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Ecologically-relevant exposure to methylmercury during early development does not affect adult phenotype in zebra finches (Taeniopygia guttata)

Abstract

Methylmercury causes behavioural and reproductive effects in adult mammals via early developmental exposure. Similar studies in birds are limited and mostly focussed on aquatic systems, but recent work has reported high blood mercury concentrations in terrestrial, passerine songbirds. We used the zebra finch (Taeniopygia guttata) as a model to explore the long-term effects of early developmental exposure to methylmercury exposure. Chicks were dosed orally with either the vehicle control, 0.0315 µg Hg/g bw/day, or 0.075 µg Hg/g bw/day throughout the nestling period (days 1–21 post-hatching). We then measured (a) short-term effects on growth, development, and behaviour (time to self-feeding, neophobia) until 30 days of age (independence), and (b) long-term effects on courtship behaviour and song (males) and reproduction (females) once methylmercury-exposed birds reached sexual maturity (90 days post-hatching). High methylmercury treated birds had mean blood mercury of 0.734 ± 0.163 µg/g at 30 days post-hatching, within the range of values reported for field-sampled songbirds at mercury contaminated sites. However, there were no short-term effects of treatment on growth, development, and behaviour of chicks, and no long-term effects on courtship behaviour and song in males or reproductive performance in females. These results suggest that the nestling period is not a critical window for sensitivity to mercury exposure in zebra finches. Growing nestlings can reduce blood mercury levels through somatic growth and depuration into newly growing feathers, and as a result they might actually be less susceptible compared to adult birds receiving the same level of exposure.

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References

  1. Airey DC, DeVoogd TJ (2000) Greater song complexity is associated with augmented song system anatomy in zebra finches. Neuroreport 11:1749–1754

    CAS  Article  Google Scholar 

  2. Bailey DJ, Rosebush JC, Wade J (2002) The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch. J Neurobiol 52:43–51

    Article  Google Scholar 

  3. Basu N, Tutino R, Zhang Z, Cantonwine DE, Goodrich JM, Somers EC, Rodriguez L, Schnaas L, Solano M, Mercado A, Peterson K, Sánchez BN, Hernández-Avila M, Hu H, Maria Téllez-Rojo M (2014) Mercury levels in pregnant women, children, and seafood from Mexico City. Environ Res 135:63–69

    CAS  Article  Google Scholar 

  4. Bennett RS, French JB, Rossmann R, Haebler R (2009) Dietary toxicity and tissue accumulation of methylmercury in American Kestrels. Arch Environ Contam Toxicol 56:149–156

    CAS  Article  Google Scholar 

  5. Beyrouty P, Stamler CJ, Liu JN, Loua KM, Kubow S, Chan HM (2006) Effects of prenatal methylmercury exposure on brain monoamine oxidase activity and neurobehavior of rats. Neurotoxicol Teratol 28:251–259

    CAS  Article  Google Scholar 

  6. Bornhausen M, Müsch HR, Greim H (1980) Operant behavior performance changes in rats after prenatal methylmercury exposure. Toxicol Appl Pharm 56:305–310

    CAS  Article  Google Scholar 

  7. Brasso RL, Cristol DA (2008) Effects of mercury exposure on the reproductive success of tree swallows (Tachycineta bicolor). Ecotoxicology 17:133–141

    CAS  Article  Google Scholar 

  8. Burbacher TM, Grant KS, Mayfield DB, Gilbert SG, Rice DC (2005) Prenatal methylmercury exposure affects spatial vision in adult monkeys. Toxicol Appl Pharm 208:21–28

    CAS  Article  Google Scholar 

  9. Castoldi AF, Coccini T, Ceccatelli S, Manzo L (2001) Neurotoxicity and molecular effects of methylmercury. Brain Res Bull 55:197–203

    CAS  Article  Google Scholar 

  10. Castoldi AF, Onishchenko N, Johansson C, Coccini T, Roda E, Vahter M, Ceccatelli S, Manzo L (2008) Neurodevelopmental toxicity of methylmercury: Laboratory animal data and their contribution to human risk assessment. Regul Toxicol Pharmcol 51:215–229

    CAS  Article  Google Scholar 

  11. Ceccatelli S, Bose R, Edoff K, Onishchenko N, Spulber S (2013) Long-lasting neurotoxic effects of exposure to methylmercury during development. J Intern Med 273(5):490–497. https://doi.org/10.1111/joim.12045

