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Secondary Exposure to Anticoagulant Rodenticides and Effects on Predators

  • Jhon J. López-Perea
  • Rafael Mateo
Chapter
Part of the Emerging Topics in Ecotoxicology book series (ETEP, volume 5)

Abstract

Anticoagulant rodenticides (ARs) are currently the most common pesticides and biocides used to control rodents. The long-term persistence in animal tissues of the second-generation compounds (SGARs) causes their bioaccumulation in predatory species. In this chapter, we evaluate some of the key parameters that are likely to determine bioaccumulation and risk in wildlife from secondary exposure to ARs, review wildlife field monitoring studies from around the world to assess the scale of that exposure, and examine the current state of knowledge as to how secondary exposure relates to risk of mortality and other adverse effects in wildlife and in humans. Using a simple modelling approach and information from the published literature, we conclude that excretion rate is key in determining the extent of bioaccumulation and resultant risk in wildlife from secondary exposure to SGARs. We also find that secondary exposure in predators is widespread and widescale throughout the world, and may be greatest in predatory mammals that specialise on feeding on rodents. The extent of secondary [lethal and sub-lethal] poisoning that results is unclear. This is largely because unequivocal diagnosis of AR-mediated mortalities is not easy to determine from necropsy and there is no clear threshold residue that is diagnostic of effect, although recent development of probabilistic modelling of residue data may help in the future. We recommend that the direct consequences for predators from AR exposure, and the potential consequent impacts on the top-down regulation of rodent populations, deserve greater study.

Keywords

Rodenticide Ecotoxicology Bioaccumulation Bird Mammal Poisoning Food safety 

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. Alterio N (1996) Secondary poisoning of stoats (Mustela erminea), feral ferrets (Mustela furo), and feral house cats (Felis catus) by the anticoagulant poison, brodifacoum. New Zeal J Zool 23:331–338CrossRefGoogle Scholar
  3. Alterio N, Moller H (2000) Secondary poisoning of stoats (Mustela erminea) in a South Island podocarp forest, New Zealand: implications for conservation. Wildl Res 27:501–508CrossRefGoogle Scholar
  4. Alterio N, Brown K, Moller H (1997) Secondary poisoning of mustelids in a New Zealand Nothofagus forest. J Zool London 243:863–869CrossRefGoogle Scholar
  5. Andersson M, Erlinge S (1977) Influence of predation on rodent populations. Oikos 29:591–597CrossRefGoogle Scholar
  6. Beklova M, Krizkova S, Supalkova V, Mikelova R, Adam V, Pikula J, Kizek R (2007) Determination of bromadiolone in pheasants and foxes by differential pulse voltammetry. Int J Environ Anal Chem 87:459–469CrossRefGoogle Scholar
  7. Berny PJ, 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
  8. Berny PJ, Buronfosse T, Buronfosse F, Lamarque F, Lorgue G (1997) Field evidence of secondary poisoning of foxes (Vulpes vulpes) and buzzards (Buteo buteo) by bromadiolone, a 4-year survey. Chemosphere 35:1817–1829CrossRefGoogle Scholar
  9. Birks JDS (1998) Secondary rodenticide poisoning risk arising from winter farmyard use by the European polecat Mustela putorius. Biol Conserv 85:233–240CrossRefGoogle Scholar
  10. Bishop CA, Williams KE, Kirk DA, Nantel P, Reed E, Elliott JE (2016) A population model of the impact of a rodenticide containing strychnine on Great Basin Gophersnakes (Pituophis catenifer deserticola). Ecotoxicology 25:1390–1405.Google Scholar
  11. Bowie MH, Ross JG (2006) Identification of weta foraging on brodifacoum bait and the risk of secondary poisoning for birds on Quail Island, Canterbury, New Zealand. N Z J Ecol 30:219–228Google Scholar
  12. 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
