Advertisement

Exposure of non-target small mammals to anticoagulant rodenticide during chemical rodent control operations

  • Morten ElmerosEmail author
  • Rossana Bossi
  • Thomas Kjær Christensen
  • Lene Jung Kjær
  • Pia Lassen
  • Christopher John Topping
Research Article
  • 33 Downloads

Abstract

The extensive use of anticoagulant rodenticides (ARs) results in widespread unintentional exposure of non-target rodents and secondary poisoning of predators despite regulatory measures to manage and reduce exposure risk. To elucidate on the potential vectoring of ARs into surrounding habitats by non-target small mammals, we determined bromadiolone prevalence and concentrations in rodents and shrews near bait boxes during an experimental application of the poison for 2 weeks. Overall, bromadiolone was detected in 12.6% of all small rodents and insectivores. Less than 20 m from bait boxes, 48.6% of small mammals had detectable levels of bromadiolone. The prevalence of poisoned small mammals decreased with distance to bait boxes, but bromadiolone concentration in the rodenticide positive individuals did not. Poisoned small mammals were trapped up to 89 m from bait boxes. Bromadiolone concentrations in yellow-necked mice (Apodemus flavicollis) were higher than concentrations in bank vole (Myodes glareolus), field vole (Microtus agrestis), harvest mouse (Micromys minutus), and common shrew (Sorex araneus). Our field trials documents that chemical rodent control results in widespread exposure of non-target small mammals and that AR poisoned small mammals disperse away from bating sites to become available to predators and scavengers in large areas of the landscape. The results suggest that the unintentional secondary exposure of predators and scavengers is an unavoidable consequence of chemical rodent control outside buildings and infrastructures.

Keywords

Rodent control Anticoagulant rodenticides Non-target exposure Secondary poisoning Rodent dispersal Insectivores 

Notes

Acknowledgements

Jennifer Lynch, Jens Peder Hounisen, and Lars Haugaard provided invaluable technical and field assistance. We thank Charlotte Dahl Schiødt and Ellen Christiansen for laboratory assistance and the Danish Nature Agency for access to the field sites. We also thanks the reviewers for valuable comments on an earlier draft of the manuscript.

Funding

The study was funded by research grants from the Danish Environmental Protection Agency (MST 667-00100 and MST 667-00112).

Compliance with ethical standards

The field trials were done in accordance with a permit issued to the Department of Bioscience by the Danish Nature Agency: SN302-009SEI.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11356_2018_4064_MOESM1_ESM.docx (19 kb)
Table S1 (DOCX 18 kb)

