Ecological and biological characteristics of Betula pendula in the conditions of urban environment

Keywords: pollution; urban environments; leaf blade; male catkins.

Abstract

This study focused on the influence of polluted environment on various indicators of Betula pendula Roth and their applicability to the bioindication of the condition of urban environments in one of the largest industrial cities of Ukraine in the steppe zone, namely Kryvyi Rih. Our investigations have been carried out for three years (2016–2018) in eight B. pendula plantations exposed to different levels of aerotechnogenic loading: to a low pollution level – in Kryvyi Rih Botanical Garden of the National Academy of Sciences of Ukraine (control), Poliana Kazok Square and Heroiv ATO Park, to an average pollution level – along three highways with heavy traffic and those exposed to a high pollution level – near the enterprises of Private JSC ‘Northern Iron Ore Dressing Works’(Northern GZK) and Public JSC ‘ArcelorMittal Kryvyi Rih’. Morphometric, anatomical and statistical methods were used to identify the most sensitive indicators of the impact of air pollutants. As a result of this research, changes associated with greater level of technogenic pollution were revealed in the morphological and anatomical parameters of the leaf blade, namely: reduction in the length of the petiole to 14.3%, in the length of the leaf blade to 8.4% and its width to 12.8%; a decrease in length, width and area of the stomata up to 29.4%, 25.9%, 48.1%, respectively; an increase in thickness of the leaf blade to 23.0% and its tissues, as well as the stomata density per 1 mm2 of the leaf to 47.3%. We also registered a decrease in the length of male catkins to 7.4% and an increase in their width to 13.7% associated with greater environmental pollution. The maximum and minimum values of the indicators were recorded near the mining and processing works and close to metallurgical plants. In addition, in order to determine the most sensitive indicators of B. pendula response to urban pollution, we carried out a comparative analysis of all the studied parameters and those, the results of which were published earlier. As a result of this analysis, these indicators were ranked according to the level of differences in relation to the control values in decreasing order: differences in 1.5 and more times in comparison with the control – seed germination, curved leaf apex, fluctuating asymmetry, crown volume, pollen viability, the amount of abnormal pollen, vital state of trees, seed quality, crown area; 25–50% differences from control – stomata area, thickness of the lower epidermis, stomata density on leaf blade, seed productivity, pollen fertility, width of fruit (female) catkins, number of scales in fruit (female) catkins, thickness of palisade parenchyma, tree height, stomata length, pollen tube length, trunk diameter at the height of 1.3 m, thickness of the upper epidermis, stomata width; a 10–24% change in indicators – leaf thickness, length of fruit (female) catkin petiole, weight of 1000 seeds, leaf petiole length, male catkin width, leaf blade width, fruit (female) catkin length; the differences from control are less than 10% – the thickness of the spongy parenchyma, the polar axis of pollen, the leaf length, the equatorial diameter of pollen, the length of male catkins and the purity of the seeds.

References

Aguraijuja, K., Klõšeiko, J., Ots, K., & Lukjanova, A. (2015). Effect of wood ash on leaf and shoot anatomy, photosynthesis and carbohydrate concentrations in birch on a cutaway peatland. Environmental Monitoring and Assessment, 187, 444–456.

Alagić, S. Č., Šerbula, S. S., Tošić, S. B., Pavlović, A. N., & Petrović, J. V. (2013). Bioaccumulation of arsenic and cadmium in birch and lime from the bor region. Archives of Environmental Contamination and Toxicology, 65(4), 671–682.

Augustaitis, A., Sopauskiene, D., & Bauziene, I. (2010). Direct and indirect effect of regional air pollution on tree crown defoliation. Baltic Forestry, 16(1), 23–34.

