, Volume 97, Issue 3, pp 273–278 | Cite as

Microbial degradation of usnic acid in the reindeer rumen

  • Monica A. SundsetEmail author
  • Perry S. Barboza
  • Thomas K. Green
  • Lars P. Folkow
  • Arnoldus Schytte Blix
  • Svein D. Mathiesen


Reindeer (Rangifer tarandus) eat and utilize lichens as an important source of energy and nutrients in winter. Lichens synthesize and accumulate a wide variety of phenolic secondary compounds, such as usnic acid, as a defense against herbivores and to protect against damage by UV-light in solar radiation. We have examined where and to what extent these phenolic compounds are degraded in the digestive tract of the reindeer, with particular focus on usnic acid. Three male reindeer were given ad libitum access to a control diet containing no usnic acid for three weeks and then fed lichens ad libitum (primarily Cladonia stellaris) containing 9.1 mg/g DM usnic acid for 4 weeks. Usnic acid intake in reindeer on the lichen diet was 91–117 mg/kg BM/day. In spite of this, no trace of usnic acid or conjugates of usnic acid was found either in fresh rumen fluid, urine, or feces. This suggests that usnic acid is rapidly degraded by rumen microbes, and that it consequently is not absorbed by the animal. This apparent ability to detoxify lichen phenolic compounds may gain increased importance with future enhanced UV-B radiation expected to cause increased protective usnic acid/phenol production in lichens.


Reindeer Lichens Usnic acid Phenolics Rumen 



We are grateful to Hans Edvin Lian and Magnus Folkow for all their help with the animals and to Jennifer Addison for her help with the chromatographic analyses. This project was funded by The Reindeer Husbandry Research Fund (Project A5299). It is linked to the framework of the International Polar Year as part of the IPY consortium IPY no. 399 EALAT: Climate change and reindeer husbandry.