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. Alomar H, Chabert A, Coeurdassier M, Vey D, Berny P (2017) Accumulation of anticoagulant rodenticides (chlorophacinone, bromadiolone and brodifacoum) in a non-target invertebrate, the slug, Deroceras reticulatum. Sci Total Environ 610-611:576–582CrossRefGoogle Scholar
  3. Alterio N, Brown K, Moller H (1997) Secondary poisoning of mustelids in a New Zealand Nothofagus forest. J Zool 243:863–869CrossRefGoogle Scholar
  4. Berny P, Gaillet J-R (2008) Acute poisoning of red kites (Milvus milvus) in France: data from the SAGIR network. J Wildl Dis 44:417–426CrossRefGoogle Scholar
  5. Booth IF, Fisher P, Heppelthwaite V, Eason CT (2003) Toxicity and residues of brodifacoum in snails and earthworm. Department of Conservation, DOC Science Internal Series 143, WellingtonGoogle Scholar
  6. Brakes CR, Smith RH (2005) Exposure of non-target small mammals to rodenticides: short-term effects, recovery and implications for secondary poisoning. J Appl Ecol 42:118–128CrossRefGoogle Scholar
  7. Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35CrossRefGoogle Scholar
  8. Carlsen M (1993) Migrations of Mus musculus musculus in Danish farmland. Z Säugetierkd 58:172–180Google Scholar
  9. Christensen TK, Lassen P, Elmeros M (2012) High exposure rates of anticoagulant rodenticides in predatory bird species in intensively managed landscapes in Denmark. Arch Environ Contam Toxicol 63:437–444CrossRefGoogle Scholar
  10. Coeurdassier M, Riols R, Decors A, Mionnet A, David F, Quintaine T, Truchetet D, Scheifler R, Giraudoux P (2014) Unintentional wildlife poisoning and proposals for sustainable management of rodents. Conserv Biol 28:315–321CrossRefGoogle Scholar
  11. Coeurdassier M, Fritsch C, Jacquot M, van den Brink N, Giraudoux P (2018) Spatial dimension of the risks of rodenticide use to non-target small mammals and applications in spatially explicit risk modeling. In: van den Brink N, Elliott J, Shore R, Rattner B (eds) Anticoagulant rodenticides and wildlife. Springer Publishers, Cham, pp 195–227Google Scholar
  12. Cox P, Smith RH (1992) Rodenticide ecotoxicology: pre-lethal effects of anticoagulants on rat behaviour. In: Borrecco JE, Marsh RE (eds) Proceedings of the 15th Vertebrate Pest Conference. University of California, Davis, pp 64–170Google Scholar
  13. Dowding CV, Shore RF, Worgan A, Baker PJ, Harris S (2010) Accumulation of anticoagulant ro-denticides in a non-target insectivore, the European hedgehog (Erinaceus europaeus). Environ Pollut 158:161–166CrossRefGoogle Scholar
  14. Eason CT, Spurr EB (1995) Review of the toxicity and impacts of brodifacoum on non-target wildlife in New Zealand. N Z J Zool 22:371–379CrossRefGoogle Scholar
  15. Eason CT, Murphy EC, Wright GRG, Spurr EB (2002) Assessment of risk of brodifacoum to non-target birds and mammals in New Zealand. Ecotoxicology 11:35–48CrossRefGoogle Scholar
  16. 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
  17. Elmeros M (2006) Food habits of stoats Mustela erminea and weasels Mustela nivalis in Denmark. Acta Theriol 51:179–186CrossRefGoogle Scholar
  18. Elmeros M, Birch MM, Madsen AB, Baagøe HJ, Pertoldi C (2008) Skovmårens biologi og levevis i Danmark. Scientific report no. 692, National Environmental Research Institute, Aarhus University, AarhusGoogle Scholar
  19. Elmeros M, Christensen TK, Lassen P (2011) Concentrations of anticoagulant rodenticides in stoats Mustela erminea and weasels Mustela nivalis from Denmark. Sci Total Environ 409:2373–2378CrossRefGoogle Scholar
  20. Elmeros M, Lassen P, Bossi R, Topping CJ (2018) Exposure of stone marten (Martes foina) and polecat (Mustela putorius) to anticoagulant rodenticides: effects of regulatory restrictions of rodenticide use. Sci Total Environ 612:1358–1364CrossRefGoogle Scholar
  21. Erickson W, Urban D (2004) Potential risks of nine rodenticides to birds and non-target mammals: a comparative approach. U.S. Environmental Protection Agency report. EPA Office of Pesticide Programs, Washington DCGoogle Scholar
  22. European Food Safety Authority (2010) Conclusion on the peer review of the pesticide risk assessment of the active substance bromadiolone. EFSA J 8:1783.  https://doi.org/10.2903/j.efsa.2010.1783 CrossRefGoogle Scholar
  23. Fraser D, Mouton A, Serieys LEK, Cole S, Carver S, Vandewoude S, Lappin M, Riley SPD, Wayne R (2018) Genome-wide expression reveals multiple systemic effects associated with detection of anticoagulant poisons in bobcats (Lynx rufus). Mol Ecol 27:1–18CrossRefGoogle Scholar
  24. Geduhn A, Esther A, Schenke D, Mattes H, Jacob J (2014) Spatial and temporal exposure patterns in non-target small mammals during brodifacoum rat control. Sci Total Environ 496:328–338CrossRefGoogle Scholar
  25. Geduhn A, Esther A, Schenke D, Gabriel D, Jacob J (2016) Prey composition modulates exposure risk to anticoagulant rodenticides in a sentinel predator, the barn owl. Sci Total Environ 544:150–157CrossRefGoogle Scholar
  26. Gómez JM, Puerta-Piñero C, Schupp EW (2008) Effectiveness of rodents as local seed dispersers of Holm oaks. Oecologia 155:529–537CrossRefGoogle Scholar
  27. Hammershøj M, Thomsen EA, Madsen AB (2004) Diet of free-ranging American mink and European polecat in Denmark. Acta Theriol 49:337–347CrossRefGoogle Scholar
