Journal of Chemical Ecology

, Volume 23, Issue 4, pp 1131–1144 | Cite as

Effect of Centaurea maculosa on Sheep Rumen Microbial Activity and Mass in Vitro

  • Bret E. Olson
  • Rick G. Kelsey
Article

Abstract

Spotted knapweed, Centaurea maculosa, a herbaceous weed from Eurasia, is altering the composition of native rangeland communities across western North America. Herbivore use of this plant is limited, possibly because glandular trichomes covering the epidermal surfaces of aerial tissues produce cnicin, a biologically active sesquiterpene lactone. We determined the concentrations of cnicin in plant parts from different growth stages (initial, mature, regrowth) of C. maculosa and the effects of these plant parts on sheep rumen microbial activity and mass (in vitro), when mixed in different proportions with grass hay. Leaves had higher crude protein and lower neutral and acid detergent fiber than stems or grass hay. Cnicin concentrations were highest in leaves, intermediate in flower buds, and lowest in stems. Cnicin concentrations in leaves increased from June to July, but decreased in stems. Regrowth had slightly lower cnicin concentrations that mature growth. High percentages (70% and 100%) of mature and regrowth leaves and flowers of C. maculosa in the mixtures depressed the rate and amount of microbial activity, whereas high percentages of stems from initial growth enhanced the rates of microbial activity. Microbial activity was more responsive to the different mixtures, plant parts, and growth stages than microbial mass, possibly because microbial populations cannot adjust rapidly to changes in diet. After cnicin was extracted from leaves, microbial activity was greater from these leaves than from grass hay. In contrast, after cnicin was extracted from flower buds, microbial activity from these flower buds was still depressed, indicating other compounds or the remaining cnicin were still affecting microbial activity. In summary, sheep rumen microbial activity was reduced significantly by mature and regrowth leaves that contained high concentrations of cnicin. Since most herbivores selectively graze leaves, the bitter-tasting cnicin could deter large ruminant feeding of C. maculosa by altering their behavior and/or by affecting rumen function.