  13. Brandt MJ, Lambin X (2007) Movement patterns of a specialist predator, the weasel Mustela nivalis exploiting asynchronous cyclic field vole Microtus agrestis populations. Acta Theriol (Warsz) 52:13–25CrossRefGoogle Scholar
  14. Brooke M, Cuthbert RJ, Harrison G, Gordon C, Taggart MA (2013) Persistence of brodifacoum in cockroach and woodlice: implications for secondary poisoning during rodent eradications. Ecotoxicoly Environ Saf 97:183–188CrossRefGoogle Scholar
  15. Brown KP, Alterio N, Moller H (1998) Secondary poisoning of stoats (Mustela erminea) at low mouse (Mus musculus) abundance in a New Zealand Nothofagus forest. Wildl Res 25:419–426CrossRefGoogle Scholar
  16. Buckle AP, Smith RH (2015) Rodent Pests and Their Control, 2nd edn. CABIGoogle Scholar
  17. Castillo E, Priotto J, Ambrosio AM, Provensal MC, Pini N, Morales MA, Steinmann A, Polop JJ (2003) Commensal and wild rodents in an urban area of Argentina. Int Biodeterior Biodegrad 52:135–141CrossRefGoogle Scholar
  18. Cavallari LH, Limdi NA (2009) Warfarin pharmacogenomics. Curr Opin Mol Ther 11:243–251Google Scholar
  19. Cavia R, Cueto GR, Suárez OV (2009) Changes in rodent communities according to the landscape structure in an urban ecosystem. Landsc Urban Plan 90:11–19CrossRefGoogle Scholar
  20. Channon D, Cole M, Cole L (2000) A long-term study of Rattus norvegicus in the London borough of Enfield using baiting returns as an indicator of sewer population levels. Epidemiol Infect 125:441–445CrossRefGoogle Scholar
  21. ChemIDplus (2015) ChemIDplus. A Toxnet Database. https://chem.nlm.nih.gov/chemidplus/name/brodifacoum. Accessed 20 June 2015
  22. ChemIDplus (2017) A Toxnet Database. https://chem.nlm.nih.gov/chemidplus/name/warfarin. Accessed 4 August 2017.
  23. 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
  24. Coeurdassier M, Poirson C, Paul J-P, Rieffel D, Michelat D, Reymond D, Legay P, Giraudoux P, Scheifler R (2012) The diet of migrant red kites Milvus milvus during a water vole Arvicola terrestris outbreak in eastern France and the associated risk of secondary poisoning by the rodenticide bromadiolone. Ibis 154:136–146CrossRefGoogle Scholar
  25. 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
  26. Craddock P (2003) Aspects of the ecology of forest invertebrates and the use of brodifacoum. Doctoral dissertation University of Auckland, New ZealandGoogle Scholar
  27. Dell’Arte GL, Laaksonen T, Norrdahl K, Korpimäki E (2007) Variation in the diet composition of a generalist predator, the red fox, in relation to season and density of main prey. Acta Oecol 31:276–281CrossRefGoogle Scholar
  28. Dowding CV, Shore RF, Worgan A, Baker PJ, Harris S (2010) Accumulation of anticoagulant rodenticides in a non-target insectivore, the European hedgehog (Erinaceus europaeus). Environ Pollut 158:161–166CrossRefGoogle Scholar
  29. Duff IF, Dennis EW, Hodgson PE, Coon EW (1953) Clinical experience with a new indandione derivative; a preliminary report. Med Bull (Ann Arbor) 19:43–48Google Scholar
  30. Eadsforth CV, Dutton AJ, Harrison EG, Vaughan JA (1991) A barn owl feeding study with [14C] flocoumafen-dosed mice – validation of a non-invasive method of monitoring exposure of barn owls to anticoagulant rodenticides in their prey. Pestic Sci 32:105–119CrossRefGoogle Scholar
  31. Eason CT, Milne L, Potts M, Morriss G, Wright GRG, Sutherland ORW (1999) Secondary and tertiary poisoning risks associated with brodifacoum. N Z J Ecol 23:219–224Google Scholar
  32. Eason CT, Wright GRG, Milne LM, Morriss GA (2001) Laboratory and field studies of brodifacoum residues in relation to risk of exposure to wildlife and people. Sci Conserv 177:11–23Google Scholar
  33. Eason CT, Murphy EC, Wright GRG, Spurr EB (2002) Assessment of risks of brodifacoum to non-target birds and mammals in New Zealand. Ecotoxicology 11:35–48CrossRefGoogle Scholar
