Tatyana S. Uligova, Senior Researcher of the Laboratory for soil and ecological researches in the Tembotov Institute of Ecology of Mountain Territories of RAS (360051, Russia, Kabardino-Balkaria Republic, Nalchik, I. Armand Street, 37a); e-mail:
Fatima V. Gedgafova, PhD, Senior Researcher of the Laboratory for soil and ecological researches in the Tembotov Institute of Ecology of Mountain Territories of RAS (360051, Russia, Kabardino-Balkaria Republic, Nalchik, I. Armand Street, 37a); e-mail:
Olga N. Gorobtsova, PhD, Senior Researcher, Head of the Laboratory for soil and ecological researches in the Tembotov Institute of Ecology of Mountain Territories of RAS (360051, Russia, Kabardino-Balkaria Republic, Nalchik, I. Armand Street, 37a); e-mail:
Nelli L. Tsepkova, PhD, Senior Researcher of the Laboratory for Mountain Nature Management in the Tembotov Institute of Ecology of Mountain Territories of RAS (360051, Russia, Kabardino-Balkaria Republic, Nalchik, I. Armand Street, 37a); e-mail:
Irina B. Rapoport, PhD, Senior Researcher, Head of the Laboratory for ecology of invetebrate species and communities in the Tembotov Institute of Ecology of Mountain Territories of RAS (360051, Russia, Kabardino-Balkaria Republic, Nalchik, I. Armand Street, 37a); e-mail:
Rustam Kh. Tembotov, PhD, Senior Researcher of the Laboratory for soil and ecological researches in the Tembotov Institute of Ecology of Mountain Territories of RAS (360051, Russia, Kabardino-Balkaria Republic, Nalchik, I. Armand Street, 37a); e-mail:
Elena M. Khakunova, Junior Researcher of the Laboratory for soil and ecological researches in the Tembotov Institute of Ecology of Mountain Territories of RAS (360051, Russia, Kabardino-Balkaria Republic, Nalchik, I. Armand Street, 37a); e-mail:

Reference to article

Uligova T.S., Gedgafova F.V., Gorobtsova O.N., Tsepkova N.L., Rapoport I.B., Tembotov R.Kh., Khakunova E.M. 2019. Meadow biogeocenoses in the subalpine belt of the Kabardino-Balkaria State High-Mountain Reserve (Central Caucasus). Nature Conservation Research 4(2): 29–47.

Section Resarch articles

The study describes the current ecological-biological state of the high-mountain meadow biogeocoenoses' components (soils, vegetation, earthworms), which were formed in the subalpine belt of the Cherek-Bezengi canyon in the Kabardino-Balkaria State High-Mountain Reserve. The vegetation has been represented mainly by subalpine meadows. In medium-grass meadow phytocoenoses, the proportion of mesophytes was 70%, xeromesophytes – 20%, mesoxerophytes – 10%. Synecological indices (Shannon Index, Simpson Index, Pielou Index, Hartley Index and integral index) indicated a high floristic and phytocenosis diversity of hay meadows and a lower diversity of phytocoenoses of disturbed areas. Lumbricidae were the best represented in the mesofauna. Six species (with dominance of Dendrobaena schmidti) have been found in a small site of the Cherek-Bezengi canyon. These species are adapted to the cold and humid climate of the high-mountain region of the Central Caucasus. Distribution of forest earthworm species in the subalpine belt and changes of their habitats indicated more comfortable temperature conditions of meadow ecosystems in comparison with forest ecosystems. It also demonstrates the role of thermal balance as the basic limiting factor forming biotic coenoses. Based on enzymatic activity parameters and humus content, we determined the levels and spatial variation of biological activity of mountain-meadow subalpine soils which have been formed under meadow phytocoenoses. We have shown the essential dominance of hydrolase activity (high and middle levels) in comparison with oxidoreductase activity (low and very low levels). This characterises the intensity and direction of biochemical processes in high-mountain soil. Under conditions of disturbed phytocoenoses, we have determined a decrease of both the total soil biological activity (at 65%) and the integral biodiversity index (at 20%). A close joint connection between the investigated biological parameters (r = 0.74–0.86) reflected the important role of biotic communities' diversity in forming biological activity of mountain-meadow subalpine soils. The obtained data serve as a basis for monitoring of the soil-vegetation cover. Their protection is a requirement to maintain the biodiversity status in the Kabardino-Balkaria State High-Mountain Reserve.


