doi: 10.15389/agrobiology.2018.4.779eng

UDC 639.111.4:636.085.19

Supported financially by Russian Science Foundation, grant 17-76-20026 “Rumen microbiocenosis of Rangifer tarandus as a basis for developing promising biotechnologies for reindeer herding in Russia’s Arctic regions”



E.A. Yildirim1, L.A. Ilina1, K.A. Laishev1, V.A. Filippova1,
A.V. Dubrowin1, T.P. Dunyashev1, G.Yu. Laptev1, I.N. Nikonov2,
A.A. Yuzhakov3,
T.M. Romanenko4, Yu.P. Vylko4

1JSC «Biotrof+», 19 korp. 1, Zagrebskii bulv., St. Petersburg, 192284 Russia, e-mail (✉ corresponding author),,,,,;
2AlI-Russin Research Veterinary Institute of Poultry Science — Branch of the Federal Scientific Center All-Russian Research and Technological Poultry Institute RAS, Federal Agency of Scientific Organizations, 48, ul. Chernikova, St. Petersburg—Lomonosov, 198412 Russia, e-mail;
3Northwest Center for Interdisciplinary Research of Food Security Problems, Federal Agency of Scientific Organizations, 7, sh. Podbel’skogo, St. Petersburg—Pushkin, 196608 Russia, e-mail,;
4Laverov Federal Center for Integrated Arctic Research (FCIARctic) RAS, Naryan-Mar Agro-Experimental Station, Federal Agency of Scientific Organizations, 1a, ul. Rybnikov, Naryan-Mar, Nenets AO, 166004 Russia, e-mail,

Yildirim E.A.
Laptev G.Yu.
Ilina L.A.
Nikonov I.N.
Laishev K.A.
Yuzhakov A.A.
Filippova V.A.
Romanenko ..
Dubrowin A.V.
Vylko Yu.P.
Dunyashev T.P.
The authors declare no conflict of interests

Received November 9, 2017


In the summer and autumn, the food base of Rangifer tarandus consists of up to 300 species of higher plants, of which lichens account for about 15 %. It is shown that in the tissues of some higher plants and in the soil under lichens there are micromycetes capable of producing mycotoxins. In the present work, we are the first to estimate the content of mycotoxins for the components of summer reindeer rations, i.e. Salix borealis, Vaccinium uliginosum, Betula nana, and B. pendula. The aim of the study was to analyze the distribution of mycotoxins in the components of the summer diet of reindeer. Samples of genera Cladonia and Nephroma lichens, higher plants of the species Salix borealis, Vaccinium uliginosum, Betula nana, B. pendula, and mixtures of perennial grasses were collected in early August 2017 in the pastures of the Harp town of the Yamalo-Nenets Autonomous District, the Nelmin-Nos town of Nenets Autonomous District and the Pushnoy town of the Murmansk region. Aflatoxins (AFLA), ochratoxin A (OTA), T-2 toxin (T-2), zearalenone (ZEN), deoxynivalenol (DON) were detected and measured in the samples using ELISA test. During the mycotoxicological evaluation of the summer food ration components of reindeer, we found multiple contaminations with the mycotoxins. The samples of Embryophyta representatives revealed a greater number of toxic metabolites compared to samples of the genera Cladonia and Nephroma lichens. Practically, in all samples of higher plants, the presence of mycotoxins T-2, ZEN and DON produced by Fusarium pathogens which affects plants during vegetation, as well as AFLA and OTA metabolites of micromycetes Aspergillus sp. and Penicillium sp. which previously were considered not adapted for growth and reproduction in plant tissues during the growing season. However, AFLA and OTA were the least represented on virtually all samples. It is of interest that OTA was not detected in any of the lichen samples assayed. In most of the samples, DON Fusarium toxins dominated with accumulation in lichens up to 0.15 mg/kg and in Embryophyta samples up to 33.8 mg/kg, as well as ZEN at the amount of up to 0.1227 mg/kg and 2.543 mg/kg, respectively. Mycotoxin contamination of the samples of genus Cladonia practically did not have regional differences, whereas in the mixture of perennial grasses and in V. uliginosum mycotoxin contamination varied to a large extent depending on the place of plant growth. The mycotoxins are found in concentrations that may pose a threat to animal health.

Keywords: Rangifer tarandus, feed, lichens, mycotoxins, ELISA.


Full article (Rus)




