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The physiological, ecological and evolutionary significance of monoglurpacetic acid in relation to plant animal interaction in Australia

Twigg, Laurie Edward (1986) The physiological, ecological and evolutionary significance of monoglurpacetic acid in relation to plant animal interaction in Australia. PhD thesis, Murdoch University.

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Abstract

The toxin monofluoroacetic acid occurs naturally in 33 species of the legume genera Gastrolobium and Oxylobium in the south west of Western Australia and in G. grandiflorum and Acacia georginae in northern Australia.

Increases in plasma citrate concentration in response to dosing with sodium fluoroacetate (Compound 1080) were shown to reflect the sensitivity to fluoroacetate intoxication of animals with similar metabolic rates and phylogenetic affinities.

Animal populations with evolutionary exposure to fluoroacetate-bearing vegetation were generally much more tolerant to fluoroacetate than were animal populations which had not been similarly exposed to the toxic plants.

Amongst the mammals, the herbivorous marsupial Setonix brachyurus, was found to have attained a high degree of tolerance to fluoroacetate. This tolerance was less developed in the omnivorous bandicoots, Isoodon obesulus, Macrotis lagotis and I. auratus, and was generally least developed in the carnivorous marsupials, Antechinus flavipes and Dasyurus geoffroii. The carnivorous marsupial Phascogale calura, however, was found to be moderately tolerant. It is suggested that the acquisition of tolerance to fluoroacetate by species of Dasyuridae living within the range of the fluoroacetate-bearing vegetation appears to have resulted from secondary exposure to fluoroacetate due to the ingestion of insects or of other items of prey which feed on the toxic plants. Caterpillars which utilize the poison plants as food were found to be highly tolerant to fluoroacetate.

The acquisition of tolerance to fluoroacetate was also evident in several species of Australian birds. In the Psittaciformes, those species which are indigenous to the south west of Western Australia (Platycercus icterotis and Purpureicephalus spurius) were more tolerant to fluoroacetate than were species of Psittaciformes whose distributions include areas outside the range of the toxic plants (Barnardius zonarius and Cacatua roseicapilla). Within these species, P. icterotis was the most tolerant followed in descending order by P. spurius, B. zonarius and C. roseicapilla.

Stretopelia senegalensis and the Barbary dove are Columbiformes with little or no prior exposure to fluoroacetate-bearing vegetation and they were found to be much more susceptible to fluoroacetate poisoning than were the Australian Columbiformes, Phaps chalcoptera and Ocyphaps lophotes, regardless of the extent of exposure of the latter species to the toxic plants. Within the species of Columbiformes from Western Australia, P. chalcoptera was the most tolerant followed in descending order by 0. lophotes, the Barbary dove and S. Senegalensis. P. chalcoptera from the south west of Western Australia was approximately 1.6-fold more tolerant to f1uoroacetate than the South Australian conspecifics which are outside the range of toxic plants. However, the tolerance of 0. lophotes from South Australia was similar to that of the conspecifics exposed to fluoroacetate-bearing vegetation in Western Australia. A similar situation also applied to the western and eastern Australian populations of Anas superciliosa and Chenonetta jubata. This suggests that during the evolution of some species of Australian birds, considerable gene flow has occurred between the bird populations of western and eastern Australia.

Of the species of birds investigated, Dromaius novaehollandiae was found to have the greatest tolerance to fluoroacetate and the LD50 value determined for this species was 102mg 1080 kg-1. This tolerance appears to result from; the substantial capacity of D. novaehollandiae detoxify defluorination; the inability of D. novaehol1andiae to readily convert fluoroacetate into f1uorocitrate, and/or to f1uoroacetate by the possession of an aconitate hydratase which is relatively insensitive to fluorocitrate.

The ectothermic vertebrate, Tiliqua rugosa possesses an innate tolerance to fluoroacetate intoxication but populations which co-exist with f1uoroacetate-bearing vegetation in Western Australia (LD50 500-800mg 1080 kg-1) were much more tolerant to f1uoroacetate than were unadapted T. rugosa from South Australia (LD50 ca. 200mg 1080 kg-1).

The innate f1uoroacetate-tolerance of T. rugosa resulted from; a low reliance on aerobic respiration; a low capacity to convert fluoroacetate to f1uorocitrate; an aconitate hydratase which is relatively insensitive to fluorocitrate; and a high capacity to defluorinate fluoroacetate or one of its metabolites by an enzymic glutathione-dependent mechanism. All of these factors contributed to the circumvention of acute fluoroacetate toxicity in this species of lizard. However, while these factors provide an explanation for the high level of innate tolerance exhibited by T. rugosa, the biochemical mechanisms responsible for the toxicity differential between the adapted and unadapted conspecifics remained unelucidated. Liver acetone-powder preparations from both conspecifics possessed similar abilities to defluorinate fluoroacetate and the aconitate hydratase in these preparations was also similarly inhibited by (-)erythrofluorocitrate.

Due to the defluorination process, administration of sub-lethal doses of sodium fluoroacetate to T. rugosa caused a depletion of liver glutathione levels which may result in hepatic damage. Furthermore, such administration caused a regression of the germinal epithelium of the seminiferous tubules in the testes of some lizards and also resulted in a decrease in plasma testosterone levels in male T. rugosa.

The acquisition of tolerance to fluoroacetate by reptilian populations exposed to fluoroacetate in nature was not unique to T. rugosa. Yaranus rosenbergi which co-exists with fluoroacetate-bearing vegetation in Western Australia could tolerate in excess of 200mg 1080 kg-1 while the South Australian conspecific from Kangaroo Island, which is outside the range of the toxic plants. succumbed to 50mg 1080 kg-1.

Both N-acetylcysteine and cysteamine proved to be ineffective antidotes to fluoroacetate intoxication. A1though N-acetylcysteine like glutathione, partially protected aconitate hydratase from fluorocitrate inhibition in rat liver preparations, they were unable to replace glutathione as a substrate for the and cysteamine. defluorination of fluoroacetate in vitro. Furthermore, N-acetylcysteine administration did not diminish the in vivo plasma citrate levels of glutathione-deficient rats and it is suggested that non-physiological sulfhydryl compounds are ineffective antidotes to fluoroacetate poisoning in vivo.

It is proposed that the development of tolerance to fluoroacetate by animal populations which co-exist with fluoroacetate-bearing vegetation is an adaptation to the presence of fluoroacetate in the diet. It is suggested that the extent to which the tolerance is developed in each species is dependent upon the degree to which the animals have found it necessary to consume food containing fluoroacetate and also upon the length of evolutionary exposure to the selection pressure. The fluoroacetate-tolerance determined is used in several cases as a genetic marker to trace the geographic origins and subsequent spread of fauna species in Australia.

The data are also discussed in relation to the use of sodium fluoroacetate (Compound 1080) as a target-specific pesticide to control exotic species in Australia in areas where native animals have acquired tolerance to fluoroacetate. Particular emphasis is given to the poisoning hazard posed to native animal populations from fluoroacetate-impregnated oat and meat baits used in 1080 poisoning programmes.

Item Type: Thesis (PhD)
Murdoch Affiliation: School of Environmental and Life Sciences
Notes: Note to the author: If you would like to make your thesis openly available on Murdoch University Library's Research Repository, please contact: repository@murdoch.edu.au. Thank you.
Supervisor(s): Mead, Robert
URI: http://researchrepository.murdoch.edu.au/id/eprint/51771
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