  1. Aagnes TH, Mathiesen SD (1994) Food and snow intake, body mass and rumen function in reindeer fed lichen and subsequently starved for 4 days. Rangifer 14:33–37Google Scholar
  2. Abo-Khatwa AN, Al-Robai AA, Al-Jawhari DA (1996) Lichens acids as uncouplers of oxidative phosphorylation of mouse-liver mitochondria. Nat Toxins 4:96–102PubMedCrossRefGoogle Scholar
  3. ACIA (2005) Arctic climate impact assessment. Cambridge University Press, New York, 1042 pGoogle Scholar
  4. Barboza PS, Parker KL (2008) Allocating protein to reproduction in arctic reindeer and caribou. Physiol Biochem Zool 81:835–855CrossRefPubMedGoogle Scholar
  5. Bjerke JW, Dahl T (2002) Distribution patterns of usnic acid-producing lichens along local radiation gradients in West Greenland. Nova Hedwigia 75:487–506CrossRefGoogle Scholar
  6. Bjerke JW, Lerfall K, Elvebakk A (2002) Effects of ultraviolet radiation and PAR on the content of usnic and divarcatic acids in two arctic-alpine lichens. Photochem Photobiol Sci 1:678–685CrossRefPubMedGoogle Scholar
  7. Buffoni-Hall RS, Bornman JF, Bjôrn LO (2002) UV-induced changes in pigment content and light penetration in the fruticose lichen Cladonia arbuscula spp. mitis. J Photochem Photobiol B Biol 66:13–20CrossRefGoogle Scholar
  8. Cetin H, Tufan-Cetin O, Turk AO, Tay T, Candan M, Yanikoglu A, Sumbul H (2008) Insecticidal activity of major lichen compounds, (−)- and (+)-usnic acid, against the larvae of house mosquito, Culex pipiens L. Parasitol Res 102:1277–1279CrossRefPubMedGoogle Scholar
  9. Cocchietto M, Skert N, Nimis PL, Sava G (2002) A review on usnic acid, an interesting natural compound. Naturwissenschaften 89:137–146CrossRefPubMedGoogle Scholar
  10. Dailey RN, Montgomery DL, Ingram JT, Siemion R, Vasquez M, Raisbeck MF (2008) Toxicity of the lichen secondary metabolite (+)-usnic acid in domestic sheep. Vet Pathol 45:19–25CrossRefPubMedGoogle Scholar
  11. Durazo FA, Lassman C, Han SHB, Saab S, Lee NP, Kawano M, Saggi B, Gordon S, Farmer DG, Yersiz H, Goldstein LI, Ghobrial M, Busuttil RW (2004) Fulminant liver failure due to usnic acid for weight loss. Am J Gastroenterol 99:950–952CrossRefPubMedGoogle Scholar
  12. Emmerich R, Giez I, Lange OL, Proksch P (1993) Toxicity and antifeedant activity of lichen compounds against the polyphagous herbivorous insect Spodoptera littoralis. Phytochemistry 33:1389–1394CrossRefGoogle Scholar
  13. Falk A, Green T, Barboza P (2008) Quantitative determination of secondary metabolites in Cladina stellaris and other lichens by micellar electrokinetic chromatography. J Chrom A 1182:141–144CrossRefGoogle Scholar
  14. Feige GB, Lumbsch HT, Huneck S, Elix JA (1993) Identification of lichen substances by a standardized high-performance liquid chromatographic method. J Chrom 646:417–427CrossRefGoogle Scholar
  15. Glad T, Falk A, Barboza P, Kohn A, Brusetti L, Mathiesen SD, Mackie RI, Sundset MA (2009) Fate and effect of usnic acid in lichen on the bacterial population in the reindeer rumen. Microb Ecol 57:570–571Google Scholar
  16. Green MJB (1987) Diet composition and quality in Himalayan musk deer based on fecal analysis. J Wildl Manag 51:880–892CrossRefGoogle Scholar
  17. Han D, Matsumaru K, Rettori D, Kaplowitz N (2004) Usnic acid-induced necrosis of cultured mouse hepatocytes: inhibition of mitochondrial function and oxidative stress. Biochem Pharmacol 67:439–451CrossRefPubMedGoogle Scholar
  18. Hesbacher S, Baur B, Baur A, Proksch P (1995) Sequestration of lichen compounds by three species of terrestrial snail. J Chem Ecol 21:233–246CrossRefGoogle Scholar
  19. Hidalgo ME, Bascuñan L, Quilhot W, Fernández E, Rubio C (2005) Spectroscopic and photochemical properties of the lichen compound lobaric acid. Photochem Photobiol 81:1447–1449CrossRefPubMedGoogle Scholar
  20. Hove K, Jakobsen E (1975) Renal excretion of urea in reindeer. Effect of nutrition. Acta Vet Scand 16:513–519PubMedGoogle Scholar
  21. Ihl C, Klein DR (2001) Habitat and diet selection by muskoxen and reindeer in western Alaska. J Wildlife Manag 65:964–972CrossRefGoogle Scholar
  22. Ingolfsdottir K (2002) Molecules of interest: usnic acid. Phytochemistry 61:729–736CrossRefPubMedGoogle Scholar