Avdashkova, L. P., & Tyulkova, E. G. (2017). Adaptivnye izmeneniya berezy povisloy Betula pendula i klena ostrolistnogo Acer platanoides v tekhnogennykh usloviyakh [Adaptive changes in the birch trees Betula pendula and the maple Acer platanoides in anthropogenic conditions]. Izvestiya Gomelskogo Gosudarstvennogo Universiteta Imeni F. Skoriny, 105, 21–26 (in Russian).

Balasooriya, B. L. W. K., Samson, R., Mbikwa, F., Vitharana, U. W. A., Boeckx, P., & Van Meirvenne, M. (2009). Biomonitoring of urban habitat quality by anatomical and chemical leaf characteristics. Environmental and Experimental Botany, 65(2), 386–394.

Barykina, P. P, Veselova, T. D., Devyatoe, A. G., Dzhalilova, K. K., Ilina, G. M., & Chubatova, N. V. (2000). Osnovy mikrotekhnicheskikh issledovaniy v botanike [Fundamentals of microtechnical research in botany]. Izdatelstvo Kafedry Vysshikh Rasteniy Biologicheskogo Fakulteta Moskovskogo Gosudarstvennogo Universiteta, Moscow (in Russian).

Bednařova, E., & Kučera, J. (2011). Monitoring the damage to epicuticular waxes at silver birch (Betula pendula Roth.) in the changing air pollution spectrum of the ore mountains. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 59(5), 9–16.

Belaeva, T. N., & Butenkova, A. N. (2018). Comparative analysis of the leaf anato­my of Echinacea purpurea and E. pallida. Biosystems Diversity, 26(2), 77–84.

Borgulat, J., Mętrak, M., Staszewski, T., Wiłkomirski, B., & Suska-Malawska, M. (2018). Heavy metals accumulation in soil and plants of Polish peat bogs. Polish Journal of Environmental Studies, 27(2), 1–8.

Brown, M. T., & Wilkins, D. A. (1986). The effects of zinc on germination, survi­val and growth of Betula seed. Environmental Pollution Series A, Ecological and Biological, 41(1), 53–61.

Brygadyrenko, V. V. (2015). Community structure of litter invertebrates of forest belt ecosystems in the Ukrainian steppe zone. International Journal of Environmental Research, 9(4), 1183–1192.

Butkus, D., & Baltrėnaitė, E. (2007). Transport of heavy metals from soil to Pinus sylvestris L. and Betula pendula trees. Ekologija, 53(1), 29–36.

Butnik, A. A., & Timchenko, O. V. (1987). Stroenie epidermy listyev vidov semey­stva Chenopodiaceae [The structure of the leaf epidermis of species of the fa­mily Chenopodiaceae]. Botanicheskiy Zhurnal, 74(8), 1021–1030 (in Russian).

Buxtiyarov, V. P. (2005). Entsyklopediya Kryvorizhzhya [Encyclopedia of Kryvyi Rig area]. Kryvyi Rih (in Ukrainian).

Cerceau-Larrival, M. T., Cauneau-Pigot, A., Bocquel, C., Carbonnier-Jarreau, M. С., Derouet, L., & Verhille, A. М. (1994). Elemental analysis of pollen grain surface: Relation to allergenic character and use as a pollution marker. Journal of Trace and Microprobe Techniques, 12, 37–50.

Cuinica, L. G., Abreu, I., Gomes, C. R., & Gomes Esteves da Silva, J. C. (2013). Exposure of Betula pendula Roth pollen to atmospheric pollutants CO, O3 and SO2. Grana, 52(4), 299–304.

Czaja, M., Kołton, A., Baran, A., Muszyńska, E., & Muras, P. (2016). Physiological respon­ses of Betula pendula Roth growing in polluted areas. Ecological Questions, 22, 39–46.

Dadea, C., Casagrande, S., La Rocca, N., Mimmo, T., Russo, A., & Zerbe, S. (2016). Heavy metal accumulation in urban soils and deciduous trees in the city of Bolzano, N Italy. Waldökologie, Landschaftsforschung und Naturschutz Heft, 15, 35–42.