biodiversity, biological activity, Caucasus, earthworms, high-mountain ecosystems, mountain-meadow subalpine soil, subalpine meadows

Artice information

Received: 16.09.2018. Revised: 04.02.2019. Accepted: 07.02.2019.

The full text of the article

Abramyan S. 1992. Changes in the enzymatic activity of the soil under the influence of natural and anthropogenic factors. Pochvovedenie 7: 39–45. [In Russian]
Akatov P.V. 2009. Changes in the upper limits of tree species distribution in the Western Caucasus (Belaya River basin) related to recent climate warming. Russian Journal of Ecology 40(1): 33–38. DOI: 10.1134/S1067413609010056
Akhmedova G.M. 2018. Ecological characteristics and protection of soils of alpine and subalpine meadows of Shahdag National Park. International Research Journal 3(69): 81–83. [In Russian]
Andreev A.V. 2002. Assessment of biodiversity, monitoring and econets. Kishinev: BIOTICA. 167 p. [In Russian]
Anthelme F., Grossi J., Brun J., Didier L. 2001. Consequences of green alder expansion on vegetation changes and arthropod communities removal in the northern French Alps. Forest Ecology and Management 145(1–2): 57–65. DOI: 10.1016/S0378-1127(00)00574-0
Arinushkina E.B. 1970. Guide to soil chemical analysis. Moscow: Moscow State University. 487 p. [In Russian]
Berman D.I., Meshcheryakova E.N., Alfimov A.V., Leirikh A.N. 2002. Distribution of the earthworm Dendrobaena octaedra (Lumbricidae, Oligochaeta) in the northern holarctic is restricted by its insufficient freeze tolerance. Zoologicheskii Zhurnal 81(10): 1210–1221. [In Russian]
Bernier N., Gillet F. 2012. Structural relationships among vegetation, soil fauna and humus form in a subalpine forest ecosystem: a Hierarchical Multiple Factor Analysis (HMFA). Pedobiology 55(6): 321–334. DOI: 10.1016/j.pedobi.2012.06.004
Bobulska L., Fazekasova D., Angelovicova L., Kotorova D. 2015. Impact of ecological and conventional farming systems on chemical and biological soil quality indices in a cold mountain climate in Slovakia. Biological Agriculture & Horticulture 31(3): 205–218. DOI: 10.1080/01448765.2014.1002537
Braun-Blanquet J. 1964. Pflanzensociologie. Grundzuge der Vegetationskunde. 3 Aufl. Wien-New-York: Springer Verlag. 865 p.
Bukowski M. 2009. Dynamika zarastania polan tatrzańskich. Długookresowe zmiany w przyrodzie i użytkowaniu TPN. Zakopane: Wydawnictwa Tatrzańskiego Parku Narodowego. P. 15–32.
Byers A. 2005. Contemporary human impacts on alpine ecosystems in the Sagarmatha (Mt. Everest) National Park, Khumbu, Nepal. Annals of the Association of American Geographers 95(1): 112–140. DOI: 10.1111/j.1467-8306.2005.00452.x
Byzov B.A., Tikhonov V.V., Nechitailo T.Yu., Demin V.V., Zvyagintsev D.G. 2015. Taxonomic composition and physiological and biochemical properties of bacteria in the digestive tracts of earthworms. Eurasian Soil Science 48(3): 268–275. DOI: 10.1134/S1064229315030035
Caldwell B.A. 2005. Enzyme activities as a component of soil biodiversity: A review. Pedobiologia 49(6): 637–644. DOI: 10.1016/j.pedobi.2005.06.003
Climate data of cities around the world. 2015. Available from:
Coulson S.J., Fjellberg A., Gwiazdowicz D.J., Lebedeva N.V., Melekhina E.N., Solhøy T., Erséus C., Maraldo K., Miko L., Schatz H., Schmelz R.M., Søli G., Stur E. 2013. The invertebrate fauna of anthropogenic soils in the High Arctic settlement of Barentsburg; Svalbard. Polar Research 32: 19273. DOI: 10.3402/polar.v32i0.19273
Сsuzdi Сs., Zicsi A. 2003. Earthworms of Hungary (Annelida: Oligochaeta; Lumbricidae). Budapest: Hungarian Natural History Museum. 271 p.
