, 0.6, 1.2 or 2.4 ppm). In contrast to a study on wild songbirds at a mercury-contaminated site, we detected no relationship between mercury level and immunological response to PHA, regardless of mode of exposure. This result represents the first major difference found by our laboratory between wild birds exposed to environmental mercury and captive birds experimentally exposed to mercury.

This is a preview of subscription content, log in to check access.

Fig. 1

References

  1. Andre J-B, Ferdy J-B, Godelle B (2003) Within-host parasite dynamics, emerging trade-off, and evolution of virulence with immune system. Evolution 57:1489–1497. doi:10.1111/j.0014-3820.2003.tb00357.x

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  3. Burger J, Gochfeld M (1997) Risk, mercury levels, and birds: relating adverse laboratory effects to field biomonitoring. Environ Res 75:160–172. doi:10.1006/enrs.1997.3778

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  5. Das K, Siebert U, Gillet A, Dupont A, Di-Poi C, Fonfara S, Mazzucchelli G, De Pauw E, De Pauw-Gillet M-C (2008) Mercury immune toxicity in harbour seals: links to in vitro toxicity. Environ Health 7:52–69. doi:10.1186/1476-069X-7-52

    Article  Google Scholar 

  6. de Visser KE, Eichten A, Coussens LM (2006) Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 6:24–37. doi:10.1038/nrc1782

    Article  Google Scholar 

  7. Finkelstein ME, Grasman KA, Croll DA, Tershy BR, Keitt BS, Jarman WM, Smith DR (2007) Contaminant-associated alteration of immune function in black-footed albatross (Phoebastria nigripes), a North Pacific predator. Environ Toxicol Chem 26:1896–1903. doi:10.1897/06-505R.1

    CAS  Article  Google Scholar 

  8. Franceschini MD, Lane OP, Evers DC, Reed JM, Hoskins B, Romero LM (2009) The corticosterone stress response and mercury contamination in free-living tree swallows, Tachycineta bicolor. Ecotoxicology 18:514–521. doi:10.1007/s10646-009-0309-2

    CAS  Article  Google Scholar 

  9. Frouin H, Loseto LL, Stern GA, Haulena M, Ross PS (2012) Mercury toxicity in beluga whale lymphocytes: limited effects of selenium protection. Aquat Toxicol 109:185–193. doi:10.1016/j.aquatox.2011.09.021

    CAS  Article  Google Scholar 

  10. Goto N, Kodama H, Okada K, Fujimoto Y (1978) Suppression of phytohemagglutinin skin response in thymectomized chickens. Poultry Sci 57:246–250. doi:10.3382/ps.0570246

    CAS  Article  Google Scholar 

  11. Hallinger KK, Cristol DA (2011) The role of weather in mediating the effect of mercury exposure on reproductive success in tree swallows. Ecotoxicology 20:1368–1377. doi:10.1007/s10646-011-0694-1

    CAS  Article  Google Scholar 

  12. Hallinger KK, Zabransky DJ, Kazmer KA, Cristol DA (2010) Birdsong differs between mercury-polluted and reference sites. Auk 127:156–161. doi:10.1525/auk.2009.09058

    Article  Google Scholar 

  13. Hawley DM, Hallinger KK, Cristol DA (2009) Compromised immune competence in free-living tree swallows exposed to mercury. Ecotoxicology 18:499–503. doi:10.1007/s10646-009-0307-4

    CAS  Article  Google Scholar 

  14. Henry KA, Varian-Ramos CW, Cristol DA, Bradley EL (2014) Oxidative damage in livers of zebra finches dosed with mercury. Ecotoxicology. doi:10.1007/s10646-014-1400-x

    Google Scholar 

  15. Herring G, Ackerman JT, Herzog MP (2012) Mercury exposure may suppress baseline corticosterone levels in juvenile birds. Environ Sci Technol 46:6339–6346. doi:10.1021/es300668c

