Review pubs.acs.org/JAFC
Monofluoroacetate-Containing Plants That Are Potentially Toxic to Livestock Stephen T. Lee,*,† Daniel Cook,† James A. Pfister,† Jeremy G. Allen,‡ Steven M. Colegate,† Franklin Riet-Correa,§ and Charlotte M. Taylor# †
Poisonous Plant Research Laboratory, Agricultural Research Service, U.S. Department of Agriculture, 1150 East 1400 North, Logan, Utah 84341, United States ‡ Department of Agriculture and Food, Western Australia, South Perth, Western Australia 6151, Australia § Hospital Veterinario, CSTR, Universidade Federal de Campina Grande, Patos 58700-310, Paraı ́ba, Brazil # Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166, United States ABSTRACT: Many plants worldwide contain monofluoroacetate and cause sudden death in livestock. These plants are primarily found in the southern continents of Africa, Australia, and South America, where they negatively affect livestock production. This review highlights past and current research investigating (1) the plants reported to contain monofluoroacetate and cause sudden death; (2) the mode of action, clinical signs, and pathology associated with poisoning by monofluoroacetatecontaining plants; (3) chemical methods for the analysis of monofluoroacetate in plants; (4) the coevolution of native flora and fauna in Western Australia with respect to monofluoroacetate-containing plants; and (5) methods to mitigate livestock losses caused by monofluoroacetate-containing plants KEYWORDS: monofluoroacetate, livestock, sudden death
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INTRODUCTION
acetate-containing plants; and (5) methods to mitigate livestock losses caused by monofluoroacetate-containing plants.
Numerous plants worldwide contain monofluoroacetate and cause sudden death in livestock. These plants are mainly found in the southern continents of Africa, Australia, and South America and belong to the Fabaceae, Rubiaceae, Bignoniaceae, Malpighiaceae, and Dichapetalaceae families (Figure 1). They have negatively affected livestock production in these regions throughout recorded history. For example, early settlers of Western Australia experienced heavy livestock losses due to animal consumption of Gastrolobium spp., which resulted in the colloquial term for the plants as “poison peas”.1 In Brazil, plants that cause sudden death (Palicourea, Arrabidaea, and Amorimia spp.) are responsible for half of all cattle deaths attributed to poisonous plants.2 In South Africa, Dichapetalum cymosum is the third most important poisonous plant and causes livestock death losses particularly during spring and episodes of drought.3 The acute toxicity of monofluoroacetate (sodium fluoroacetate (1080)) is well documented and has been employed extensively in several countries, including Australia,4 Israel,5 Japan,5 Mexico,5 New Zealand,6,7 and the United States,8 as a pesticide known as “1080” for the control of mammalian pests such as rodents, introduced foxes, feral dogs and cats, introduced possums, and native predators such as coyotes. This review discusses past and current research investigating (1) the plants reported to contain monofluoroacetate and cause sudden death; (2) the mode of action, clinical signs, and pathology associated with poisoning by monofluoroacetatecontaining plants; (3) chemical methods for the analysis of monofluoroacetate in plants; (4) the coevolution of native flora and fauna in Western Australia with respect to monofluoro© XXXX American Chemical Society
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PLANT TAXA THAT CONTAIN MONOFLUOROACETATE AND/OR CAUSE SUDDEN DEATH Fabaceae. Gastrolobium, Acacia, Oxylobium, and Nemcia species are historically known to produce monofluoroacetate.4,9 These plants have had a profound impact upon grazing patterns in the settlement of Australia and continue to affect modernday farming in Australia. A recent taxonomic revision of the 109 known species of Gastrolobium described 29 new species and formally placed Nemcia with the genus Gastrolobium.9 More recent molecular phylogenetic studies supported the inclusion of Nemcia with the Gastrolobium along with Oxylobium lineare and the other Oxylobium spp. present in Western Australia.10 All Oxylobium spp. that were known to produce monofluoroacetate have been moved into Gastrolobium spp.1 Thus, Oxylobium is now exclusively found in eastern Australia, whereas Gastrolobium spp. are found in southwestern Australia except for G. brevipes and G. grandiflorum, which occur in northern and/or central Australia along with A. georginae. An early report describes several species of Gastrolobium and Oxylobium that are capable of producing toxic levels of monofluoroacetate.11 This report described monofluoroacetate Special Issue: Poisonous Plant Symposium, Inner Mongolia Received: January 31, 2014 Revised: April 8, 2014 Accepted: April 11, 2014
A
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Figure 1. Photographs of representative plants containing monofluoroacetate: (A) Gastrolobium spinosum, image courtesy of John E. McLennan; (B) Palicourea marcgravii; (C) Amorimia septentrionalis; (D) Arrabidaea bilabiata; and (E) Dichapetalum cymosum, image provided courtesy of JMK (http://commons.wikimedia.org).
