Application of morphogeometric method estimation of fluctuating asymmetry of Acer pseudoplatanus L.

S. A. Prikhodko, Yu. A. Shtirts

Abstract


The possibility of using a morpho-geometric method for determining the indices of the fluctuating asymmetry of Асеr pseudoplatanus L. leaf for bioindication is evaluated. The material was collected on the roadside territories of motorways of the city of Donetsk with different traffic intensity. The values of the fluctuating asymmetry of A. pseudoplatanus leaf blade, grown in conditions of city roadside ecosystems, are increased with the increase in the transport load, obtained through Procrustean analysis of variance. The morphogeometric method for determining the fluctuating asymmetry showed greater sensitivity in comparison with the use of an index calculated by the normalizing formula based on measurements of individual bilateral features. It is expedient to carry out studies in which the task is to accumulate data on the dynamics of fluctuating asymmetry indices obtained by a morphogeometric method, with a view to the subsequent widespread application of this approach for bioindication and biomonitoring of the state of the environment.


Keywords


Acer pseudoplatanus; leaf blade; morpho-geometric indices; fluctuating asymmetry; directed asymmetry; bioindication

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References


Andreeva, M.V. (2007). Assessment of the state of the environment in plantations in zones of industrial emissions with the help of plant-indicators. St. Petersburg (in Russian).

Balandaykin, M.E. (2014). Variability of the complex of morphological features of the Betula pendula leaf plate under the influence of the phytopathological factor. Agro, 10-12, 46-48 (in Russian).

Baranov, S.G. (2014). The use of the morphometric method for determining the fluctuating asymmetry of Tilia cordata. Biosecurity and biosafety, VI, 10-17 (in Russian).

Baranov, S.G. (2016a). Phenogenetic aspect of the asymmetry of the Betula pendula Roth. Scientific bulletins. Series of Natural Sciences, 11(232), 35, 10-20 (in Russian).

Baranov, S.G. (2016b). Experience in using the MorfoJ program for testing phenotypic and genotypic variability (on the example of populations of Quercus robur). Ecological genetics, ХIV, 4, 3-13, doi:10.17816/ecogen 1443-13 (in Russian).

Baranov, S.G. (2016c). Use of a morpho-geometric method for determining the asymmetry of leaf blades of Acer platanoides. Journal of Natural Science Studies, 1(1), doi:10.12737/11646 (in Russian).

Baranov, S.G., Burdakova, N.E. (2015). Evaluation of the stability of development. Methodical approaches. Vladimir (in Russian).

Baranov, S.G., Gavrikov, D.E. (2008). Comparison of evaluation methods of fluctuating asymmetry in Betula pendula Roth leaf blades. Proceedings of International Scientific Conference ‘XXI Century Science’. Belgorod, Available from: http://www.rusnauka.com/14_APSN_2008/Ecologia/32522.doc.htm/ Accessed on 17.01.2018 (in Russian).

Baranov, S.G., Maleev, A.V. (2009). On the use of harmonic analysis in phenogenetic studies. Mathematical morphology, 8(3), 1-10 (in Russian).

Baranov, S.G., Zykov, I.E., Fedorova, L.V. (2015a). Asymmetry of Acer platanoides leaf blades: genotypic and phenotypic variability. Fundamental research, 7(4), 659-663 (in Russian).

Baranov, S.G., Zykov, I.E., Fedorova, L.V. (2015b). Environmental factors that affect the asymmetry of Acer platanoides leaf blades. Modern problems of science and education, 2(2), Available from: https://www.science-education.ru/ru/article/view?id=21581/ Accessed on 17.01.2018 (in Russian).

Bessonova, N.V. (2009). Use of the bioindication method for

assessing the ecological status of various regions in Khabarovsk. Forests of Russia in the 21st Century. St. Petersburg, 11-13 (in Russian).

Black-Samuelsson, S., Andersson, S. (2003). The effect of nutrient stress on developmental instability in leaves of Acer platanoides (Aceraceae) and Betula pendula (Betulaceae). American Journal of Botany, 90(8), 1107-1112, doi:10.3732/ajb.90.8.1107

Budilov, V.V., Isaykin, A.Yu. (2009). Fluctuating asymmetry of Arthropoda of biocenoses of right bank of Sura River. Actual problems of biology, ecology, methods of teaching and pedagogy. 45 Evseevskie readings: theses of reports of All-Russian Conference, Saransk, 10-13 (in Russian).