    CAS  Article  Google Scholar 

  12. Clarkson TW, Magos L (2006) The toxicology of mercury and its chemical compounds. Crit Rev Toxicol 36:609–662

    CAS  Article  Google Scholar 

  13. Condon AM, Cristol DA (2009) Feather growth influences blood mercury level of young songbirds. Environ Toxicol Chem 28:395–401

    CAS  Article  Google Scholar 

  14. Crino OL, Buchanan KL, Trompf L, Mainwaring MC, Griffith SC (2017) Stress reactivity, condition, and foraging behavior in zebra finches: effects on boldness, exploration, and sociality. Gen Comp Endocrinol 244:101–107

    CAS  Article  Google Scholar 

  15. 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 320:335–335

    CAS  Article  Google Scholar 

  16. Elliott KH, Elliott JE (2016) Origin of sulfur in diet drives spatial and temporal mercury trends in seabird eggs from Pacific Canada 1968–2015. Environ Sci Technol 50:13380–13386

    CAS  Article  Google Scholar 

  17. Eng ML, Elliott JE, MacDougall-Shackleton SA, Letcher RJ, Williams TD (2012) Early exposure to 2,2’,4,4’,5-Pentabromodiphenyl Ether (BDE-99) affects mating behavior of zebra finches. Toxicol Sci 127:269–276

    CAS  Article  Google Scholar 

  18. Evers DC, Savoy LJ, DeSorbo CR, Yates DE, Hanson W, Taylor KM, Siegel LS, Cooley JH, Bank MS, Major A, Munney K, Mower BF, Vogel HS, Schoch N, Pokras M, Goodale MW, Fair J (2008) Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 17:69–81

    CAS  Article  Google Scholar 

  19. Falluel-Morel A, Sokolowski K, Sisti HM, Zhou X, Shors TJ, DiCicco-Bloom E (2007) Developmental mercury exposure elicits acute hippocampal cell death, reductions in neurogenesis, and severe learning deficits during puberty. J Neurochem 103:1968–1981

    CAS  Article  Google Scholar 

  20. Forstmeier W, Segelbacher G, Mueller C, Kempanaers B (2007) Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata). Mol Ecol 16:4039–4050

    CAS  Article  Google Scholar 

  21. Gillet A-MTY, Seewagen CL (2014) Mercury exposure of a wetland songbird, Agelaius phoeniceus, in the New York metropolitan area and its effect on nestling growth rate. Environ Monit Assess 186:4029–4036

    CAS  Article  Google Scholar 

  22. Griffith SC, Buchanan KL (2010) The Zebra Finch: The ultimate Australian supermodel. Emu 110:v–xii

    Article  Google Scholar 

  23. Hallinger KK, Zabransky DJ, Kazmer KA, Cristol DA (2010) Birdsong differs between mercury-polluted and reference Sites. Auk 127:156–161

    Article  Google Scholar 

  24. Henry KA, Cristol DA, Varian-Ramos CW, Bradley EL (2015) Oxidative stress in songbirds exposed to dietary methylmercury. Ecotoxicology 24:520–526

    CAS  Article  Google Scholar 

  25. Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR, Kondrad SL, Erwin CA (2009) Species differences in the sensitivity of avian embryos to methylmercury. Arch Environ Contam Toxicol 56:129–138

    CAS  Article  Google Scholar 

  26. Hodgson ZG, Meddle SL, Roberts ML, Buchanan KL, Evans MR, Metzdorf R, Gahr M, Healy SD (2007) Spatial ability is impaired and hippocampal mineralocorticoid receptor mRNA expression reduced in zebra finches (Taeniopygia guttata) selected for acute high corticosterone response to stress. Proc R Soc B 274:239–245

    CAS  Article  Google Scholar 

  27. Hu G, Jin M, Lin X, Guo C, Zhang L, Sun Z (2010) Mercury distribution in neonatal rat brain after intrauterine methylmercury exposure. Environ Toxicol Pharmacol 29:7–11

    CAS  Article  Google Scholar 

  28. Jackson AK, Evers DC, Adams EM, Cristol DA, Eagles-Smith C, Edmonds ST, Gray CE, Hoskins B, Lane OP, Sauer A et al. (2015) Songbirds as sentinels of mercury in terrestrial habitats of eastern North America. Ecotoxicology 24:453–467