Cnicin spotted knapweed sesquiterpene lactone ruminant rumen herbivory secondary compounds weeds sheep Centaurea maculosa 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. ARNOLD, G. W., and DUDZINSKI, M. L. 1978. Ethology of Free Ranging Domestic Animals. Elsevier, New York.Google Scholar
  2. AOAC. 1980. Official Methods of Analysis, 10th ed. Association of Official Agricultural Chemists, Washington, D.C.Google Scholar
  3. BOHLMANN, F., RODE, K. M., and ZDERO, C. 1966. Neue polyine der Gattung Centaurea L. Chem. Ber. 99:3544–3551.Google Scholar
  4. BRYANT, J. P., CHAPIN, F. S., III, and KLEIN, D. R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368.Google Scholar
  5. CAVALLITO, C. J., and BAILEY, J. H. 1949. An antibacterial principle from Centaurea maculosa. J. Bacteriol. 57:207–212.Google Scholar
  6. COX, J. W. 1989. Observations, experiments and suggestions for research on the sheep-spotted knapweed relationship, pp. 79–82, in P. K. Fay and J. R. Lacey (eds.). Proceedings, 1989 Knapweed Symposium, Montana State University EB45, Bozeman, Montana.Google Scholar
  7. FAHN, A. 1979. Secretory Tissues in Plants. Academic Press, London.Google Scholar
  8. GERSHENZON, J. 1984. Changes in the levels of plant secondary metabolites under water and nutrient stress. Recent Adv. Phytochem. 18:273–320.Google Scholar
  9. GERSHENZON, J. 1994. Metabolic costs of terpenoid accumulation in higher plants. J. Chem. Ecol. 20:1281–1328.Google Scholar
  10. GERSHENZON, J., and CROTEAU, R. 1991. Terpenoids, pp. 165–219, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores, Their Interactions with Secondary Metabolites, Vol. 1, The Chemical Participants. Academic Press, New York.Google Scholar
  11. GOERING, H. K., and VAN SOEST, P. J. 1970. Forage fibre analysis (apparatus, reagents, procedures, and some applications). ARS, USDA Agriculture Handbook 379.Google Scholar
  12. GONZALEZ, A. G., DARIAS, V., ALONSO, G., BOADA, J. N., and FERIA, M. 1978. Cytostatic activity of sesquiterpene lactones from Compositae of the Canary Islands. Planta Med. 33:356–359.Google Scholar
  13. HARBORNE, J. B. 1991. The chemical basis of plant defense, pp. 46–59, in R. T. Palo and C. T. Robbins (eds.) Plant Defenses against Mammalian Herbivory. CRC Press, London.Google Scholar
  14. HUNECK, S., JAKUPOVIC, J., and SCHUSTER, A. 1986. Weitere inhaltsstoffe aus Centaurea stoebe (Further compounds from Centaurea stoebe). Planta Med. 5:343–532.Google Scholar
  15. KELSEY, R. G., and LOCKEN, L. J. 1987. Phytotoxic properties of cnicin, a sesquiterpene lactone from Centaurea maculosa (spotted knapweed). J. Chem. Ecol. 13:19–33.Google Scholar
  16. KELSEY, R. G., and MILHALOVICH, R. D. 1987. Nutrient composition of spotted knapweed (Centaurea maculosa). J. Range Manage. 40:277–281.Google Scholar
  17. KRONBERG, S. L., and WALKER, J. W. 1993. Ruminal 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.Google Scholar
  18. LANDAU, I., MULLER-SCHARER, H., and WARD, P. I. 1994. Influence of cnicin, a sesquiterpene lactone of Centaurea maculosa (Asteraceae), on specialist and generalist insect herbivores. J. Chem. Ecol. 20:924–942.Google Scholar
  19. LANGENHEIM, J. H. 1994. Higher plant terpenoids: A phytocentric overview of their ecological roles. J. Chem. Ecol. 20:1223–1280.Google Scholar
  20. LOCKEN, L. J., and KELSEY, R. G. 1987. Cnicin concentrations in Centaurea maculosa, spotted knapweed. Biochem. Syst. Ecol. 15:313–320.Google Scholar
  21. MARCO, J. A., SANZ, J. F., SANCENON, SUSANNA, A., FUSTAIYAN, A., and SABERI, M. 1992. Sesquiterpene lactones and lignans from Centaurea species. Phytochemistry 31:3527–3530.Google Scholar
  22. MAZLIAK, P. 1968. Chemistry of plant cuticles. Prog. Phytochem. 1:49–111.Google Scholar
  23. MIHALIAK, C. A., and LINCOLN, D. E. 1989. Plant biomass partitioning and chemical defense: Response to defoliation and nitrate limitation. Oecologia 80:122–126.Google Scholar
  24. MILLER, V. 1990. Knapweed as forage for big game in the Kootenays. Knapweed 4:3.Google Scholar
  25. OLSON, B. E., WALLANDER, R. W., and LACEY, J. R. 1997. Effects of sheep grazing on a spotted knapweed-infested Idaho fescue community. J. Range Manage. In press.Google Scholar
  26. PROVENZA, F. D. 1995. Postingestive feedback as an elementary determinant of food selection and intake in ruminants. J. Range Manage. 48:2–17.Google Scholar
  27. PROVENZA, F. D. 1996. Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. J. Anim. Sci. 74:2010–2020.Google Scholar
  28. PROVENZA, F. D., and MALECHEK, J. C. 1984. Diet selection by domestic goats in relation to blackbrush twig chemistry. J. Appl. Ecol. 21:831–841.Google Scholar
  29. PROVENZA, F. D., LYNCH, J. J., BURRITT, E. A., and SCOTT, C. B. 1994. How goats learn to distinguish between novel foods that differ in postingestive consequences. J. Chem. Ecol. 20:609–624.Google Scholar
  30. ROBERTSON, K. 1989. Living with spotted knapweed in the Bitterroot Valley, pp. 33–36, in P. K. Fay and J. R. Lacey (eds.). Proceedings, 1989 Knapweed Symposium, Montana State University EB45, Bozeman, Montana.Google Scholar
  31. SAS. 1988. SAS/STAT User's Guide: Volume 2, Version 6, 4th ed. SAS Institute, Cary, North Carolina.Google Scholar
  32. STRIBY, K. D., WAMBOLT, C. L., KELSEY, R. G., and HAVSTAD, K. M. 1987. Crude terpenoid influence on in vitro digestibility of sagebrush. J. Range Manage. 40:244–248.Google Scholar
  33. SUCHÝ, M., and HEROUT, V. 1962. Identity of the bitter principle from Centaurea stoebe (L.) Sch. et Thell. with cnicin. Coll. Czech. Chem. Commun. 27:1510–1512.Google Scholar
  34. THOMAS, V. M., CLARK, C. K., KOTT, R. W., and OLSON, B. E. 1994. Influence of leafy spurge on ruminal digestion and metabolism and blood metabolite profiles in sheep. Sheep Goat Res. J. 10:168–172.Google Scholar
  35. THOMPSON, M. J. 1996. Winter foraging response of elk to spotted knapweed removal. Northwest Sci. 70:10–19.Google Scholar
  36. TUOMI, J. P., NIEMELA, P., HAUKIOJA, E., and NEUVONEN, S. 1984. Nutrient stress: An explanation for plant anti-herbivore responses to defoliation. Oecologia 61:208–210.Google Scholar
  37. VANHAELEN-FASTRE, R. 1972. Activities antibiotique et cytotoxique de la cnicine, isolee de Cnicus benedictus L. J. Pharm. Belg. 27:683–688.Google Scholar
  38. VANHAELEN-FASTRÉ, R., and VANHAELEN, M. 1976. Active antibiotique et cytotoxique de la cnicine et de ses produits d'hydrolyse. Planta Med. 29:179–189.Google Scholar
  39. WATSON, A. K., and RENNEY, A. J. 1974. The biology of Canadian weeds. 6. Centaurea diffusa and C. maculosa. Can. J. Plant Sci. 54:687–701.Google Scholar
  40. YOKOYAMA, M. T., and JOHNSON, K. A. 1988. Microbiology of the rumen and intestine, pp. 125–144, in D. C. Church (ed.). The Ruminant Animal: Digestive Physiology and Nutrition. Prentice-Hall, Englewood Cliffs, New Jersey.Google Scholar
  41. ZINN, R. A., and OWENS, F. N. 1986. A rapid procedure for purine measurements and its use for estimating net ruminal protein synthesis. Can. J. Anim. Sci. 66:157.Google Scholar

Copyright information

© Plenum Publishing Corporation 1997

Authors and Affiliations

  • Bret E. Olson
    • 1
  • Rick G. Kelsey
    • 2
  1. 1.Department of Animal and Range SciencesMontana State UniversityBozeman
  2. 2.Forestry Sciences LaboratoryCorvallis

Personalised recommendations