Advertisement

Ecotoxicology

, Volume 26, Issue 8, pp 1041–1050 | Cite as

Anticoagulant rodenticide exposure and toxicosis in four species of birds of prey in Massachusetts, USA, 2012–2016, in relation to use of rodenticides by pest management professionals

  • Maureen MurrayEmail author
Article

Abstract

Restrictions on second-generation anticoagulant rodenticides (SGARs) in the United States, which were partially implemented in 2011, prohibit the sale of SGAR products through general consumer outlets to minimize use by non-professional or non-agricultural applicators. This study analyzed liver tissue from four species of birds of prey admitted to a wildlife clinic in Massachusetts, USA, from 2012–2016 for residues of anticoagulant rodenticides (ARs). Ninety-four birds were analyzed; 16 were symptomatic for AR toxicosis, and 78 asymptomatic. Ninety-six percent of all birds tested were positive for SGARs: 100% of those diagnosed with AR toxicosis ante-mortem and/or post-mortem and 95% of subclinically exposed birds. Brodifacoum was found in 95% of all birds. Sixty-six percent of all birds contained residues of two or more SGARs. A significant increase in exposures to multiple SGARs occurred in later years in the study. Pesticide use reports (PURs) filed with the Massachusetts Department of Agricultural Resources were reviewed to determine the frequency of use of different ARs by pest management professionals (PMPs) across five years. This study finds that the three SGARs favored by PMPs—bromadiolone, difethialone, brodifacoum—were present in combination in the majority of birds, with increases in multiple exposures driven by increased detections of bromadiolone and difethialone. Continued monitoring of AR residues in nontarget species following full implementation of sales and packaging restrictions in the US is needed in order to elucidate the role of PMP use of SGARs in wildlife exposures and to evaluate the effectiveness of current mitigation measures.

Keywords

Anticoagulant rodenticides Birds of prey Pesticide use reports Regulatory approach Diagnosis of toxicosis 

Notes

Acknowledgements

Funding for this research was provided by the Ruby Memorial Research Fund, administered by the Cummings School of Veterinary Medicine at Tufts University and supported by numerous generous donors, as well as the Blake-Nuttall Fund, Nuttall Ornithological Club. The author thanks Drs. Robert Poppenga and Adrienne Bautista for assistance with sample analysis, Michael Filigenzi for assistance with sample analysis and manuscript preparation, the Massachusetts Department of Agricultural Resources for assistance with access to public pesticide use records, and Jef C. Taylor for valuable input on this project.

Funding

This study was partially funded by the Nuttall Ornithological Club (grant number N/A).

Compliance with ethical standards

Conflict of interest

The author declares that she has no competing interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by the author.

