Abstract
Anticoagulant rodenticides (ARs) are increasingly recognized as a threat to nontarget wildlife. High exposure to ARs has been documented globally in nontarget predatory species and linked to the high prevalence of an ectoparasitic disease, notoedric mange. In southern California, mange associated with AR exposure has been the proximate cause of a bobcat (Lynx rufus) population decline. We measured AR exposure in bobcats from two areas in southern California, examining seasonal, demographic and spatial risk factors across landscapes including natural and urbanized areas. The long-term study included bobcats sampled over a 16-year period (1997–2012) and a wide geographic area. We sampled blood (N = 206) and liver (N = 172) to examine exposure ante- and post-mortem. We detected high exposure prevalence (89 %, liver; 39 %, blood) and for individuals with paired liver and blood data (N = 64), 92 % were exposed. Moreover, the animals with the most complete sampling were exposed most frequently to three or more compounds. Toxicant exposure was associated with commercial, residential, and agricultural development. Bobcats of both sexes and age classes were found to be at high risk of exposure, and we documented fetal transfer of multiple ARs. We found a strong association between certain levels of exposure (ppm), and between multiple AR exposure events, and notoedric mange. AR exposure was prevalent throughout both regions sampled and throughout the 16-year time period in the long-term study. ARs pose a substantial threat to bobcats, and likely other mammalian and avian predators, living at the urban-wildland interface.
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References
Albert CA, Wilson LK, Mineau P et al (2009) Anticoagulant rodenticides in three owl species from western Canada, 1988–2003. Arch Environ Contam Toxicol 58:451–459
Anderson EM, Lovallo MJ (2003) Bobcat and lynx. In: Feldhamer GA, Thompson BC, Chapman JA (eds) Wild mammals of North America: biology, management, and conservation. John Hopkins University Press, Baltimore, pp 758–786
Bartos M, Dao S, Douk D, Falzone S (2012) Use of anticoagulant rodenticides in single-family neighborhoods along an urban-wildland interface in California. Cities Environ 4(1):12
Beier P, Riley S, Sauvajot R (2010) Mountain Lions (Puma concolor). In: Gehrt S, Riley S, Cypher BL (eds) Urban carnviores. John Hopkins University Press, Baltimore, pp 141–155
Belij S, Miljkovic D, Popov A et al (2012) Effects of subacute oral warfarin administration on peripheral blood granulocytes in rats. Food Chem Toxicol 50:1499–1507
Berny P (2007) Pesticides and the intoxication of wild animals. J Vet Pharmacol Ther 30:93–100
Berny P, Gaillet J-R (2008) Acute poisoning of red kites (Milvus milvus) in France: data from the SAGIR network. J Wildl Dis 44:417–426
Berny PJ, Buronfosse T, Buronfosse F et al (1997) Field evidence of secondary poisoning of foxes (Vulpes vulpes) and buzzards (Buteo buteo) by bromadiolone, a 4-year survey. Chemosphere 35:1817–1829
Burnham K, Anderson D (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York, pp 1–488
California Department of Pesticide Regulation (2013) DPR 13-002 Notice of Proposed Regulatory Action. http://www.cdpr.ca.gov/docs/legbills/rulepkgs/13-002/notice.pdf. Accessed 14 Nov 2014
Cox P, Smith R (1992) Rodenticide ecotoxicology: pre-lethal effects of anticoagulants on rat behavior. In: Proceedings of the 15th vertebrate pest conference. University of California Davis, Davis, California, pp 164–170
Crowe DM (1972) The presence of annuli in bobcat tooth cementum layers. J Wildl Manag 36:1330–1332
Eason CT, Murphy EC, Wright GRG, Spurr EB (2002) Assessment of risks of brodifacoum to non-target birds and mammals in New Zealand. Ecotoxicology 11:35–48
