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Effects of Condensed Tannins on the Toxicity of Fireweed (Senecio Madagascariensis) to Cattle

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Effects of Condensed Tannins on the Toxicity of Fireweed (Senecio Madagascariensis) to Cattle Utah State University DigitalCommons@USU All Graduate Theses and Dissertations Graduate Studies 5-2014 Effects of Condensed Tannins on the Toxicity of Fireweed (Senecio madagascariensis) to Cattle Carolyn L. Wong Utah State University Follow this and additional works at: https://digitalcommons.usu.edu/etd Part of the Animal Sciences Commons Recommended Citation Wong, Carolyn L., "Effects of Condensed Tannins on the Toxicity of Fireweed (Senecio madagascariensis) to Cattle" (2014). All Graduate Theses and Dissertations. 3859. https://digitalcommons.usu.edu/etd/3859 This Thesis is brought to you for free and open access by the Graduate Studies at DigitalCommons@USU. It has been accepted for inclusion in All Graduate Theses and Dissertations by an authorized administrator of DigitalCommons@USU. For more information, please contact [email protected]. EFFECTS OF CONDENSED TANNINS ON THE TOXICITY OF FIREWEED (SENECIO MADAGASCARIENSIS) TO CATTLE by Carolyn L. Wong A thesis submitted in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE in Range Science Approved: --------------------------------------------- --------------------------------------------- Frederick D. Provenza, PhD. Dale Gardner, PhD Major Professor Committee Member --------------------------------------------- -------------------------------------------- Jim Pfister, PhD Mark Thorne, PhD Committee Member Committee Member --------------------------------------------- Mark R. McLellan, PhD Vice President for Research and Dean of the School of Graduate Studies UTAH STATE UNIVERSITY Logan, Utah 2014 ii Copyright © Carolyn Wong 2014 All Rights Reserved iii ABSTRACT Effects of Condensed Tannins on the Toxicity of Fireweed (Senecio madagascariensis) to Cattle by Carolyn L. Wong, Master of Science Utah State University, 2014 Major Professor: Dr. Frederick D. Provenza Department: Wildland Resources Senecio madagascariensis, also known as fireweed, is a noxious weed that has invaded pastures in Hawaii, Australia, and South America. Fireweed contains pyrrolizidine alkaloids (PAs) that, when metabolized into highly reactive pyrroles, are toxic to most grazing mammals. Toxic effects to cattle include irreversible damage to liver cells, liver fibrosis, and loss of liver function, which may lead to jaundice, edema, ascites, and other physiological malfunctions. External effects include rough appearance, diarrhea, prolapsed rectum, lassitude and dullness, photosensitization, and abnormal behavior, many of which can lead to death. Fireweed also can reduce pasture productivity by as much as 30-40%, particularly in Hawaii. As a result of these adverse effects on cattle and pasture production, people are seeking ways to manage fireweed and cattle. Condensed tannins, which are common in many forage legumes, have a high affinity for binding with other molecules such as protein and alkaloids. Complementarities among secondary compounds such as condensed tannins and alkaloids can increase intake of forages high in intake-limiting compounds such as alkaloids; however, information is lacking on the protective effects these iv complementarities have against toxicity. The effects of condensed tannins on the toxicity of fireweed to cattle were examined in studies in vitro and in vivo. The in vitro studies showed that tannins bound pyrrolizidine alkaloids in cattle rumen fluid and binding was highest when mixed with tannins at 8%, with some effect at 12% as well, by weight of fireweed. The in vivo research sought to determine if tannins reduced toxicity in cattle as measured by various behavioral observations and physiological responses. The results were inconclusive as animals from both the Fireweed and Fireweed-Tannin groups demonstrated ill effects. The quantitative data gathered in the form of serum analyses and liver biopsies did not identify a clear protective effect of tannin in the diet, but the results likely were confounded by the unanticipated effects brought on by the method of treatment administration, which involved dosing animals daily with large amounts of plant material. The findings also illustrate how strongly cattle avoid eating fireweed while grazing on pasture. In summary, management to reduce fireweed effects on cattle should focus on improving pasture diversity and resiliency, on multi-species grazing to take advantage of the innate resistance of sheep and goats to fireweed’s toxicity, and on ways to enable cattle to utilize fireweed. (59 pages) v PUBLIC ABSTRACT Effects of Condensed Tannins on the Toxicity of Fireweed (Senecio madagascariensis) to Cattle by Carolyn L. Wong, Master of Science Utah State University, 2014 Major