Bukharina, I.L., Povarnitsina, Т.М., Vedernikov, K.E. (2007). Ecological and biological features of woody plants in an urbanized environment. Izhevsk (in Russian).

Buzuk, G.N., Ershik, O.A., Kuzmicheva, N.A. (2007). Morphometry of medicinal plants. 3. Vaccinium myrtillus L.: the relationship between the size, shape and chemical composition of the leaves. Bulletin of Pharmacy, 2(36), 26-37 (in Russian).

Carpentero, E.R., Tabugo, S.R.M. (2014). Determining developmental instability via fluctuating asymmetry in the shell shape of Arctica islandica Linn. 1767 (ocean quahog). European J. of Zool. Res., 3(3), 1-7.

Cornelissen, T., Stiling, P. (2005). Perfect is best: low leaf fluctuating asymmetry reduces herbivory by leaf miners. Oecologia, 142(1), 46-56, doi:10.1007/s00442-004-1724-y

Cowart, N.M., Graham, J.H. (1999). Within- and among-individual variation in fluctuating asymmetry of leaves in the fig (Ficus carica L.). International Journal of Plant Sciences, 160(1), 116-121, doi:10.1086/314104

Drake, A.G., Klingenberg, C.P. (2010). Large-scale diversification of skull shape in domestic dogs: disparity and modularity. Am. Nat., 175, 289-301, doi:10.1086/650372

Druzhkina, T.A., Lebed, L.V. (2010). Study of bioindicative properties of tree species in the urban environment. Moscow (in Russian).

Ershik, O.A., Buzuk, G.N., Sozinov, O.V. (2009). Morphometry of the Comarum palustre: the relationship between the size, shape and chemical composition of the leaves. Bulletin of Pharmacy, 1(43), 13-27 (in Russian).

Fair, J.M., Breshearsa, D.D. (2005). Drought stress and fluctuating asymmetry in Quercus undulata leaves: confounding effects of absolute and relative amounts of stress? Journal of Arid Environments, 62(2), 235-249, doi:10.1016/j.jaridenv.2004.11.010

Gavrikov, D.Ye., Grechanyi, G.V. (1999). To the question of estimating the parameters of fluctuating asymmetry. Ecological and geographical problems of the Baikal region. Ulan-Ude, 108-113 (in Russian).

Gelashvili, D.B., Soldatov, E.N., Chuprunov, E.V. (2004). Measures of similarity and diversity in the evaluation of the fluctuating asymmetry of bilateral features. Povolzhsky Ecological Journal, 2, 132-143 (in Russian).

Gelashvili, D.B., Yakimov, V.N., Loginov, V.V., Yeplanova, G.V. (2004). Statistical analysis of fluctuating asymmetry in bilateral features of stepperunner Eremias arguta. Actual problems of herpetology and toxinology. Proceedings, 7, 45-59 (in Russian).

Givnish, T.J. (1978). Ecological aspects of plant morphology: Leaf form in relation to environment. Acta Biotheoretica (Supplement: Folia Biotheoretica no. 7), 27, 83-142.

Givnish, T.J. (1984). Leaf and canopy adaptations in tropical forests. Physiological ecology of plants of the wet tropics, 51-84.

Givnish, T.J. (1987). Comparative studies of leaf form: assessing the relative roles of selective pressures and phylogenetic constraints. New Phytologist, 106(s1), 131-160, doi:10.1111/j.1469-8137.1987.tb04687.x

Glukhov, A.Z., Shtirts, Yu.A. (2015). Characteristics of the shape asymmetry of leaf tip and base in Populus nigra L. under industrial dump conditions. Applied ecology and environmental research, 13(3), 819-831, doi:10.15666/aeer/1303_819831_

Glukhov, A.Z., Shtirts, Yu.A., Demkovich, A.E., Zhukov, S.P. (2011). Evaluation of the demonstration of fluctuating asymmetry of bilateral characteristics of the Acer pseudoplatanus L. leaf blade in the conditions of roadside ecosystems of an industrial city (on the example of Donetsk). Industrial, 90-96 (in Russian).

Glukhov, A.Z., Zhukov, S.P., Agurova, I.V., Prokhorova, S.I., Shtirts, Yu.A. (2012). Method of phytotesting of technogenic ecotopes. Patent of Ukraine 70512 UA, A01G7/00, N u201115376 (in Ukrainian).