Elmeros M, Christensen TK, Lassen P (2011) Concentrations of anticoagulant rodenticides in stoats (Mustela erminea) and weasels (Mustela nivalis) from Denmark. Sci Total Environ 409:2373–2378
Erickson W, Urban D (2004) Potential risks of nine rodenticides to birds and nontarget mammals: a comparative approach. United States Environmental Protection Agency Report. http://pi.ace.orst.edu/search/getDocketDocument.s?document=EPA-HQ-OPP-2006-0955-0005. Accessed 14 Nov 2014
Fedriani JM, Fuller TK, Sauvajot R, York E (2000) Competition and intraguild predation among three sympatric carnivores. Oecologia 125:258–270
Fournier-Chambrillon C, Berny PJ, Coiffier O et al (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 40:688–695
Gabriel MW, Woods LW, Poppenga R et al (2012) Anticoagulant rodenticides on our public and community lands: spatial distribution of exposure and poisoning of a rare forest carnivore. PLoS ONE 7:e40163. doi:10.1371/journal.pone.0040163
Gehrt S, Riley S (2010) Coyotes (Canis latrans). In: Gehrt S, Riley SPD, Cypher BL (eds) Urban carnivores. John Hopkins University Press, Baltimore, pp 78–95
Ginsberg JS, Hirsh J (1989) Anticoagulants during pregnancy. Ann Rev Med 40:79–86
Hadler M, Buckle A (1992) Forty-five years of anticoagulant rodenticides-past, present, and future. In: Proceedings of the fifteenth vertebrate pest conference. University of California Davis, Davis, California, pp 149–155
Hosea R (2000) Exposure of non-target wildlife to anticoagulant rodenticides in California. In: Proceedings of the 19th vertebrate pest conference. University of California, Davis, Davis, California, pp 236–244
Jaques LB (1959) Dicoumarol drugs and the problem of hæmorrhage. Can Med Assoc J 81:848
Kamil N (1987) Kinetics of bromadiolone, anticoagulant rodenticide, in the Norway rat (Rattus norvegicus). Pharmacol Res Commun 19:767–775
Kurohara M, Yasuda H, Moriyama H et al (2008) Low-dose warfarin functions as an immunomodulator to prevent cyclophosphamide-induced NOD diabetes. Kobe J Med Sci 54:E1–E13
Littrell EE (1988) Wild carnivore deaths due to anticoagulant intoxication. California Fish Game 74:183
Lyren LM, Turschak GM, Ambat ES, et al (2006) Carnivore activity and movement in a southern California protected area, the North/Central Irvine Ranch. Sacramento, California. Department of the Interior, United States Geological Survey, Western Ecological Research Center, Sacramento, California, Technical Report
Lyren LM, Alonso RS, Crooks K, Boydston E (2008) GPS telemetry, camera trap, and mortality surveys of bobcats in the San Joaquin Hills, Orange County, California. Department of the Interior, United States Geological Survey, Western Ecological Research Center, Sacramento, California, Technical Report
Maehr DS, Greiner EC, Lanier JE, Murphy D (1995) Notoedric mange in the Florida panther (Felis concolor coryi). J Wildl Dis 31:251–254
McDonald RA, Harris S, Turnbull G et al (1998) Anticoagulant rodenticides in stoats (Mustela erminea) and weasels (Mustela nivalis) in England. Environ Pollut 103:17–23
McMillin SC, Hosea RC, Finlayson BF (2008) Anticoagulant rodenticide exposure in an urban population of San Joaquin kit fox. Proceedings of the 23rd Verterbrate Pest Conference. University of California Davis, Davis, pp 163–165
Meserve PL (1976) Habitat and resource utilization by rodents of a California coastal sage scrub community. J Anim Ecol 45:647–666
Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405
Morzillo AT, Mertig AG (2011a) Urban resident attitudes toward rodents, rodent control products, and environmental effects. Urban Ecosyst 14:243–260
Morzillo AT, Mertig AG (2011b) Linking human behaviour to environmental effects using a case study of urban rodent control. Int J Environ Stud 68:107–123
