Abstract
Cattle generally avoid grazing leafy spurge (LS; Euphorbia esula), whereas sheep and goats will often eat it. Understanding metabolism of toxic phytochemicals in LS by bovine rumen microflora may help explain why cattle often develop aversions to LS after initially eating it. Toxicity of LS compounds after in vitro fermentation with normal vs. antibiotic-modified bovine rumen digesta was evaluated at different lengths of fermentation. Levels of toxic and aversion-inducing ingenols were determined for fermented and nonfermented mixtures of LS and bovine rumen digesta, and the toxicity of an aversion-inducing extract of LS to rumen microbial species that are common in cattle, sheep, and goats was evaluated. Fermentation of LS with bovine digesta increased the toxicity of extracted compounds. Introduction of neomycin (an antibiotic that preferentially inhibits gram-negative bacteria) into the LS and bovine rumen digesta mixtures did not appear to affect toxicities regardless of fermentation length. Levels of ingenol were observed in LS and bovine digesta mixtures (both fermented and nonfermented) that were consistent with levels of ingenols reported for LS. Finally, a toxic extract of LS had little or no negative effect on the growth of several common species of rumen bacteria. The results indicate that LS is not generally toxic to the ruminal bacteria, but that microbial activity in the rumen may be responsible for enhancing LS toxicity to cattle.
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References
J. E. Anderson C. M. Goetz J. L. McLaughlin (1991) ArticleTitleA blind comparison of simple bench-top bioassays and human tumour cell cytotoxicities as antitumor prescreens Phytochem. Anal. 2 107–111 Occurrence Handle1:CAS:528:DyaK3MXlvFOmu7s%3D
M. K. Campbell (1999) Biochemistry Saunders College Publishing Philadelphia
J. R. Carlson R. G. Breeze (1984) ArticleTitleRuminal metabolism of plant toxins with emphasis on indolic compounds J. Anim. Sci. 58 1040–1049 Occurrence Handle1:CAS:528:DyaL2cXitVyhs7k%3D Occurrence Handle6373706
A. M. Craig C. J. Latham L. L. Blythe W. B. Schmotzer O. O'Connor (1992) ArticleTitleMetabolism of toxic pyrolizidine alkaloids from tansy ragwort in bovine ruminal fluid under anaerobic conditions Appl. Environ. Microbiol. 58 2730–2736 Occurrence Handle1:CAS:528:DyaK38XlvVyjt74%3D Occurrence Handle1444382
A. J. Duncan J. A. Milne (1992) ArticleTitleRumen microbial degradation of allyl cyanide as a possible explanation for the tolerance of sheep to brass ica-derived glucosinolates J. Sci. Food Agric. 58 15–19 Occurrence Handle1:CAS:528:DyaK38Xhslalsrw%3D
F. T. Halaweish S. L. Kronberg M. B. Hubert J. A. Rice (2002) ArticleTitleToxic and aversive diterpenes of Euphorbia esula J. Chem. Ecol. 28 1599–1611 Occurrence Handle10.1023/A:1019976413040 Occurrence Handle1:CAS:528:DC%2BD38Xms1els7o%3D Occurrence Handle12371812
C. M. Hasler A. Geza P. M. Blumberg (1992) ArticleTitleSpecific binding to protein kinase C by ingenol and its induction of biological responses Cancer Res. 52 202–208 Occurrence Handle1:CAS:528:DyaK38XnvVaqsA%3D%3D Occurrence Handle1727380
D. G. Hein S. D. Miller (1992) ArticleTitleInfluence of leafy spurge on forage utilization by cattle J. Range Manag. 45 405–407
L. F. James M. J. Allison E. T. Littledike (1975) Production and modification of toxic substances in the rumen I. W. McDonald A. C. I. Warner (Eds) Digestion and Metabolism in the Ruminant University of New England Publishing Unit Armidale, New South Wales, Australia 576–590
D. R. Kirby T. P. Hanson C. Hull-Sieg (1997) ArticleTitleDiets of Angora goats grazing leafy spurge Euphorbia esula-infested rangeland Weed Technol. 11 734–738
Kronberg S. L. 1999. Rumen microbial metabolism affects diet selection of ruminants, pp. 460–461, in D. Eldridge and D. Freudenberger (eds.). Proceedings of the 6th International Rangeland Congress. Townsville, Australia.
