Analysis of insecticide exposure in California hummingbirds using liquid chromatography-mass spectrometry

Abstract

External feather rinses and homogenized whole-carcass tissue matrix from two hummingbird species found in California (Calypte anna and Archilochus alexandri) were analyzed for the presence of nine insecticides commonly used in urban settings. Using a liquid chromatography-high-resolution mass spectrometry (LC-HRMS) analytical method, samples were quantitatively tested for the following neonicotinoids: dinotefuran, nitenpyram, thiamethoxam, acetamiprid, thiacloprid, clothianidin, imidacloprid, and sulfoxaflor. This analytical method was also used to qualitatively screen for the presence of approximately 150 other pesticides, drugs, and natural products. Feather rinsates from both hummingbird species had detectable concentrations of carbamate and neonicotinoid classes of insecticides. Combined results of the rinsate and homogenized samples (n = 64 individual hummingbirds) showed that 44 individuals (68.75%) were positive for one to four target compounds. This study documented that hummingbirds found in California are exposed to insecticides. Furthermore, feather rinsates and carcass homogenates are matrices that can be used for assessing pesticide exposure in small bird species. The small body size of hummingbirds limits traditional sampling methods for tissues and whole blood to evaluate for pesticide exposure. Thus, utilization of this analytical method may facilitate future research on small-sized avian species, provide insight into pesticide exposure, and ultimately lead to improved conservation of hummingbirds.

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

References

  1. Bacandritsos N, Granato A, Budge G, Papanastasiou I, Roinioti E, Caldon M, Falcaro C, Gallina A, Mutinelli F (2010) Sudden deaths and colony population decline in Greek honey bee colonies. J Invertebr Pathol 105(3):335–340. https://doi.org/10.1016/j.jip.2010.08.004

    Article  CAS  Google Scholar 

  2. Bargańska Ż, Ślebioda M, Namieśnik J (2014) Determination of pesticide residues in honeybees using modified QUEChERS sample work-up and liquid chromatography-tandem mass spectrometry. Molecules 19:2911–2924. https://doi.org/10.3390/molecules19032911

    Article  CAS  Google Scholar 

  3. Bayat S, Geiser F, Kristiansen P, Wilson SC (2014) Organic contaminants in bats: trends and new issues. Environ Int 63:40–52

    Article  CAS  Google Scholar 

  4. Bennett RS, Etterson MA, Bennett RS, Etterson MA (2007) Incorporating results of avian toxicity tests into a model of annual reproductive success. Integr Environ Assess Manag 3(4):498–507. https://doi.org/10.1897/IEAM

    Article  Google Scholar 

  5. Bernhardt ES, Rosi EJ, Gessner MO (2017) Synthetic chemicals as agents of global change. Front Ecol Environ 15(2):84–90. https://doi.org/10.1002/fee.1450

    Article  Google Scholar 

  6. Berny PJ, Buronfosse F, Videmann B, Buronfosse T (1999) Evaluation of the toxicity of imidacloprid in wild birds: a new high performance thin layer chromatography (HPTLC) method for the analysis of liver and crop samples in suspected poisoning cases. J Liq Chromatogr Relat Technol 22(10):1547–1559. https://doi.org/10.1081/JLC-100101750

    Article  CAS  Google Scholar 

  7. Bishop CA, Moran AJ, Toshack MC, Elle E, Maisonneuve F, Elliott J (2018) Hummingbirds and bumble bees exposed to neonicotinoid and organophosphate insecticides in the Fraser Valley, British Columbia, Canada. Environ Toxicol Chem 37(8):2143–2152

    Article  CAS  Google Scholar 

  8. Callahan J, Mineau P (2008) An evaluation of clinical sign data from avian acute oral toxicity studies. Appendix 11; Scientific opinion of the panel on plant protection products and their residues on risk assessment for birds and mammals. EFSA J 734:1–10

    Google Scholar 

  9. Chauzat M-P, Martel AC, Cougoule N, Porta P, Lachaize J, Zeggane S, Aubert M, Carpentier P, Faucon JP (2011) An assessment of honeybee colony matrices, Apis mellifera (Hymenoptera: Apidae) to monitor pesticide presence in continental France. Environ Toxicol 30(1):103–111. https://doi.org/10.1002/etc.361

    Article  CAS  Google Scholar 

  10. Cohen J (1960) A coefficient of agreement for nominal scales. Educ Psychol Meas 20(1):37–46

    Article  Google Scholar 

  11. Contra Costa County (2015) Pesticide use reports. http://www.co.contra-costa.ca.us/6243/Pesticide-Use-Data

  12. Cutler P, Slater R, Edmunds AJF, Maienfisch P, Hall RG, Earley FGP, Pitterna T, Pal S, Paul V, Goodchild J, Blacker M, Hagmann L, Crossthwaite AJ (2012) Investigating the mode of action of sulfoxaflor: a fourth-generation neonicotinoid. Pest Manag Sci 69:607–619

