Incomplete degradation of lichen usnic acid and atranorin in Svalbard reindeer (Rangifer tarandus platyrhynchus)

Keywords: Lichen secondary metabolites, ruminant, faecal samples, Spitsbergen, Arctic


Previous studies of Eurasian tundra reindeer (Rangifer tarandus tarandus) in Norway indicate that their rumen microbiota play a key role in degrading lichen secondary metabolites. We investigated the presence of usnic acid and atranorin in faecal samples from Svalbard reindeer (R. tarandus platyrhynchus). Samples were collected in Bolterdalen valley together with vegetation samples from the study site. The mesic tundra in this area was dominated by vascular plants (59% of vegetation cover). Bryophytes (16%) and lichens (25%) were also present. Qualitative and quantitative analyses of usnic acid and atranorin in lichen and faeces samples were performed using high-performance liquid chromatography. Contents of atranorin averaged 12.49 ± 0.41 mg g–1in the thalli of Stereocaulon alpinum, while the average level of usnic acid was lowest in Cladonia mitis (12.75 ± 2.86 mg g–1) and highest in Flavocetraria cucullata (34.87 ± 0.47 mg g–1). Atranorin and usnic acid were detected in the faecal samples, averaging 0.41 ± 0.53 and 0.74 ± 1.11 (mean ± SD) mg g–1 dry matter, respectively. The presence of lichen secondary compounds in faeces from Svalbard reindeer shows that lichens are indeed included in their diet, although probably in small amounts because of depleted pastures. Contrary to previous findings in reindeer on mainland Norway, atranorin and usnic acid are not completely degraded or absorbed in Svalbard reindeer. To elucidate the mechanisms behind detoxification of lichen secondary compounds in reindeer, more research is needed on their respective rumen microbiomes and digestive enzymes.


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Araújo A.A.S., de Melo M.G.D., Rabelo T.K., Nunes P.S., Santos S.L., Serafini M.R., Santos M.R.V., Quintans-Júnior L.J. & Gelain D.P. 2015. Review of the biological properties and toxicity of usnic acid. Natural Product Research 29, 2167–2180,

Barboza P.S., Bennet A., Lignot J.-H., Macie R.I., McWhorter T.J., Secor S.M., Skovgaard N., Sundset M.A. & Wang T. 2010. Digestive challenges for vertebrate animals: microbial diversity, cardiorespiratory coupling, and dietary specialization. Physiological and Biochemical Zoology 83, 764–774,

BeGora M.D. & Fahlset D. 2000. An alternative method for quantification of lichen secondary products. The Bryologist 103, 563–567,[0563:AAMFTQ]2.0.CO;2.

BeGora M.D. & Fahlset D. 2001. Usnic acid and atranorin concentrations in lichens in relation to bands of UV irradiance. The Bryologist 104, 134–140,[0134:UAAACI]2.0.CO;2.

Bjerke J.W., Elvebakk A., Domínguez E. & Dahlback A. 2005. Seasonal trends in usnic acid concentrations of Arctic, alpine and Patagonian populations of the lichen Flavocetraria nivalis. Phytochemistry 66, 337–344,

Bjerke J.W., Joly D., Nilsen L. & Brossard T. 2004. Spatial trends in usnic acid concentrations of the lichen Flavocetraria nivalis along local climatic gradients in the Arctic (Kongsfjorden, Svalbard). Polar Biology 27, 409–417,

Bjørkvoll E., Pedersen B., Hytteborn H., Jónsdóttir I.S. & Langvatn R. 2009. Seasonal and interannual dietary variation during winter in female Svalbard reindeer (Rangifer tarandus platyrhynchus). Arctic, Antarctic, and Alpine Research 41, 88–96,

Borch-Iohnsen B., Nilssen K.J. & Norheim G. 1996. Influence of season and diet on liver and kidney content of essential elements and heavy metals in Svalbard reindeer. Biological Trace Element Research 51, 235–247,

Bourgeois G., Suire C., Vivas N. & Vitry C. 1999. Atraric acid, a marker for epiphytic lichens in the wood used in cooperage: identification and quantification by GC/MS/(MS). Analusis 27, 281–283,

Braun-Blanquet J. 1964. Pflanzensoziologie. Grundzüge der Vegetationskunde. (Plant sociology. Basics of vegetation science.) Vienna: Springer.