References

  1. Albert CA, Wilson LK, Mineau P, Trudeau S, Elliott JE (2010) Anticoagulant rodenticides in three owl species from western Canada, 1988–2003. Arch Environ Contam Toxicol 58:451–459CrossRefGoogle Scholar
  2. Berny P, Gaillet J (2008) Acute poisoning of red kites (Milvus milvus) in France: data from the SAGIR network. J Wildl Dis 44:417–426CrossRefGoogle Scholar
  3. California Department of Pesticide Regulation (2013) DPR 13-002 Designating brodifacoum, bromadiolone, difenacoum, and difethialone (second generation anticoagulant rodenticide products) as restricted materials. http://www.cdpr.ca.gov/docs/legbills/rulepkgs/13-002/13-002.htm. Accessed 29 April 2017
  4. Damin-Pernik M, Espana B, Besse S, Fourel I, Caruel H, Popowycz F, Benoit E, Lattard V (2016) Development of an ecofriendly anticoagulant rodenticide based on the stereochemistry of difenacoum. Drug Metab Dispos 44:1872–1880CrossRefGoogle Scholar
  5. Elliott JE, Hindmarch S, Albert CA, Emery J, Mineau P, Maisonneuve F (2014) Exposure pathways of anticoagulant rodenticides to nontarget wildlife. Environ Monit Assess 186:895–906CrossRefGoogle Scholar
  6. Elliott JE, Rattner BA, Shore RF, Van Den Brink NW (2016) Paying the pipers: Mitigating the impact of anticoagulant rodenticides on predators and scavengers. BioScience 66:401–407CrossRefGoogle Scholar
  7. Erickson W, Urban D (2004) Potential risks of nine rodenticides to birds and nontarget mammals: a comparative approach. Office of prevention, pesticides, and toxic substances. United States Environmental Protection Agency, Washington, DC, http://www.fwspubs.org/doi/suppl/10.3996/052012-JFWM-042/suppl_file/10.3996_052012-jfwm-042.s4.pdf. Accessed 17 Feb 2017Google Scholar
  8. Hegdal PL, Colvin BA (1988) Potential hazard to eastern screech-owls and other raptors of brodifacoum bait used for vole control in orchards. Environ Toxicol Chem 7:245–260CrossRefGoogle Scholar
  9. Hindmarch S, Elliott JE (2015) When owls go to town: the diet of urban barred owls. J Raptor Res 49:66–74CrossRefGoogle Scholar
  10. Huang AC, Elliott JE, Hindmarch S, Lee SL, Maisonneuve F, Bowes V, Cheng KM, Martin K (2016) Increased rodenticide exposure rate and risk of toxicosis in barn owls (Tyto alba) from southwestern Canada and linkage with demographic but not genetic factors. Ecotoxicology 25:1061–1071CrossRefGoogle Scholar
  11. Justice-Allen A, Loyd KA (2017) Mortality of western burrowing owls (Athene cunicularia hypugaea) associated with brodifacoum exposure. J Wildl Dis 53:165–169CrossRefGoogle Scholar
  12. Krueger L, Newton J, Semrow A, Levy L, Nguyen K, Morgan T, Sun S, Sims J, Koenig S, Shaw L, Cummings R (2015) An analysis of the largest publically funded rodent control program in California: orange county mosquito and vector control district’s rodent control program, 2004–2014. Proc Papers Mosq Vector Control Assoc Calif 83:52–56Google Scholar
  13. Langford KH, Reid M, Thomas KV (2013) The occurrence of second generation anticoagulant rodenticides in non-target raptor species in Norway. Sci Total Environ 450–451:205–208CrossRefGoogle Scholar
  14. Liu J, Xiong K, Ye X, Zhang J, Yan Y, Ji L (2015) Toxicity and bioaccumulation of bromadiolone to earthworm Eisenia fetida. Chemosphere 135:250–256CrossRefGoogle Scholar
  15. Memmott K, Murray M, Rutberg A (2017) Use of anticoagulant rodenticides by pest management professionals in Massachusetts, USA. Ecotoxicology 26:90–96CrossRefGoogle Scholar
  16. Mendenhall VM, Pank LF (1980) Secondary poisoning of owls by anticoagulant rodenticides. Wildl Soc Bull 8:311–315Google Scholar
  17. Merson MH, Byers RE, Kaukeinen DE (1984) Residues of the rodenticide brodifacoum in voles and raptors after orchard treatment. J Wildl Manage 48:212–216CrossRefGoogle Scholar
  18. Morrison JL, Gottlieb IGW, Pias KE (2016) Spatial distribution and the value of green spaces for urban red-tailed hawks. Urban Ecosyst 19:1373–1388CrossRefGoogle Scholar
  19. Mosterd JJ, Thijssen HHW (1991) The long-term effects of the rodenticide, brodifacoum, on blood coagulation and vitamin K metabolism in rats. Br J Pharmacol 104:531–535CrossRefGoogle Scholar
  20. Murray M (2011) Anticoagulant rodenticide exposure and toxicosis in four species of birds of prey presented to a wildlife clinic in Massachusetts, 2006–2010. J Zoo Wildl Med 42:88–97CrossRefGoogle Scholar
  21. Murray M, Tseng F (2008) Diagnosis and treatment of secondary anticoagulant rodenticide toxicosis in a red-tailed hawk (Buteo jamaicensis). J Avian Med Surg 22:41–46CrossRefGoogle Scholar
  22. Pest Control Technology (2014) State of the rodent market. Pest control technology, PCT http://www.pctonline.com/FileUploads/file/State-Rodent-Market.pdf. Accessed 17 Feb 2017
  23. Pest Control Technology (2015) State of the rodent market. Pest control technology, PCT. http://www.pctonline.com/article/exclusive-market-research-december-2015/. Accessed 17 Feb 2017
