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Ecology, management and conservation in natural and modified habitats
REVIEW

Fumigation of rabbit warrens with chloropicrin produces poor welfare outcomes – a review

Clive A. Marks
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Nocturnal Wildlife Research Pty Ltd, PO Box 2126, Wattletree Road Post Office, East Malvern, Vic. 3145, Australia. Email: camarks@attglobal.net

Wildlife Research 36(4) 342-352 https://doi.org/10.1071/WR06128
Submitted: 6 October 2006  Accepted: 15 September 2008   Published: 1 June 2009

Abstract

Chloropicrin (CLPN) is used in Australia and New Zealand as a warren fumigant for the control of exotic European rabbits (Oryctolagus cuniculus) but is no longer registered for this purpose in the United States or the European Union. This review summarises the mammalian toxicology and clinical records from 56 accounts where signs, symptoms and pathology have been related to a range of CLPN concentrations. The approach follows a general principle where an assessment of the humaneness of vertebrate pest control techniques should be firstly based upon a thorough synopsis of published behavioural, physiological and pathological impacts. Chloropicrin produces intense irritation by stimulation of trigeminal nerves and brief exposures to concentrations of ≤1 ppm can severely irritate the eyes and cause lacrimation in mammals. Beyond 8 ppm, exposures are reported to be painful and incapacitating in humans. Mammals experience an array of common signs and symptoms including: headache, nausea, diarrhoea, laboured breathing, decrease in spontaneous motor activity, salivation, rhinorrhea, blood stains around the nose and mouth, painful irritation of mucous membranes, profuse lacrimation, audible obstruction of respiration and distress vocalisation. Acute pathological changes from CLPN exposure can cause death in mammals from pulmonary oedema, bronchopneumonia, emphysema or general destructive changes and necrosis of the small and medium bronchi. Overall, the signs, symptoms and pathology arising from CLPN exposure at any airborne concentration beyond 0.3 ppm indicate that it must be assumed to cause suffering in all mammals. Exposure to CLPN that is not acutely lethal may debilitate rabbits and other species and cause a protracted death over hours or days. To produce a humane death a fumigant must be non-irritating, have an initial depressive action on the central nervous system and/or produce a rapid death without protracted distress while having little ability to cause debilitation or chronic injury. Given that CLPN has none of these characteristics, it cannot be considered to be acceptably humane.


Acknowledgements

This review was commissioned by the Bureau of Animal Welfare (Victoria) with funds provided to the Animal Welfare Science Centre. The author thanks Dr John Barnett and Dr Ellen Jongman for their efforts to initiate this review. Ms Jane Malcolm’s valuable constructive feedback, proof reading and support was a big help throughout. The review benefited from discussions and suggestions from Dr Kate Blaszak, Dr Steve Tate, Dr Ellen Jongman and Dr Charles Hackman. Ms Sue Darby collected some important references for the review. The paper benefited from the constructive criticisms and suggestions made by three anonymous referees and editorial staff of Wildlife Research. I thank John Eisemann (United States Department of Agriculture, National Wildlife Research Center, Fort Collins), Eileen Mahoney (Pesticide Registration Branch, California), Helen Dunnett (Pesticide Information, European Crop Protection Association), Dr Eugene Georgiades (Environmental Risk Management Authority, New Zealand) for clarifying the registration status of chloropicrin as a vertebrate pest control product in their country or region.


References

ACGIH (1991). Documentation of the threshold limit values and biological exposure indices. American Conference of Government Industrial Hygienists, Cincinnati, OH.

ACGIH (1997). Documentation of the threshold limit values and biological exposure indices. American Conference of Government Industrial Hygienists, Cincinnati, OH.

Alarie, Y. (1966). Irritating properties of airborne materials to the upper respiratory tract. Archives of Environmental Health 14, 433–449.
Alarie Y. , Nielsen G. D. , and Schaper M. M. (2000). Animal bioassays for evaluation of indoor air quality. In ‘Indoor Air Quality Handbook’. (Eds J. D. Spengler, J. M. Samet and J. F. McCarthy.) pp. 23.1–23.49. (McGraw-Hill: New York.)

Andrews, D. (1964). Effects of tear gas on some mammals. Journal of Mammalogy 45, 321.
Crossref | GoogleScholarGoogle Scholar | Anon. (1987). ‘Drinking Water and Health: Disinfectants and Disinfectant By-products.’ (National Academy Press: Washington, DC.)