Morzillo AT, Schwartz MD (2011) Landscape characteristics affect animal control by urban residents. Ecosphere 2:1–16
Munday JS, Thompson LJ (2003) Brodifacoum toxicosis in two neonatal puppies. Vet Path 40:216–219
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 25:307–314
Peakall DB (1992) Animal biomarkers as pollution indicators. Chapman & Hall, London
Pence DB, Ueckermann E (2002) Sarcoptic mange in wildlife. Rev Sci Tech 21:385–398
Pence DB, Matthews FD, Windberg LA (1982) Notoedric mange in the bobcat, Felis rufus, from south Texas. J Wildl Dis 18:47–50
Pence DB, Tewes ME, Shindle DB, Dunn DM (1995) Notoedric mange in an ocelot (Felis pardalis) from southern Texas. J Wildl Dis 31:558–561
Petterino C, Paolo B (2001) Toxicology of various anticoagulant rodenticides in animals. Vet Hum Toxicol 43:353–360
Poessel SA, Burdett CL, Boydston EE et al (2014) Roads Influence movement and home ranges of a fragmentation-sensitive carnivore, the bobcat, in an urban landscape. Biol Cons 180:224–232
Popov A, Belij S, Subota V et al (2013) Oral warfarin affects peripheral blood leukocyte IL-6 and TNFα production in rats. J Immunotoxicol 10:17–24
Riley SPD (1999) Spatial organization, food habits and disease ecology of bobcats (Lynx rufus) and gray foxes (Urocyon cinereoargenteus) in national park areas in urban and rural Marin County, California. Dissertation. University of California, Davis
Riley SPD, Sauvajot RM, Fuller TK et al (2003) Effects of urbanization and habitat fragmentation on bobcats and coyotes in southern California. Conserv Biol 17:566–576
Riley SPD, Pollinger JP, Sauvajot RM et al (2006) A southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15:1733–1741
Riley SPD, Bromley C, Poppenga R et al (2007) Anticoagulant exposure and notoedric mange in bobcats and mountain lions in urban southern California. J Wildl Manag 71:1874–1884
Riley SPD, Boydston EE, Crooks KR, Lyren LM (2010) Bobcats (Lynx rufus). In: Gehrt SD, Riley SPD, Cypher BL (eds) Urban carnivores. Johns Hopkins University Press, Baltimore, pp 121–138
Robben JH, Kuijpers EAP, Mout HCA (1998) Plasma superwarfarin levels and vitamin K1 treatment in dogs with anticoagulant rodenticide poisoning. Vet Q 20:24–27
Roberts LJ, Huffam SE, Walton SF, Currie BJ (2005) Crusted scabies: clinical and immunological findings in seventy-eight patients and a review of the literature. J Infect 50:375–381
Robinson MH, Twigg LE, Wheeler SH, Martin GR (2005) Effect of the anticoagulant, pindone, on the breeding performance and survival of merino sheep, Ovis aries. Comp Biochem Phys Part B 140:465–473
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 47:212–216
Sage M, Courdassier M, Defaut R et al (2008) Kinetics of bromadiolone in rodent populations and implications for predators after field control of the water vole, Arvicola terrestris. Sci Total Environ 407:211–222
Salmon T (2010) The Rat Island rat eradication project: a critical evaluation of nontarget mortality. The Ornithological Council. http://www.seabirdrestoration.org/pdf/RatIslandReview.pdf. Accessed 14 Nov 2014
Sánchez-Barbudo IS, Camarero PR, Mateo R (2012) Primary and secondary poisoning by anticoagulant rodenticides of non-target animals in Spain. Sci Total Environ 420:280–288
Scheuhammer AM (1987) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295
Serieys, LEK, Lea A, Pollinger JP, et al (2014) Disease and freeways drive genetic change in urban bobcat populations. Evol App (in press) doi:10.1111/eva.12226
Serieys LEK, Foley J, Owens S et al (2013) Serum chemistry, hematologic and post-mortem findings in bobcats (Lynx rufus) with notoedric mange. J Parasitol 99:989–996
Shore R (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 122:183–193. doi:10.1016/S0269-7491(02)00297-X
