Impacts of Rodenticide and Insecticide Toxicants from Marijuana Cultivation Sites on Fisher Survival Rates in the Sierra National Forest, California

Conservation Letters

Volumn 7, Issue 2, 2014, Pages 91-102

  Thompson, Craig ^a   Sweitzer, Richard ^b   Gabriel, Mourad ^c   Purcell, Kathryn ^a   Barrett, Reginald ^b   Poppenga, Robert ^d  

^a PACIFIC SOUTHWEST RESEARCH STATION   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Integral Ecology Research Center   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anticoagulant rodenticide; Fisher; Marijuana; Pekania pennanti; Pesticide; Survival

Indexed keywords

EID: 84897394175     PISSN: None     EISSN: 1755263X     Source Type: Journal    
DOI: 10.1111/conl.12038     Document Type: Article

References (79)

1. Ahdaya, S.M., Shah, P.V. & Guthrie, F.E. (1976). Thermoregulation in mice treated with parathion, carbaryl, or DDT. Toxicol. Appl. Pharm., 35, 575-580.
2. Allen, G. T., Veatch, J.K., Stroud, R.K. et al. (1996). Winter poisoning of coyotes and raptors with furadan laced carcass baits. J. Wildlife Dis., 32, 385-389.
3. Alterio, N., Brown, K. & Moller, H. (1997). Secondary poisoning of mustelids in a New Zealand Nothofagus forest, London. J. Zool., 243, 863-869.
4. Arnot, L.F., Veale, D.J.H., Steyl, J.C.A. & Myburgh, J.G. (2011). Treatment rationale for dogs poisoned with alicarb (carbamate pesticide). J. S. Afr. Vet. Assoc., 82, 232-238.
5. Bailey, C., Fisher, P. & Eason, C.T. (2005). Assessing anticoagulation resistance in rats and coagulation effects in birds using small volume blood samples. Sci. Conserv., 249, 5-22.
6. Berny, P. (2007). Pesticides and the intoxication of wild animals. J. Vet. Pharm. Therapy, 30, 93-100.
7. Berny, P.J., 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, 1817-1829.
8. Booth, I.H., Fisher, P., Heppelthwaite, V., & Eason, C.T., 2003. Toxicity and residues of brodifacoum in snails and earthworms. DOC Science Internal Series, 143, New Zealand Department of Conservation, Wellington, NZ. 14 p.
9. Burklow, T.R., Yu, C.E. & Madsen, J.M. (2003). Industrial chemicals: terrorist weapons of opportunity. Pediatr, Ann., 32, 230-234.
10. Cooke, A.S. (1971). Selective predation by newts on frog tadpoles treated with DDT. Nature, 229, 275-276.
11. Cope, O.B. (1971). Interactions between pesticides and wildlife. Ann. Rev. Entomol., 16, 325-364.
12. Davidson, R.S. & Armstrong, D.P. (2002). Estimating impacts of poison operations on non-target species using mark-recapture analysis and simulation modeling: an example with saddlebacks. Biol. Conserv., 105, 375-381.
13. Dowding, C.V., Shore, R.F., Worgan, A., Baker, P.J. & Harris, S. (2010). Accumulation of anticoagulant rodenticides in a non-target insectivore, the European hedgehog (Erinaceus europaeus). Environ. Pollut., 158, 161-166.
14. Environmental Protection Agency (EPA) (2009). Carbofuran; Final Tolerance Revocations; Final Rule. Federal Register 74 (93), 23045-23095.
15. Erickson, W. & Urban, D. 2004. Potential risks of nine rodenticides to birds and nontarget mammals: a comparative approach. U.S. Environmental Protection Agency, Office of Pesticides Programs, Environmental Fate and Effects Division, Washington DC, USA.
16. Farr, J.A. (1977). Impairment of antipredator behavior in Palaemonetes pugio by exposure to sublethal doses of parathion. Trans. Am. Fish. Soc., 106, 287-290.
17. Fournier-Chambrillon, C., Berny, P.J., 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 (Mustella letreola). J. Wildlife Dis., 40, 688-695.
18. Gabriel, M.W., Wengert, G.M., Higley, J.M., Krogan, S., Sargent, W. & Clifford, D.L., (2013). Silent forests? Wildlife Prof., 7, 46-50.
19. Gabriel, M.W., Woods, L.W., 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.
20. Golomb, B.A. (2008). Acetylcholinesterase inhibitors and Gulf War Illnesses. Proc. Natl. Acad. Sci. U.S.A., 105, 4295-4300.