Cocchietto M., Skert N., Nimis P. & Sava G. 2002. A review on usnic acid, an interesting natural compound. Naturwissenschaften 89, 137–146,

Dailey R.N., Montgomery D.L., Ingram J.T., Siemion R., Vasquez M. & Raisbeck M.F. 2008. Toxicity of the lichen secondary metabolite (+)-usnic acid in domestic sheep. Veterinary Pathology 45, 19–25,

de Carvalho M.G., de Carvalho G.J. & Braz-Filho R. 2000. Chemical constituents from Ouratea floribunda: complete 1H and 13C NMR assignments of atranorin and its new acetyl derivative. Journal of the Brazilian Chemical Society 11, 143–147,

de Melo M.G.D., de Souza Araújo A.A., Serafini M.R., Carvalho L.F., Bexerra M.S., Ramos C.S., Bonjardim L.R., Albuquerque-Jùnior R.L.C., Lima J.T., Siqueira R.S., Fortes V.S., Fonseca M.J.V. & Quintans-Júnior L.J. 2011. Anti-inflammatory and toxicity studies of atranorin extracted from Cladina kalbii Ahti in rodents. Brazilian Journal of Pharmaceutical Sciences 47, 861–872,

Denryter K.A., Cook R.C., Cook J.G. & Parker K.L. 2017. Straight from the caribou’s (Rangifer tarandus) mouth: detailed observations of tame caribou reveal new insights into summer–autumn diets. Canadian Journal of Zoology 95, 81–94,

Durazo F.A., Lassman C., Han S.H., Saab S., Lee N.P., Kawano M., Saggi B., Gordon S., Farmer D.G., Yersiz H., Goldstein R.L.I., Ghobrial M. & Busuttil R.W. 2004. Fulminant liver failure due to usnic acid for weight loss. The American Journal of Gastroenterology 99, 950–952,

Falk A., Green T.K. & Barboza P. 2008. Quantitative determination of secondary metabolites in Cladina stellaris and other lichens by micellar electrokinetic chromatography. Journal of Chromatography A 1182, 141–144,

Foti R.S., Dickmann L.J., Davis J.A., Greene R.J., Hill J.J., Howard M.L., Pearson J.T., Rock D.A., Tay J.C., Wahlstrom J.L. & Slatter J.G. 2008. Metabolism and related human risk factors for hepatic damage by usnic acid containing nutritional supplements. Xenobiotica 38, 264–280,

Glad T., Barboza P., Mackie R.I., Wright A.D.G., Brusetti L., Mathiesen S.D. & Sundset M.A. 2014. Dietary supplementation of usnic acid, an antimicrobial compound in lichens, does not affect rumen bacterial diversity or density in reindeer. Current Microbiology 68, 724–728,

Hakala A.V.K., Staaland H., Pulliainen E. & Røed K.H. 1986. Taxonomy and history of Arctic island reindeer with special reference to Svalbard reindeer–a preliminary report. Rangifer, Special Issue 1, 360,

Hansen B.B., Aanes R. & Sæther B.-E. 2010. Partial seasonal migration in High-Arctic Svalbard reindeer (Rangifer tarandus platyrhynchus). Canadian Journal of Zoology 88, 1202–1209,

Henriksen S., Aanes R., Sæther B. & Ringsby T.H. 1997. Does availability of resources influence grazing strategies in female Svalbard reindeer? Rangifer 23, 25–37,

Honda N.K., Pavan F.R., Coelho R.G., de Andrade Leite S.R., Micheletti A.C., Lopes T.I.B., Misutsu M.Y., Beatriz A., Brum R.L. & Leite C.Q.F. 2010. Antimycobacterial activity of lichen substances. Phytomedicine 17, 328–332,

Ingólfsdóttir K. 2002. Usnic acid. Phytochemistry 61, 729–736,

Joo S., Han D., Lee E.J. & Park S. 2014. Use of length heterogeneity polymerase chain reaction (LH-PCR) as non-invasive apporach for dietary analysis of Svalbard reindeer, Rangifer tarandus tarandus. PLoS One 9, e91552,

Kärnefelt I., Thell A., Randlane T. & Saag A. 1994. The genus Flavocetraria Kärnefelt & Thell (Parmeliaceae, Ascomycotina) and its affinities. Acta Botanica Fennica 150, 79–86.

Krishna D.R. & Venkataramana D. 1992. Pharmacokinetics of d(+)-usnic acid in rabbits after intravenous and oral administration. Drug Metabolism and Disposition 20, 909–911,

Kutney J.P., Baarschers W.H., Chin O., Ebizuka Y., Hurley L., Leman J.D., Salisbury P.J., Sanchez I.H., Yee T. & Bandoni R.J. 1977a. Studies in the usnic acid series. VIII. The biodegradation of (+)-usnic acid by Mortierella isabellina. Canadian Journal of Chemistry 55, 2930–2940,

Kutney J.P., Leman J.D., Salisbury P.J., Sanchez I.H., Yee T. & Bandoni R.J. 1977b. Studies in the usnic acid series. VII. The biodegradation of (+)-usnic acid by a Pseudomonas species. Isolation, structure determination, and synthesis of (+)-6-desacetylusnic acid. Canadian Journal of Chemistry 55, 2336–2352,