Anon. (1999). Rabbits: methods of fumigating rabbit burrows. Natural Resources and Environment, Melbourne.

Anon. (2000). Review of Burleigh-Flayer et al. 1995. ‘Chloropicrin: Vapour Inhalation Oncogenicity Study in CD-1 Mice’. California Emissions Inventory Development and Reporting System, Los Angeles.

Anon. (2004). Australian code of practice for the care and use of animals for scientific purposes. Australian Government Publishing Service, Canberra.

Anon. (2005). The Australian animal welfare strategy. Australian Government Publishing Service, Canberra.

Anon. (2007). Response from the Pest Management Regulatory Agency (PMRA) to the request for special reviews of pesticides from the David Suzuki Foundation. Pest Management Regulatory Agency, Ottawa.

Baumans, V. , Brain, P. F. , Brugere, H. , Clausing, P. , Jeneskog, J. , and Perretta, G. (1994). Pain and distress in laboratory rodents and lagomorphs: report of the federation of European laboratory animal science associations (FELASA) working group on pain and distress accepted by the FELASA board of management. Laboratory Animals 28, 97–112.
Crossref | GoogleScholarGoogle Scholar | PubMed | Budavari S. , O’Neil M. J. , Smith A. , and Hechelmanm P. E. (Eds) (1989). ‘The Merck Index.’ (Merck and Co.: Rahway, NJ.)

Buehler, E. V. , and Newmann, E. A. (1964). A comparison of eye irritation in monkeys and rabbits. Toxicology and Applied Pharmacology 6, 701–704.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Burleigh-Flayer H. D. and Benson C. L. (1995). ‘Chloropicrin: Vapour inhalation oncogenicity study in CD rats.’ (Union Carbide: Export.)

Clayton G. D. , and Clayton F. E. (1981). ‘Patty’s Industrial Hygiene and Toxicology.’ (Wiley: New York.)

Clelatt K. N. (Ed.) (1981). ‘Textbook of Veterinary Ophthalmology.’ (Lea and Febiger: Philadelphia, PA.)

Clerc, M. (1950). Technique for extermination of rats on ships with chloropicrin. Les entretiens de Bichat. Médecine. Entretiens de Bichat 31, 3–8.
Davis R. A. (1993). Aliphatic nitro, nitrates and nitrite compounds. In ‘Patty’s Industrial Hygiene and Toxicology’. pp. 624–625. (Wiley Interscience: New York.)

Deblauwe F. (2003). Ypres 1915: When chemicals first became an effective weapon of war. http://writing.deblauwe.org/ypres1915.html.

Duguet J. P. , Tsutsumi Y. , Bruchet A. , and Mallevialle J. (1985). Chloropicrin in potable water: conditions of formation and production during treatment processes. In ‘Water Chlorination: Chemistry, Environmental Impact and Health Effects’. (Eds R. L. Jolley, R. J. Bull, W. P. Davis, S. Katz, M. H. Roberts and V. A. Jacobs.) pp. 79–96. (M. I. Lewis: Chelsea, UK.)

Extoxnet (1999). Chloropicrin. Extension Toxicology Network. http://extoxnet.orst.edu/pips/chloropi.htm

Flury F. , and Zernik F. (1931). ‘Schadliche Gas.’ (Springer: Berlin.)

Fries A. A. , and West C. J. (1921). Chloropicrin. In ‘Chemical Warfare’. (Eds A. A. Fries and C. J. West.) pp. 144–149. (McGraw-Hill: New York.)

Fuhr, I. , Bronsford, A. V. , and Silver, S. D. (1948). Sorption of fumigant vapours by soil. Soap and Sanitary Chemicals 26, 127–129.
Gmelin L. (1852). ‘Handbook of Chemistry.’ (Cavendish Society: London.)

Gonmori, K. , Muto, H. , Yamamoto, T. , and Takahashi, K. (1987). A case of homicidal intoxication with chloropicrin. The American Journal of Forensic Medicine and Pathology 8, 135–138.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Haber L. F. (1986). ‘The Poisonous Cloud: Chemical Warfare in the First World War.’ (Claredon Press: Oxford.)