Csuzdi Cs., Zicsi A., Misirlioğlu M. 2006. An annotated checklist of the earthworm fauna of Turkey (Oligochaeta: Lumbricidae). Zootaxa 1175(1): 1–29. DOI: 10.11646/zootaxa.1175.1.1
Dick R.P. 1997. Soil enzyme activities as integrative indicators of soil health. In: Pankhurst C.E., Doube B.M., Gupta V.V. (Eds.): Biological indicators of soil health. CAB International. P. 121–156.
Dobrovolskiy G.V., Nikitin E.D. 1990. Soil functions in biosphere and ecosystems (Ecological significance of soils). Moscow: Nauka. 261 p. [In Russian]
Dobrovolskiy G.V., Chernov I.U. (Eds). 2011. Role of soil in formation and conservation of biological diversity. Moscow: KMK Scientific Press Ltd. 273 p. [In Russian]
Dobrovolskiy G.V. (Ed.). 2012. Soils of reserves and national parks of Russian Federation. Moscow: NIA-Nature – InfoSphere. 478 p. [In Russian]
Dominguez J., Edwards C.A. 2011. Relationship between composting and vermicomposting. In: Edwards C.A., Arancon N.Q., Sherman R. (Eds.): Vermiculture Technology – Earthworms, Organic Wastes, and Environmental Management. Boca Raton: CRC Press. P. 27–40.
Edwards C.A., Bohlen P.J. 1996. Biology and Ecology of Earthworms. London: Chapman and Hall. 426 p.
Egorov V.V., Ivanova E.N., Fridland V.M. 1977. Classification and diagnostics of soils of the USSR. Moscow: Kolos. 224 p. [In Russian]
Fiapshev B.Kh. 1996. Alpine soils in the central part of the North Caucasus (Kabardino-Balkaria and adjacent territories). Nalchik: Publishing House of Kabardino-Balkari State Agricultural Academy. 135 p. [In Russian]
Frontier S. 1985. Diversity and structure in aquatic ecosystems. Oceanography and Marine Biology: An Annual Review 23: 253–312.
Galstyan A.Sh. 1974. Enzymatic activity of soils in Armenia. Yerevan: Aiastan. 275 p. [In Russian]
Gaponyuk E.I., Malakhov S.V. 1985. Complex system of indicators of soil ecological monitoring. In: Proceedings of 4th All-Union Conference. Obninsk: Gidrometeoizdat. P. 3–10. [In Russian]
Gebremedihin K.M., Birhane E., Tadesse T., Gbrewahid H. 2018. Restoration of degraded drylands through exclosures enhancing woody species diversity and soil nutrients in the highlands of Tigray, Northern Ethiopia. Nature Conservation Research 3(1): 1–20. DOI: 10.24189/ncr.2018.001
Gilyarov M.S. 1975. Consideration of large soil invertebrates (mesofauna). In: Methods of soil-zoological studies. Moscow: Nauka. P. 12–29. [In Russian]
Jaccard P. 1901. Distribution de la flore alpine dans le Bassin des Dranses et dans quelques regions voisines. Bulletin de la Societe Vaudoise des Sciences Naturelles 37: 547–549.