    CAS  Article  Google Scholar 

  29. Jackson AK, Evers DC, Etterson MA, Condon AM, Folsom SB, Detweiler J, Schmerfeld J, Cristol DA (2011) Mercury exposure affects the reproductive success of a free-living terrestrial songbird, the Carolina Wren (Thryothorus ludovicianus). Auk 128:759–769

    Article  Google Scholar 

  30. Kenow KP, Meyer MW, Hines RK, Karasov WH (2007) Distribution and accumulation of mercury in tissues of captive-reared common loon (Gavia immer) chicks. Environ Toxicol Chem 26:1047–1055

    CAS  Article  Google Scholar 

  31. Kobiela ME, Cristol DA, Swaddle JP (2015) Risk-taking behaviours in zebra finches affected by mercury exposure. Anim Behav 103:153–160

    Article  Google Scholar 

  32. McKay JL, Maher CR (2012) Relationship between blood mercury levels and components of male song in Nelson’s sparrows (Ammodramus nelsoni). Ecotoxicology 21:2391–2397

    CAS  Article  Google Scholar 

  33. Monteiro LR, Furness RW (2001) Kinetics, dose-response, excretion, and toxicity of methylmercury in free-living Cory’s shearwater chicks. Environ Toxicol Chem 20:1816–1823

    CAS  Google Scholar 

  34. Oberlander JG, Schlinger BA, Clayton NS, Saldanha CJ (2004) Neural aromatization accelerates the acquisition of spatial memory via an influence on the songbird hippocampus. Horm Behav 45:250–258

    CAS  Article  Google Scholar 

  35. Pacyna EG, Pacyna JM, Steenhuisen F, Wilson S (2006) Global anthropogenic mercury emission inventory for 2000. Atmos Environ 40:4048–4063

    CAS  Article  Google Scholar 

  36. Patel SN, Clayton NS, Krebs JR (1997) Hippocampal tissue transplants reverse lesion-induced spatial memory deficits in zebra finches (Taeniopygia guttata). J Neurosci 17:3861–3869

    CAS  Google Scholar 

  37. Provencher JF, Mallory ML, Braune BM, Forbes MR, Gilchrist HG (2014) Mercury and marine birds in Arctic Canada: effects, current trends, and why we should be paying closer attention. Environ Rev 22:244–255

    CAS  Article  Google Scholar 

  38. Rimmer CC, McFarland KP, Evers DC, Miller EK, Aubry Y, Busby D, Taylor RJ (2005) Mercury concentrations in Bicknell’s Thrush and other insectivorous passerines in montane forests of Northeastern North America. Ecotoxicology 14:223–240

    CAS  Article  Google Scholar 

  39. Rimmer CC, Miller EK, McFarland KP, Taylor RJ, Faccio SD (2010) Mercury bioaccumulation and trophic transfer in the terrestrial food web of a montane forest. Ecotoxicology 19:697–709

    CAS  Article  Google Scholar 

  40. Rutkiewicz J, Basu N (2013) Methylmercury egg injections: Part 1-Tissue distribution of mercury in the avian embryo and hatchling. Ecotoxicol Environ Saf 93:68–76

    CAS  Article  Google Scholar 

  41. Sadananda M, Bischof H-J (2004) c-fos is induced in the hippocampus during consolidation of sexual imprinting in the zebra finch (Taeniopygia guttata). Hippocampus 14:19–27

    CAS  Article  Google Scholar 

  42. Sakamoto M, Kakita A, Bezerra de Oliveira R, Sheng Pan H, Takahashi H (2004) Dose-dependent effects of methylmercury administered during neonatal brain spurt in rats. Dev Brain Res 152:171–176

    CAS  Article  Google Scholar 

  43. Salvante KG, Vézina F, Williams TD (2010) Evidence for within-individual energy reallocation in cold-challenged, egg-producing birds. J Exp Biol 213(12):1991–2000. https://doi.org/10.1242/jeb.036319

    Article  Google Scholar 

  44. Scheuhammer AM, Lord S, Wayland M, Burgess N, Champoux L, Elliott JE (2016) Major correlates of mercury in small fish and common loons (Gavia immer) across four large study sites in Canada. Environ Pollut 210:361–370