Professor: Dr. Frederick D. Provenza Department: Wildland Resources Fireweed (Senecio madagascariensis) is a noxious and invasive weed affecting pastures in Hawaii, Australia, and South America. Fireweed contains compounds called pyrrolizidine alkaloids that are toxic to most grazing mammals. Toxic effects to cattle include irreversible damage to liver cells, hardening of the liver, and loss of liver function, which may lead to jaundice, swelling, and the accumulation of fluids in the stomach and other physiological malfunctions. External effects include rough appearance, diarrhea, low energy and dullness, photosensitization, and abnormal behavior, many of which can lead to death. Fireweed also can reduce pasture productivity by as much as 30-40%, particularly in Hawaii. As a result of these adverse effects on cattle and pasture production, people are seeking ways to manage fireweed and cattle. Condensed tannins, which are common in many forage legumes, bind with other molecules such as protein and alkaloids. Complementarities among secondary compounds such as condensed tannins and alkaloids can allow animals to consume more of plant material they would otherwise avoid due to toxicity; however, there is very little information on whether tannins actually protect animals from the toxic effect of vi alkaloids like the ones found in fireweed. The effects of condensed tannins on the toxicity of fireweed to cattle were examined in two stages of a research project that included studies in the lab (in vitro) and in live animals (in vivo). The in vitro studies showed that tannins bound pyrrolizidine alkaloids in cattle rumen fluid and binding was highest when mixed with tannins at 8%, with some effect at 12% as well, by weight of fireweed. The in vivo studies were inconclusive as animals from both the Fireweed and Fireweed-Tannin group demonstrated ill-effects brought on by the fireweed. The data gathered in the form of blood tests and liver tests did not identify a clear protective effect provided by having tannin in the diet, but the results likely were affected by the way we conducted the research, which involved dosing animals daily with large amounts of plant material. The findings also illustrate how strongly cattle avoid eating fireweed while grazing on pasture. In summary, management to reduce fireweed effects on cattle should focus on improving pasture diversity and resiliency, on multi-species grazing to take advantage of the innate resistance of sheep and goats to fireweed’s toxicity, and on ways to enable cattle to utilize fireweed. vii ACKNOWLEDGMENTS I would never have endeavored, nor could I have completed this thesis were it not for the encouragement and inspiration (and tireless review and editing!) of my major professor, Dr. Fred Provenza. Thank you for your passion for understanding animal behavior and the intricate and complex interactions that occur from the soil, through the plants, into the animals and ultimately affect the health of our ecosystems and communities. You’ve helped me to look at landscapes and the organisms that inhabit them in a completely different way. Mahalo Fred. I’d also like to thank Dr. Mark Thorne for finding the financial resources to support this research and for overcoming so many obstacles in order to literally “make it happen.” Mahalo nui Mark. Mahalo to Greg Friel and Haleakala Ranch for allowing us to conduct the in vivo research at their facility, for providing the steers, and for their help with logistical support. Major appreciation goes out to Dr. Dale Gardner, Dr. Jim Pfister and Dr. Bryan Stegelmeier for their expertise, support, patience and assistance in the many phases of my research. Dale, thanks for putting up with me and my "thumbs' in your lab” and for giving me a newfound understanding and appreciation for plant analysis. Jim, thanks for helping us set up and conduct bite counts on those cows that never did eat fireweed, for all the work you and Bryan and all your crews did in conducting the fireweed toxicity studies at the PPRL, and for all of your help with the data analyses and editing of my thesis. Bryan, thank you for your entertaining wit and sarcasm while we did our feeding trials here in Hawaii, for training us in oral drenching and liver biopsies, and for you and your guys work in the lab analyzing the samples. Thank you all so much. viii To my girl, Mele Abran. Thank you for being there when I couldn’t and for your organization and patience with me as I fumbled through my notes for information you always had right there. Your skills in animal medicine and necropsy were invaluable, not to mention all that fireweed you helped collect, dry, grind, and ship! I would’ve been so lost without you. Mahalo Mele. To Alex Beaton. Thank you for collecting so much fireweed for me!!! And drying, grinding, bagging, and shipping!!! To Juan Villalba, for coming to
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