S. L. Kronberg J. W. Walker (1993) ArticleTitleRuminal metabolism of leafy spurge in sheep and goats: a potential explanation for differential foraging on spurge by sheep, goats, and cattle J. Chem. Ecol. 19 2007–2017 Occurrence Handle10.1007/BF00983803
S. L. Kronberg R. B. Muntifering E. L. Ayers C. B. Marlow (1993a) ArticleTitleCattle avoidance of leafy spurge: a case of conditioned aversion J. Range Manag. 46 364–366
S. L. Kronberg R. B. Muntifering E. L. Ayers (1993a) ArticleTitleFeed aversion learning in cattle with delayed negative consequences J. Anim. Sci. 71 1767–1770 Occurrence Handle1:STN:280:ByyA2M3jsVI%3D
B. K. Landgraf P. K. Fay K. M. Havstad (1984) ArticleTitleUtilization of leafy spurge (Euphorbia esula) by sheep Weed Sci. 32 348–352
R. G. Lym D. R. Kirby (1987) ArticleTitleCattle foraging behavior in leafy spurge infested rangeland Weed Tech. 1 314–318
J. L. McLaughlin C. Chang D. Smith (1991) ArticleTitle“Bench-Top” bioassays for the discovery of bioactive natural products: an update Stud. Nat. Prod. Chem. 9 383–405 Occurrence Handle1:CAS:528:DyaK38Xkt1amur0%3D
B. N Meyer N. R. Ferrigni J. E. Putnam L. B. Jacobsen D. E. Nichols J. L. McLaughlin (1982) ArticleTitleBrine shrimp: a convenient general bioassay for active plant constituents J. Med. Plant Res. 45 31–34 Occurrence Handle1:CAS:528:DyaL38Xks1Onsr0%3D
M. A. Pass W. Majak A. D. Muir G. S. Yost (1984) ArticleTitleConversion of 3-nitropropanol to 3-nitropropionic acid in cattle and sheep Toxicol. Lett. 23 1–7 Occurrence Handle10.1016/0378-4274(84)90002-X Occurrence Handle1:CAS:528:DyaL2cXmtVGktrc%3D Occurrence Handle6485010
J. B. Russell H. L. Strobel (1988) ArticleTitleEffects of additives on in vitro ruminal fermentations: a comparison of monensin and bacitracin, another gram-positive antibiotic J. Anim. Sci. 66 552–558 Occurrence Handle1:CAS:528:DyaL1cXhsV2gtr0%3D Occurrence Handle3372392
InstitutionalAuthorNameSAS (1988) STAT User's Guide Statistical Analysis System Institute Cary, NC
E. H. Seip E. Hecker (1982) ArticleTitleSkin irritant ingenol esters from Euphornia esula J. Med. Plant Res. 46 215–218 Occurrence Handle1:CAS:528:DyaL3sXos1alsQ%3D%3D
G. S. Smith (1992) ArticleTitleToxification and detoxification of plant compounds by ruminants: an overview J. Range Manag. 45 25–30
V. M. Thomas C. K. Clark R. W. Knott B. Olson (1994) ArticleTitleInfluence of leafy spurge on ruminal digestion and metabolism and blood metabolite profiles in sheep Sheep Goat Res. J. 10 168–172 Occurrence Handle1:CAS:528:DyaK2MXivVajtrs%3D
J. M. A. Tilley R. A. Terry (1963) ArticleTitleA two stage technique for the in vitro digestion of forage crops J. Br. Grassl. Soc. 18 104–111 Occurrence Handle1:CAS:528:DyaF3sXks1Cmurk%3D
R. R. Upadhyay K. Khalesi G. Kharazi M. Ghaisarzadeh (1977) ArticleTitleIsolation of ingenol from the plants of Euphorbiaceae Indian J. Chem. 15 294
G. Vogg E. Mattes J. Rothenburger N. Hertkorn S. Achatz H. Sanderman SuffixJr (1999) ArticleTitleTumor promoting diterpenes from Euphorbia leuconeura Phytochemistry 51 289–295 Occurrence Handle10.1016/S0031-9422(99)00016-3 Occurrence Handle1:CAS:528:DyaK1MXjslCrsL4%3D Occurrence Handle10365450
D. E. Wachenheim L. L. Blythe A. M. Craig (1992) ArticleTitleEffects of antibacterial agents on in vitro ovine ruminal biotransformation of the hepatotoxic pyrrolizidine alkaloid jacobine Appl. Environ. Microbiol. 58 2559–2564 Occurrence Handle1:CAS:528:DyaK38Xlt1yjurs%3D Occurrence Handle1514802
J. W. Walker S. L. Kronberg S. L. Al-Rowaily N. E. West (1994) ArticleTitleComparison of sheep and goat preferences for leafy spurge J. Range Manag. 47 434–439
P. J. Weimer S. M. Abrams (2001) ArticleTitleIn vitro fermentation of polydextrose by bovine ruminal microorganisms Anim. Feed Sci. Technol. 93 115–123 Occurrence Handle10.1016/S0377-8401(01)00256-5 Occurrence Handle1:CAS:528:DC%2BD3MXms12gtr4%3D
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We thank Kristine Nichols, Douglas Ranynie, Igor Sergeev, and anonymous reviewers for their helpful comments on the manuscript and Kjersten Grong for help with the brine shrimp toxicity assays.
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Kronberg, S.L., Halaweish, F.T., Hubert, M.B. et al. Interactions Between Euphorbia esula Toxins and Bovine Ruminal Microbes. J Chem Ecol 32, 15–28 (2006). https://doi.org/10.1007/s10886-006-9348-9
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DOI: https://doi.org/10.1007/s10886-006-9348-9