Dmuchowski, W., Gozdowski, D., Brągoszewska, P., Baczewska, A. H., & Su­wara, I. (2014). Phytoremediation of zinc contaminated soils using silver birch (Betula pendula Roth). Ecological Engineering, 71, 32–35.

Dobrowolska, I., Kurczynska, E. U., & Dmuchowski, W. (2001). Anatomy of abscission zone of Betula pendula (Roth.) leaves from trees growing under different levels of pollution. Dendrobiology, 46, 13–19.

Dzierżanowski, K., & Gawroński, S. W. (2011). Use of trees for reducing particulate matter pollution in air. Challenges of Modern Technology, 184, 69–73.

Egorova, N. N., & Kulagin, A. A. (2008). Anatomicheskie i morfologicheskie oso­bennosti assimilyatsionnogo apparata i provodyashchikh korney drevesnykh rasteniy v ekstremalnykh lesorastitelnykh usloviyakh [Anatomical and morphological features of the assimilation apparatus and the conducting roots of woody plants in extreme forest conditions]. Izvestiya Samarskogo Nauchnogo Tsentra RAN, 10(2), 310–324 (in Russian).

Ekologichnyj pasport mista Kryvogo Rogu (2017) [Ecological passport of the city of Kryvyi Rih]. Kryvyi Rih (in Ukrainian).

Fedorovskiy, V. D., & Mazur, A. E. (2007). Drevesnye rasteniya Krivorozhskogo botanicheskogo sada: Itogi introduktsii (za 25 let) [Woody plants of the Krivoy Rog Botanical Garden: the results of the introduction (at 25 years)]. Prospekt, Donetsk (in Russian).

Fostad, O., & Pedersen, P. A. (1997). Vitality, variation, and causes of decline of trees in Oslo center (Norway). Journal of Arboriculture, 23(4), 155–165.

Franiel, I., & Babczyńska, A. (2011). The growth and reproductive effort of Betu­la pendula Roth in a heavy-metals polluted area. Polish Journal of Environmental Studies, 20(4), 1097–1101.

Franiel, I., & Blocka, A. (2008). The seeds quality of Betula pendula Roth and Betula oscura Kotula from semi-natural and anthropogenic habitats. Pakistan Journal of Biological Sciences, 11, 1455–1460.

Franiel, I., & Więski, K. (2005). Leaf features of silver birch (Betula pendula Roth). Variability within and between two populations (uncontaminated vs Pb-contaminated and Zn-contaminated site). Trees, 19(1), 81–88.

Gallagher, F. J., Pechmann, I., Isaacson, B., & Grabosky, J. (2011). Morphological variation in the seed of gray birch (Betula populifolia): The effects of soil-metal contamination. Urban Habitats, 6(1), 1–11.

Goransson, A. (1994). Growth and nutrition of small Betula pendula plants at diffe­rent relative addition rates of manganese. Tree Physiology, 14(4), 375–388.

Ha, J., & Martinez, H. (2018). Influence of environmental pollution on leaf pro­perties of urban trees in China and USA: A comparative study using stomatal density. Asian Journal of Plant Science and Research, 8(6), 1–7.

Hoshika, Y., Watanabe, M., Inada, N., Mao, Q., & Koike, T. (2013). Photosynthetic response of early and late leaves of white birch (Betula platyphylla var. japoni­ca) grown under free-air ozone exposure. Environment Pollution, 182, 242–247.

Hrdlička, P., & Kula, E. (1998). Element content in leaves of birch (Betula verrucosa Ehrh.) in an air polluted area. Trees, 13, 68–73.

Hrdlička, P., & Kula, E. (2004). Changes in the chemical content of birch (Betula pendula Roth) leaves in the air polluted Krusne hory mountains. Trees, 18(2), 237–244.

Hrdlička, P., & Kula, E. (2009). The content of total sulphur and sulphur forms in birch (Betula pendula Roth) leaves in the air-polluted Krusne hory mountains. Trees, 23(3), 531–538.

