Advertisement

Stopover departure behavior and flight orientation of spring-migrant Yellow-rumped Warblers (Setophaga coronata) experimentally exposed to methylmercury

  • Chad L. SeewagenEmail author
  • Yanju Ma
  • Yolanda E. Morbey
  • Christopher G. Guglielmo
Original Article

Abstract

Mercury (Hg) is a global pollutant that has wide-ranging impacts on the physiological systems of birds, but almost nothing is known about how this affects migration. We manipulated methylmercury (MeHg) burdens of 24 wild-caught Yellow-rumped Warblers (Setophaga coronata) before releasing them and tracking their spring migration with automated radiotelemetry to study the effect of MeHg on stopover departure behavior and flight orientation. Dosing half the birds for 14 days prior to release resulted in environmentally relevant mean blood total Hg (THg) concentrations of 6.61 (± 0.16) p.p.m., while a group of 12 controls had nearly undetectable blood THg. We observed starkly different departure behavior between groups, with dosed birds leaving the release site significantly sooner than controls. Among birds that were detected beyond the release site, seven (three dosed, four control) initially made a landscape-scale relocation before a longer-distance migratory flight, while two (controls) migrated directly from the release site. All flights were in the seasonally appropriate direction regardless of group. Rapid departures by dosed birds could have been the result of hyperactivity that can be induced by MeHg, or due to decreased social dominance that caused them to seek areas with less resource competition. We found no evidence that MeHg impaired orientation, although sample sizes were small and we had less ability to detect birds flying in “incorrect” than northward directions. The dramatic difference in departure decisions between groups indicates a potential effect of MeHg on the neurological and/or physiological mechanisms that control migratory behaviors of birds.

Keywords

Migration Toxicant Radiotelemetry Hyperactivity Social dominance 

Zusammenfassung

Fortsetzung des Zuges und Orientierung nach Zwischenstopp beim Frühjahrszug von Kronenwaldsängern (Setophaga coronata), nachdem sie im Experiment Methylquecksilber ausgesetzt waren.

Quecksilber ist ein weltweit verbreitetes Umweltgift mit vielfältigen Auswirkungen auf die Physiologie von Vögeln, wobei jedoch fast nichts über eine mögliche Beeinflussung des Vogelzugs bekannt ist. Wir veränderten im Experiment die Methylquecksilber-Belastung (MeHg) von 24 Wildfängen des Kronenwaldsängers (Setophaga coronata) vor dem Wiederauflassen und verfolgten ihren Frühjahrszug mit automatischer Radio-Telemetrie, um die Effekte von MeHg auf die Wiederaufnahme des Zugs und auf die Orientierung zu untersuchen. Eine Hälfte der Vögel wurde 14 Tage vor Freilassung dem MeHg ausgesetzt, was in ihrem Blut zu einer umweltbiologisch relevanten mittleren Quecksilber-Konzentration (THg) von 6,61 (+/- 0,16) p.p.m. führte, wohingegen die 12 Tiere der Kontrollgruppe kein praktisch nachweisbares Quecksilber im Blut hatten. Das Abflugverhalten der beiden Gruppen war sehr unterschiedlich: die dem MeHg ausgesetzten Vögel verließen den Ort der Freilassung signifikant früher als die der Kontrollgruppe. Von den Vögeln, die in einiger Entfernung zum Ort der Freilassung wiedergefunden wurden, unternahmen sieben (drei mit MeHg, vier Kontrollvögel) zunächst Flüge in die Umgebung, bevor sie ihren Langstreckenzug wieder aufnahmen, während zwei der Kontrollvögel ihren Zug unmittelbar ab dem Freilassungsort fortsetzten. Unabhängig von der Gruppe zogen alle Vögel in die der Jahreszeit entsprechende, korrekte Richtung weiter. Die frühen Abflüge der Vögel mit MeHg könnten an einer von Quecksilber verursachten Hyperaktivität oder an einer verringerten sozialen Dominanz liegen, die sie dazu brachte, Gebiete mit geringerer Konkurrenz um vorhandene Ressourcen aufzusuchen. Wir fanden keinen Hinweis darauf, dass MeHg einen Einfluss auf die Orientierung hatte, wobei allerdings die Stichproben sehr klein und wir nicht in der Lage waren, Vögel, die in falsche Richtungen (also nicht nach Norden) zogen, nachzuweisen. Der dramatische Unterschied zwischen den Gruppen in der Entscheidung, den Zug wieder aufzunehmen, weist aber auf einen möglichen Einfluss von MeHg auf diejenigen neurologischen und/oder physiologischen Mechanismen hin, die die Zugbewegungen von Vögeln kontrollieren.