Graham, J.H., Freeman, D.C., Emlen, J.M. (1993). Antisymmetry, directional asymmetry, and dynamic morphogenesis. Genetica, 89(1-3), 121-137, doi:10.1007/BF02424509

Graham, J.H., Shimizu, K., Emlen, J.M., Freeman, D.C., Merkel, J.

(2003). Growth models and the expected distribution of fluctuating asymmetry. Biological Journal of the Linnean Society, 80(1), 57-65, doi:10.1046/j.1095-8312.2003.00220.x

Gurtyak, A.A., Uglev, V.V. (2010). Assessment of the urban environment state with using Betula pendula as a bioindicator. Proceedings of Tomsk Polytechnic University, 317(1), 200-204 (in Russian).

Hódarf, J.A. (2002). Leaf fluctuating asymmetry of Holm oak in response to drought under contrasting climatic conditions. Journal of Arid Environments, 52(2), 233-243, doi:10.1006/jare.2002.0989

Isakov, V.N., Viskovatov, L.I., Leishovnik, Ya.Ya. (1984).

Investigation of leaf morphology by means of automation. Riga (in Russian).

Ivanović, A., Kalezić, M.L. (2010). Testing the hypothesis of morphological integration on a skull of a vertebrate with a biphasic life cycle: a case study of the alpine newt. J. Exp. Zool. B. Mol. Dev. Evol., 314, 527-538.

Jamniczky, H.A., Hallgrimsson, B. (2011). Modularity in the skull and cranial vasculature of laboratory mice: implications for the evolution of complex phenotypes. Evol. Dev., 13, 28-37, doi:10.1111/j.1525-142X.2010.00453.x

Kalyakina, R.G., Zhuravlev, A.S., Dmitriev, A.A. (2017). Influence of remoteness from the motor road on the asymmetry of Betula pendula leaf blade. Forest-2017: materials of the XVIII International Conference. Bryansk, 47, 113-116, (in Russian).

Kapranov, S.V. (1998). Motor transport, air and health. Lugansk (in Russian).

Khikmatulina, G.R. (2013). Comparative analysis of morphological parameters of woody plants leaves in urbanized environment. Kazan (in Russian).

Khuzina, G.R. (2010). Influence of the urban boundary on the morphometric parameters of the leaf blade Betula pendula Roth. Bulletin of the Udmurt University. Biology, 3, 53-57 (in Russian).

Klingenberg, C.P. (2003). Developmental instability as a research tool: using patterns of fluctuating asymmetry to infer the developmental origins of morphological integration. Developmental instability: causes and consequences, New York, 427-442.

Klingenberg, C.P. (2008). Morphological integration and developmental modularity. Ann. Rev. Ecol. Evol. Syst., 39, 115-132, doi:10.1146/annurev.ecolsys.37.091305.110054

Klingenberg, C.P. (2009). Morphometric integration and modularity in configurations of landmarks: tools for evaluating a-priori hypotheses. Evol. Dev., 11, 405-421, doi:10.1111/j.1525-142X.2009.00347.x

Klingenberg, C.P. (2010). Evolution and development of shape: integrating quantitative approaches. Nat. Rev. Genet., 11, 623-635.

Klingenberg, C.P. (2015). Analyzing fluctuating asymmetry with geometric morphometrics: concepts, methods, and applications. Symmetry, 7, 843-934, doi:10.3390/sym 7020843

Klingenberg, C.P., Barluenga, M., Meyer, A. (2002). Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution, 56, 1909-1920.

Klingenberg, C.P., Debat, V., Roff, D.A. (2010). Quantitative genetics of shape in cricket wings: developmental integration in a functional structure. Evolution, 64, 2935-2951.

Klingenberg, C.P., McIntyre, G.S. (1998). Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution, 52(5), 1363-1375.

Koroteeva, E.V., Veselkin, D.V., Kuyantseva, N.B., Chaschina, O.E. (2015). In the gradient of the effect of the Karabash copper smelter emissions, the size but not the fluctuating asymmetry of Betula pendula leaf blade is changed. Reports of Russian Academy of Sciences, 460(3), 364-367 (in Russian).

Kryazheva, N.G., Chistyakov, E.K., Zakharov, V.M. (1996). Stability analysis of silver birch development in conditions of chemical pollution. Ecology, 6, 441-444 (in Russian).