Hrdlička, P., & Kula, E. (2011). Changes in element content of birch leaves (Betu­la pendula Roth) in polluted air. Polish Journal of Environmental Studies, 20(3), 661–670.

Janjić, N., Hasanagić, D., & Maksimović, T. (2017). Stomatal apparatus response of Tilia cordata (Mill.) and Betula pendula (Roth.) to air quality conditions in the city of Banja Luka (Bosnia and Herzegovina). Biologia Serbica, 39(2), 9–16.

Jochner, S., Höfler, J., Beck, I., Göttlein, A., Ankerst, D. P., Traidl-Hoffmann, C., & Menzel, A. (2013). Nutrient status: A missing factor in phenological and pollen research? Journal of Experimental Botany, 64(7), 2081–2092.

Jochner, S., Markevych, I., Beck, I., Traidl-Hoffmann, C., Heinrich, J., & Menzel, A. (2015). The effects of short- and long-term air pollutants on plant phenol­logy and leaf characteristics. Environmental Pollution, 206, 382–389.

Kalaev, V. N., Karpova, S. S., & Artyukhov, V. G. (2010). Cytogenetic characteris­tics of weeping birch (Betula pendula Roth) seed progeny in different ecological conditions. Bioremediation, Biodiversity and Bioavailability, 4(1), 77–83.

Kardel, F., Wuyts, K., Babanezhad, M., Wuytack, T., Adriaenssens, S., & Samson, R. (2012). Tree leaf wettability as passive bio-indicator of urban habitat quality. Environmental and Experimental Botany, 75, 277–285.

Khromykh, N., Lykholat, Y., Shupranova, L., Kabar, A., Didur, O., Lykholat, T., & Kulbachko, Y. (2018). Interspecific differences of antioxidant ability of introduced Chaenomeles species with respect to adaptation to the steppe zone conditions. Biosystems Diversity, 26(2), 132–138.

Kicińska, A., & Gruszecka-Kosowska, A. (2016). Long-term changes of metal contents in two metallophyte species (Olkusz area of Zn-Pb ores, Poland). Environmental Monitoring and Assessment, 188, 339.

Kirkey, F. M., Matthews, J., & Ryser, P. (2012). Metal resistance in populations of red maple (Acer rubrum L.) and white birch (Betula papyrifera Marsh.) from a metal-contaminated region and neighbouring non-contaminated regions. Environmental Pollution, 164, 53–58.

Kitao M., Lei, T. Т., & Koike, T. (1999). Effects of manganese in solution culture on the growth of five deciduous broad-leaved tree species with different successional characters from Northern Japan. Photosynthetica, 36(1), 31–40.

Kitao, M., Lei, T. Т., & Koike, T. (1997). Effects of manganese toxicity on photosynthesis of the white birch (Betula platyphylla var. japonica) seedlings. Phy­siologia Plantarum, 101, 249–256.

Kolon, K., Ruczakowska, A., Samecka-Cymerman, A., & Kempers, A. J. (2015). Brachythecium rutabulum and Betula pendula as bioindicators of heavy metal pollution around a chlor-alkali plant in Poland. Ecological Indicators, 52, 404–410.

Korshykov, I. I., & Petrushkevych, Y. M. (2017). Zhyttyezdatnist Betula pendula Roth v urbosystemi m. Kryvoho Rohu [Viability of Betula pendula Roth. in urbansystem of Kryvyi Rih]. Introduktsiya Roslyn, 1, 28–35 (in Ukrainian).

Kovacic, S., & Nikolic, T. (2005). Relations between Betula pendula Roth. (Betulaceae) leaf morphology and environmental factors in five regions of Croatia. Acta Biologica Cracoviensia Series Botanica, 47(2), 7–13.