concentrations of up to 0.26% in G. bilobum, 0.040% in G. spinosum, 0.13% in G. floribundum, 0.13% in G. bennettsianum, and 0.25% in O. parviflorum. However, the report warned against extrapolating too much from these values because of the large variation in monofluoroacetate content that was observed within a species. Nonetheless, it was reported that monofluoroacetate concentrations were highest in the reproductive tissues, such as pods, flowers, and young leaves, and much lower in mature leaves and wood.11−14 Table 1 lists 31 species of Gastrolobium and one species of Acacia (A. georginae) that have been reported to contain monofluoroacetate.11,13−21 Not listed in Table 1 are five Gastrolobium species, G. appressum,11,16 G. densifolium,11,16,17 G. heterophyllum,11,16 G. ovalifolium,9,16 and G. trilobum,16 that have been reported to be toxic but have not been demonstrated to contain monofluoroacetate. The variability of monofluoroacetate content is documented throughout the Gastrolobium/Acacia literature. Some of this variation may be due to differences in analysis including the method, the place of analysis, and sampling procedures. However, it is clear that some variation is due to intrinsic
biology of the plants. This variation is illustrated by the monofluoroacetate concentration in individual plants within stands of G. brevipes (0.0017−0.0099% in leaves and 0.0056− 0.030% in pods, expressed as percent dry weight here and all subsequent occurences)14 and between populations of G. bilobum with 0.0010% in leaves and 0.0073% in flowers from one location compared to 0.017% in leaves and 0.11% in flowers from another location.13 There can be considerable intrastand variability between individual plants growing within meters of each other. For example, the monofluoroacetate concentrations in the leaves of different G. bilobium and G. calycinum plants within stands ranged from 0.023 to 0.39% and from 0.0029 to 0.058%, respectively.13 In addition, reports of the presence of high concentrations of monofluoroacetate in leaves of A. georginae, G. bilobum, G. calycinum, G. oxylobiodes, G. villosum, and G. spinosum were not confirmed by a 19F NMR analysis. 19F NMR failed to detect monofluoroacetate in leaves from each of these species except G. bilobum, for which a concentration 10 times less than reports was measured.18 B
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Table 1. Monofluoroacetate-Containing Genera of the Fabaceae (Acacia, Gastrolobium), Rubiaceae (Palicourea), Bignoniaceae (Arrabidaea), Malpighiaceae (Amorimia), and Dichapetalaceae (Dichapetalum, Tapura) genus
a
species
references
Acacia
georginae
15, 16
Gastrolobium
bennettsianum bilobum brevipes brownii callistachys calycinum crassifolium crispatum cuneatum f loribundum glaucum grandif lorum graniticum hamulosum laytonii microcarpum oxylobioides parvif lorum polystachyum pycnostachyum racemosum rigidum rotundifolium spathulatum spectrabile spinosum stenophyllum tetragonophyllum tomentosum vellutinum villosum
11, 11, 14 21 16 11, 11, 21 11, 11, 11, 21 11, 11, 11, 11, 11, 11, 11, 11, 11, 11, 11, 13, 11, 11, 11, 11, 16 11, 11,
genus
species
references
Palicourea
aeneofusca amapaensis grandiflora aff. juruana longiflora aff. longiflora macarthurorum marcgravii nigricans vacillans
27, 28 27 27 27 27 27 27 25−27 27 27
Tanaecium
bilabiatuma
35
Amorimia
amazonica camporum exotropica pubiflora rigida septentrionalis
28 28 28 28 28 28
Dichapetalum
barteri braunii cymosum edule heudelotii michelsonii toxicarium
43 44 45 44 46 44, 47 48
Tapura
f ischeri
3
15 13, 16−20
13, 16, 18−20 16 16, 21 16, 17 16, 17 16, 17 16, 17 16 16−18 16−18 16−20 16−18 16, 17 16−19 16, 17 16, 17 19, 22 17 13, 17, 19 16−19 16−19 16, 17 13, 16−20
Tanaecium bilabiatum was previously known as Arrabidaea bilabiata.