    Article  CAS  Google Scholar 

  13. Eng ML, Stutchbury BJM, Morrissey CA (2017) Imidacloprid and chlorpyrifoc insecticides impair migratory ability in a seed-eating songbird. Sci Rep 7:15176. https://doi.org/10.1038/s41598-017-15446-x

    Article  CAS  Google Scholar 

  14. Etterson MA, Bennett RS (2013) Quantifying the effects of pesticide exposure on annual reproductive success of birds. Integr Environ Assess Manag 9(4):590–599. https://doi.org/10.1002/ieam.1450

    Article  Google Scholar 

  15. Fairbrother A, Purdy J, Anderson T, Fell R (2014) Risks of neonicotinoid insecticides to honeybees. Environ Toxicol Chem 33(4):719–731. https://doi.org/10.1002/etc.2527

    Article  CAS  Google Scholar 

  16. Farooqui T (2013) A potential link among biogenic amines-based pesticides, learning and memory, and colony collapse disorder: a unique hypothesis. Neurochem Int 62(1):122–136. https://doi.org/10.1016/j.neuint.2012.09.020

    Article  CAS  Google Scholar 

  17. Filigenzi M, Graves E, Tell L, Jelks K, Poppenga R (2019) Quantitative analysis for neonicotinoid insecticides combined with broad range screening for other xenobiotics in small mass avian tissue samples using UHPLC-high resolution mass spectrometry. J Vet Diagn Investig. https://doi.org/10.1177/1040638719834329

  18. Fry DM (1995) Reproductive effects in birds exposed to pesticides and industrial chemicals. Environ Health Perspect 19:165–171

    Google Scholar 

  19. García GMD, Martínez Galera M, Uclés S, Lozano A, Fernández-Alba AR (2018) Ultrasound-assisted extraction based on QuEChERS of pesticide residues in honeybees and determination by LC-MS/MS and GC-MS/MS. Anal Bioanal Chem 410(21):5195–5210. https://doi.org/10.1007/s00216-018-1167-7

    Article  CAS  Google Scholar 

  20. Gibbons D, Morrissey C, Mineau P (2015) A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife. Environ Sci Pollut Res 22:103–118

    Article  CAS  Google Scholar 

  21. Giorio C, Safer A, Sánchez-Bayo F, Tapparo A, Lentola A, Girolami V, van Lexmond MB, Bonmatin J (2017) An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 1: new molecules, metabolism, fate, and transport. Environ Sci Pollut Res https://doi.org/10.1007/s11356-017-0394-3

  22. Godoy LA, Tell LA, Ernest HB (2014) Hummingbird health: pathogens and disease conditions in the family Trochilidae. J Ornithol 155(1):1–12. https://doi.org/10.1007/s10336-013-0990-z

    Article  Google Scholar 

  23. Goulson D (2013) An overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50(4):977–987. https://doi.org/10.1111/1365-2664.12111

    Article  Google Scholar 

  24. Goulson D (2014) Pesticides linked to bird declines. Nature 511:295–296. https://doi.org/10.1038/nature13642

    Article  CAS  Google Scholar 

  25. Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347(6229):1255957. https://doi.org/10.1126/science.1255957

    Article  CAS  Google Scholar 

  26. Hallmann CA, Foppen RPB, Turnhout C a M, Van Kroon H, De Jongejans E, van Turnhout C a M et al (2014) Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511(7509):341–343. https://doi.org/10.1038/nature13531

    Article  CAS  Google Scholar 

  27. Hladik ML, Main AR, Goulson D (2018) Environmental risks and challenges associated with neonicotinoid insecticides. Environ Sci Technol 52:3329–3335

    Article  CAS  Google Scholar 

  28. Lu C, Warchol KM, Callahan RA (2014) Sub-lethal exposure to neonicotinoids impaired honey bees winterization before proceeding to colony collapse disorder. Bull Insectol 67(1):125–130

    CAS  Google Scholar 

  29. Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB (2001) Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22(11):573–580. https://doi.org/10.1016/S0165-6147(00)01820-4

    Article  CAS  Google Scholar 

  30. Mineau P, Palmer C (2013) The impact of the nation’s most widely used insecticides on birds. The American Bird Conservancy. http://abcbirds.org/wp-content/uploads/2015/05/Neonic_FINAL.pdf

