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Dietary mercury exposure causes decreased escape takeoff flight performance and increased molt rate in European starlings (Sturnus vulgaris)

Ecotoxicology volume 23, pages 1464–1473 (2014)Cite this article

Abstract

Mercury is a widespread and persistent environmental contaminant that occurs in aquatic and terrestrial habitats. Recently, songbirds that forage from primarily terrestrial sources have shown evidence of bioaccumulation of mercury, but little research has assessed the effects of mercury on their health and fitness. There are many indications that mercury negatively affects neurological functioning, bioenergetics, and behavior through a variety of mechanisms and in a wide array of avian taxa. Effective flight is crucial to avian fitness and feather molt is an energetically expensive life history trait. Therefore, we investigated whether mercury exposure influenced flight performance and molt in a common songbird, the European starling (Sturnus vulgaris). Specifically, we dosed the diet of captive starlings with methylmercury cysteine at 0.0, 0.75, or 1.5 μg/g wet weight and recorded changes in flight performance after 1 year of dietary mercury exposure. We also recorded the annual molt of wing feathers. We found that individuals dosed with mercury exhibited decreased escape takeoff flight performance compared with controls and blood mercury was also correlated with an increased rate of molt, which can reduce flight performance and thermoregulatory ability. This study reveals two novel endpoints, flight performance and molt, that may be affected by dietary mercury exposure. These findings suggest a potential impact on wild songbirds exposed to mercury levels comparable to the high dosage levels in the present study. Any decrease in flight efficiency could reduce fitness due to a direct impact on survival during predation events or by decreased efficiency in other critical activities (such as foraging or migration) that require efficient flight.

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References

  • Alvarez MC, Murphy CA, Rose KA, McCarthy ID, Fuiman LA (2006) Maternal body burdens of methylmercury impair survival skills of offspring in Atlantic croaker (Micropogonias undulatus). Aquat Toxicol 80:329–337. doi:10.1016/j.aquatox.2006.09.010

    Article  CAS  Google Scholar 

  • Aschner M, Syversen T, Souza DO, Rocha JBT, Farina M (2007) Involvement of glutamate and reactive oxygen species in methylmercury neurotoxicity. Braz J Med Biol Res 40:285–291. doi:10.1590/S0100-879X2007000300001

    Article  CAS  Google Scholar 

  • Boening DW (2000) Ecological effects, transport, and fate of mercury: a general review. Chemosphere 40:1335–1351. doi:10.1016/S0045-6535(99)00283-0

    Article  CAS  Google Scholar 

  • Bouton SN, Frederick PC, Spalding MG, McHill H (1999) Effects of chronic, low concentrations of dietary methylmercury on the behavior of juvenile great egrets. Environ Toxicol 18:1934–1939. doi:10.1002/etc.5620180911

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Burke JN, Bergeron CM, Todd BD, Hopkins WA (2010) Effects of mercury on behavior and performance of northern two-lined salamanders (Eurycea bislineata). Environ Poll 158:3546–3551. doi:10.1016/j.envpol.2010.08.017

    Article  CAS  Google Scholar 

  • Cai Y, Liu G, O’Driscoll N (2011) Environmental chemistry and toxicology of mercury. Wiley, Hoboken

    Google Scholar 

  • Cambier S, Benard G, Mesmer-Dudons N, Gonzalez P, Rossignol R, Brethes D, Bourdineaud JP (2009) At environmental doses, dietary methylmercury inhibits mitochondrial energy metabolism in skeletal muscles of the zebra fish (Danio rerio). Int J Biochem Cell Biol 41:791–799. doi:10.1016/j.biocel.2008.08.008

    Article  CAS  Google Scholar 

  • Condon AM, Cristol DA (2009) Feather growth influences blood mercury level of young songbirds. Environ Toxicol Chem 28:395–401. doi:10.1897/08-094.1

    Article  CAS  Google Scholar 

  • Criscuolo F, Monaghan P, Proust A, Skorpilová J, Laurie J, Metcalfe NB (2011) Costs of compensation: effect of early life conditions and reproduction on flight performance in zebra finches. Oecologia 167:315–323. doi:10.1007/s00442-011-1986-0