Notes

Acknowledgements

We are grateful to the staff and volunteers of the Long Point Bird Observatory for support and assistance. We also thank Stuart MacKenzie and other Bird Studies Canada staff for their advice and assistance with the Motus Wildlife Tracking System, Jessica Deakin for assistance with radio-tagging, Andrew Beauchamp for performing the molecular sexing analyses, Kevin Young for support with animal care, and Dan Cristol for thoughts on our results. Funding was provided to C. G. G. and Y. E. M. by Natural Sciences and Engineering Research Council of Canada Discovery Grants. All methods were compliant with Canadian law and conducted under appropriate government permits.

Compliance with ethical standards

Ethical standards

All procedures were approved under a University of Western Ontario animal use protocol (2010–216) and permits from the Canadian Wildlife Service (CA-0256, 10169BU).

References

  1. Ball SC (1952) Fall bird migration on the Gaspe Peninsula. Peabody Mus Nat Hist Yale Univ Bull 7:1–211Google Scholar
  2. Carlson JR, Cristol D, Swaddle JP (2014) Dietary mercury exposure causes decreased escape takeoff flight performance and increased molt rate in European Starlings (Sturnus vulgaris). Ecotoxicology 23:1464–1473CrossRefPubMedGoogle Scholar
  3. 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 320:335CrossRefPubMedGoogle Scholar
  4. Dossman BC, Mitchell GW, Norris DR, Taylor PD, Guglielmo CG, Matthews SN, Rodewald PG (2016) The effects of wind and fuel stores on stopover departure behavior across a migratory barrier. Behav Ecol 27:567–574CrossRefGoogle Scholar
  5. Driscoll CT, Mason RP, Chan HM, Jacob DJ, Pirrone N (2013) Mercury as a global pollutant: sources, pathways, and effects. Environ Sci Technol 47:4967–4983CrossRefPubMedPubMedCentralGoogle Scholar
  6. Dunn EH (2001) Mass change during migration stopover: a comparison of species groups and sites. J Field Ornithol 72:419–432CrossRefGoogle Scholar
  7. Eng ML, Stutchbury B, Morrissey CA (2017) Imidacloprid and chlorpyrifos insecticides impair migratory ability in a seed-eating songbird. Sci Rep 7:15176CrossRefPubMedPubMedCentralGoogle Scholar
  8. Evans HL, Garman RH, Laties VG (1982) Neurotoxicity of methylmercury in the pigeon. Neurotoxicology 3:21–36PubMedGoogle Scholar
  9. Evers D (2018) The effects of methylmercury on wildlife: a comprehensive review and approach for interpretation. In: DellaSala D, Goldstein M (eds) Encyclopedia of the Anthropocene, 1st edn. Elsevier, Oxford, pp 181–194CrossRefGoogle Scholar
  10. Flahr LM, Michel NL, Zahara ARD, Jones PD, Morrissey CA (2015) Developmental exposure to Aroclor 1254 alters migratory behavior in juvenile European Starlings (Sturnus vulgaris). Environ Sci Technol 49:6274–6283CrossRefPubMedGoogle Scholar
  11. Fournier F, Karasov WH, Kenow KP, Meyer MW, Hines RK (2002) The oral bioavailability and toxicokinetics of methylmercury in Common Loon (Gavia immer) chicks. Comp Biochem Physiol A 133:703–714CrossRefGoogle Scholar
  12. Gerson AR, Cristol DA, Seewagen CL (2019) Environmentally relevant methylmercury exposure reduces the metabolic scope of a model songbird. Environ Pollut 246:790–796CrossRefPubMedGoogle Scholar