  34. Eisemann JD, Swift CE (2006) Ecological and human health hazards from broadcast application of 0.005% diphacinone rodenticide baits in native Hawaiian ecosystems. In: Timm RM, O’Brien JM (eds) Proceedings 22nd of the Vertebrate Pest Conference, Berkeley, 6–9 March 2006. University of California, Davis, pp 413–433Google Scholar
  35. 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
  36. Elliott JE, Rattner B, Shore RF, van den Brink N (2016) Paying the pipers: mitigating the impact of anticoagulant rodenticides on predators and scavengers. Bioscience 66:401–407CrossRefGoogle Scholar
  37. 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
  38. Erickson W, Urban D (2004) Potential risks of nine rodenticides to birds and nontarget mammals: a comparative approach. EPA P.2004.27 A. Office of Prevention, Pesticides and Toxic Substances, U.S. Environmental Protection Agency, Washington, DCGoogle Scholar
  39. Figala J (1964) The reproduction and population structure of the black rat, Rattus rattus (L.) in the Czechoslovak habitats. Acta Soc Zool Bohemoslov 28:48–67Google Scholar
  40. Fisher PM (2006) Persistence of residual diphacinone concentrations in pig tissues following sublethal exposure. DOC Research & Development Series 249. Department of Conservation, Wellington, p 19Google Scholar
  41. Fisher PM (2009) Residual concentrations and persistence of the anticoagulant rodenticides brodifacoum and diphacinone in fauna. Lincoln University. PhD Thesis. 166 ppGoogle Scholar
  42. Fletcher DW (2002) Seven-day range-finding oral toxicity study of Ramik Green (0.005% diphacinone) in domestic swine (Sus scrofa). Unpublished Genesis Midwest Laboratories Report 203–0023-17, Neillsville, WI, p 38Google Scholar
  43. Fournier-Chambrillon C, Berny PJ, Coiffier O, Barbedienne P, Dassé B, Delas G, Galineau H, Mazet A, Pouzenc P, Rosoux R, Fournier P (2004) Evidence of secondary poisoning of free-ranging riparian mustelids by anticoagulant rodenticides in France: implications for conservation of European mink (Mustela lutreola). J Wildl Dis 40:688–695CrossRefGoogle Scholar
  44. Gabriel MW, Woods LW, Poppenga R, Sweitzer RA, Thompson C, Matthews SM, Higley JM, Keller SM, Purcell K, Barrett RH, Wengert GM, Sacks BN, Clifford DL (2012) Anticoagulant rodenticides on our public and community lands: spatial distribution of exposure and poisoning of a rare forest carnivore. PLoS One 7:e40163CrossRefGoogle Scholar
  45. Geduhn A, Jacob J, Schenke D, Keller B, Kleinschmidt S, Esther A (2015) Relation between intensity of biocide practice and residues of anticoagulant rodenticides in red foxes (Vulpes vulpes). PLoS One 10:e0139191CrossRefGoogle Scholar
  46. Giraudoux P, Tremollières C, Barbier B, Defaut R, Rieffel D, Bernard N, Lucot É, Berny P (2006) Persistence of bromadiolone anticoagulant rodenticide in Arvicola terrestris populations after field control. Environ Res 102:291–298CrossRefGoogle Scholar
  47. Godfrey MER (1985) Non-target and secondary poisoning hazards of “second generation” anticoagulants. Acta Zool Fenn 173:209–212Google Scholar
  48. Gómez-Canela C, Barata C, Lacorte S (2014a) Occurrence, elimination, and risk of anticoagulant rodenticides and drugs during wastewater treatment. Environ Sci Pollut Res 21:7194–7203CrossRefGoogle Scholar
  49. Gómez-Canela C, Vázquez-Chica A, Lacorte S (2014b) Comprehensive characterization of rodenticides in wastewater by liquid chromatography-tandem mass spectrometry. Anal Bioanal Chem 406:345–358CrossRefGoogle Scholar
  50. Gray A, Eadsforth CV, Dutton AJ, Vaughan JA (1994) The toxicity of three second-generation rodenticides to Barn Owls. Pestic Sci 42:179–184CrossRefGoogle Scholar
  51. Hafner DJ, Yensen E, Kirkland Jr GL (Compilers and eds) (1998) North American rodents. Status survey and conservation action plan. IUCN, Gland, Switzerland and Cambridge, UKGoogle Scholar
  52. Hanski I, Korpimäki E (1995) Microtine rodent dynamics in Northern Europe: parameterized models for the predator-prey interaction. Ecology 76:840–850CrossRefGoogle Scholar