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Dawson A (2003) A detailed analysis of primary feather moult in European starlings—new feather mass increases at a constant rate. Ibis 145:E69–E76. doi:10.1046/j.1474-919X.2003.00161.x

    Article  Google Scholar 

  • Dawson A, Hinsley SA, Ferns PN, Bosner RH, Eccleston L (2000) Rate of moult affects feather quality: a mechanism linking current reproductive effort to future survival. Proc R Soc Lond B 267:2093–2098. doi:10.1098/rspb.2000.1254

    Article  CAS  Google Scholar 

  • Dial KP, Jackson BE, Segre P (2008) A fundamental avian wing-stroke provides a new perspective on the evolution of flight. Nature 451:985–989. doi:10.1038/nature06517

    Article  CAS  Google Scholar 

  • Dickens MJ, Romero LM (2009) Wild European starlings (Sturnus vulgaris) adjust to captivity with sustained sympathetic nervous system drive and a reduced flight-to-flight response. Phys Biochem Zool 82:603–610. doi:10.1086/603633

    Article  Google Scholar 

  • Driscoll C, Han YJ, Chen CY, Evers DC, Lambert KF, Holsen TM, Kamman NC, Munson RK (2007) Mercury contamination in forest and freshwater ecosystems in the Northeastern United States. Bioscience 57:17–28. doi:10.1641/b570106

    Article  Google Scholar 

  • Evers DC, Savoy LJ, DeSorbo CR, Yates DE, Hanson W, Taylor KM, Siegel LS, Cooley JH Jr, 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. doi:10.1007/s10646-007-0168-7

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Frederick P, Jayasena N (2011) Altered pairing behaviour and reproductive success in white ibises exposed to environmentally relevant concentrations of methylmercury. Proc R Soc Lond B 278:1851–1857. doi:10.1098/rspb.2010.2189

    Article  Google Scholar 

  • Friedman AS, Chen H, Rabuck LD, Zirkin BR (1998) Accumulation of dietary methylmercury in the testes of the adult brown Norway rats: impaired testicular and epididymal function. Environ Toxicol Chem 17:867–871. doi:10.1002/etc.5620170514

    Article  Google Scholar 

  • Fryday SL, Hart ADM, Marczylo TH (1995) Effects of sublethal exposure to an organophosphate on the flying performance of captive starlings. Bull Environ Contam Toxicol 55:366–373. doi:10.1007/bf00206674

    CAS  Google Scholar 

  • Giesy J, Feyk L, Jones P, Kannan K, Sanderson T (2003) Review of the effects of endocrine-disrupting chemicals in birds. Pure Appl Chem 75:2287–2303. doi:10.1351/pac200375112287

    Article  CAS  Google Scholar 

  • Ginn HB, Melville DS (1983) Moult in birds. British Trust for Ornithology, Norfolk

    Google Scholar 

  • Glaser V, Leipnitz G, Straliotto MR, Oliveira J, dos Santos VV, Duval Wannmacher CM, de Bern AF, Teixeira Rocha JB, Farina M, Latini A (2010) Oxidative stress-mediated inhibition of brain creatine kinase activity by methylmercury. Neurotoxicology 31:454–460. doi:10.1016/j.neuro.2010.05.012

    Article  CAS  Google Scholar 

  • Hahn T, Swingle J, Wingfield J, Ramenofsky M (1992) Adjustments of the prebasic molt schedule in birds. Ornis Scand 23:314–321. doi:10.2307/3676655

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 

  • 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

    Article  CAS  Google Scholar 

  • Heath JA, Frederick PC (2005) Relationships among mercury concentrations, hormones, and nesting effort of white ibises (Eudocimus albus) in the Florida everglades. Auk 122:255–267. doi:10.1642/0004-8038(2005)122[0255:RAMCHA]2.0.CO;2

