Skip to main content
Log in

Prevalence of anticoagulant rodenticide exposure in red-tailed hawks (Buteo jamaicensis) and utility of clotting time assays to detect coagulopathy

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Anticoagulant rodenticides (ARs) continue to be used across the United States as a method for controlling pest rodent species. As a consequence, wild birds of prey are exposed to these toxicants by eating poisoned prey items. ARs prevent the hepatic recycling of vitamin K and thereby impede the post-translational processing of coagulation factors II, VII, IX, and X that are required for procoagulant complex assembly. Through this mechanism of action, ARs cause hemorrhage and death in their target species. Various studies have documented the persistence of these contaminants in birds of prey but few have attempted to use affordable and accessible diagnostic tests to diagnose coagulopathy in free-ranging birds of prey. In our study free-ranging red-tailed hawks were found to be exposed to difethialone and brodifacoum. Eleven of sixteen (68%) livers tested for AR exposure had detectable residues. Difethialone was found in 1/16 (6%), and brodifacoum was detected in 10/16 (62%) liver samples that were tested for rodenticide residues. Difethialone was found at a concentration of 0.18 ug/g wet weight and brodifacoum concentrations ranged from 0.003–0.234 ug/g wet weight. Two out of 34 (6%) RTHA assessed for blood rodenticide had brodifacoum in serum with measured concentrations of 0.003 and 0.006 ug/g. The range of clotting times in the prothrombin time (PT) and Russell’s viper venom time assays for control RTHA were 16.7 to 39.7 s and 11.5 to 91.8 s, respectively. One study bird was diagnosed with clinical AR intoxication with a brodifacoum levels in blood of 0.006 and 0.234 ug/g wet weight in blood and liver respectively, a packed cell volume (PCV) of 19%, and PT and RVVT times of >180 s. No correlation was found between PT and RVVT in the control or free-range RTHA, and there was no relationship found between the presence of liver anticoagulant residues and clotting times in the PT and RVVT.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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(2):451–459

    Article  CAS  Google Scholar 

  • Anderson B, Borges S, Barber K, Hartless C, Housenger J, Mastrota N, Odenkirchen E, Riley E, Wagman M (2011) Risks of non-compliant rodentiides to nontarget wildlife. USEPA Office of Chemical Safety and Pollution Prevention. p 1–183

  • Buckle AP, Prescott CV, Ward KJ (1994) Resistance to the first and second generation anticoagulant rodenticides—a new perspective. Proc Vertebr Pest Conf 16(16):138–144

    Google Scholar 

  • Buckle AP, Prescott C (2018) Anticoagulants and risk mitigation. In: van den Brink N, Elliott JE, Shore RF, Rattner BA (Eds.) Anticoagulant rodenticides and wildlife. Springer International Publishing, Cham, Switzerland, p 319–355

    Chapter  Google Scholar 

  • Clauss A (1957) Gerinnungsphysiologische Schnellmethode zur Bestimmung des Fibrinogens. Acta Haematol 17:237–246

    Article  CAS  Google Scholar 

  • Cray C, Zaias J, Altman NH (2009) Acute phase response in animals: a review. Comp Med 59:517–526

    CAS  Google Scholar 

  • Dickson AJ (2020) Prevalence of Anticoagulant Rodenticides in Ferruginous Hawk Nestlings and Evaluation of a Novel Method to Rapidly Assess Exposure. Boise State University. p 1-98

  • 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(2):895–906

    Article  CAS  Google Scholar 

  • Elmeros M, Bossi R, Christensen TK, Kjær LJ, Lassen P, Topping CJ (2019) Exposure of non-target small mammals to anticoagulant rodenticide during chemical rodent control operations. Environ Sci Pollut Res 26(6):6133–6140

    Article  CAS  Google Scholar 

  • Erickson W, Urban D (2004) Potential risks of nine rodenticides to birds and nontarget mammals: a comparative approach. Environmental Protection Agency. p 1–214