  24. Pest Control Technology (2016a) State of the rodent market. Pest control technology, PCT. http://www.pctonline.com/fileuploads/file/2016_State_of_the_rodent_market.pdf. Accessed 17 Feb 2017
  25. Pest Control Technology, PCT (2016b) Contrapest rodent control product earns EPA approval. http://www.pctonline.com/article/senestech-contrapest-rodent-product-epa-approval/. Accessed 17 Feb 2017
  26. Petterino C, Paolo B (2001) Toxicology of various anticoagulant rodenticides in animals. Vet Hum Toxicol 43:353–360Google Scholar
  27. Pitt WC, Berentsen AR, Shiels AB, Volker SF, Eisemann JD, Wegmann AS, Howald GR (2015) Non-target species mortality and the measurement of brodifacoum rodenticide residues after a rat (Rattus rattus) eradication on palmyra atoll, tropical pacific. Biol Conserv 185:36–46CrossRefGoogle Scholar
  28. Radvanyi A, Weaver P, Massari C, Bird D, Broughtont E (1988) Effects of chlorophacinone on captive kestrels. Bull Environ Contam Toxicol 41:441–448CrossRefGoogle Scholar
  29. Rattner BA, Horak KE, Warner SE, Day DD, Meteyer CU, Volker SF, Eisemann JD, Jonston JJ (2011) Acute toxicity, histopathology, and coagulopathy in American kestrels (Falco sparverius) following administration of the rodenticide diphacinone. Environ Toxicol Chem 30:1213–1222CrossRefGoogle Scholar
  30. Rattner BA, Horak KE, Lazarus RS, Eisenreich KM, Meteyer CU, Volker SF, Campton CM, Eisemann JD, Johnston JJ (2012) Assessment of toxicity and potential risk of the anticoagulant rodenticide diphacinone using Eastern screech-owls (Megascops asio). Ecotoxicology 21:832–846CrossRefGoogle Scholar
  31. Rattner BA, Horak KE, Lazarus RS, Goldade DA, Johnston JJ (2014a) Toxicokinetics and coagulopathy threshold of the rodenticide diphacinone in eastern screech‐owls (Megascops asio). Environ Toxicol Chem 33:74–81CrossRefGoogle Scholar
  32. Rattner BA, Horak KE, Lazarus RS, Schultz SL, Knowles S, Abbo BG, Volker SF (2015) Toxicity reference values for chlorophacinone and their application for assessing anticoagulant rodenticide risk to raptors. Ecotoxicology 24:720–734CrossRefGoogle Scholar
  33. Rattner BA, Lazarus RS, Elliott JE, Shore RF, van den Brink N (2014b) Adverse outcome pathway and risks of anticoagulant rodenticides to predatory wildlife. Environ Sci Technol 48:8433–8445CrossRefGoogle Scholar
  34. Salim H, Noor HM, Hamid, Omar NH, Kasim D, Abidin CMRZ (2014) Secondary poisoning of Captive barn owls, Tyto alba javanica, through feeding with rats poisoned with chlorophacinone and bromadiolone. J Oil Palm Res 26:62–72Google Scholar
  35. Savarie PJ, Hayes DJ, McBride RT, Roberts JD (1979) Efficacy and safety of diphacinone as a predacide. In: Kenaga EE (ed) Avian and mammalian wildlife toxicology. STP 693. American Society for Testing and Materials, Philadelphia, PA, p 69–79CrossRefGoogle Scholar
  36. Stansley W, Cummings M, Vudathala D, Murphy LA (2014) Anticoagulant rodenticides in red-tailed hawks, Buteo jamaicensis, and great horned owls, Bubo virginianus, from New Jersey, USA, 2008–2010. Bull Environ Contam Toxicol 92:6–9CrossRefGoogle Scholar
  37. Stone WB, Okoniewski JC, Stedelin JR (1999) Poisoning of wildlife with anticoagulant rodenticides in New York. J Wildl Dis 35:187–193CrossRefGoogle Scholar
  38. Stone WB, Okoniewski JC, Stedelin JR (2003) Anticoagulant rodenticides and raptors: recent findings from New York, 1998–2001. Bull Environ Contam Toxicol 70:34–40CrossRefGoogle Scholar
  39. US Environmental Protection Agency, EPA (2008) Risk mitigation decision for ten rodenticides. USEPA office of prevention, pesticides and toxic substances. http://www.regulations.gov/#!documentDetail;D=EPA-HQ-OPP-2006-0955-0764. Accessed 17 Feb 2017
  40. US Environmental Protection Agency, EPA (2014) Product cancellation order for certain rodenticide registrations. Federal register: the daily journal of the United States Government. https://www.federalregister.gov/articles/2014/08/06/2014-18361/product-cancellation-order-for-certain-rodenticide-registrations. Accessed 17 Feb 2017
  41. Vyas NB, Rattner BA (2012) Critique on the use of the standardized avian acute oral toxicity test for first generation anticoagulant rodenticides. Hum Ecol Risk Assess 18:1069–1077CrossRefGoogle Scholar
  42. Walker LA, Turk A, Long SM, Wienburg CL, Best J, Shore RF (2008) Second generation anticoagulant rodenticides in tawny owls (Strix aluco) from Great Britain. Sci Total Environ 392:93–98CrossRefGoogle Scholar
  43. Watanabe KP, Kawata M, Ikenaka Y, Nakayama SM, Ishii C, Darwish wS, Saengtienchai AS, Mizukawa H, Ishizuka M (2015) Cytochrome P450-mediated warfarin sensitivity in avian species: in vitro assays in several birds and in vivo assays in chickens. Environ Toxicol Chem 34:2328–2334CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Wildlife ClinicCummings School of Veterinary Medicine at Tufts UniversityNorth GraftonUSA

Personalised recommendations