  • Hoffman DJ, Heinz GH (1998) Effects of mercury and selenium on glutathione metabolism and oxidative stress in mallard ducks. Environ Toxicol Chem 17:161–166. doi:10.1897/1551-5028(1998)017<0161:eomaso>2.3.co;2

    Article  CAS  Google Scholar 

  • Hontela A, Rasmussen JB, Audet C, Chevalier G (1992) Impaired cortisol response in fish from environments polluted by PAHs, PCBs, and mercury. Arch Environ Contam Toxicol 22:278–283. doi:10.1007/bf00212086

    Article  CAS  Google Scholar 

  • 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 Poll 159:3302–3308. doi:10.1016/j.envpol.2011.08.046

    Article  CAS  Google Scholar 

  • Jakka NM, Rao TG, Rao JV (2007) Locomotor behavioral response of mosquitofish (Gambusia affinis) to subacute mercury stress monitored by video tracking system. Drug Chem Toxicol 30:383–397. doi:10.1080/01480540701522551

    Article  CAS  Google Scholar 

  • Laties VG, Evans HL (1980) Methylmercury induced changes in operant discrimination by the pigeon. J Pharmacol Exp Ther 214:620–628

    CAS  Google Scholar 

  • Leblond VS, Hontela A (1999) Effects of in vitro exposures to cadmium, mercury, zinc, and 1-(2-chlorophenyl)-1-(4-chlorophenyl)-2,2-dichloroethane on steroidogenesis by dispersed interrenal cells of rainbow trout (Oncorhynchus mykiss). Toxicol Appl Pharm 157:16–22. doi:10.1006/taap.1999.8660

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lima SL (1993) Ecological and evolutionary perspectives on escape from predatory attack: a survey of North American birds. Wilson Bull 105:1–47

    Google Scholar 

  • Lodenius M, Solonen T (2013) The use of feathers of birds of prey as indicators of metal pollution. Ecotoxicology 22:1319–1334. doi:10.1007/s10646-013-1128-z

    Article  CAS  Google Scholar 

  • Metcalfe NB, Ure SE (1995) Diurnal-variation in-flight performance and hence potential predation risk in small birds. Proc R Soc Lond B 261:395–400. doi:10.1098/rspb.1995.0165

    Article  Google Scholar 

  • Nam D, Rutkiewicz J, Basu N (2012) Multiple metals exposure and neurotoxic risk in bald eagles (Haliaeetus leucocephalus) from two Great Lakes states. Environ Toxicol Chem 31:623–631. doi:10.1002/etc.1712

    Article  CAS  Google Scholar 

  • Nocera JJ, Taylor PD (1998) In situ behavioral response of common loons associated with elevated mercury (Hg) exposure. Conserv Ecol [Ecology and Society] 2(2):10

  • Nolan V, Ketterson ED, Ziegenfus C, Chandler CR, Cullen DP (1992) Testosterone and avian life histories: effects of experimentally elevated testosterone on molt and survival in male dark-eyed juncos. Condor 94:364–370. doi:10.2307/1369209

    Article  Google Scholar 

  • Olsen B, Evers DC, DeSorbo C (2000) Effect of methylated mercury on the diving frequency of the common loon. J Ecol Res 2:67–72

    Google Scholar 

  • Pyle P (1997) Identification guide to North American birds. Slate Creek Press, Bolinas

    Google Scholar 

  • Ralph CJ, Geupel GR, Pyle P, Martin TE, DeSante DF (1993) Handbook of field methods for monitoring landbirds. General technical report PSW-GTR-144. Pacific Southwest Research Station, Forest Service, Department of Agriculture, Albany, CA

  • Rayner J (1985) Bounding and undulating flight in birds. J Theor Biol 117:47–77. doi:10.1016/s0022-5193(85)80164-8

    Article  Google Scholar 

  • Renner M (2006) Repeatable measures of take-off flight performance in auklets. J Zool 268:395–404. doi:10.1111/j.1469-7998.2005.00036.x

    Article  Google Scholar 

  • 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. doi:10.1007/s10646-004-6270-1

    Article  CAS  Google Scholar 

  • Seewagen CL (2010) Threats of environmental mercury to birds: knowledge gaps and priorities for future research. Bird Conserv Int 20:112–123. doi:10.1017/S095927090999030X