  1. Chikalev A.I., Yuldashbaev Yu.A., Rodionov G.V. Olenevodstvo [Reindeer herding]. Moscow, 2015 (in Russ.).
  2. Bennett J.W., Klich M. Mycotoxins. Clin. Microbiol. Rev., 2003, 16(3): 497-516 CrossRef
  3. Burkin A.A., Kononenko G.P. Prikladnaya biokhimiya i mikrobiologiya, 2013, 5(49): 522-530 CrossRef (in Russ.).
  4. Orina A.S., Gavrilova O.P., Gagkaeva T.Yu. Zashchita i karantin rastenii, 2017, 6: 25-27 (in Russ.).
  5. Diaz D. Mikotoksiny i mikotoksikozy [Mycotoxins and mycotoxicoses]. Moscow, 2006 (in Russ.).
  6. Palo R.T. Usnic acid, a secondary metabolite of lichens and its effect on in vitro digestibility in reindeer. Rangifer, 1993, 13: 39-43.
  7. Sundset M.A., Edwards J.E., Cheng Y.F., Senosiain R.S., Fraile M.N., Northwood K.S., Praesteng K.E., Glad T., Mathiesen S.D., Wright A.D. Rumen microbial diversity in Svalbard reindeer, with particular emphasis on methanogenic archaea. FEMS Microbiol. Ecol., 2009, 70(3): 553-562 CrossRef
  8. Luzina O.A., Salakhutdinov N.F. Bioorganicheskaya khimiya, 2016, 3(42), 2016: 276 CrossRef (in Russ.).
  9. Burkin A.A., Kononenko G.P. Izvestiya Rossiiskoi akademii nauk. Seriya Biologicheskaya, 2014, 3: 228 CrossRef (in Russ.).
  10. Kingsbury J.M. Poisonous plants of the United States and Canada. NY, 1964.
  11. Kononenko G.P., Burkin A.A. V sbornike: Uspekhi meditsinskoi mikologii [Advances in medical mycology]. Moscow, 2003: 141-144 (in Russ.).
  12. Burkin A.A. V sbornike: Uspekhi meditsinskoi mikologii [Advances in medical mycology]. Moscow, 2003: 122-124 (in Russ.).
  13. Hernandez-Mendoza A., Garcia H.S., Steele J.L. Screening of Lactobacillus casei strains for their ability to bind aflatoxin B1. Food Chem. Toxicol., 2009, 47(6): 1064-1068 CrossRef
  14. ?vek D., Markov K., Frece J., Friganovi? M., Durakovi? L., Delaš F. Adhesion of zearalenone to the surface of lactic acid bacteria cells. Croatian Journal for Food Technology, Biotechnology & Nutrition, 2012, 7(Special Issue): 49-52.
  15. Shi L., Liang Z., Li J., Hao J., Xu Y., Huang K., Tian J., He X., Xu W. Ochratoxin A biocontrol and biodegradation by Bacillus subtilis CW 14. J. Sci. Food Agr., 2014, 94(9): 1879-1885 CrossRef
  16. Levitin M.M., Novozhilov K.V., Afanasenko O.S., Mikhailov L.A., Mironenko N.V., Gagkaeva T.Yu., Gannibal F.B. V knige: Mikologiya segodnya. Tom 2 [In: Mycology today. V. 2]. Moscow, 2011: 261-274 (in Russ.).
  17. Gagkaeva T.Yu., Gavrilova O.P. Materialy Mezhdunarodnoi nauchnoi konferentsii, posvyashchennoi 150-letiyu so dnya rozhdeniya chl.-korr. AN SSSR, prof. A.A. Yachevskogo «Problemy mikologii i fitopatologii v XXI veke» [Proc. Int. Conf. dedicated to 150 anniversary of Prof. A.A. Yachevskii «Challenges of mycology and phytopathology in the 21st century»].  St. Petersburg, 2013: 400 (in Russ.).
  18. Christensen C.M., Kaufmann H.H. Storage of cereal grains and their products. 2nd ed. American Association of Cereal Chemists. St. Paul, Minnesota, 1974: 158-192.
  19. Laptev G.Yu., Novikova N.I., Il'ina L.A., Iyldyrym E.A., Soldatova V.V., Nikonov I.N., Filip-pova V.A., Brazhnik E.A., Sokolova O.N. Dynamics of mycotoxin accumulation in silage during storage. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2014, 6: 123-130 CrossRef
  20. Tolpysheva T.Yu. Vestnik Moskovskogo Universiteta. Seriya 16: Biologiya, 2014, 3: 37-41 (in Russ.).
  21. Girlanda M., Isocrono D., Bianco C., Luppi-Mosca A.M. Two foliose lichens as microfungal ecological niches. Mycologia, 1997, 89(4): 531-536 CrossRef
  22. Burdov L.G. Monitoring mikotoksinov, profilaktika i lechenie mikotoksikozov v Udmurtskoi Respublike. Kandidatskaya dissertatsiya [Monitoring of mycotoxins, mycotoxicosis prevention and treatment in the Udmurt Republic. PhD Thesis]. Kazan', 2013 (in Russ.).
  23. Burkin A.A., Kononenko G.P. Mycotoxin contamination of meadow grasses in European Russia. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2015, 50(4): 503-512 CrossRef
  24. Laptev G.Yu., Novikova N.I., Dubrovina E.G., Il'ina L.A., Iyldyrym E.A., Filippova V.A., Nikonov I.N., Brazhnik E.A. Kormoproizvodstvo, 2014, 10: 35-39 (in Russ.).
  25. Boudra H., Morgavi D.P. Reduction in fusarium toxin levels in corn silage with low dry matter and storage time. J. Agr. Food Chem., 2008, 56(12): 4523-4528 CrossRef
  26. Mansfield M.A., Jones A.D., Kuldau G.A. Contamination of fresh and ensiled maize by multiple Penicillium mycotoxins. Phytopathology, 2008, 98(3): 330-336 CrossRef
  27. Teller R.S., Schmidt R.J., Whitlow L.W., Kung L. Jr. Effect of physical damage to ears of corn before harvest and treatment with various additives on the concentration of mycotoxins, silage fermentation, and aerobic stability of corn silage. J. Dairy Sci., 2012, 95(3): 1428-1436 CrossRef
  28. Watanabe I., Kakishima M., Adachi Y., Nakajima H. Potential mycotoxin productivity of Alternaria alternata isolated from garden trees. Mycotoxins, 2007, 57(1): 3-9 CrossRef