  • Fisher P, O’Connor C, Wright G, Eason CT (2003) Persistence of four anticoagulant rodenticides in the livers of laboratory rats. DOC Science Internal Series 139. Department of Conservation, Wellington, p 1–91

    Google Scholar 

  • Guddorf V, Kummerfeld N, Mischke R (2014) Methodical aspects of blood coagulation measurements in birds applying commercial reagents—a pilot study. Berliner Münchener Tierärztliche Wochenschrift 127:322–327

    Google Scholar 

  • Harvey JW (2012) Evaluation of hemostasis: Coagulation and Platelet Disorders. Harvey JW (ed) Veterinary hematology. W B Saunders. Ch 7, p 191–233

  • Hindmarch S, Rattner BA, Elliott JE (2019) Use of blood clotting assays to assess potential anticoagulant rodenticide exposure and effects in free-ranging birds of prey. Sci Total Environ 657:1205–1216

    Article  CAS  Google Scholar 

  • Huckle KR, Warburton PA, Forbes S, Logan CJ (1999) Studies on the Fate of flocoumafen in the Japanese quail (Coturnix coturnix japonica). Xenobiotica. 19(1):51–62

    Article  Google Scholar 

  • Hydock KL, Declementi C, Fish PH (2017) Second-generation anticoagulant rodenticide poisoning in a captive andean condor (Vultur gryphus). J Avian Med Surg 31(3):256–261

    Article  Google Scholar 

  • Jackson WB, Kaukeinen DE. (1972) The problem of anticoagulant rodenticide resistance in the United States. In: Proceedings of the Vertebrate Pest Conference. pp.142–148.

  • Jacob J, Buckle AP (2018) Use of anticoagulant rodenticides in different applications around the world. In: van den Brink N, Elliott JE, Shore RF, Rattner BA (Eds.) Anticoagulant rodenticides and wildlife. Springer International Publishing, Cham, Switzerland, p 11–44

    Chapter  Google Scholar 

  • Kase F (1978) The effect of homo- and heterologous thromboplastins on plasmas of man, seven mammalian and two avian species. Comp Biochem Physiol 61:65–68

    Article  Google Scholar 

  • Kelly TR, Poppenga RH, Woods LA, Hernandez YZ, Boyce WM, Samaniego FJ, Torres SG, Johnson CK (2014) Causes of mortality and unintentional poisoning in predatory and scavenging birds in California. Vet Record Open 1(1):1–9

    Google Scholar 

  • Kwasnoski LA, Dudus KA, Fish AM, Abernathy EV, Briggs CW (2019) Examining sublethal effects of anticoagulant rodenticides on haemosporidian parasitemia and body condition in migratory red-tailed hawks. J Raptor Res 53(4):402–409

    Article  Google Scholar 

  • Lambert O, Pouliquen H, Larhantec M, Thorin C, L’Hostis M (2007) Exposure of raptors and waterbirds to anticoagulant rodenticides (difenacoum, bromadiolone, coumatetralyl, coumafen, brodifacoum): epidemiological survey in Loire Atlantique (France). Bull Environ Contam Toxicol 79(1):91–94

    Article  CAS  Google Scholar 

  • Lohr MT, Davis RA (2018) Anticoagulant rodenticide use, non-target impacts and regulation: a case study from Australia. Sci Total Environ 634:1372–1384

    Article  CAS  Google Scholar 

  • López-Perea L, Mateo R (2018) Secondary exposure of anticoagulant rodenticides and effects in predators. In: van den Brink N, Elliott JE, Shore RF, Rattner BA (Eds.) Anticoagulant rodenticides and wildlife. Springer International Publishing, Cham, Switzerland, p 159–193

    Chapter  Google Scholar 

  • Memmott K, Murray M, Rutberg A (2017) Use of anticoagulant rodenticides by pest management professionals in Massachusetts, USA. Ecotoxicology. 26(1):90–96