  31. Mineau P, Tucker KR (2002) Improving detection of pesticide poisoning in birds. J Wildlife Rehabil 25(2):4–13

    Google Scholar 

  32. Mineau P, Collins BT, Baril A (1996) On the use of scaling factors to improve interspecies extrapolation of acute toxicity in birds. Regul Toxicol Pharmacol 24(1):24–29. https://doi.org/10.1006/rtph.1996.0061

    Article  CAS  Google Scholar 

  33. Mineau P, Baril A, Collins BT, Duffe J, Joerman G, Luttik R (2001) Pesticide acute toxicity reference values for birds. Rev Environ Contam Toxicol 170:13–74

    CAS  Google Scholar 

  34. Pamminger T, Botías C, Goulson D, Hughes WOH (2018) A mechanistic framework to explain the immunosuppressive effects of neurotoxic pesticides on bees. Funct Ecol 32(8):1921–1930. https://doi.org/10.1111/1365-2435.13119

    Article  Google Scholar 

  35. Phillips AR (1975) The migrations of Allen’s and other hummingbirds. Condor 77(2):196–205

    Article  Google Scholar 

  36. Pisa LW, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Downs CA, Goulson D, Kreutzweiser DP, Krupke C, Liess M, McField M, Morrissey CA, Noome DA, Simon-Delso J, Stark JD, Van der Sluijs JP, Van Dyck H, Wiemers M (2015) Effects of neonicotinoids and fipronil on non-target invertebrate. Environ Sci Pollut Res 22:68–102

    Article  CAS  Google Scholar 

  37. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25(6):345–353

    Article  Google Scholar 

  38. Pritchard DJ, Tello Ramos MC, Muth F, Healy SD (2017) Treating hummingbirds as feathered bees: a case of ethological cross-pollination. Biol Lett 13:20170610. https://doi.org/10.1098/rsbl.2017.0610

    Article  Google Scholar 

  39. R Core Team (2017) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

    Google Scholar 

  40. Rouchaud J, Gustin F, Wauters A (1994) Soil biodegradation and leaf transfer of insecticide imidacloprid applied in seed dressing in sugar beet crops. Bull Environ Contam Toxicol 53:344–350

    Article  CAS  Google Scholar 

  41. Sanchez-Bayo F, Goka K (2014) Pesticide residues and bees—a risk assessment. PLoS One 9(4):e94482. https://doi.org/10.1371/journal.pone.0094482

    Article  CAS  Google Scholar 

  42. Stanton RL, Morrissey CA, Clark RG (2018) Analysis of trends and agricultural drivers of farmland bird declines in North America: a review. Agric Ecosyst Environ 254:244–254

    Article  Google Scholar 

  43. Taliansky-Chamudis A, Gómez-Ramírez P, León-Ortega M, García-Fernández AJ (2017) Validation of a QuECheRS method for analysis of neonicotinoids in small volumes of blood and assessment of exposure in Eurasian eagle owl (Bubo bubo) nestlings. Sci Total Environ 595:93–100. https://doi.org/10.1016/j.scitotenv.2017.03.246

    Article  CAS  Google Scholar 

  44. Tomizawa M, Casida JE (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247–268. https://doi.org/10.1146/annurev.pharmtox.45.120403.095930

    Article  CAS  Google Scholar 

  45. U.S. General Accounting Office (1992) Comparison of U.S. and Mexican pesticide standards and enforcement, pp 58. http://www.Gao.Gov/Assets/160/151984.Pdf

  46. Zhu Y, Loso MR, Watson GB, Sparks TC, Rogers RB, Huang JX, Gerwick BC, Babcock JM, Kelley D, Hegde VB, Nugent BM, Renga JM, Denholm I, Gorman K, DeBoer GJ, Hasler J, Meade T, Thomas JD (2011) Discovery and characterization of sulfoxaflor, a novel insecticide targeting sap-feeding pests. J Agric Food Chem 59:2950–2957

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Lindsey Wildlife Museum and the California Wildlife Center for providing hummingbird carcasses for this study. This work is dedicated to Dr. Richard Melnicoe for his passion for birding and his expertise in integrated pest management.

Funding

This study was funded by the Western Hummingbird Partnership and the Daniel and Susan Gottlieb Foundation.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Lisa A. Tell.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible editor: Roland Peter Kallenborn

Electronic supplementary material

ESM 1

(DOCX 25.4 kb)

ESM 2

(DOCX 27.3 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Graves, E.E., Jelks, K.A., Foley, J.E. et al. Analysis of insecticide exposure in California hummingbirds using liquid chromatography-mass spectrometry. Environ Sci Pollut Res 26, 15458–15466 (2019). https://doi.org/10.1007/s11356-019-04903-x

Download citation

Keywords

  • Hummingbirds
  • Urban
  • Neonicotinoids
  • Insecticides
  • Pesticides
  • Birds
  • Non-target species