    Article  Google Scholar 

  • Spalding M, Frederick P, McGill H, Bouton S, Richey L, Schumacher I, Blackmore C, Harrison J (2000) Histologic, neurologic, and immunologic effects of methylmercury in captive great egrets. J Wildl Dis 36:423–435. doi:10.7589/0090-3558-36.3.423

    Article  CAS  Google Scholar 

  • Swaddle JP, Witter MS (1997) The effects of molt on the flight performance, body mass, and behavior of European starlings (Sturnus vulgaris): an experimental approach. Can J Zool 75:1135–1146. doi:10.1139/z97-136

    Article  Google Scholar 

  • Swaddle JP, Witter MS, Cuthill IC, Budden A, McCowen P (1996) Plumage condition affects flight performance in common starlings: implications for developmental homeostasis, abrasion and moult. J Avian Biol 27:103–111. doi:10.2307/3677139

    Article  Google Scholar 

  • Swaddle JP, Williams EV, Rayner JMV (1999) The effect of simulated flight feather moult on escape take-off performance in starlings. J Avian Biol 30:351–358. doi:10.2307/3677007

    Article  Google Scholar 

  • Tobalske BW, Puccinelli LA, Sheridan DC (2005) Contractile activity of the pectoralis in the zebra finch according to mode and velocity of flap-bounding flight. J Exp Biol 208:2895–2901. doi:10.1242/jeb.01734

    Article  Google Scholar 

  • Vagasi CI, Pap PL, Tokolyi J, Szekely E, Barta Z (2011) Correlates of variation in flight feather quality in the great tit Parus major. Ardea 99:53–60. doi:10.5253/078.099.0107

    Article  Google Scholar 

  • 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 

  • Veasey JS, Metcalfe NB, Houston DC (1998) A reassessment of the effect of body mass upon flight speed and predation risk in birds. Anim Behav 56:883–889

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wiersma P, Salomons HM, Verhulst S (2005) Metabolic adjustments to increasing foraging costs of starlings in a closed economy. J Exp Biol 208:4099. doi:10.1242/jeb.01855

    Article  Google Scholar 

  • Witter MS, Cuthill IC, Bonser RHC (1994) Experimental investigations of mass dependent predation risk in the European starling (Sturnus vulgaris). Anim Behav 48:201–222. doi:10.1006/anbe.1994.1227

    Article  Google Scholar 

  • Wolfe M, Norman D (1998) Effects of waterborne mercury on terrestrial wildlife at Clear Lake: evaluation and testing of a predictive model. Environ Toxicol Chem 17:214–227. doi:10.1002/etc.5620170213

    Article  CAS  Google Scholar 

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Acknowledgments

This study was funded by E.I. DuPont de Nemours and Company and research was completed with oversight from the South River Science Team, which is a collaboration of state and federal agencies, academic institutions, and environmental interests. This study was also supported by NSF award IOS-1257590. The College of William and Mary provided additional funds. Thank you to Margaret Whitney for dose preparation and analyses. Special thanks S. Laurie Sanderson for advice and to all the graduate and undergraduate researchers who assisted in developing and carrying out this project.

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The authors declare that they have no conflict of interest.

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  1. Department of Biology, Institute for Integrative Bird Behavior Studies, The College of William and Mary, 500 Landrum Drive, Williamsburg, VA, 23187-8795, USA

    Jenna R. Carlson, Daniel Cristol & John P. Swaddle

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  1. Jenna R. Carlson
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  2. Daniel Cristol
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Correspondence to Jenna R. Carlson.

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Carlson, J.R., Cristol, D. & Swaddle, J.P. Dietary mercury exposure causes decreased escape takeoff flight performance and increased molt rate in European starlings (Sturnus vulgaris). Ecotoxicology 23, 1464–1473 (2014). https://doi.org/10.1007/s10646-014-1288-5

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Keywords

  • Flight
  • Mercury
  • Molt
  • Sub-lethal effects
  • European starling