    CAS  Article  Google Scholar 

  16. Holloway J, Scheuhammer AM, Chan HM (2003) Assessment of white blood cell phagocytosis as an immunological indicator of methylmercury exposure in birds. Arch Environ Contam Toxicol 44:493–501. doi:10.1007/s00244-002-2095-1

    CAS  Article  Google Scholar 

  17. Jackson AK, Evers DC, Folsom SB, Condon AM, Diener J, Goodrick LF, McGann AJ, Schmerfeld J, Cristol DA (2011) Mercury exposure in terrestrial birds far downstream of an historical point source. Environ Pollut 159:3302–3308. doi:10.1016/j.envpol.2011.08.046

    CAS  Article  Google Scholar 

  18. Kawai T, Akira S (2006) Innate immune recognition of viral infection. Nat Immunol 7:131–137. doi:10.1038/ni1303

    CAS  Article  Google Scholar 

  19. Keller RH, Xie L, Buchwalter DB, Franzreb KE, Simons TR (2014) Mercury bioaccumulation in Southern Appalachian birds, assessed through feather concentrations. Ecotoxicology 23:304–316. doi:10.1007/s10646-013-1174-6

    CAS  Article  Google Scholar 

  20. Kenow KP, Grasman KA, Hines RK, Meyer MW, Gendron-Fitzpatrick A, Spalding MG, Gray BR (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

    CAS  Article  Google Scholar 

  21. Lewis CA, Cristol DA, Swaddle JP, Varian-Ramos CW, Zwollo P (2013) Decreased immune response in zebra finches exposed to sublethal doses of mercury. Arch Environ Contam Toxicol 64:327–336. doi:10.1007/s00244-012-9830-z

    CAS  Article  Google Scholar 

  22. Martin LB II, Han P, Lewittes J, Kuhlman KC, 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 

  23. Moore CS, Cristol DA, Maddux SL, Varian-Ramos CW, Bradley EL (2014) Lifelong exposure to methylmercury disrupts stress-induced corticosterone response in zebra finches (Taeniopygia guttata). Environ Toxicol Chem 33:1072–1076. doi:10.1002/etc.2521

    CAS  Article  Google Scholar 

  24. Moszczynski P (1997) Mercury compounds and the immune system: a review. Int J Occup Med Environ Health 10:247–258

    CAS  Google Scholar 

  25. Navarro C, Marzal A, De Lope F, Moller AP (2003) Dynamics of an immune response in house sparrows Passer domesticus in relation to time of day, body condition and blood parasite infection. Oikos 101:291–298. doi:10.1034/j.1600-0706.2003.11663.x

    Article  Google Scholar 

  26. Nicholson JK, Osborn D (1984) Kidney lesions in juvenile starlings Sturnus vulgaris fed on a mercury-contaminated synthetic diet. Environ Pollut Ser A Ecol Biol 33:195–206. doi:10.1016/0143-1471(84)90010-2

    CAS  Article  Google Scholar 

  27. Reiche EMV, Nunes SOV, Morimoto HK (2004) Stress, depression, the immune system, and cancer. Lancet Oncol 5:617–625. doi:10.1016/S1470-2045(04)01597-9

    CAS  Article  Google Scholar 

  28. Scheuhammer AM, Meyer MW, 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

    CAS  Article  Google Scholar 

  29. Schmid-Hempel P (2008) Parasite immune evasion: a momentous molecular war. Trends Ecol Evol 23:318–326. doi:10.1016/j.tree.2008.02.011

    Article  Google Scholar 

  30. Selin NE (2013) Global change and mercury cycling: challenges for implementing a global mercury treaty. Environ Toxicol Chem. doi:10.1002/etc.2374

    Google Scholar 

  31. Siebert U, Joiris C, Holsbeek L, Benke H, Failing K, Frese K, Petzinger E (1999) Potential relation between mercury concentrations and necropsy findings in cetaceans from German waters of the North and Baltic Seas. Mar Pollut Bull 38:285–295. doi:10.1016/S0025-326X(98)00147-7