Hartley R.V.L. 1928. Transmission of information. Bell System Technical Journal 7(3): 535–563. DOI: 10.1002/j.1538-7305.1928.tb01236.x
Kazeev K.Sh. 2009. Geographical regularities of enzymatic activity changes in soils of different natural zones of the Western part of the North Caucasus. In: Soil and flora of mountain areas. Moscow: KMK Scientific Press Ltd. P. 30–32. [In Russian]
Kazeev K.Sh., Kolesnikov S.I. 2012. Biological diagnostics of soils: methodology and research methods. Rostov-on-Don: Publisher of Southern Federal University. 258 p. [In Russian]
Kazeev K.Sh., Kolesnikov S.I., Valkov V.F. 2004. Biology of soils of Southern Russia. Rostov-on-Don: Centre of Valeology of Russian Higher Education Institutions. 350 p. [In Russian]
Kazeev K.Sh., Ovdienko R.V., Kolesnikov S.I., Valkov V.F. 2003. Features of distribution of microorganisms in mountain-meadow soils of the Caucasian Biosphere Reserve. University News. North-Caucasian Region. Natural Sciences Series 2: 82–84. [In Russian]
Kelemen A., Török P., Valkó O., Deák B., Miglécz T., Tóth K., Ölvedi T., Tóthmérész B. 2014. Sustaining recovered grasslands is not likely without proper management: vegetation changes and largescale evidences after cessation of mowing. Biodiversity and Conservation 23(3): 741–751. DOI 10.1007/s10531-014-0631-8
Khaziev F.Kh. 1982. Systematic-ecological analysis of enzymatic activity of soils. Moscow: Nauka. 203 p. [In Russian]
Khaziev F.Kh. 2011. Soil and biodiversity. Russian Journal of Ecology 42(3): 199–204. DOI: 10.1134/S1067413611030088
Kizilova A.K., Stepanov A.L., Makarov M.I. 2006. Biological activity of alpine mountain-meadow soils in the Teberda Reserve. Eurasian Soil Science 39(1): 67–70. DOI: 10.1134/S1064229306010091
Komac B., Domenech M., Fanlo R. 2014. Effects of grazing on plant species diversity and pasture quality in subalpine grasslands in the eastern Pyrenees (Andorra): implications for conservation. Journal for Nature Conservation 22(3): 247–255. DOI: 10.1016/j.jnc.2014.01.005
Koptsik S.V., Koptsik G.N., Livantsova S.Yu., Berezina N.A., Vakhrameeva M.G. 2003. Analysis of the Relationship between Soil and Vegetation in Forest Biogeocenoses by the Principal Component Method. Russian Journal of Ecology 34(1): 34–42. DOI: 10.1023/A:1021862921242
Korzeniak J. 2009. Murawy bliźniczkowe w Bieszczadzkim Parku narodowym – ocena stanu zachowania siedliska i zmian składu gatukowego zbiorowisk. Roczniki Bieszczadzki 17: 217–242.
Krivolutskiy D. A. 1994. Mesofauna in ecological monitoring. Moscow: Nauka. 269 p. [In Russian]
Li W., Zhang R., Liu S., Li W., Li J., Zhou H., Knops J. 2018. Effect of loss of plant functional group and simulated nitrogen deposition on subalpine ecosystem properties on the Tibetan Plateau. Science of the Total Environment 631–632: 289–297. DOI: 10.1016/j.scitotenv.2018.02.287
Lochon I., Colace M., Devaux C., Grigulis K., Rettinger R., Lavorel S. 2018. Taxonomic and functional facets of the resilience to management of mown subalpine grasslands. Applied Vegetation Science 21(4): 636–646. DOI: 10.1111/avsc.12392
Meshcheryakova E.N., Berman D.I. 2014. The cold hardiness and geographic distribution of earthworms (Oligochaeta, Lumbricidae, Moniligastridae). Zoologicheskii Zhurnal 93(1): 53–64. [In Russian]
Mirkin B M., Rozenberg G.S., Naumova L.G. 1989. Dictionary of definitions and terms of current phytocenology. Мoscow: Nauka. 223 p. [In Russian]
Molchanov E.N. (Ed.). 1990. Soil map of Kabardino-Balkaria ASSR. Novosibirsk: Roskartografia.
Nannipieri P., Kandeler E., Ruggiero P. 2002. Enzyme activities and microbiological and biochemical processes in soil. In: R.G. Burns, R.P. Dick, M. Dekker (Eds.): Enzymes in the Environment. New York: CRC Press. P. 1–34.
Niedrist G., Tasser E., Bertoldi G., Chiesa S.D., Obojes N., Egarter-Vigl L., Tappeiner U. 2016. Down to future: Transplanted mountain meadows react with increasing phytomass or shifting species composition. Flora 224: 172–182. DOI: 10.1016/j.flora.2016.07.013
Onipchenko V.G., Vertelina O.S., Makarov M.I. 1998. Spatial heterogeneity of high altitude phytocenoses and soil properties. Pochvovedenie 6: 689–695. [In Russian]
Onipchenko V.G., Thompson K. 2002. Alpine Vegetation of the Teberda Reserve, the Northwestern Caucasus. Vol. 130. Zürich: Geobotanisches Institut ETH, Stiftung Rübel. 168 p.