  13. Guglielmo CG, McGuire LP, Gerson AR, Seewagen CL (2011) Simple, rapid, and non-invasive measurement of fat, lean, and total water masses of live birds using quantitative magnetic resonance. J Ornithol 152(Suppl. 1):75–85CrossRefGoogle Scholar
  14. Hunt PD, Flaspohler DJ (1998) Yellow-rumped Warbler (Setophaga coronata), version 2.0. In: Poole AF, Gill FB (eds) The birds of North America. Cornell Lab of Ornithology, New YorkGoogle Scholar
  15. Kennedy LV, Morbey YE, Mackenzie SA, Taylor PD, Guglielmo CG (2017) A field test of the effects of body composition analysis by quantitative magnetic resonance on songbird stopover behaviour. J Ornithol 158:593–601CrossRefGoogle Scholar
  16. Kobiela ME, Cristol DA, Swaddle JP (2015) Risk-taking behaviours in Zebra Finches affected by mercury exposure. Anim Behav 103:153–160CrossRefGoogle Scholar
  17. Ma Y, Branfireun BA, Hobson KA, Guglielmo CG (2018a) Evidence of negative seasonal carry over effects of breeding ground mercury exposure on survival of migratory songbirds. J Avian Biol.  https://doi.org/10.1111/jav.01656 Google Scholar
  18. Ma Y, Perez CR, Branfireun BA, Guglielmo CG (2018b) Dietary exposure to methylmercury affects flight endurance in a migratory songbird. Environ Pollut 234:894–901CrossRefPubMedGoogle Scholar
  19. Moore F, Mabey S, Woodrey M (2003) Priority access to food in migratory birds: age, sex and motivational asymmetries. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer, Berlin, pp 281–292CrossRefGoogle Scholar
  20. Morbey YE, Guglielmo CG, Taylor P, Maggini I, Deakin J, Mackenzie S, Brown JM, Zhao L (2018) Evaluation of sex differences in the stopover behavior and post departure movements of Wood-warblers. Behav Ecol 29:117–127CrossRefGoogle Scholar
  21. Moye JK, Perez CR, Pritsos CA (2016) Effects of parental and direct methylmercury exposure on flight activity in young Homing Pigeons (Columba livia). Environ Pollut 5:23–30CrossRefGoogle Scholar
  22. Newton I (2006) Can conditions experienced during migration limit the population levels of birds? J Ornithol 147:146–166CrossRefGoogle Scholar
  23. Powell TJ (2000) Chronic neurobehavioural effects of mercury poisoning on a group of Zulu chemical workers. Brain Inj 14:797–814CrossRefPubMedGoogle Scholar
  24. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  25. Rappole JH, Tipton AR (1991) New harness design for attachment of radio transmitters to small passerines. J Field Ornithol 63:335–337Google Scholar
  26. 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 14:223–240CrossRefPubMedGoogle Scholar
  27. 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 19:697–709CrossRefPubMedGoogle Scholar
  28. Rowse LM, Rodewald AD, Sullivan SMP (2014) Pathways and consequences of contaminant flux to Acadian Flycatchers (Empidonax virescens) in urbanizing landscapes of Ohio, USA. Sci Total Environ 485:461–467CrossRefPubMedGoogle Scholar
  29. SAS Institute (2011) Base SAS 9.3 procedures guide. SAS Institute, CaryGoogle Scholar