    CAS  Article  Google Scholar 

  32. Singaram G, Harikrishnan T, Chen F-Y, Jun B, Giesy JP (2013) Modulation of immune-associated parameters and antioxidant responses in the crab (Scylla serrata) exposed to mercury. Chemosphere 90:917–928. doi:10.1016/j.chemosphere.2012.06.031

    CAS  Article  Google Scholar 

  33. Smits JE, Bortolotti GR, Tella JL (2002) 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 

  34. Spickler JL (2014) Effects of sublethal methylmercury exposure on pigment coloration in a model songbird. Masters thesis, College of William and Mary, Williamsburg

  35. Takeda K, Smyth MJ, Cretney E, Hayakawa Y, Kayagaki N, Yagita H, Okumura K (2002) Critical role for tumor necrosis factor-related apoptosis-inducing ligand in immune surveillance against tumor development. J Exp Med 195:161–169. doi:10.1084/jem.20011171

    CAS  Article  Google Scholar 

  36. Tella JL, Lemus JA, Carrete M, Blanco G (2008) The PHA test reflects acquired T-cell mediated immunocompetence in birds. PLoS One 3:e295. doi:10.1371/journal.pone.0003295

    Article  Google Scholar 

  37. Thompson CK, Sakaluk SK, Masters BS, Johnson BGP, Vogel LA, Forsman AM, Johnson LS (2014) Condition-dependent sex difference in nestling house wren (Troglodytes aedon) response to phytohaemagglutinin injection. Can J Zool 92:1–7. doi:10.1139/cjz-2013-0140

    CAS  Article  Google Scholar 

  38. Varian-Ramos CW, Swaddle JP, Cristol DA (2014) Mercury reduces avian reproductive success and imposes selection: an experimental study with adult- or lifetime-exposure in zebra finch. PLoS One 9:e95674. doi:10.1371/journal.pone.0095674

    Article  Google Scholar 

  39. Wada H, Cristol DA, McNabb FMA, Hopkins WA (2009) Suppressed adrenocortical responses and thyroid hormone levels in birds near a mercury-contaminated river. Environ Sci Technol 43:6031–6038. doi:10.1021/es803707f

    CAS  Article  Google Scholar 

  40. White AE, Cristol DA (2014) Plumage coloration in belted kingfishers (Megaceryle alcyon) at a mercury-contaminated river. Waterbirds 37:144–152. doi:10.1675/063.037.0203

    Article  Google Scholar 

  41. Wolfe MF, Schwarzbach S, Sulaiman RA (1998) Effects of mercury on wildlife: a comprehensive review. Environ Toxicol Chem 17:146–160. doi:10.1002/etc.5620170203

    CAS  Article  Google Scholar 

Download references

Acknowledgments

Research was completed with oversight from the South River Science Team, a collaboration of state and federal agencies, academic institutions, and environmental interests. Funding was provided by E. I. duPont de Nemours and company. Thank you to M. Whitney and R. Ellick for technical assistance. Special thanks to all the student researchers who assisted with data gathering, particularly K. Buck, J. Ebers, J. Kihm, M. Kobiela, S. Maddux, G. Mahjoub, J. Spickler, S. Talegaonkar, and K. Wright.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Daniel A. Cristol.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Caudill, M.T., Spear, E.L., Varian-Ramos, C.W. et al. PHA-Stimulated Immune-Responsiveness in Mercury-Dosed Zebra Finches Does Not Match Results from Environmentally Exposed Songbirds. Bull Environ Contam Toxicol 94, 407–411 (2015). https://doi.org/10.1007/s00128-015-1472-1

Download citation

Keywords

  • Immune responsiveness
  • Mercury
  • Phytohemagglutinin
  • Zebra finch