Kozlov, M. V., Wilsey, B. J., Koricheva, J., & Haukioja, E. (1996). Fluctuating asymmetry of birch leaves increases under pollution impact. British Ecological Society, 33(6), 1489–1495.

Krutul, D., Zielenkiewicz, T., Radomski, A., Zawadzki, J., Antczak, A., & Drożdżek, M. (2014). Impact of the environmental pollution originated from sulfur mining on the chemical composition of wood and bark of birch (Betula pendula Roth.). Ann. WULS - SGGW, Forestry and Wood Technology, 88, 117–125.

Kurteva, M., & Stambolieva, K. (2007). Acer pseudoplatanus L., Acer platanoi­des L. and Betula pendula Roth. as bioindicators of urban pollution in Sofia. Silva Balcanica, 8(1), 32–46.

Lykholat, Y. V., Khromykh, N. O., Pirko, Y. V., Alexeyeva, A. A., Pastukhova, N. L., & Blume, Y. B. (2018). Epicuticular wax composition of leaves of Tilia L. trees as a marker of adaptation to the climatic conditions of the steppe Dnieper. Cytology and Genetics, 52(5), 323–330.

Mäenpää, M., Riikonen, J., Kontunen, S., Matti Rousi, S., & Oksanen, E. (2011). Vertical profiles reveal impact of ozone and temperature on carbon assimilation of Betula pendula and Populus tremula. Tree Physiology, 31(8), 808–818.

Mcdonald, J. H. (2014). Handbook of biolological statistics. 3rd ed. Baltimore.

Mleczek, M., Goliński, P., Krzesłowska, M., Gąsecka, M., Magdziak, Z., Rutkowski, P., Budzyńska, S., Waliszewska, B., Kozubik, T., Karolewski, Z., & Niedzielski, P. (2017). Phytoextraction of potentially toxic elements by six tree species growing on hazardous mining sludge. Environmental Science and Pollution Research International, 24(28), 22183–22195.

Molotkovskiy, G. K. (1935). Izucheniya sostoyaniya ustits metodom tsellyuloz­nykh otpechatkov [Study of stomatal shape using cellulosic prints]. DAN SSSR, 9(8), 19–25 (in Russian).

Nikolaychuk, A. M. (2017). Osobennosti anatomicheskoy struktury listyev dreves­nykh rasteniy, proizrastayushchikh vblizi tsementnykh zavodov Belarusi [Features of the anatomical structure of the leaves of woody plants growing near cement plants in Belarus]. Vestnik VDU, Biyalogiya, 95, 27–34 (in Russian).

Nock, C. A., Paquette, A., Follett, M., Nowak, D. J., & Messier, C. (2013). Effects of urbanization on tree species functional diversity in eastern North America. Ecosystems, 16(8), 1–11.

Oksanen, E. (2003). Responses of selected birch (Betula pendula Roth) clones to ozone change over time. Plant, Cell and Environment, 26, 875–886.

Oksanen, E., & Saleem, A. (1999). Ozone exposure results in various carry-over effects and prolonged reduction in biomass in birch (Betula pendula Roth). Plant, Cell and Environment, 22, 1401–1411.

Onete, M. P., Pop, O. G., Gruia, R. (2010). Plants as indicators of environmental conditions of urban spaces from central parks of Bucharest. Environmental Engineering and Management Journal, 9(12), 1637–1645.

Paakkonen, E., Gunthardt-Goerg, M. S., & Holopainen, T. (1998). Responses of leaf processes in a sensitive birch (Betula pendula Roth) clone to ozone combined with drought. Annals of Botany, 82, 49–59.

Paakkonen, E., Paasisalo, S., Holopainen, T., & Karenlampp, L. (1993). Growth and stomatal responses of birch (Betula pendula Roth.) clones to ozone in open-air and chamber fumigations. New Phytologist, 125, 615–623.