Kutney J.P., Leman J.D., Salisbury P.J., Yee T. & Sanchez I.H. 1984. Studies in the usnic acid series. IX. The biodegradation of (+)-usnic acid by Mucor globosus. Canadian Journal of Chemistry 62, 320–325,

Lindner E. 2003. Use of vegetation types by Svalbard reindeer from Arctic winter to spring. Polar Record 39, 245–247,

Manojlović N., Vasiljević P., Jusković M. & Slobodan S.N. 2010. HPLC analysis and cytotoxic potential of extracts from the lichen, Thamnolia vermicularis var. subuliformis. Journal of Medicinal Plants Research 4, 817–823,

Nasser J.A., Yaacob W.A., Din L.B., Yamin B.M. & Latip J. 2009. Isolation of atranorin, bergenin and goniothalamin from Hopea sangal. ARPN Journal of Engineering and Applied Sciences 4, 92–95.

Olech M., Węgrzyn M., Lisowska M., Słaby A. & Angiel P. 2011. Contemporary changes in vegetation of polar regions. Papers on Global Change IGBP 18, 35–51,

Orange A., James P.W. & White F.J. 2001. Microchemical methods for the identification of lichens. London: British Lichen Society.

Orpin C.G., Mathiesen S.D., Greenwood Y. & Blix A.S. 1985. Seasonal changes in the ruminal microflora of the High-Arctic Svalbard reindeer (Rangifer tarandus platyrhynchus). Applied and Environmental Microbiology 50, 144–151.

Palo R. 1993. Usnic acid, a secondary metabolite of lichens and its effect on in vitro digestibility in reindeer. Rangifer 13, 39–43,

Piska K., Galanty A., Koczurkiewicz P., Żmudzki P., Potaczek J., Podolak I. & Pękala E. 2018. Usnic acid reactive metabolites formation in human, rat, and mice microsomes. Implication for hepatotoxicity. Food and Chemical Toxicology 120, 112–118,

Podterob A.P. 2008. Chemical composition of lichens and their medicinal applications. Pharmaceutical Chemistry Journal 42, 582–588,

Pope P.B., Mackenzie A.K., Gregor I., Smith W., Sundset M.A., McHardy A.C., Morrison M. & Eijsink V.G.H. 2012. Metagenomics of the Svalbard reindeer rumen microbiome reveals abundance of polysaccharide utilization loci. PLoS One 7, e38571,

Ragasa C.Y., Tan M.C.S., Alba L.D. & Shen C.C. A depside from Frullania trichodes Mitt. 2016. Der Pharmacia Lettre 8, 76–78.

Reimers E. 1982. Winter mortality and population trends of reindeer on Svalbard, Norway. Arctic, Antarctic, and Alpine Research 14, 295–300,

Reimers E. 2012. Svalbard reindeer population size and trends in four sub-areas of Edgeøya. Polar Research 31, article no. 11089,

Salgado-Flores A., Hagen L.H., Ishaq S.L., Zamanzadeh M., Wright A.D.G., Pope P.B. & Sundset M.A. 2016. Rumen and cecum microbiomes in reindeer (Rangifer tarandus tarandus) are changed in response to a lichen diet and may affect enteric methane emissions. PLoS One 11, e0155213,

Shoji J. 1962. Decomposition of usnic acid. VII. Pyrolysis of dihydrousnic acid. (3) Isodihydrousnic acid. Chemical and Pharmaceutical Bulletin 10, 483–491,

Smith C.W., Aptroot A., Coppins R.J., Fletcher A., Gilbert O.L., James P.W. & Wolseley P.A. 2009. Lichens of Great Britain and Ireland. London: British Lichen Society.

Solberg E.J., Jordhøy P., Strand O., Aanes R., Loison A., Sæther B.-E. & Linnell J.D.C. 2001. Effects of density-dependence and climate on the dynamics of a Svalbard reindeer population. Ecography 24, 441–451,

Sørmo W., Haga Ø.E., Gaare E., Lagvatn R. & Mathiesen S.D. 1999. Forage chemistry and fermentation chambers in Svalbard reindeer (Rangifer tarandus platyrhynchus). Journal of Zoology London 247, 247–256,

Staaland H., Scheie J.O., Grøndahl F.A., Persen E., Leifseth A.B. & Holand Ø. 1993. The introduction of reindeer to Brøggerhalvøya, Svalbard: grazing preference and effect on vegetation. Rangifer 13, 15–19,

Stark J.B., Walter E.D. & Owens H.S. 1950. Method of isolation of usnic acid from Ramalina reticulate. Journal of the American Chemical Society 72, 1819–1820,