  53. Hanski I, Hansson L, Henttonen H (1991) Specialist predators, generalist predators, and the microtine rodent cycle. J Anim Ecol 60:353–367CrossRefGoogle Scholar
  54. Hanski I, Turchin P, Korpimäki E, Henttonen H (1993) Population oscillations of boreal rodents: regulation by mustelid predators leads to chaos. Nature 364:232–235CrossRefGoogle Scholar
  55. Hegdal PL (1985) Primary hazards to game birds associated with the use of ramik brown (diphacinone bait) for controlling voles in orchards. Unpublished Report U02591, Denver Wildlife Research Center, U.S. Fish and Wildlife Service, Denver, CO, p 60Google Scholar
  56. 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
  57. Howard WE, Marsh RE, Cole RE (1970) A diphacinone bait for deer mouse control. J For 68:220–222Google Scholar
  58. Hughes J, Sharp E, Taylor MJ, Melton L, Hartley G (2013) Monitoring agricultural rodenticide use and secondary exposure of raptors in Scotland. Ecotoxicology 22:974–984CrossRefGoogle Scholar
  59. Hunter K (1985) High-performance liquid chromatographic strategies for the determination and confirmation of anticoagulant rodenticide residues in animal tissues. J Chromatogr 321:255–272CrossRefGoogle Scholar
  60. Ishizuka M, Tanikawa T, Tanaka KD, Heewon M, Okajima F, Sakamoto KQ, Fujita S (2008) Pesticide resistance in wild mammals mechanisms of anticoagulant resistance in wild rodents. J Toxicol Sci 33:283–291CrossRefGoogle Scholar
  61. Jacob J, Tradlec E (2010) Rodent outbreaks in Europe: dynamics and damage. In: Singleton GR, Belmain S, Brown P, Hardy B (eds) Rodent outbreaks: ecology and impacts. International Rice Research Institute, Los Baños – Philippines, pp 207–224Google Scholar
  62. Jacquot M, Coeurdassier M, Couval G, Renaude R, Pleydell D, Truchetet D, Raoul F, Giraudoux P (2013) Using long-term monitoring of red fox populations to assess changes in rodent control practices. J Appl Ecol 50:1406–1414CrossRefGoogle Scholar
  63. Katz R, Ducci H, Roeschmann W, Toriello L (1954) Clinical experience with dipaxin and with the combined use of prothrombopenic agents. Circulation 10:685–690CrossRefGoogle Scholar
  64. Keith JO, Hirata DN, Espy DL, Greiner S, Griffin D (2009) Field evaluation of 0.00025% diphacinone bait for mongoose control in Hawaii. Unpublished Report QA-16, Denver Wildlife Research Center, Denver COGoogle Scholar
  65. Knopper LD, Mineau P, Walker LA, Shore RF (2007) Bone density and breaking strength in UK raptors exposed to second generation anticoagulant rodenticides. Bull Environ Contam Toxicol 78:249–251CrossRefGoogle Scholar
  66. Korpimaki E, Norrdahi K (1998) Experimental reduction of predators reverses the crash phase of small-rodent cycles. Ecology 79:2448–2455CrossRefGoogle Scholar
  67. Korpimäki E, Brown PR, Jacob J, Pech RP (2004) The puzzles of population cycles and outbreaks of small mammals solved? Bioscience 54:1071–1079CrossRefGoogle Scholar
  68. Krebs CJ, Myers H (1974) Population Cycles in Small Mammals. Adv Ecol Res 8:267–273CrossRefGoogle Scholar
  69. Krieger R (ed) (2010) Hayes’ handbook of pesticide toxicology, vol Vol. 1. Academic, AmsterdamGoogle Scholar
  70. 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 79:91–94CrossRefGoogle Scholar
  71. Lazarus RS, Rattner BA, Brooks BW, Du B, McGowan PC, Blazer VS, Ottinger MA (2014) Exposure and food web transfer of pharmaceuticals in ospreys (Pandion haliaetus): predictive model and empirical data. Integr Environ Assess Manag 11:118–129CrossRefGoogle Scholar
  72. Lemarchand C, Rosoux R, Berny P (2010) Organochlorine pesticides, PCBs, heavy metals and anticoagulant rodenticides in tissues of Eurasian otters (Lutra lutra) from upper Loire River catchment (France). Chemosphere 80:1120–1124CrossRefGoogle Scholar
  73. López-Perea JJ, Camarero PR, Molina-López RA, Parpal L, Obón E, Solá J, Mateo R (2015) Interspecific and geographical differences in anticoagulant rodenticide residues of predatory wildlife from the Mediterranean region of Spain. Sci Total Environ 511C:259–267CrossRefGoogle Scholar