    CAS  Article  Google Scholar 

  45. Scheuhammer AM, Meyer MW, Sandheinrich MB, Murray MW (2007) Effects of environmental methylmercury on the health of wild birds, mammals, and fish. AMBIO 36(1):12–19https://doi.org/10.1579/0044-7447(2007)36[12:eoemot]2.0.co;2

    CAS  Article  Google Scholar 

  46. Seewagen CL (2010) Threats of environmental mercury to birds: knowledge gaps and priorities for future research. Bird Conserv Int 20:112–123

    Article  Google Scholar 

  47. Selin NE (2009) Global biogeochemical cycling of mercury: a review. Annu Rev Environ Resour 34:43–63

    Article  Google Scholar 

  48. Sitarek K, Gralewicz S (2009) Early developmental effects of separate or combined perinatal exposure to Methylmercury (MeHg) and 2,2’,4,4’,5,5’-Hexachlorobiphenyl (PCB 153) in the rat. Int J Occup Med Environ Health 22:89–105

    Article  Google Scholar 

  49. Sokolowski K, Falluel-Morel A, Zhou X, DiCicco-Bloom E (2011) Methylmercury (MeHg) elicits mitochondrial-dependent apoptosis in developing hippocampus and acts at low exposures. Neurotoxicology 32:535–544

    CAS  Article  Google Scholar 

  50. Spalding MG, Frederick PC, McGill HC, Bouton SN, Richey LJ, Schumacher IM, Blackmore CGM, Harrison J (2000) Histologic, neurologic, and immunologic effects of methylmercury in captive great egrets. J Wildl Dis 36:423–435

    CAS  Article  Google Scholar 

  51. 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

    Article  Google Scholar 

  52. Weiner J, Krabbenhoft D, Heinz G, Scheuhammer A (2003) Ecotoxicology of mercury. In: Hoffman DJ, Rattner BA, Burton Jr GA, Cairns Jr J (eds) Handbook of ecotoxicology, 2nd edn. CRC Press, Boca Raton, FL, p 409–463

  53. Weiss B, Stern S, Cox C, Balys M (2005) Perinatal and lifetime exposure to methylmercury in the mouse: behavioral effects. Neurotoxicology 26:675–690

    CAS  Article  Google Scholar 

  54. Whitney M, Cristol D (2017) Rapid depuration of mercury in songbirds accelerated by feather molt. Environ Toxicol Chem. https://doi.org/10.1002/etc.3888

  55. Whitney MC, Cristol DA (2018) Impacts of Sublethal Mercury Exposure on Birds: A Detailed Review Rev Environ Contam Toxicol 244:113–163. https://doi.org/10.1007/398_2017_4

    Google Scholar 

  56. Williams TD (1996) Intra- and inter-individual variation in reproductive effort in captive-breeding zebra finches (Taeniopygia guttata).Can J Zool 74:85–91

    Article  Google Scholar 

  57. Yu MS, Eng ML, Williams TD, Basu N, Elliott JE (2016) Acute embryotoxic effects but no long term reproductive effects of in ovo methylmercury exposure in zebra finches (Taeniopygia guttata): acute but no long-term effects of in ovo methylmercury exposure in a passerine model. Environ Toxicol Chem 9999:1–7

    Google Scholar 

  58. Yu MS, Eng ML, Williams TD, Guigueno MF, Elliott JE (2017) Assessment of neuroanatomical and behavioural effects of in ovo methylmercury exposure in zebra finches (Taeniopygia guttata). Neurotoxicology 59:33–39

    CAS  Article  Google Scholar 

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Funding

Funding was provided by the Canadian Atmospheric Regulatory Agenda program of Environment Canada and National Science and Engineering Research Council Discovery grants RGPIN-155395-2012 (TDW) and RGPIN-2016-04583 (JE).

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Correspondence to Tony D. Williams.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Specifically, work was conducted under a Simon Fraser University Animal Committee Permit (1070B-08) according to the guidelines of the Canadian Committee on Animal Care. This article does not contain any studies with human participants performed by any of the authors.

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Morran, S.A.M., Elliott, J.E., Young, J.M.L. et al. Ecologically-relevant exposure to methylmercury during early development does not affect adult phenotype in zebra finches (Taeniopygia guttata). Ecotoxicology 27, 259–266 (2018). https://doi.org/10.1007/s10646-017-1890-4

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Keywords

  • Methylmercury
  • Avian
  • Growth
  • Behaviour
  • Reproduction
  • Zebra Finch