Hart S. , Marks C. A. , and Staples L. (1996). DEN-CO-FUME – Humane control of foxes (Vulpes vulpes) in natal dens. In ‘Humaneness and Vertebrate Pest Control’. (Eds P. M. Fisher and C. A. Marks.) pp. 58–61. (Ropet Printing: Tynong North, Australia.)

Hayes W. J. (1982). ‘Pesticides Studied in Man’. (Williams and Wilkins: Baltimore, MD.)

Hearn, C. E. D. (1973). A review of agricultural pesticide incidents in man in England and Wales, 1952–71. British Journal of Industrial Medicine 30, 253–258.
CAS | PubMed | HSDB (1996). Hazardous substances data bank. National Library of Medicine, Bethesda, MD.

Jackson, K. E. (1934). Chloropicrin. Chemical Reviews 14, 251–286.
Crossref | GoogleScholarGoogle Scholar | CAS | Jacobs M. B. (1942). ‘War Gases: their Identification and Decontamination.’ (Interscience Publishers: New York.)

Jordan, B. (2005). Science-based assessment of animal welfare: wild and captive animals. Revue Scientifique Et Technique-Office International Des Epizooties 24, 515–528.
CAS | Kaufman S. R. (1989). Problems with the Draize test. (Americans for Medical Advancement. www.curedisease.com/Perspectives/vol_1_1989/Problems%20with%20the%20Draize.html

Kootz, A. R. (1925). When do lungs return to normal following exposure to war gases? Archives of Internal Medicine 36, 204–219.
Lambert R. A. , and Jackson L. (1920). The pathology of chloropicrin poisoning. In ‘Collected Studies of the Pathology of War Gas Poisoning’. (Ed. M. C. Winternitz.) pp. 69–90. (Yale University Press: New Haven, CT.)

Littin, K. E. , Mellor, D. , Warburton, B. , and Eason, C. T. (2004). Animal welfare and ethical issues relevant to the humane control of vertebrate pests. New Zealand Veterinary Journal 52, 1–10.
CAS | PubMed | Mackinson R. W. , Stricoff R. S. , and Partridge L. J. (1978). Occupational health guidelines for chemical hazards. National Technical Information Service, Springfield, VA.

Mackworth, J. F. (1948). Inhibition of thiol enzymes by lachrymators. The Biochemical Journal 42, 82–90.
CAS | Marks C. A. (1996). Research directions for humane burrow fumigation and 1080 predator baiting. In ‘Humaneness and Vertebrate Pest Control’. (Eds P. M. Fisher and C. A. Marks.) pp. 58–61. (Ropet Printing: Tynong North, Australia.)

Marks C. A. (1998). Review of the humaneness of destruction techniques used on the common wombat (Vombatus ursinus) in Victoria. In ‘Wombats’. (Eds R. T. Wells and P. A. Pridmore.) pp. 287–297. (Surrey Beatty: Sydney.)

Marks C. A. (1999). Ethical issues in vertebrate pest management: can we balance the welfare of individuals and ecosystems? In ‘The Use of Wildlife for Research’. (Eds D. Mellor and V. Monamy.) pp. 79–89. (ANZCCART: Adelaide.)

Marks C. A. (2003). What is possible to ensure that existing control methods are more humane? In ‘Proceedings of the 2003 RSPCA Australia Scientific Seminar’. (Ed. B. Jones.) pp. 287–297. (RSPCA Australia: Canberra.)

Marks C. A. , Leighty R. , and Carolen J. (1989). Pest behaviour and management of the common wombat (Vombatus ursinus) in eastern Victoria. Monash University Graduate School of Environmental Science: Melbourne.

Martini, A. , Lorenzini, R. N. , Cinotti, S. , Fini, M. , Giavaresi, G. , and Giandino, R. (2000). Evaluation of pain and stress levels of animals used in experimental research. The Journal of Surgical Research 88, 114–119.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Matschke G. H. , and Fagerstone K. A. (1984). Efficacy of a two ingredient fumigant for Richardson’s ground squirrels. In ‘Proceedings of the 11th Vertebrate Pest Control Conference’. (Ed. D. O. Clark.) pp. 17–29. (University of California: Sacramento, CA.)