Pavlov V.N., Onipchenko V.G., Lomaeva T.G., Salpagarov A.D. 2005. Environmental studies mountains of the Teberda Nature Reserve at the present stage. Proceedings of the Teberda State Biosphere Reserve 30: 9–19. [In Russian]
Perel T.S. 1979. Range and regularities in the distribution of the earthworms of the USSR. Moscow: Nauka. 272 p. [In Russian]
Peterson N.B. 1967. The soil degydrogenase activity as an action of its microflora activity. Microbiology 36(3): 518–525. [In Russian]
Pickering C.M., Barros A. 2015. Using functional traits to assess the resistance of subalpine grassland to trampling by mountain biking and hiking. Journal of Environmental Management 164: 129–136. DOI: 10.1016/j.jenvman.2015.07.003
Pielou E.C. 1975. Ecological Diversity. New York: John Wiley and Sons. 165 p.
Polivanova N.N. 1990. Teberda Reserve. In: Reserves of the USSR. Nature Reserves of the Caucasus. Moscow: Mysl. P. 10–28. [In Russian]
Portenier N.N. 1988. Floristic finds in the Cherek-Bezengi river basin (North Caucasus, KBASSR). Botanichesky Zhurnal 73(2): 1756–1760. [In Russian]
Rapoport I.B. 2008. High-zone distribution of earthworms of the Kabardino-Balkaria State High-Mountain Reserve (Central Caucasus). In: Proceedings of 15th All-Union Conference on Soil Zoology. Moscow: KMK Scientific Press Ltd. P. 74–76. [In Russian]
Rapoport I.B. 2012. Ecology and horology of earthworms (Oligochaeta, Lumbricidae) of Kabardino-Balkaria State High-Mountain Reserve (Central Caucasus). Bulletin of Moscow Society of Naturalists 117(2): 65–71. [In Russian]
Rapoport I.B. 2013. Vertical distribution of earthworms (Oligochaeta, Lumbricidae) in the central part of the North Caucasus. Zoologicheskii Zhurnal 92(1): 3–10. [In Russian]
Razumov V.V. 1986. Variability of soil properties in subalpine ecosystems. Proceedings of the High-Mountain Geophysical Institute 64: 87–98. [In Russian]
Razumov V.V., Portenier N.N., Makhiev M.T. 1990. Soil of Bezengi сamp in Kabardino-Balkaria State High-Mountain Reserve. In: Alpine ecosystem under human influence. Proceedings of the High-Mountain Geophysical Institute 79: 84–99. [In Russian]
Red Data Book of the Russian Federation (plants and fungi). Moscow: KMK Scientific Press Ltd., 2008. 855 p. [In Russian]
Schmidt A.N., Li Y.X., Tang Y. 2017. Unintended side effects of conservation: a case study of changing land use in Jiuzhaigou Sichuan, China. Mountain Research and Development 37(1): 56–65.