  74. Luque-Larena JJ, Mougeot F, Viñuela J, Jareño D, Arroyo L, Lambin X, Arroyo B (2013) Recent large-scale range expansion and outbreaks of the common vole (Microtus arvalis) in NW Spain. Basic Appl Ecol 14:432–441Google Scholar
  75. Marsh RE (1994) Roof rats. In: Hygnstrom SE, Timm RM, Larson GE (eds) The handbook: prevention and control of wildlife damage. Digital Commons@University of Nebraska, Lincoln, pp 125–132Google Scholar
  76. Marti CD (1973) Ten years of barn owl prey data from a Colorado nest site. Wilson Bull 85:85–86Google Scholar
  77. Mayol J, Mcminn M, Rodriguez A, Domenech O, Oliver J (2012) Sa Dragonera, la mayor isla mediterranea (posiblemente) libre de roedores. Quercus 314:27–33Google Scholar
  78. McDonald RA, Harris S, Turnbull G, Brown P, Fletcher M (1998) Anticoagulant rodenticides in stoats (Mustela erminea) and weasels (Mustela nivalis) in England. Environ Pollut 103:17–23CrossRefGoogle Scholar
  79. Mendenhall VM, Pank LF (1980) Secondary poisoning of owls by anticoagulant rodenticides. Wildl Soc Bull 8:311–315Google Scholar
  80. Merson MH, Byers RE, Kaunkeinen DE (1984) Residues of the rodenticide brodifacoum in voles and raptors after orchad treatment. J Wildl Dis 48:212–216CrossRefGoogle Scholar
  81. Montaz J, Jacquot M, Coeurdassier M (2014) Scavenging of rodent carcasses following simulated mortality due to field applications of anticoagulant rodenticide. Ecotoxicology 23:1671–1680CrossRefGoogle Scholar
  82. Morzillo AT, Mertig AG (2011) Urban resident attitudes toward rodents, rodent control products, and environmental effects. Urban Ecosyst 14:243–260CrossRefGoogle Scholar
  83. Mougeot F, Garcia JT, Viñuela J (2011) Breeding biology, behaviour, diet and conservation of the red kite (Milvus milvus), with particular emphasis on Mediterranean populations. In: Zuberogoitia I, Martínez JE (eds) Ecology and conservation of European dwelling forest raptors and owls. Editorial Diputación Foral de Vizcaya, Bilbao, pp 190–204Google Scholar
  84. Murphy EC, Clapperton BK, Bradfield PMF, Speed HJ (1998) Brodifacoum residues in target and non-target animals following large-scale poison operations in New Zealand podocarp-hardwood forests. New Zeal J Zool 25:307–314CrossRefGoogle Scholar
  85. 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
  86. Naim M, Noor HM, Kasim A, Abu J (2011) Comparison of the breeding performance of the barn owl Tyto alba javanica under chemical and bio-based rodenticide baiting in immature oil palms in Malaysia. Dyn Biochem Process Biotechnol Mol Biol 5:5–11Google Scholar
  87. Newton I, Wyllie I, Freestone P (1990) Rodenticides in British barn owls. Environ Pollut 68:101–117CrossRefGoogle Scholar
  88. Newton I, Wyllie I, Gray A, Eadsforth CV (1994) The toxicity of the rodenticide flocoumafen to barn owls and its elimination via pellets. Pestic Sci 41:187–193CrossRefGoogle Scholar
  89. Nogeire TM, Lawler JJ, Schumaker NH, Cypher BL, Phillips SE (2015) Land use as a driver of patterns of rodenticide exposure in modeled Kit Fox populations. PLoS One 10(8):e0133351CrossRefGoogle Scholar
  90. Ogilvie SC, Pierce RJ, Wright GRG, Booth LH, Eason CT (1997) Brodifacoum residue analysis in water, soil, invertebrates, and birds after rat eradication on Lady Alice Island. N Z J Ecol 21:195–197Google Scholar
  91. Olea PP, Sánchez-Barbudo IS, Viñuela J, Barja I, Mateo-Tomás P, Piñeiro A, Mateo R, Purroy FJ (2009) Lack of scientific evidence and precautionary principle in massive release of rodenticides threatens biodiversity: old lessons need new reflections. Environ Conserv 36:1–4CrossRefGoogle Scholar
  92. Pitt WC, Eisemann JD, Swift CE, Sugihara R, Dengler-Germain B, Driscoll L (2005) Diphacinone residues in free-ranging wild pigs following aerial broadcast of a rodenticide bait in a Hawaiian forest. Unpublished Report QA-1077. National Wildlife Research Center, Fort Collins, p 35Google Scholar