Mayer, J. (2007). Use of behavior analysis to recognize pain in small mammals. Lab Animal 36, 43–48.
Crossref | GoogleScholarGoogle Scholar | PubMed | McLaren W. D. (1966). Contributions to the biology of wombats in south-eastern Australia. Ph.D. Thesis. Monash University, Melbourne.

Mehler L. N. , O’Malley M. A. , and Krieger R. I. (1992). ‘Acute Pesticide Morbidity and Mortality: California.’ (Springer-Verlag: New York.)

Mellor, D. , and Stafford, K. J. (2001). Integrating practical, regulatory and ethical strategies for enhancing farm animal welfare. Australian Veterinary Journal 79, 762–768.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Morris J. (2001). Nasal toxicology. In ‘Inhalation Toxicology’. (Eds H. Salem and S. A. Katz.) pp. 349–366. (CRC Press: London.)

Moseby, K. E. , De Jong, S. , Munro, N. , and Pieck, A. (2005). Home range, activity and habitat use of European rabbits (Oryctolagus cuniculus) in arid Australia: implications for control. Wildlife Research 32, 305–311.
Crossref | GoogleScholarGoogle Scholar | OEHHA (1999). Chloropicrin. Determination of non-cancer chronic reference exposure levels. Office of Environmental Health Hazard Assessment. Data base. http://www.oehha.ca.gov/air/chronic_rels/pdf/chloropicrin.pdf.

Okada, E. , Takahashi, K. , and Nakamura, H. (1970). A study of CP intoxication. Nippon Naika Gakkai Zasshi 59, 60–67.
Paxman J. , and Harris R. A. (1982). ‘A Higher Form of Killing: The Secret Story of Chemical and Biological Warfare.’ (Hill and Wang: New York.)

Prentis A. M. (1937). ‘Chemicals in War: A Treatise on Chemical Warfare.’ (McGraw Hill: New York.)

Prince J. H. , Diesem C. D. , Eglitis I. , and Ruskell G. L. (1960). ‘Anatomy and Histology of the Eye and Orbit in Domestic Animals’. (Charles C. Thomas: Springfield.)

Proctor N. H. , and Hughes J. P. (1996). ‘Chemical Hazards of the Workplace.’ (Van Nostrand Reinhold: New York.)

Prudhomme, J. C. , Bhatia, R. , Nutik, J. M. , and Shusterman, D. J. (1999). Chest wall pain and possible rhabdomyolysis after chloropicrin exposure. A case series. Journal of Occupational and Environmental Medicine 41, 17–22.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Ratcliffe F. N. (1951). The rabbit problem: a survey of research needs and possibilities. CSIRO Australia Leaflet 1.

Reilly J. S. (Ed.) (2001). Euthanasia of animals used for scientific purposes. Australian and New Zealand Council for the Care of Animals in Research and Teaching, Adelaide.

Rollin M. , and Kessel L. (1990). ‘The Experimental Animal in Biomedical Research.’ (CRC Press: London.)

Rolls E. (1984). ‘They All Ran Wild.’ (Angus and Robertson: London.)

Ross J. (1986). Comparison of fumigant gases used for rabbit control in Great Britain. In ‘Proceedings of the 12th Vertebrate Pest Control Conference’. (Ed. T. P. Salmon.) pp. 153–157. (University of California: Davis, CA.)

Ross, R. , Page, R. J. C. , Nadian, A. K. , and Langton, S. D. (1998). The development of a carbon monoxide producing cartridge for rabbit control. Wildlife Research 25, 305–314.
Crossref | GoogleScholarGoogle Scholar | Rowsell H. C. , Ritchey J. , and Cox F. (1979). Assessment and humaneness of vertebrate pesticides. In ‘Proceedings of the Canadian Association for Laboratory Animal Science 1978–1979’. pp. 236–249. (Canadian Association for Laboratory Animal Science: Calgary.)

RSPCA (2004). A national approach towards humane vertebrate pest control. Discussion paper arising from the proceedings of an RSPCA Australia/AWC/VPC joint workshop. RSPCA Australia, Canberra.

Rutherford, K. M. D. (2002). Assessing pain in animals. Animal Welfare (South Mimms, England) 11, 31–53.
CAS | Salmon T. P. , and Bentley W. J. (1982). Aluminium phosphide (Phostoxin) as a burrow fumigant for ground squirrel control. In ‘Proceedings of the 10th Vertebrate Pest Control Conference’. (Ed. R. E. Marsh.) pp. 143–146. (University of California: Davis, CA.)