Shore RF, Malcolm HM, McClennan D et al (2006) Did foot-and-mouth disease-control operations affect rodenticide exposure in raptors? J Wildl Manag 70:588–593
Stephenson N, Clifford D, Worth SJ et al (2013) Development and validation of a fecal PCR assay for Notoedres cati and application to notoedric mange cases in bobcats (Lynx rufus) in Northern California, USA. J Wildl Dis 49:303–311
Stone WB, Okoniewski JC, Stedelin JR (1999) Poisoning of wildlife with anticoagulant rodenticides in New York. J Wildl Dis 35:187–193
Stone WB, Okoniewski JC, Stedelin JR (2003) Anticoagulant rodenticides and raptors: recent findings from New York, 1998–2001. Bull Environ Contam Toxicol 70:34–40. doi:10.1007/s00128-002-0152-0
R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 14 Nov 2014
Tosh DG, McDonald RA, Bearhop S et al (2012) Rodenticide exposure in wood mouse and house mouse populations on farms and potential secondary risk to predators. Ecotoxicology 21:1325–1332. doi:10.1007/s10646-012-0886-3
US Environmental Protection Agency, EPA (2008) Risk mitigation decision for ten rodenticides. USEPA Office of Prevention, Pesticides and Toxic Substances. http://www.epa.gov/oalj/filings/Reckitt_HrgReq_Ex03.pdf. Accessed 14 Nov 2014
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 31:437–445. doi:10.1111/j.1365-2885.2008.00979.x
Vidal D, Alzaga V, Luque-Larena J, Mateo R (2009) Possible interaction between a rodenticide treatment and a pathogen in common vole (Microtus arvalis) during a population peak. Sci Total Environ 408:267–271
Waddell LS, Poppenga R, Drobatz KJ (2013) Anticoagulant rodenticide screening in dogs: 123 cases (1996–2003). J Am Vet Med Assoc 242:516–521. doi:10.2460/javma.242.4.516
Walker LA, Turk A, Long SM et al (2008) Second generation anticoagulant rodenticides in tawny owls (Strix aluco) from Great Britain. Sci Total Environ 392:93–98. doi:10.1016/j.scitotenv.2007.10.061
Walton S, Holt D, Currie B, Kemp D (2004) Scabies: new future for a neglected disease. Adv Parasitol 54:309–376
Wesseling J, Van Driel D, Heymans HS et al (2001) Coumarins during pregnancy: long-term effects on growth and development of school-age children. Thromb Haemost 85:609–613
Acknowledgments
Funding was provided by the National Science Foundation (Graduate Research Fellowship), Summerlee Foundation, Santa Monica Bay Audubon Society, National Science Foundation Ecology of Infectious Disease research program (NSF EF-0723676), University of California, Los Angeles, U.S. Geological Survey, Panthera, Dan and Susan Gottlieb, the G2 gallery, Barry Rowan, the California Mediterranean Research and Learning Center, Julie Newsome, and Joel and Kian Schulman. We thank C. Schoonmaker, E.C. York, J. Sikich, D. Fraser, C. Reddell, I. Kelsey, K. Fragiacomo, J. Warner, R. Alonso, R. Mowry, J. Kraft, J. Purdum, D. Newell, and B. Nerhus for field assistance. For veterinary support in OCSA, we thank S. Weldy and K. Krause. Thanks to UCLA ATS consulting and S. Carver for help with data analysis. We appreciate all support and editorial comments provided by P. Jackson, T. Smith, J. Lloyd-Smith, and anonymous reviewers. Any use of trade, product, or firm names is for descriptive purposes only and does not imply an endorsement by the U.S. Government.
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The funders had no role in study design, data collection and analysis, or preparation of the manuscript and no competing interests exist.
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Serieys, L.E.K., Armenta, T.C., Moriarty, J.G. et al. Anticoagulant rodenticides in urban bobcats: exposure, risk factors and potential effects based on a 16-year study. Ecotoxicology 24, 844–862 (2015). https://doi.org/10.1007/s10646-015-1429-5
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DOI: https://doi.org/10.1007/s10646-015-1429-5