  93. Pitt WC, Higashi M, Primus TM (2011) The effect of cooking on diphacinone residues related to human consumption of feral pig tissues. Food Chem Toxicol 49:2030–2034CrossRefGoogle Scholar
  94. Pocock MJO, Searle JB, White PCL (2004) Adaptations of animals to commensal habitats: population dynamics of house mice Mus musculus domesticus on farms. J Anim Ecol 73:878–888CrossRefGoogle Scholar
  95. Proulx G, Mackenzie N (2012) Relative abundance of american badger (Taxidea taxus) and red fox (Vulpes vulpes) in landscapes with high and low rodenticide poisoning levels. Integr Zool 7:41–47CrossRefGoogle Scholar
  96. 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
  97. Rammell CG, Hoogenboom JJL, Cotter M, Williams JM, Bell J (1984) Brodifacoum residues in target and non-target animals following rabbit poisoning trials. New Zeal J Exp Agric 12:107–111CrossRefGoogle Scholar
  98. 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). In: Timm RM, Fagerstone KA (eds) Proceedings 24th of the Vertebrate Pest Conference, Sacramento 22–25 February 2010. University of California, Davis, pp 146–152Google Scholar
  99. Rattner BA, Horak KE, Warner SE, Day DD, 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 30:1213–1222CrossRefGoogle Scholar
  100. 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
  101. 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
  102. 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
  103. 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
  104. Redpath SM, Thirgood SJ (1999) Numerical and functional responses in generalist predators: hen harriers and peregrines on Scottish grouse moors. J Anim Ecol 68:879–892CrossRefGoogle Scholar
  105. Riley SPD, Bromley C, Poppenga RH, Uzal FA, Whited L, Sauvajot RM (2007) Anticoagulant exposure and notoedric mange in bobcats and mountain lions in urban Southern California. J Wildl Manag 71:1874–1884CrossRefGoogle Scholar
  106. Ruder MG, Poppenga RH, Bryan JA, Bain M, Pitman J, Keel MK (2011) Intoxication of nontarget wildlife with rodenticides in northwestern Kansas. J Wildl Dis 47:212–216CrossRefGoogle Scholar
  107. Ruiz-Suárez N, Henríquez-Hernández LA, Valerón PF, Boada LD, Zumbado M, Camacho M, Almeida-González M, Luzardo OP (2014) Assessment of anticoagulant rodenticide exposure in six raptor species from the Canary Islands (Spain). Sci Total Environ 485–486:371–376CrossRefGoogle Scholar
  108. Sage M (2008) Transfert de bromadiolone (appâts/sols – campagnols de prairie – renards): Etude environnementale de la persistance et mesure indirecte de l’exposition. Universite de Franche-Comte. U.F.R. Des Sciences et Techniques. These Docteur, 227 ppGoogle Scholar
  109. Sage M, Coeurdassier M, Defaut R, Lucot E, Barbier B, Rieffel D, Berny P, Giraudoux P (2007) How environment and vole behaviour may impact rodenticide bromadiolone persistence in wheat baits after field controls of Arvicola terrestris? Environ Pollut 148:372–379CrossRefGoogle Scholar
  110. 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
  111. Sage M, Fourel I, Cœurdassier M, Barrat J, Berny P, Giraudoux P (2010) Determination of bromadiolone residues in fox faeces by LC/ESI-MS in relationship with toxicological data and clinical signs after repeated exposure. Environ Res 110:664–674CrossRefGoogle Scholar
  112. Salim H, Noor HM, Hamid NH, Omar D, Kasim A, 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 26:6272Google Scholar
  113. Sánchez-Barbudo IS, Camarero PR, Mateo R (2012) Primary and secondary poisoning by anticoagulant rodenticides of non-target animals in Spain. Sci Total Environ 420:280–288CrossRefGoogle Scholar
  114. Sarabia J, Sánchez-Barbudo IS, Siqueira W, Mateo R, Rollán E, Pizarro M (2008) Lesions associated with the plexus venosus subcutaneus collaris of pigeons with chlorophacinone toxicosis. Avian Dis 52:540–543CrossRefGoogle Scholar