  23. Klein DR (1982) Fire, lichens, and caribou. J Range Manag 35:390–395CrossRefGoogle Scholar
  24. Larsen TS, Nilsson NÖ, Blix AS (1985) Seasonal changes in lipogenesis and lipolysis in isolated adipocytes from Svalbard and Norwegian reindeer. Acta Physiol Scand 123:97–104CrossRefPubMedGoogle Scholar
  25. Mackie RI, Aminov RI, Hu W, Klieve AV, Ouwerkerk D, Sundset MA, Kamagata Y (2003) Ecology of uncultivated Oscillospira species in the rumen of cattle, sheep, and reindeer as assessed by microscopy and molecular approaches. Appl Environ Microbiol 69:6808–6815CrossRefPubMedGoogle Scholar
  26. Nash TH III (1996) Photosynthesis, respiration, productivity and growth. In: Nash TH III (ed) Lichen biology. Cambridge University Press, Cambridge, pp 88–120Google Scholar
  27. Nybakken L, Julkunen-Tiitto R (2006) UV-B induces usnic acid in reindeer lichens. Lichenologist 38:477–485CrossRefGoogle Scholar
  28. Palo RT (1993) Usnic acid, a secondary metabolite of lichens and its effect on in vitro digestibility in reindeer. Rangifer 13:39–43Google Scholar
  29. Parker KL, Barboza PS, Stephenson TR (2005) Protein conservation in female caribou (Rangifer tarandus): effects of decreasing diet quality during winter. J Mammalogy 86:610–622CrossRefGoogle Scholar
  30. Roach JAG, Musser SM, Morehouse K, Woo JYJ (2006) Determination of usnic acid in lichen toxic to elk by liquid chromatography with ultraviolet and tandem mass spectrometry detection. J Agric Food Chem 54:2484–2490CrossRefPubMedGoogle Scholar
  31. Singelton VL, Orthofer R, Lamuela-Raventós RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagents. Methods Enzymol 299:152–178CrossRefGoogle Scholar
  32. Storeheier PV, Mathiesen SD, Tyler NJC, Olsen MA (2002a) Nutritive value of terricolous lichens for reindeer in winter. The Lichenologist 34:247–257CrossRefGoogle Scholar
  33. Storeheier PV, Mathiesen SD, Tyler NJC, Schelderup I, Olsen MA (2002b) Utilization of nitrogen and mineral-rich vascular plants by reindeer in winter. J Agric Sci Cambr 139:151–160Google Scholar
  34. Sundset MA, Præsteng KE, Cann IKO, Mathiesen SD, Mackie RI (2007) Novel rumen bacterial diversity in two geographically separated sub-species of reindeer. Microbial Ecol 54:424–438CrossRefGoogle Scholar
  35. Sundset MA, Kohn A, Mathiesen SD, Præsteng KE (2008) Eubacterium rangiferina, a novel usnic acid resistant bacterium from the reindeer rumen. Naturwissenschaften 95:741–749CrossRefPubMedGoogle Scholar
  36. Sundset MA, Edwards JE, Cheng YF, Sensoiain RS, Fraile MN, Northwood KS, Præsteng KE, Glad T, Mathiesen SD, Wright A-DG (2009) Molecular diversity of the rumen microbiome of Norwegian reindeer on natural summer pasture. Microbial Ecol 57:335–348CrossRefGoogle Scholar
  37. Sunnerheim K, Palo RT, Theander O, Knutsson P-G (1988) Chemical defence in birch. Platyphylloside: A phenol from Betula pendula inhibiting digestibility. J Chem Ecol 14:549–560CrossRefGoogle Scholar
  38. Sunnerheim-Sjöberg K, Knutsson P-G (1995) Platyphylloside: metabolism and digestibility reduction in vitro. J Chem Ecol 21:1339–1348CrossRefGoogle Scholar
  39. Turunen M, Soppela P, Kinnunen H, Sutinen M-L, Martz F (2009) Does climate change influence the availability and quality of reindeer forage plants? Polar Biol 32:813–832CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Monica A. Sundset
    • 1
    • 2
    Email author
  • Perry S. Barboza
    • 3
  • Thomas K. Green
    • 4
  • Lars P. Folkow
    • 1
  • Arnoldus Schytte Blix
    • 1
  • Svein D. Mathiesen
    • 5
    • 6
  1. 1.Department of Arctic Biology and Institute Medical BiologyUniversity of TromsøTromsøNorway
  2. 2.Institute of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and EconomicsUniversity of TromsøTromsøNorway
  3. 3.Department of Biology and Wildlife, Institute of Arctic BiologyUniversity of AlaskaFairbanksUSA
  4. 4.Department of Chemistry, Institute of Arctic BiologyUniversity of AlaskaFairbanksUSA
  5. 5.The Norwegian School of Veterinary ScienceTromsøNorway
  6. 6.Saami University CollegeGuovdageaidnuNorway

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