Saunders G. , Coman B. J. , Kinnear J. , and Braysher M. (1995). ‘Managing Vertebrate Pests: Foxes.’ (Australian Government Publishing Service: Canberra.)

Saunders L. Z. , and Rubin L. F. (1975). ‘Ophthalmic Pathology in Animals.’ (S. Karger: New York.)

Savarie P. J. , Tigner J. R. , Elias D. J. , and Hayes D. J. (1980). Development of a simple two ingredient pyrotechnic fumigant. In ‘Proceedings of the 9th Vertebrate Pest Conference’. (Ed. R. Marsh.) pp. 215–221. (University of California: Fresno, CA.)

Scott W. N. (1976). The use of poisons in animal destruction: humane destruction of unwanted animals. Universities Federation for Animal Welfare, Hertfordshire, UK.

Selala, M. I. , Janssen, J. J. , Jorens, P. G. , Bossaert, L. L. , Beaucourt, L. , and Schepens, P. J. (1989). An improperly labelled container with chloropicrin: a farmer’s nightmare. Bulletin of Environmental Contamination and Toxicology 42, 202–208.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Sexton M. (1983). ‘Declared Animal Control.’ (Technical Publications Trust: Perth.)

Sharp T. , and Saunders G. (2008). A model for assessing the relative humaneness of pest animal control methods. Australian Government Department of Agriculture, Canberra.

Sharpe, R. (1985). The Draize test: motivations for change. Food and Chemical Toxicology 23, 139–143.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Stafleu F. , Vorstenbosch J. , Tramper R. , de Jong M. , Eckelboom E. , and Krijger F. (2000). The concepts of “severe suffering” of experimental animals and “essential needs of man and animal” as used in cost–benefit analyses. In ‘Proceedings of the 3rd World Congress on Alternatives and Animal Use in the Life Sciences, Bologna, Italy, 29 August to 2 September 1999’. pp. 833–839. (Elsevier: Amsterdam.)

Swanston D. W. (1983). ‘Eye Irritancy Testing.’ (Academic Press: New York.)

Tamagawa, S. , Irimajiri, T. , and Oyamada, M. (1985). Persistence of chloropicrin in the soil and environmental effects on it. Journal of Pesticide Science 10, 205–210.
CAS | Timm R. M. (1983). ‘Prevention and Control of Wildlife Damage’. (Great Plains Agricultural Council: Denver, CO.)

Tomlinson, A. R. , and Crawford, J. S. (1951). The destruction of rabbits: with notes on methods of destroying emus, kangaroos, mice, rats and eagles. Journal of Agricultural 28, 121–148.
Underhill F. P. (1920). ‘The Lethal War Gases’. (Yale University Press: New Haven, CT.)

Verminpac (1984 a). ‘Wombats.’ (Department of Conservation, Forests and Lands: Melbourne.)

Verminpac (1984 b). ‘Foxes.’ (Department of Conservation, Forests and Lands: Melbourne.)

Williams, C. K. , and Moore, R. J. (1995). Effectiveness and cost-efficiency of control of the wild rabbit, Oryctolagus cuniculus (L.), by combinations of poisoning, ripping, fumigation and maintenance fumigation. Wildlife Research 22, 253–269.
Crossref | GoogleScholarGoogle Scholar | Williams J. (2004). CBRNE – Lung damaging agents, chloropicrin. eMedicine Knowledge Base. http://www.emedicine.com/emerg/topic907.htm

Williams K. , Parer I. , Coman B. , Burley J. , and Braysher M. (1995). ‘Managing Vertebrate Pests: Rabbits.’ (Government Publishing Service: Canberra.)

York, R. G. , Butala, J. H. , Ulrich, C. E. , and Schardein, J. L. (1994). Inhalation developmental toxicity studies of chloropicrin in rats and rabbits. Teratology 49, 419.
Zhi D. , and Chang Z. W. (1986). Efficacy of a carbon monoxide gas cartridge against field rodents. In ‘Proceedings of the 12th Vertebrate Pest Conference’. (Eds R. E. Marsh and D. E. Beadle.) pp. 163–165. (University of California: Davis, CA.)