  28. Lemus JA, Bravo C, García-Montijano M, Palacín C, Ponce C, Magaña M, Alonso JC (2011) Side effects of rodent control on non-target species: rodenticides increase parasite and pathogen burden in great bustards. Sci Total Environ 409:4729–4734CrossRefGoogle Scholar
  29. Love R, Webbon C, Glue DE, Harris S (2000) Changes in the food of British barn owls (Tyto alba) between 1974 and 1997. Mammal Rev 30:107–129CrossRefGoogle Scholar
  30. Macdonald DW, Tew TE, Todd IA, Garner JP, Johnson PJ (2000) Arable habitat use by wood mice (Apodemus sylvaticus). 3. A farm-scale experiment on the effects of crop rotation. J Zool 250:313–320CrossRefGoogle Scholar
  31. Madsen SA, Madsen AB, Elmeros M (2002) Seasonal food of badgers (Meles meles) in Denmark. Mammalia 66:341–352CrossRefGoogle Scholar
  32. Montgomery WI (1989) Population regulation in the wood mouse, Apodemus sylvaticus. II. Density dependence in spatial distribution and reproduction. J Anim Ecol 58:477–494Google Scholar
  33. By- og Landskabsstyrelsen (2010) Plan for fokuseret forebyggelse og bekæmpelse af rotter i Danmark. By- og Landskabsstyrelsen, Miljøministeriet, Copenhagen (in Danish)Google Scholar
  34. Pocock MJO, Hauffe H, Searle JB (2005) Dispersal in house mice. Biol J Linn Soc 84:565–583CrossRefGoogle Scholar
  35. 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 48:8433–8445CrossRefGoogle Scholar
  36. Ruiz-Suarez N, Melero Y, Giela A, Henriquez-Hernandez LA, Sharp E, Boada LD, Taylor MJ, Camacho M, Lambin X, Luzardo OP, Hartley G (2016) Rate of exposure of a sentinel species, invasive American mink (Neovison vison) in Scotland, to anticoagulant rodenticides. Sci Total Environ 569:1013–1021CrossRefGoogle Scholar
  37. Sage M, Coeurdassier M, Defaut R, Gimbert F, Berny P, Giraudoux P (2008) Kinetics of bromadiolone in rodent populations and implications for predators after field control of the water vole, Arvicola terrestris. Sci Total Environ 407:211–222CrossRefGoogle Scholar
  38. Sainsbury KA, Shore RF, Schofield H, Croose E, Pereira MG, Sleep D, Kitchener AC, Hantke G, McDonald RA (2018) Long-term increase in secondary exposure to anticoagulant rodenticides in European polecats Mustela putorius in Great Britain. Environ Pollut 236:689–698CrossRefGoogle Scholar
  39. Sandell M, Agrell J, Erlinge S, Nelson J (1991) Adult philopatry and dispersal in the field vole Microtus agrestis. Oecologia 86:153–158CrossRefGoogle Scholar
  40. Serieys LE, Armenta TC, Moriarty JG, Boydston EE, Lyren LM, Poppenga RH, Crooks KR, Wayne RK, Riley SP (2015) Anticoagulant rodenticides in urban bobcats: exposure, risk factors and potential effects based on a 16-year study. Ecotoxicology 24:844–862CrossRefGoogle Scholar
  41. Shore RF, Birks JDS, Afsar A, Wienburg CL, Kitchener AC (2003) Spatial and temporal analysis of second-generation anticoagulant rodenticide residues in polecat (Mustela putorius) from throughout their range in Britain, 1992-1999. Environ Pollut 122:183–193CrossRefGoogle Scholar
  42. Stradiotto A, Cagnacci F, Delahay R, Tioli S, Nieder L, Rizzoli A (2009) Spatial organization of the yellow-necked mouse: effects of density and resource availability. J Mammal 90:704–714CrossRefGoogle Scholar
  43. Szacki J (1999) Spatially structured populations: how much do they match classic metapopulation concept? Landsc Ecol 14:369–379CrossRefGoogle Scholar
  44. Taylor KD (1978) Range of movement and activity of common rats (Rattus norvegicus) on agricultural land. J Appl Ecol 15:663–677CrossRefGoogle Scholar
  45. Topping CJ, Elmeros M (2016) Modeling exposure of mammalian predators to anticoagulant rodenticides. Front Environ Sci 4:80.  https://doi.org/10.3389/fenvs.2016.00080 CrossRefGoogle Scholar
  46. Tosh DG, McDonald RA, Bearhop S, Llewellyn NR, Montgomery I, Shore RF (2012) Rodenticide exposure in wood mouse and house mouse populations on farms and potential secondary risk to predators. Ecotoxicology 21:1325–1332CrossRefGoogle Scholar
  47. Townsend MG, Entwhistle P, Hart ADM (1995) Use of two halogenated biphenyls as indicators of non-target exposure during rodenticide treatments. Bull Environ Contam Toxicol 54:526–533CrossRefGoogle Scholar
  48. Vandenbrough V, Bouquet-Melou A, De Backer P, Croubels S (2008) Pharmacokinetics of eight anticoagulant rodenticides in mice after single oral administration. J Vet Pharmacol Therap 31:437–445CrossRefGoogle Scholar
  49. Wolton RJ, Flowerdew JR (1985) Spatial distribution and movements of wood mice, yellow necked mice and bank voles. Symp Zool Soc Lond 55:249–275Google Scholar
  50. World Health Organization (WHO) (1995) Environmental health criteria 175: anticoagulant rodenticides. World Health Organization, GenevaGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Morten Elmeros
    • 1
    Email author
  • Rossana Bossi
    • 2
  • Thomas Kjær Christensen
    • 1
  • Lene Jung Kjær
    • 1
    • 3
  • Pia Lassen
    • 2
  • Christopher John Topping
    • 1
  1. 1.Department of BioscienceAarhus UniversityRøndeDenmark
  2. 2.Department of Environmental ScienceAarhus UniversityRoskildeDenmark
  3. 3.National Veterinary InstituteTechnical University of DenmarkKgs. LyngbyDenmark

Personalised recommendations