Storeheier P., Mathiesen S., Tyler N. & Olsen M. 2002. Nutritive value of terricolous lichens for reindeer in winter. Lichenologist 34, 247–257,

Studzinska-Sroka E., Galanty A. & Bylka W. 2017. Atranorin—an interesting lichen secondary metabolite. Mini Reviews in Medicinal Chemistry 17, 1633–1645,

Sundset M.A., Barboza P.S., Green T.K., Folkow L.P., Blix A.S. & Mathiesen S.D. 2010. Microbial degradation of usnic acid in the reindeer rumen. Naturwissenschaften 97, 273–278,

Sundset M.A., Edwards J.E., Chen Y.F., Sensiain R.S., Fraile M.N., Northwood K.S., Præsteng, K.E., Glad T.G., Mathiesen S.D. & Wright A.D.G. 2009. Rumen microbial diversity in Svalbard reindeer, with particular emphasis on methanogenic archaea. Microbial Ecology 70, 553–562,

Sundset M.A., Kohn A., Mathiesen S.D. & Præsteng K.E. 2008. Eubacterium rangiferina, a novel usnic acid-resistant bacterium from the reindeer rumen. Naturwissenschaften 95, 741–749,

Sundset M.A., Præsteng K.E., Cann I.K., Mathiesen S.D. & Mackie R.I. 2007. Novel rumen bacterial diversity in two geographically separated sub-species of reindeer. Microbial Ecology 54, 424–438,

Sundset M.A., Salgado-Flores A., Wright A.D.G. & Pope P.B. 2015. The reindeer rumen microbiome. In K.E. Nelson (ed.): Encyclopedia of metagenomics. Pp. 722–731. Dordrecht: Springer.

Svihus B. & Holand Ø. 2000. Lichen polysaccharides and their relation to reindeer/caribou nutrition. Journal of Range Management 53, 642–648,

Tyler N.J.C. 1986. The relationship between the fat content of Svalbard reindeer in autumn and their death from starvation in winter. Rangifer, Special Issue 1, 311–314,

Van der Knaap W.O. 1986. On the presence of reindeer (Rangifer tarandus L.) on Edgeøya, Spitzbergen in the period 3800 5000 BP. Circumpolar Journal 2, 3–10.

Wang X.N., Yu W.T. & Lou H.X. 2005. Antifungal constituents from the Chinese moss Homalia trichomanoides. Chemistry & Biodiversity 2, 139–145,

Wegener C., Hansen M. & Jacobsen L.B. 1992. Effekter av reinbeite ved Kongsfjorden, Svalbard, 1992. Vegetasjonsovervåkning på Svalbard 1991. (Effects of reindeer grazing at Kongsfjorden, Svalbard, Kongsfjorden, Svalbard. Vegetation monitoring in Svalbard 1991.) Norsk Polarinstitutt Meddelelser 121. Oslo: Norwegian Polar Institute.

Wegener C. & Odasz-Albrigtsen A.M. 1998. Do Svalbard reindeer regulate standing crop in the absence of predators? A test of the “exploitation ecosystems” model. Oecologia 116, 202–206,

Węgrzyn M., Lisowska M. & Nicia P. 2013. The value of the terricolous Cetrariella delisei in the biomonitoring of heavy-metal levels in Svalbard. Polish Polar Research 34, 87–99,

Węgrzyn M. & Wietrzyk P. 2015. Phytosociology of snowbed and exposed ridge vegetation of Svalbard. Polar Biology 38, 1905–1917,

Węgrzyn M., Wietrzyk P., Lisowska M., Klimek B. & Nicia P. 2016. What influences heavy metals accumulation in Arctic lichen Cetrariella delisei in Svalbard? Polar Science 10, 532–540,

White P.A.S., Oliveira R.C.M., Oliveira A.P., Seafini M.R., Araújo A.A.S., Gelain D.P., Moreira J.C.F., Almeida J.R.G.S., Quintans J.S.S., Quintans-Junior L.J. & Santos M.R.V. 2014. Antioxidant activity and mechanisms of action of natural compounds isolated from lichens: a systematic review. Molecules 19, 14496–14527,

Ziaja W., Dudek J., Ostafin K., Węgrzyn M., Lisowska M., Olech M. & Osyczka P. 2016 Transformation of the natural environment in western Sørkapp Land (Spitsbergen) since the 1980s. Dordrecht: Springer.

How to Cite
Węgrzyn M. H., Wietrzyk-Pełka P., Galanty A., Cykowska-Marzencka B., & Alterskjær Sundset M. (2019). Incomplete degradation of lichen usnic acid and atranorin in Svalbard reindeer (<em>Rangifer tarandus platyrhynchus</em&gt;). Polar Research, 38.
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