specimens were tested for monofluoroacetate (Table 1).25−28 Monofluoroacetate was confirmed in P. marcgravii and P. aeneof usca and was detected in P. grandif lora and P. aff. juruana, which is consistent with these species causing sudden death.29−31 P. aff. juruana likely corresponds to P. juruana as described by Tokarnia,24 but the identity of P. juruana is problematic as this name has been used variously for several different species. Additionally, monofluoroacetate was detected in several other species including P. amapaensis, P. macarthurorum, and P. nigricans27 (taxonomically similar to P. grandif lora32), and P. longiflora, P. aff. longif lora, and P. vacillans27 (taxonomically similar to P. marcgravii and P. aeneof usca32). There are limited data on monofluoroacetate concentrations from Palicourea field collections. Studies suggest that monofluoroacetate concentrations in mature leaves are highly variable within populations of P. marcgravii and P. aeneof usca, ranging from 0.03 to 0.58% and from 0.03 to 0.18%, respectively.28 Mean concentrations of monofluoroacetate within field collections of mature leaves of P. marcgravii and P. aeneof usca were approximately 0.20 and 0.10%, respectively.28 Young leaves from one population of P. marcgravii contained monofluoroacetate at concentrations of 0.88 ± 0.08%, in contrast to that in mature leaves at 0.21 ± 0.17%.28
A recent re-examination of some Gastrolobium spp. from Western Australia using a HPLC-APCI-MS method of analysis again documented variability reported in the literature with respect to their monofluoroacetate content (Table 1).20 The presence of monofluoroacetate was confirmed in G. bilobum, G. calycinum, G. parvif lorum, and G. villosum. However, none was detected in G. spinosum, G. laytonii, or a sample of G. calycinum that was collected from the Murdoch University Toxic Plant Garden (Perth, Australia), removed from its native environment over two decades ago.20 Rubiaceae. Palicourea is a genus composed of approximately 200 species, which range in growth habit from small shrubs to trees. The genus is distributed throughout the tropics of the New World.22,23 Palicourea marcgravii was the first poisonous plant studied in Brazil and is the single most important toxic plant in Brazil due to its acute toxicity, palatability, and broad geographical distribution.2,24 Three other Palicourea species, P. aeneofusca, P. grandiflora, and P. juruana, are also reported to cause sudden death. These plants have less impact due to their restricted distribution. P. marcgravii is documented to contain monofluoroacetate,25−27 and a recent report demonstrated that P. aeneofusca contains monofluoroacetate.27,28 A systematic screening of Palicourea taxa was recently initiated wherein herbarium C
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Figure 2. (A) Partial tricarboxylic acid cycle illustrating the incorporation of acetyl-CoA into the cycle. (B) Partial tricarboxylic acid cycle illustrating the incorporation of fluoroacetyl-CoA into the cycle resulting in the formation of fluorocitrate and subsequent inhibition of aconitase.
Bignoniaceae. Several lianas in the family Bignoniaceae, previously classified as Arrabidaea and Pseudocalymma, are reported to cause sudden death. A recent taxonomic study using molecular and morphological characters has changed the generic circumscriptions in this group.33 Currently, most Arrabidaea and Pseudocalymma are now included in Fridericia and Mansoa, respectively. However, some species such as Arrabidaea bilabiata and Pseudocalymma elgans were incorrectly
classified as to genus and are known as Tanaecium bilabiatum and Fridericia elegans, respectively. Fridericia comprises approximately 70 species that typically grow as high-climbing woody vines or occasionally as small shrubs and trees and is distributed throughout the Neotropics from Mexico and the West Indies to Argentina. Tanaecium comprises about 20 species of similar habit found across the same range.33 Three species of Bignoniaceae have been reported to cause sudden D
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plant material required to cause sudden death with Palicourea and Mascagnia species.40−42 Dichapetalaceae. Dichapetalum spp. occur as trees or shrubs throughout the lowland tropical regions of the world, with more than 80 species reported from Africa.3 Dichapetalum cymosum (Gifblaar) causes sudden death or “Gifblaar poisoning” and is the third most important toxic plant in South Africa.3 Seven Dichapetalum spp., D. barteri,43 D. braunii,44 D. cymosum,45 D. edule,44 D. heudelotii,46 D. michelsonii44,47 (possibly the same as D. stuhlmanii), and D. toxicarium,48 have been documented to contain monofluoroacetate (Table 1), and three of these, D. cymosum, D. barteri, and D. toxicarium, are reported to be lethally toxic to livestock.3 D. ruhlandii has also been reported to be lethally toxic, but, apparently, has not been shown to contain monofluoroacetate.3 Similar to the other species thus far described herein, monofluoroacetate concentrations have been shown to vary between species and plant parts in that young leaves contain greater amounts of monofluoroacetate than do mature leaves. For example, O’Hagan et al.44 analyzed leaves of three Dichapetalum spp. and found concentrations of monofluoroacetate to be 0.72 ± 0.02% in the young leaves of D. braunii, 0.012 ± 0.002 and 0.007 ± 0.002% in the young leaves of D. edule, and 0.004 ± 0.002% in the young leaves of D. stuhlmanni; however, the concentrations in the mature leaves from these three plants were all