21. Gordon, C.J. (1994). Thermoregulation in laboratory mammals and humans exposed to anticholinesterase agents. Neurotoxicol. Teratol., 16, 427-453.
22. Grue, C.E., Gilbert, P.L. & Seeley, M.E. (1997). Neurophysiological and behavioral changes in non-target wildlife exposed to organophosphate and carbamate pesticides: thermoregulation food consumption, and reproduction. Am. Zool., 37, 269-388.
23. Grue, C.E., Hart, A.D.M. & Mineau, P. (1991). Biological consequences of depressed brain cholinesterase activity in wildlife. Pages 151-209 in P. Mineau, editor. Cholinesterase-inhibiting insecticides-their impact on wildlife and the environment. Elsevier Science Publishers B.V., Amsterdam, Netherlands.
24. Hosea, R.C. (2000). Exposure of non-target wildlife to anticoagulant rodenticides in California. Proceedings of the 19th 507 Vertebrate Pest Conference, University of California, Davis, CA, USA.
25. Hunt, K.A., Bird, D.M., Mineau, P. & Shutt, L. (1992). Selective predation of organophosphate-exposed prey by American kestrels. Anim. Behav., 43, 971-976.
26. Janeway, C. A., Travers, P. & Walport, M. (2007). Immunobiology. 7th edition. Garland Science, New York, USA
27. Jaques, L.B. (1959). Dicoumarol drugs and the problem of haemorrhage. Can. Med. Assoc. J., 81, 848-854.
28. Keller, S.M., Gabriel, M., Terio, K.A. et al. (2012). Canine distemper in an isolated population of fishers (Martes pennanti) from California. J. Wildlife Dis., 48, 1035-1041.
29. Kendall, R.J. & Smith, P.N. (2003). Wildlife toxicology revisited. Envirn. Sci. Technol., 37, 179A-183A.
30. Kiesecker, J.M. (2002). Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? PNAS, 99, 9900-9904.
31. Knaus, B.J., Cronn, R. Liston, A., Pilgrim, K. & Schwartz, M. K. (2011). Mitochondrial genome sequences illuminate maternal lineages of conservation concern in a rare carnivore. BMC Ecol., 11, 10. doi:10.1186/1472-6785-11-10
32. Lemarchand, C., Rosoux, R. & Berny, P. (2011). Semi-aquatic top predators as sentinels of diversity and dynamics of pesticides in aquatic food webs: the case of Eurasian otter (Lutra lutra) and Osprey (Pandion haliaetus) in the Loire River catchment, France. Pages 298-310 in M. Stoytcheva, editor. Pesticides in the modern world: risks and benefits. InTech, Manhattan, NY, USA, ISBN 978-953-307-458-0.
33. Lemus, J.A., Bravo, C., Garcia-Montijano, M., Palacin, C., Ponce, C., Magana, M.M & Alonso, J.C. (2011). Side effects of rodent control on non-target species: Rodenticides increase parasite and pathogen burden in great bustards. Sci. Total Environ. 409, 4729-4734.
34. Li, Q. & Kawada, T. (2006). The mechanism of OP pesticide-induced inhibition of cytolytic activity of killer cells. Cell. Mole. Immunol., 3, 171-178.
35. Littrell, E. E. (1988). Wild carnivore deaths due to anticoagulant intoxication. Calif. Fish Game, 74, 183.
36. Lotti, M. & Moretto, A. (2006). Do carbamates cause polyneuropathy? Muscle Nerve, 34, 499-502
37. Macek, K.J. (1969). Screening of pesticides against fish, p. 92. In Progress in Sport Fishery Research, 1968. Bureau of Sport Fisheries and Wildlife, U.S. Res. Publ., 77, 259 pp.
38. Martin, P.A. & Solomon, K.R. (1991). Acute carbofuran exposure and cold stress: 537 Interactive effects in mallard ducklings. Pestic. Biochem. Physiol., 40, 117-127.
39. Mayer, K.E. & Laudenslayer, W.F. (1989). A guide to wildlife habitats of California. California Department of Forestry, Sacramento, USA.
40. McMillan, S.C., Hosea, R.C., Finlayson, B.F., Cypher, B.L. & Mekebri A. (2008). Anticoagulant rodenticide exposure in an urban population of San Joaquin kit, in R.M. Timm, M.B. Madon, editors. Proceedings of the 23rd Vertebrate Pest Conference 23, 163-165.
41. Mendenhall, V.M. & Pank, L.F.. (1980). Secondary poisoning of owls by anticoagulant rodenticides. Wildlife Soc. Bull., 8, 311-315.