  115. Saravanan K, Kanakasabai R (2004) Evaluation of secondary poisoning of difethialone, a new second-generation anticoagulant rodenticide to barn owl, Tyto alba Hartert under captivity. Indian J Exp Biol 42:1013–1016Google Scholar
  116. Savarie PJ, Hayes DJ, McBride RT, Roberts JD (1979) Efficacy and safety of diphacinone as a predacide. Avian Mamm Wildl Toxicol 693:69–79CrossRefGoogle Scholar
  117. Shore RF, Birks JDS, Freestone P, Kitchener AC (1996) Second-generation rodenticides and polecats (Mustela putorius) in Britain. Environ Pollut 91:279–282CrossRefGoogle Scholar
  118. Shore RF, Birks JDS, Freestone P (1999) Exposure of non-target vertebrates to second-generation rodenticides in Britain, with particular reference to the polecat Mustela putorius. N Z J Ecol 23:199–206Google Scholar
  119. Shore RF, Birks JDS, Afsar A, Wienburg CL, Kitchener AC (2003) Spatial and temporal analysis of second-generation anticoagulant rodenticide residues in polecats (Mustela putorius) from throughout their range in Britain, 1992-1999. Environ Pollut 122:183–193CrossRefGoogle Scholar
  120. Shore RF, Malcolm HM, Wienburg CL, Walker LA, Turk A, Horne JA (2005) Wildlife and pollution: 2001/2002 – Annual Report. Joint Nature Conservation Committee Report 352. Peterborough, UKGoogle Scholar
  121. Shore RF, Malcolm HM, Mclennan D, Turk A, Walker LA, Wienburg CL, Burn AJ (2006) Did foot-and-mouth disease-control operations affect rodenticide exposure in raptors? J Wildl Manag 70:588–593CrossRefGoogle Scholar
  122. Singleton GR, Krebs CJ, Davis S, Chambers L, Brown P (2001) Reproductive changes in fluctuating house mouse populations in southeastern Australia. Proc R Soc London/Biol Sci 268:1741–1748CrossRefGoogle Scholar
  123. Singleton GR, Hinds LA, Krebs CJ, Spratt DM (eds) (2003) Rats, mice and people: rodent biology and management. ACIAR Monograph No. 96, Canberra – Australia, p 564Google Scholar
  124. Singleton GR, Belmain S, Brown P, Hardy B (eds) (2010) Rodent outbreaks: ecology and impacts. International Rice Research Institute, Los Baños – Philippines, p 286Google Scholar
  125. Spurr EB, Foote D, Perry CF, Lindsey GD (2003a) Efficacy of aerial broadcast application of baits containing 0.005% diphacinone in reducing rat populations in Hawaiian forests. Pacific Islands Ecosystems Research Center, U.S.Geological Survey, Unpublished Report QA-02. Washington, DCGoogle Scholar
  126. Spurr EB, Lindsey GD, Forbes PC, Foote D (2003b) Effectiveness of hand broadcast application of baits containing 0.005% diphacinone in reducing rat populations in Hawaiian forests. Pacific Island Ecosystems Research Center. US Geological Survey, Unpublished Report QA-01. Washington, DCGoogle Scholar
  127. Spurr EB, Maitland MJ, Taylor GE, Wright GRG, Radford CD, Brown LE (2005) Residues of brodifacoum and other anticoagulant pesticides in target and non-target species, Nelson Lakes National Park, New Zealand. New Zeal J Zool 32:237–249CrossRefGoogle Scholar
  128. Stansley W, Cummings M, Vudathala D, Murphy LA (2014) Anticoagulant rodenticides in red-tailed hawks, B uteo jamaicensis, and great horned owls, Bubo virginianus, from New Jersey, USA, 2008-2010. Bull Environ Contam Toxicol 92:6–9Google Scholar
  129. Stenseth NC, Leirs H, Skonhoft A, Davis SA, Pech RP, Andreassen HP, Singleton GR, Lima M, Machang’u RS, Makundi RH, Zhang Z, Brown PR, Shi D, Wan X (2003) Mice, rats, and people: the bio-economics of agricultural rodent pests. Front Ecol Environ 1:367–375CrossRefGoogle Scholar
  130. Stone WB, Okoniewski JC, Stedelin JR (1999) Poisoning of wildlife with anticoagulant rodenticides in New York. J Wildl Dis 35:187–193CrossRefGoogle Scholar
  131. 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
  132. Terraube J, Arroyo B, Madders M, Mougeot F (2011) Diet specialisation and foraging efficiency under fluctuating vole abundance: A comparison between generalist and specialist avian predators. Oikos 120:234–244CrossRefGoogle Scholar