Laffont, R., Renvoise, E., Navarro, N., Alibert, P., Montuire, S. (2009). Morphological modularity and assessment of developmental processes within the vole dental row (Microtus arvalis, Arvicolinae, Rodentia). Evol. Dev., 11, 302-311, doi:10.1111/j.1525-142X.2009.00332.x

Laius, D.L., Gram, D.X., Katolikova, M.V., Yurtseva, A.O. (2009). Fluctuating asymmetry and random phenotypic variability in population studies: history, achievements, problems, prospects. Bulletin of St. Petersburg University, Biology, 3, 98-110 (in Russian).

Leung, B., Forbes, M.R. (1997). Modelling fluctuating asymmetry in relation to stress and fitness. Oikos, 78, 397-405.

Mal, T.K., Uveges, J.L., Turk, K.W. (2002). Fluctuating asymmetry as an ecological indicator of heavy metal stress in Lythrum salicaria. Ecological Indicators, 1(3), 189-195, doi:10.1016/S1470-160X(02)00004-3

Mandra, Yu.A., Eremenko, R.S. (2010). Bioindicative assessment of the environment state of Kislovodsk city based on the analysis of fluctuating asymmetry. Izvestiya of the Samara Scientific Center of the RAS, 12, 1(8), 1990-1994 (in Russian).

Mardia, K.V., Bookstein, F.L., Moreton, I.J. (2000). Statistical assessment of bilateral symmetry of shapes. Biometrika, 87, 285-300.

Migalina, S.V., Ivanova, L.A., Makhnev, A.K. (2009). Dimensions of the birch leaf as an indicator of its productivity far from the climatic optimum. Physiology of Plants, 56, 6, 948-953 (in Russian).

Møller, A.P. (1995). Leaf-mining insects and fluctuating asymmetry in elm Ulmus glabra leaves. Journal of Animal Ecology, 64(6), 697-707, doi:10.2307/5849

Møller, A.P. (1999). Elm, Ulmus glabra, leaf asymmetry and Dutch elm disease. Oikos, 85(1), 109-116, doi:10.2307/3546796

Møller, A.P., Swaddle, J.P. (1997). Asymmetry, developmental stability and evolution. Oxford.

Møller, A.P., van Dongen, S. (2003). Ontogeny of asymmetry and compensational growth in elm Ulmus glabra leaves under different environmental conditions. International Journal of Plant Sciences, 164(4), 519-526, doi:10.1086/374197

Niinemets, Ü., Portsmuth, A., Tobias, M. (2007). Leaf shape and venation pattern alter the support investments within leaf lamina in temperate species: a neglected source of leaf physiological differentiation. Funct. Ecol., 21, 28-40.

Niinemets, Ü., Kull, O., Tenhunen, J.D. (1999). Variability in leaf morphology and chemical composition as a function of canopy light environment in coexisting deciduous trees. International Journal of Plant Sciences, 160, 837-848.

Nizhegorodtsev, A.A. (2010). Pseudosymmetry of plant objects as a bioindication indicator: theoretical justification, evaluation automation, approbation. Nizhny Novgorod (in Russian).

Nizkiy, S.E., Sergeeva, A.S. (2012). Fluctuating asymmetry of Betula platypliylla leaves as an indicator of the ecological state of a residential area. Bulletin of the Krasnoyarsk State Agrarian University, 5, 221-223 (in Russian).

Opekunova, M.G. (2012). The use of woody plants in the geoecological monitoring of the state of technogenic ecosystems. Biological recultivation and monitoring of disturbed lands. Ekaterinburg, 184-190 (in Russian).

Palmer, A.R. (1994). Fluctuating asymmetry analyses: a primer. Developmental instability: its origins and evolutionary implications. Contemporary Issues in Genetics and Evolution, 2, 335-364, doi:10.1007/978-94-011-0830-0_26

Palmer, A.R., Strobeck, C. (1986). Fluctuating asymmetry:

measurement, analysis, patterns. Annual Review of Ecology and Systematics, 17, 391-421.

Palmer, A.R., Strobeck, C. (2003). Fluctuating asymmetry analysis revisited. Developmental instability (DI): causes and consequences. Oxford.

Pavlinov, I.Ya. (2001). Geometric morphometry – a new analytical approach to the comparison of computer images. Information and telecommunication resources in zoology and botany, St. Petersburg, 65-90 (in Russian).

Pavlinov, I.Ya., Mikeshina, N.G. (2002). Principles and methods of geometric morphometry. Journal Society Biol., 63(6), 473-493 (in Russian).