    Article  CAS  Google Scholar 

  • Morrisey JK, Paul-Murphy J, Fialkowski JP, Hart A, Darien BJ (2003) Estimation of Prothrombin Times of Hipaniolan Amazon parrots (Amazona ventralis) and Umbrella Cockatoos (Cacatua alba). J Avian Med Surg 17(2):72–77

    Article  Google Scholar 

  • 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(1):88–97

    Article  Google Scholar 

  • Murray M (2017) 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. Ecotoxicology. 26:1041–1050

    Article  CAS  Google Scholar 

  • Murray M (2018) Ante-mortem and post-mortem signs of anticoagulant rodenticide toxicosis in birds of prey. In: van den Brink N, Elliot JE, Shore RF, Rattner BA ed Anticoagulant rodenticides and wildlife. Springer Nature, Cham, p 109–134

    Chapter  Google Scholar 

  • Murray M (2020) Continued anticoagulant rodenticide exposure of red-tailed hawks (Buteo jamaicensis) in the Northeastern United States with an evaluation of serum for biomonitoring. Environ Toxicol Chem 39(11):2325–2335

    Article  CAS  Google Scholar 

  • Newton I, Wyllie I (1990) Rodenticides in British Barn Owls (Tyto alba). Ecol Conserv Owls 68(1–2):101–117

    CAS  Google Scholar 

  • Okoniewski JC, VanPatten C, Ableman AE, Hynes KP, Martin AL, Furdyna P (2022) Anticoagulant Rodenticides in Red-tailed Hawks (Buteo jamaicensis) from New York City, New York, USA, 2012-18. J Wildl Dis 57(1):162–167

    Google Scholar 

  • Quinn NQ, Kenmuir S, Krueger L (2019) A California without rodenticides: challenges for commensal rodent management in the future. Hum-Wildl Interactions 13(2):212–225

    Google Scholar 

  • Rattner BA, Horak KE, Warner SE, Day DD, Johnston JJ (2010) Comparative toxicity of diphacinone to Northern Bobwhite (Colinus virginianus) and American Kestrels (Falco sparverius). Proc Vertebr Pest Conf 24:146–152

    Google Scholar 

  • Rattner BA, Horak KE, Warner, Sarah E, Day, Daniel D, Meteyer CU, Volker SF, Eisemann JD, Johnston JJ (2011) Acute toxicity, histopathology, and coagulopathy in american kestrels (falco sparverius) following administration of the rodenticide diphacinone. Environ Toxicol Chem 30(5):1213–1222

    Article  CAS  Google Scholar 

  • 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(3):832–846

    Article  CAS  Google Scholar 

  • Rattner BA, Horak KE, Lazarus RS, Goldade DA, Johnston JJ (2014) Toxicokinetics and coagulopathy threshold of the rodenticide diphacinone in eastern screech-owls (Megascops asio). Environ Toxicol Chem 33(1):74–81

    Article  CAS  Google Scholar 

  • Rattner BA, Lazarus RS, Elliott JE, Shore RF, Van Den Brink N (2014) Adverse outcome pathway and risks of anticoagulant rodenticides to predatory wildlife. Environ Sci Technol 48(15):8433–8445

    Article  CAS  Google Scholar 

  • 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. 24:720–734

    Article  CAS  Google Scholar 

  • Rattner BA, Mastrota FN (2018) Anticoagulant rodenticide toxicity to non-target wildlife under controlled exposure conditions. In: van den Brink N, Elliott JE, Shore RF, Rattner BA (Eds.) Anticoagulant rodenticides and wildlife. Springer International Publishing, Cham, Switzerland, p 45–86

    Chapter  Google Scholar 

  • Rattner BA, Volker SF, Lankton JS, Bean TG, Lazarus RS, Horak KE (2020) Brodifacoum toxicity in American kestrels (Falco sparverius) with evidence of increased hazard upon subsequent anticoagulant rodenticide exposure. Environ Toxicol Chem 39:468–481

    Article  CAS  Google Scholar 

  • Rattner BA, Harvey JJ (2021) Challenges in the interpretation of anticoagulant rodenticide residues and toxicity in predatory and scavenging birds. Pest Manag Sci 77:604–610