  133. 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 37:914–920CrossRefGoogle Scholar
  134. Tosh DG, McDonald RA, Bearhop S, Lllewellyn NR, Fee S, Sharp EA, Barnett EA, Shore RF (2011a) Does small mammal prey guild affect the exposure of predators to anticoagulant rodenticides? Environ Pollut 159:3106–3112CrossRefGoogle Scholar
  135. Tosh DG, Shore RF, Jess S, Withers A, Bearhop S, Montgomery IW, McDonald RA (2011b) User behaviour, best practice and the risks of non-target exposure associated with anticoagulant rodenticide use. J Environ Manag 92:1503–1508CrossRefGoogle Scholar
  136. Tosh DG, McDonald RA, Bearhop S, Llewellyn NR, Montgomery WI, 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
  137. Valchev I, Binev R, Yordanova V, Nikolov Y (2008) Anticoagulant rodenticide intoxication in animals – a review. Turkish J Vet Anim Sci 32:237–243Google Scholar
  138. 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 31:437–445CrossRefGoogle Scholar
  139. Vidal D, Alzaga V, Luque-Larena JJ, Mateo R, Arroyo L, Viñuela J (2009) Possible interaction between a rodenticide treatment and a pathogen in common vole (Microtus arvalis) during a population peak. Sci Total Environ 408:267–271CrossRefGoogle Scholar
  140. Viñuela J, Villafuerte R, Blanco JC (1999) Incremento de la persecución de depredadores en España: sus causas y su efecto sobre el milano real. In: Viñuela J, Martí R, Ruiz A (eds) El milano Real en España. SEO/BirdLife, Madrid, Spain, pp 199–211Google Scholar
  141. Walker LA, Shore RF, Turk A, Pereira MG, Best J (2008a) The predatory bird monitoring scheme: identifying chemical risks to top predators in Britain. J Hum Environ 37:466–471CrossRefGoogle Scholar
  142. Walker LA, Turk A, Long SM, Wienburg CL, Best J, Shore RF (2008b) Second generation anticoagulant rodenticides in tawny owls (Strix aluco) from Great Britain. Sci Total Environ 392:93–98CrossRefGoogle Scholar
  143. Walker LA, Chaplow JS, Moeckel C, Pereira MG, Potter ED, Shore RF (2014) Anticoagulant rodenticides in predatory birds 2012: a Predatory Bird Monitoring Scheme (PBMS) report. Centre for Ecology & Hydrology, Lancaster. 18 pp. http://pbms.ceh.ac.uk/sites/pbms.ceh.ac.uk/files/PBMS%20Report%20Rodentocide%202012.pdf
  144. Watt BE, Proudfoot AT, Bradberry SM, Vale JA (2005) Anticoagulant rodenticides. Toxicol Rev 24:259–269CrossRefGoogle Scholar
  145. Weber P (2001) Vitamin K and bone health. Nutrition 17:880–887CrossRefGoogle Scholar
  146. Welling PG, Lee KP, Khanna U, Wagner JG (1970) Comparison of plasma concentrations of warfarin measured by both simple extraction and TLC methods. J Pharm Sci 59:1621–1625CrossRefGoogle Scholar
  147. Willis P, Macris J, Denis E, Hodgson P, Coon W, Gamble J, Duff I (1953) Clinical evaluation of dipaxin, an oral anticoagulant. J Lab Clin Med 52:968–968Google Scholar
  148. Wilson DE, Reeder DM (eds) (2005) Mammal species of the world: a taxonomic and geographic reference, vol Vol. 12. JHU Press, BaltimoreGoogle Scholar
  149. Winters AM, Rumbeiha WK, Winterstein SR et al (2010) Residues in Brandt’s voles (Microtus brandti) exposed to bromadiolone-impregnated baits in Mongolia. Ecotoxicol Environ Saf 73:1071–1077CrossRefGoogle Scholar
  150. Witmer GW (2007) The ecology of vertebrate pests and integrated pest management (IPM). In: Kogan M, Jepson P (eds) Perspectives in ecological theory and integrated pest management. Cambridge University Press, Cambridge, UK, pp 393–410CrossRefGoogle Scholar
  151. Zamorano E, Palomo L, Vargas J (1988) La rata negra (Rattus rattus Linneo, 1758) como plaga de los cultivos ibéricos de caña de azúcar. Detección, estima y control de los daños ocasionados. Boletín Sanid Veg Plagas 14:227–240Google Scholar

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© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.Instituto de Investigación en Recursos Cinegéticos (IREC) CSIC-UCLM-JCCMCiudad RealSpain

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