42. Morner, T., Obendorff, D.L., Artois, M. & Woodford, M.H. (2002). Surveillance and monitoring of wildlife diseases. Revue Scientifique et Technique de l'Office International des Epizooties, 21, 67-76.
43. Olgun, S. (2004). Immunotoxicity of pesticide mixtures and the role of oxidative stress. PhD dissertation. Virginia Polytechnic Institute, Blacksburg VA.
44. Paul, N. & Mannathukkaran, T.J. 2005. Intermediate syndrome following carbamate poisoning. Clin. Toxicol., 43, 867-868
45. Proulx, G. (2011). Field evidence of non-target and secondary poisoning by strychnine and chlorophacinone used to control Richardson's ground squirrels in southwest Saskatchewan. Pages 128-134 in Danyluk, D., editor. Proc. Ninth Prairie Conserv. Endang. Species Conf. Winnepeg, MB, Canada.
46. 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, 41-47.
47. Rattner, B.A., Horak, K.E., Lazarus, R.S. et al. (2012). Assessment of toxicity and potential risk of the anticoagulant rodenticide diphacinone using Eastern screech-owls (Megascops asio). Ecotoxicology, 21, 832-846.
48. Relyea, R.A. (2003). Predator cues and pesticides: a double dose of danger for amphibians. Ecol. Appl., 13, 1515-1521.
49. Releya, R.A. & Diecks, N. (2008). An unforeseen chain of events: lethal effects of pesticides on frogs at sublethal concentrations. Ecol. Appl., 18, 1728-1742.
50. Richards, N. (2011). Carbofuran and wildlife poisoning: global perspectives and forensic approaches. John Wiley and Sons, West Sussex. UK. 304 pp.
51. Riley, S.P., Bromley, C., Poppenga, R.H., Uzal, F.A., Whited, L. & Sauvajot, R.M. (2007). Anticoagulant exposure and notoedric mange in bobcats and mountain lions in urban Southern California. J. Wildlife Manage., 71, 1874-1884.
52. Roelofs, W., Crocker, D.R., Shore, R.F. et al. (2005). Case Study Part 2: Probabilistic modelling of long-term effects of pesticides on individual breeding success in birds and mammals. Ecotoxicology, 14, 895-923.
53. Robertson, H.A & Colbourne, R.M. (2001). Survival of little spotted kiwi exposed to the rodenticide brodifacoum. J. Wildlife Manage., 65, 29-34.
54. Rohr, J.R., Schotthoefer, A.M., Raffel, T.R. et al. (2008). Agrochemicals increase trematode infections in a declining amphibian species. Nature, 455, 1235-1239.
55. Sanchez-Barbudo, I.S., Camarero, P.R., & Mateo, R. (2012). Primary and secondary poisoning by anticoagulant rodenticides of non-target animals in Spain. Sci. Total Environ. 420, 280-288.
56. Scheller, R.M., Spencer, W.D., Rustigian-Romsos, H., Syphard, A.D., Ward, B.C. & Strittholt, J. (2011). Using stochastic simulation to evaluate competing risks of wildfires and fuels management on an isolated forest carnivore. Landscape Ecol., 26, 1491-1504.
57. Shore, R.F., Birks, J.D.S. & Freestone, P. (1999). Exposure of non-target vertebrates to second-generation rodenticides in Britain, with particular reference to the polecat (Mustela putorius). New Zeal. J. Ecol., 23, 199-206.
58. Sibley, R.M., Newton, I. & Walker, C.H. (2000). Effects of dieldrin on population growth rates of sparrowhawks 1963-1986. J. Appl. Ecol., 37, 540-546.
59. Spencer, W.D., Rustigian-Romsos, H., Strittholt, J., Scheller, R., Zielinski, W. & Truex, R. (2011). Using occupancy and population models to assess habitat conservation opportunities for an isolated carnivore population. Biol. Conserv., 144, 788-803.
60. Stone, W.B., Okoniewski, J.C. & Stedelin, J.R. (1999). Poisoning of wildlife with anticoagulant rodenticides in New York. J. Wildlife Dis., 35, 187-193.
61. Susser, M. (1973). Causal thinking in the health sciences: concepts and strategies of epidemiology. Oxford University Press. Oxford, England.
62. Terry, A.V. (2012). Functional consequences of repeated organophosphate exposure: potential non cholinergic mechanisms. Pharmacol. Therap., 134, 355-365.