  30. Seewagen CL (2010) Threats of environmental mercury to birds: knowledge gaps and priorities for future research. Bird Conserv Int 20:112–123CrossRefGoogle Scholar
  31. Seewagen CL (2013) Blood mercury levels and the stopover refueling performance of a long-distance migratory songbird. Can J Zool 91:41–45CrossRefGoogle Scholar
  32. Seewagen CL (2018) The threat of global mercury pollution to bird migration: potential mechanisms and current evidence. Ecotoxicology.  https://doi.org/10.1007/s10646-018-1971-z PubMedGoogle Scholar
  33. Seewagen CL, Cristol DA, Gerson AR (2016) Mobilization of mercury from lean tissues during simulated migratory fasting in a model songbird. Sci Rep 6:25762CrossRefPubMedPubMedCentralGoogle Scholar
  34. Selin NE (2009) Global biogeochemical cycling of mercury: a review. Annu Rev Environ Resour 34:43–63CrossRefGoogle Scholar
  35. Siblerud RL, Motl J, Kienholz E (1994) Psychometric evidence that mercury from silver dental fillings may be an etiological factor in depression, excessive anger, and anxiety. Psychol Rep 74:67–80CrossRefPubMedGoogle Scholar
  36. Swaddle JP, Diehl TR, Taylor CE, Fanaee AS, Benson JL, Huckstep NR, Cristol DA (2017) Exposure to dietary mercury alters cognition and behavior of Zebra Finches. Curr Zool 63:213–219CrossRefPubMedPubMedCentralGoogle Scholar
  37. Taylor PD, Crewe TL, Mackenzie SA, Lepage D, Aubry Y, Crysler Z, Finney G, Francis CM, Guglielmo CG, Hamilton DJ, Holberton RL, Loring PH, Mitchell GW, Norris DR, Paquet J, Ronconi RA, Smetzer JR, Smith PA, Welch LJ, Woodworth BK (2017) The Motus Wildlife Tracking System: a collaborative research network to enhance the understanding of wildlife movement. Avian Conserv Ecol 12:8CrossRefGoogle Scholar
  38. United Nations Environment Programme (UNEP) (2013) UNEP global mercury assessment. UNEP Chemicals Branch, GenevaGoogle Scholar
  39. Vyas NB, Hill EF, Sauer JR, Kuenzel WJ (1995) Acephate affects migratory orientation of the White-throated Sparrow (Zonotrichia albicollis). Environ Toxicol Chem 14:1961–1965CrossRefGoogle Scholar
  40. Wang Y, Finch DM, Moore FR, Kelly JF (1998) Stopover ecology and habitat use of migratory Wilson's Warblers. Auk 115:829–842CrossRefGoogle Scholar
  41. Whitney MC, Cristol DA (2017) Impacts of sublethal mercury exposure on birds: a detailed review. Rev Environ Contam Toxicol 244:113–163Google Scholar
  42. Woodrey M (2000) Age-dependent aspects of stopover biology of passerine migrants. Stud Avian Biol 20:43–52Google Scholar
  43. Woodworth BK, Mitchell GW, Norris DR, Francis CM, Taylor PD (2015) Patterns and correlates of songbird movements at an ecological barrier during autumn migration assessed using landscape and regional scale automated radiotelemetry. Ibis 157:326–339CrossRefGoogle Scholar

Copyright information

© Deutsche Ornithologen-Gesellschaft e.V. 2019

Authors and Affiliations

  • Chad L. Seewagen
    • 1
    Email author
  • Yanju Ma
    • 2
  • Yolanda E. Morbey
    • 2
  • Christopher G. Guglielmo
    • 2
  1. 1.Great Hollow Nature Preserve and Ecological Research CenterNew FairfieldUSA
  2. 2.Department of Biology, Advanced Facility for Avian ResearchUniversity of Western OntarioLondonCanada

Personalised recommendations