Shannon C.E. 1948. A Mathematical Theory of Communication. Bell System Technical Journal 27(3): 379–423. DOI: 10.1002/j.1538-7305.1948.tb01338.x
Shennikov A.P. 1950. Plant ecology. Moscow: Sovetskaya Nauka. 375 p. [In Russian]
Shkhagapsoev S.Kh., Kirginov G.Kh. 2006. Flora of the Kabardino-Balkaria State High-Mountain Reserve and its analysis. Nalchik: Elbrus. 245 p. [In Russian]
Simpson E.H. 1949. Measurement of diversity. Nature 163: 688. DOI: 10.1038/163688a0
Soils of Kabardino-Balkaria ASSR and recommendations for their use. Nalchik: SevKavNIIGiprozem, 1984. 201 p. [In Russian]
Sokolov V.E., Tembotov A.K. 1989. Vertebrates of the Caucasus. Mammals. Insectivores. Moscow: Nauka. 547 p. [In Russian]
Stojanović M., Karaman S. 2005. Further contribution to knowledge of the earthworm of Šumadija (Serbia). Archives of Biological Sciences 57(2): 127–132. DOI: 10.2298/ABS0502127S
Striganova B.R. 1999. The structure and functions of soil animal populations. In: The structure-functional role of soil in biosphere. Moscow: GEOS. P. 135–143. [In Russian]
Striganova B.R., Emets V.M., Starodubtseva E.A., Emets N.S. 2001. The recent trend of the biodiversity dynamic of biotic communities in forest-steppe oak forests. Biology Bulletin 28(5): 508–516. DOI: 10.1023/A:1016752429044
Syers J.K., Springett J.A. 1984. Earthworms and soil fertility. Plant and Soil 76(1): 93–104. DOI: 10.1007/BF02205570
Theurillat J.P., Felber F., Geissler P., Gobat J.M., Fierz M., Fischlin A., Kupfer P., Schlussel A., Velutti C., Zhao G.F. 1998. Sensitivity of Plant and Soils Ecosystems of the Alps to Climate Change. In: Cebon P., Dahinden U., Davies H., Imboden D., Jaeger C. (Eds.): Views from the Alps: Regional Perspectives on Climate Change. Cambridge: MIT Press. P. 225–308.
The PlantList. 2018. The PlantList. Version 1.1. Available from:
Tsepkova N.L. 2007. Antropogenic dynamic of high mountain meadows of the Central Caucasus. Proceedings of the Samara Scientific Centre of RAS 9(4): 919–925. [In Russian]
Tsepkova N.L. 2011. Meadow communities in Cherek-Bezengi canyon (Kabardino-Balkaria State High-Mountain Reserve). Proceedings of the Kabardino-Balkaria Scientific Centre of RAS 6: 57–64. [In Russian]
Tsepkova N.L. 2016. The syntaxonomy of the mesophilous meadows of the Central Caucasus (within the Kabardino-Balkaria Republic). Proceedings of the Ural Scientific Centre of RAS 4: 62–68. [In Russian]
Uligova T.S., Gorobtsova O.N., Tsepkova N.L. Rapoport I.B., Gedgafova F.V., Tembotov R.Kh. 2016. Ecologo-biological characteristic of natural steppe biogeocenoses in the Central Caucasus (the Terskiy variant of vertical zonation, Kabardino-Balkaria). Povolzhskiy Journal of Ecology 3: 330–340. [In Russian]
Uligova T.S., Gorobtsova O.N., Tsepkova N.L., Rapoport I.B., Gedgafova F.V., Tembotov R.Kh. 2017. Ecological and biological studies in the haplic chernozems pacnic soils area in the Central Caucasus (Kabardino-Balkaria). Biological Communications 62(4): 244–255. DOI: 10.21638/11701/spbu03.403
Valkov V.F., Kazeev K.Sh., Kolesnikov S.I. 1999. Methodology of studies on soil biological activity exemplified by the North Caucasus. Scientific Thought of Caucasus 1: 32–37 [In Russian]
Volokitin M.P. 2007. On the relationship of soil and vegetation in the National Natural Park «Chavash Varmane». Proceedings of the Samara Scientific Centre of RAS 9(1): 38–46. [In Russian]
Volokitin M.P. 2012. Mountain-meadow soils of the Central Caucasus and the influence of vegetation on their formation. Proceedings of the Samara Scientific Centre of RAS 14(5): 36–44. [In Russian]
Vsevolodova-Perel T.S. 1988. Distribution of earthworms in the North of the Palearctic (within the USSR). In: Soil biology in Northern Europe. Moscow: Nauka. P. 84–103. [In Russian]
Vsevolodova-Perel T.S. 1997. Earthworms of Russian fauna. Moscow: Nauka. 102 p. [In Russian]
Zalikhanov M.Ch. (Ed.). 2018. Red Data Book of Kabardino-Balkaria Republic. Nalchik: Pechatnyi dvor. 486 p. [In Russian]
Zalikhanov M.Ch., Kolomyts E.G., Sharaya L.S., Tsepkova N.L., Surovaya N.A. 2010. High-Mountain Geoecology in the models. Moscow: Nauka. 487 p. [In Russian]
Zvyagintsev D.G. 1978. Soil biological activity and the estimation scales for some indicators. Pochvovedenie 6: 48–54. [In Russian]