    Article  CAS  Google Scholar 

  • Ruiz-Suarez N, Henriquez-Hernandez LA, Valeron PF, Boada LD, Zumbado M, Camacho M, Almeida-Gonzalez M, Luzardo OP (2014) Sci Total Environ. 485–486, p 371–376

  • Seljetun KO, Sandvik M, Vindenes V, Eliassen E, Oiestad EL, Madslien K, Moe L (2020) Comparison of anticoagulant rodenticide concentrations in liver and feces from apparently healthy red foxes. J Vet Diagn Investig 32(4):560–564

    Article  CAS  Google Scholar 

  • Slankard KG, Gaskill CL, Cassone LM, Rhoden CM (2019) Changes in detected anticoagulant rodenticide exposure in barn owls (Tyto alba) in Kentucky, USA, in 2012–16. J Wildl Dis 55(2):432–437

    Article  CAS  Google Scholar 

  • 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(1):6–9

    Article  CAS  Google Scholar 

  • Stone WB, Okoniewski JC, Stedelin JR (1999) Poisoning of wildlife with anticoagulant rodenticides in New York. J Wildl Dis 35(2):187–193

    Article  CAS  Google Scholar 

  • Stone WB, Okoniewski JC, Stedelin JR (2003) Anticoagulant rodenticides and raptors: recent findings from New York, 1998-2001. Bull Environ Contam Toxicol 70(1):34–40

    Article  CAS  Google Scholar 

  • Thomas PJ, Mineau P, Shore RF, Champoux L, Martin PA, Wilson LK, Fitzgerald G, Elliott JE (2011) Second generation anticoagulant rodenticides in predatory birds: probabilistic characterisation of toxic liver concentrations and implications for predatory bird populations in Canada. Environ Int 37(5):914–920

    Article  CAS  Google Scholar 

  • Vandenbroucke V, Bousquet-Melou A, De Backer P, Croubels S (2008) Pharmacokinetics of eight anticoagulant rodenticides in mice after single oral administration. J Vet Pharmacol Ther 31(5):437–445

    Article  CAS  Google Scholar 

  • Vyas NB, Lockhart JM, Rattner BA, Kuncir F (2014) Coagulopathy and survival of red-tailed hawks following exposure to the anticoagulant rodenticide Rozol®. Society of Environmental Toxicology and Chemistry-North America 35th Annual Meeting. MP043.

  • Vyas NB, Kuncir F, Clinton CC (2017) Influence of poisoned prey on foraging behavior of ferruginous hawks. Am. Midl. Nat. 177:75–83

    Article  Google Scholar 

  • Witmer GW (2018) Perspectives on existing and potential new alternatives to anticoagulant rodenticides and the implications for integrated pest management. In: van den Brink N, Elliott JE, Shore RF, Rattner BA (Eds.) Anticoagulant rodenticides and wildlife. Springer International Publishing, Cham, Switzerland, p 357–378

    Chapter  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the staff of the Janet L. Swanson Wildlife Hospital as well as the staff in the Wildlife Health Lab and Comparative Coagulation Lab who assisted with obtaining and processing the samples used in this study. The authors would also like to thank Tatiana Weisbrod for her invaluable help in establishing this project.

Funding

This study was funded by the Wiederhold Foundation at the Cornell University College of Veterinary Medicine.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cynthia Hopf-Dennis.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Consent for publication

This paper and all its contents were review and approved for publication by all contributing authors.

Ethical approval

This study was approved by the Cornell University Animal Care and Use Committee.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hopf-Dennis, C., Kaye, S., Hollingshead, N. et al. Prevalence of anticoagulant rodenticide exposure in red-tailed hawks (Buteo jamaicensis) and utility of clotting time assays to detect coagulopathy. Ecotoxicology 31, 919–932 (2022). https://doi.org/10.1007/s10646-022-02558-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-022-02558-y

Keywords

Navigation