Pavlović, D., Pavlović, M., Marković, M., Karadžić, B., Kostić, O., Jarić, S., Mit­rovic, M., Gržetić, I., & Pavlovic, P. (2017). Possibilities of assessing trace metal pollution using Betula pendula Roth. leaf and bark. Experience in Serbia Journal of the Serbian Chemical Society, 82(6), 723–737.

Peltonen, P. A., Vapaavuori, E., & Julkunen-tiitto, R. (2005). Accumulation of phenolic compounds in birch leaves is changed by elevated carbon dioxide and ozone. Global Change Biology, 11(8), 1305–1324.

Petrova, S. T. (2011). Biomonitoring study of air pollution with Betula pendula Roth., from Plovdiv, Bulgaria. Ecologia Balkanica, 3(1), 1–10.

Petrova, S., Todorova, K., Dakova, M., Mehmed, E., Nikolov, B., Denev, I., Stratiev, M., Georgiev, G., Delchev, A., Stamenov, S., Firkova, L., Gesheva, N., Kadirova, D., & Velcheva, I. (2017). Photosynthetic pigments as parameters indicators of tree tolerance to urban environment (Plovdiv, Bulgaria). Ecologia Balkanica, 9(1), 53–62.

Petrova, S., Yurukova, L., & Velcheva, I. (2014). Possibilities of using deciduous tree species in trace element biomonitoring in an urban area (Plovdiv, Bulgaria). Atmospheric Pollution Research, 5(2), 196–202.

Petrushkevych, Y. M. (2018b). Vplyv promyslovykh umov na velychynu fluktuyu­choi asymetrii lystkovoi plastynky Betula pendula [Influence of industrial conditions on the fluctuating asymmetry magnitude of leaf blade of Betula pendula]. Naukovi Zapysky TNPU, Seria Biolohiya, 72, 82–89 (in Ukrainian).

Petrushkevych, Y. M. (2018а). Nasinnyeva produktyvnist ta posivni yakosti na­sinnya Betula pendula Roth. v nasadzhennyakh Kryvoho Rohu [Seed production and seed quality of Betula pendula Roth. in plantations of Kryvyi Rih]. Pytannya Stepovoho Lisoznavstva ta Lisovoi Rekultyvatsii Zemel, 47, 39–47 (in Ukrainian).

Petrushkevych, Y. M., & Korshykov, I. I. (2018). Morfo-fiziolohichna kharakte­rystyka pylku Betula pendula Roth v umovakh Kryvorizhzhya [Morpho-physiological characteristics of pollen Betula pendula Roth in the conditions of Kryvyi Rih area]. Introduktsiya Roslyn, 79, 58–66 (in Ukrainian).

Piotrowska, K., & Panek, E. (2012). Testing of selected phytoindicators for the environmental assessment of areas under various levels of pollution. Geomatics and Environmental Engineering, 6(4), 73–81.

Polyakov, A. K. (2009). Introduktsiya drevesnykh rasteniy v usloviyakh technogen­noy sredy [The introduction of woody plants in the conditions of technogenic environment]. Noulidzh, Donetskoe Otdelenie, Donetsk (in Russian).

Popova, E. I. (2018). Accumulation of heavy metals in birch and pine forest road­side phytocenoses in the south of Tyumen region. Biosystems Diversity, 26(3), 233–238.

Rehionalna dopovid pro stan navkolyshnoho pryrodnoho seredovyshcha v Dnipropetrovskiy oblasti za 2017 rik (2018) [Regional report on the state of the environment in Dnipropetrovsk region for 2017]. Dnipro (in Ukrainian).

Rey, А., & Jarvis, P. G. (1998). Long-term photosynthetic acclimation to increa­sed atmospheric CO2 concentration in young birch (Betula pendula) trees. Tree Physiology, 18, 441–450.

Riikonen, J., Holopainen, T., Oksanen, E., & Vapaavuori, E. (2005). Leaf photosynthetic characteristics of silver birch during three years of exposure to elevated concentrations of CO2 and O3 in the field. Tree Physiology, 25, 621–632.