63. Thompson, H. (1996). Interactions between pesticides: a review of reported effects and their implications for wildlife risk assessment. Ecotoxicology, 5, 59-81.
64. Thompson, C.M., Purcell, K.L., Garner, J. & Green, R.E. (2010). Kings River Fisher Project progress report 2007-2010. Unpublished report to the USDA Forest Service, Pacific Southwest Research Center. Albany, CA. 37 pp.
65. Thompson, C.M., Zielinski, W.J. & Purcell, K.L. (2011). Evaluating management risks using landscape trajectory analysis: a case study of California fisher. J. Wildlife Manage., 75, 1164-1176.
66. Townsend, M.G., Bunyan, P.J., Odum, E.M., Stanley, P.I. & Wardall, H.P. (1984) Assessment of secondary poisoning hazard of warfarin to least weasels. J. Wildlife Manage., 48, 628-632.
67. Tucker, J.M., Schwartz, M.K., Truex, R.L., Pilgrim, K.L. & Allendorf, F.W. (2012). Historical and contemporary DNA indicate fisher decline and isolation occurred prior to European settlement of California. PLoS ONE. 7, e52803. doi:10.1371/journal.pone.0052803.
68. Vidal, D., Alzaga, V., Luque-Larena, J.J., Mateo, R., Arroyo, L. & Vinuela, J. (2009). Possible interaction between a rodenticide treatment and a pathogen in common vole (Microtus arvalis) during a population peak. Sci. Total Environ., 408, 267-271.
69. Villafuerte, R., Vinuela, J. & Blanco, J.C. (1998). Extensive predator persecution caused by population crash in a game species: the case of red kites and rabbits in Spain. Biol. Conserv., 84, 181-188.
70. Webster, K.H. 2009. Validation of a prothrombin time (PT) 613 assay for assessment of brodifacoum exposure in Japanese quail and barn owls. Master's Thesis, Simon Fraser University
71. Wengert, G.M., Gabriel, M.W. & Clifford, D.L. (2012). Investigating cause-specific mortality and diseases in carnivores: tools and techniques. Pages 294-313 in L. Boitani, R.A. Powell, editors. Carnivore ecology and conservation: a handbook of techniques. Oxford University Press, USA.
72. Winters, A.M., Rumbeiha, W.K., Winterstein, S.R., Fine, A.E., Munkhtsog, B. & Hickling, G.J. (2010). Residues in Brandt's voles (Microtus brandti) exposed to bromadiolone-impregnated baits in Mongolia. Ecotoxicol. Environ., 73, 1071-1077.
73. Wobeser, G., Bollinger, T., Leighton, F.A., Blakley, B. & Mineau, P. (2004). Secondary poisoning of eagles following intentional poisoning of coyotes with anticholinesterase pesticides in western Canada. J. Wildlife Dis., 40, 163-172.
74. Zabrodskii, P.F., Germanchuk, V.G., Kirichuk, V.F., Birdin, V.S. & Chuev, A.N. (2002). Combined effects of toxicants with various mechanisms of action and mechanical trauma on the immune system. Bull. Experime. Biol. Med., 6, 594-596.
75. Zabrodskii, P.F., Lim, V.G. & Strel'tsova E.V. (2012). Disturbances of immune status and cytokine profile caused by chronic intoxication with OP compounds ad their correction by administration of imunofan. Eksp Klin Farmakol., 75, 35-37.
76. Zielinski, W.J., Kucera, T.E. & Barrett, R.H. (1995). Current distribution of the fisher, Martes pennanti, in California. Calif. Fish Game, 81, 104-112.
77. Zielinski, W.J., Duncan, N.P., Farmer, E.C., Truex, R.L., Clevanger, A.P. & Barrett, R.H. (1999). Diet of fishers (Martes pennanti) at the southernmost extent of their range. J. Mammal., 80, 961-971.
78. Zielinski, W.J., Truex, R.L., Schlexer, F.V., Campbell, L.A. & Carroll, C. (2005). Historical and contemporary distributions of carnivores in forests of the Sierra Nevada, California, USA. J. Biogeogr., 32, 1385-1407.
79. Zielinski, W. J., Baldwin, J.A., Truex, R.L., Tucker, J.M. & Flebbe, P.A. (2013). Estimating trend in occupancy for the Southern Sierra Fisher (Martes pennanti) population. J. Fish Wildlife Manage, 4, doi: http://dx.doi.org/10.3996/012012-JFWM-002.