Samecka-Cymerman, A., Kolon, K., & Kempers, A. (2009). Shot shoots of Betu­la pendula Roth as a bioindicators of urban environmental pollution in Wroclaw (Poland). Trees, 23, 923–929.

Serbula, S. M., Radojevic, A. A., Kalinovic, J. V., & Kalinovic, T. S. (2014). Indication of airborne pollution by birch and spruce in the vicinity of copper smelter. Environmental Science and Pollution Research, 21(19), 11510–11520.

Shevtsova, T., Brindza, J., Garkava, K., Ostrovsky, R., & Maltsov, I. (2012). Morphological characteristics of pollen Betula verrucosa Ehrh. (syn. B. pendula) depending on habitat. Conservation of plant diversity: International scientific symposium. Chişinău, Republic of Moldova. Pp. 44–54.

Shyam, S., Nath, K., & Singh, D. (2008). Harmful effects of air pollutants in biochemical parameters of plants. Research in Environment and Life Sciences, 1(2), 65–68.

Sklyarenko, А. V., & Bessonova, V. P. (2018). Accumulation of sulfur and gluta­thione in leaves of woody plants growing under the conditions of outdoor air pollution by sulfur dioxide. Biosystems Diversity, 26(4), 334–338.

Supuka, J., Feriancová, L., & Bihuňová, M. (2008). Leaf impact trends of silver birch (Betula pendula Roth.) by allochtonous elements at Nitra town urban Vegetation. Journal of Botany, Košice, 18, 37–49.

Šuškalo, N., Hasanagić, D., Topalić-Trivunović, L., Kukrić, Z., Samelak, I., Savić, A., & Kukavica, B. (2018). Antioxidative and antifungal response of woody species to environmental conditions in the urban area. Ecotoxicology, 27(8), 1095–1106.

Vasilev, B. R. (1988). Stroenie lista drevesnykh rasteniy razlichnykh klimatiches­kikh zon [Leaf structure of woody plants of different climatic zones]. Izda­tel’stvo LGU, Leningrad. Рр. 21–49 (in Russian).

Vostrikova, T. V. (2007). Instability of cytogenetic parameters and genome instability in Betula pendula Roth. Russian Journal of Ecology, 38(2), 80–84.

Waugh, N. D., Shukla, P. V., Tambe, S. B., & Ingle, S. T. (2006). Biological mo­nitoring of road side plants exposed to vehicular pollution in Jalgaon city. Journal Environment Biological, 27(2), 421–421.

Wulff, A., Anttonen, S., Pellinen, R., Savonen, E.-M., Sutinen, M.-L., Heller, W., Sandermann Jr., H., & Kangasjärvi, J. (1998). Birch (Betula pendula Roth.) responses to high UV-B radiation. Boreal Environment Research, 4, 77–88.

Wаrdlе, J. (1970). The ecology of Nothofagus solandri. 3. Regeneration. New Zealand Journal of Botany, 8(4), 571–608.

Zakharov, V. M., Baranov, A. S., Borisov, V. I., Valetskiy, A. V., Kryazheva, N. G., Chistyakova, E. K., & Chubinishvili, A. T. (2000). Zdorove sredy: Praktika otsenki [Environmental health: Evaluation practice]. Tsentr Ekologicheskoy Poli­tiki Rossii, Moscow (in Russian).

Zakrzewska, M., & Klimek, B. (2017). Trace element concentrations in tree leaves and lichen collected along a metal pollution gradient near Olkusz (Southern Poland). Bulletin of Environmental Contamination and Toxicology, 100(2), 245–249.

Published
2020-02-21
How to Cite
PetrushkevуchY. M., & KorshуkovI. I. (2020). Ecological and biological characteristics of Betula pendula in the conditions of urban environment . Regulatory Mechanisms in Biosystems, 11(1), 29-36. https://doi.org/10.15421/022004