Peligro, V.C., Jumawan, J.C. (2016). Assessment of fluctuating asymmetry in the body shapes of Nile tilapia (Oreochromis niloticus) from Masao river, Butuan city, Philippines. AACL Bioflux, 9(3), 604-613.

Pogotskaya, A.A., Buzuk, G.N., Sozinov, O.V. (2010). Morphometry Chelidonium majus L.: interrelation of sizes, shape of leaf blade and content of alkaloids and phenolic compounds. Bulletin of Pharmacy, 3(49), 26-39 (in Russian).

Pojas, R.G., Tabugo, S.R.M. (2015). Fluctuating asymmetry of paraside infested and non-infested Sardinella sp. from Misamis Oriental, Philippines. AACL Bioflux, 8(1), 7-14.

Polonsky, V.I. (2016). Use of fluctuating asymmetry of opposite leaves Syringa josikaea Jacq. in bioindication of pollution in Krasnoyarsk. Biological Sciences, 77-82 (in Russian).

Polonsky, V.I., Polyakova, I.S. (2014). Syringa josikaea is a promising bioindicator for a comparative assessment of degree pollution of the urban environment. Bulletin of the Krasnoyarsk State Agrarian University, 2, 89-92 (in Russian).

Polyakov, A.K. (2009). Introduction of woody plants in the conditions of anthropogenic environment. Donetsk (in Russian).

Premchamd, A., Mawri, F., Gladstone, S., Freeman D.C. (1998). Is fluctuating asymmetry a reliable biomonitor of stress? A test using life history parameters in soybean. International Journal of Plant Sciences, 159(4), 559-565.

Rahmangulov, R.S., Ishbirdin, A.R., Salpagarova, A.S. (2014). Fluctuating asymmetry – an indicator of destabilization or the search for ways of adaptive morphogenesis? Bulletin of the Bashkir University, 19(3), 831-834 (in Russian).

Ramazanova, Z.R., Asadulayev, Z.M. (2012). Morphological and anatomical parameters of running systems Celtis caucasica Willd. in the conditions of Makhachkala city. Biological recultivation and monitoring of disturbed lands. Ekaterinburg, 209-214 (in Russian).

Roy, B.A., Stanton, M.L. (1999). Asymmetry of wild mustard, Sinapis arvensis (Brassicaceae), in response to severe physiological stresses. J. of Evol. Biol., 12, 440-449.

Safargalina, A.T., Khusainova, S.A., Ishbirdin, A.R. (2011). Manifestations of Atriplex patula L. life strategies in ontogenesis. Bulletin Samara Scientific Center of the Russian Academy of Sciences, 13, 5(2), 112-114 (in Russian).

Safonov, A.I. (2012). Approbation of ecosystem standardization criteria according to phytoindication component. Problems of ecology and nature protection of technogenic region, 1(12), 108-114.

Safonov, A.I. (2016). Phytoindicational monitoring in Donetsk. A science. Thought: Scientific journal, 4, 58-70.

Safonov, A.I. (2017). Functional botany in Donbass: ecological monitoring, information resource technologies, phytodesign. Problems of ecology and nature protection of technogenic region, 1-2, 6-12.

Savintseva, L.S., Egoshina, T.L., Shiryaev, V.V. (2012). Evaluation of the quality of Kirov city on the basis of an analysis of the fluctuating asymmetry of leaf blade Betula pendula Roth. Bulletin of the Udmurt University, Biology, 2, 31-37 (in Russian).

Savriama, Y., Klingenberg, C.P. (2011). Beyond bilateral symmetry: geometric morphometric methods for any type of symmetry. Evol. Biol., 11, 280, doi:10.1186/1471-2148-11-280

Scherbakov, A.V., Korolkova, E.O. (2015). Fluctuating asymmetry of the leaf of Acer platanoides L. as indicative indicator of the quality of the environment. Socio-ecological technologies, Available from: https://cyberleninka.ru/article/v/fluktuiruyuschaya-asimmetriya-lista-klena-ostrolistnogo-acer-platanoides-l-kak-indikatsionnyy-pokazatel-kachestva-sredy/ Accessed on 17.01.2018 (in Russian).

Shavyrkina, M.A., Golyshkin, L.V., Knyszev, S.D. (2014). Features of the integral evaluation environment in connection with the determination of the fluctuating asymmetry of the leaf blade Ribes nigrum L. Modern gardening, 4, 64-70 (in Russian).

Shtirts, Yu.A. (2011). Variation in the size of the leaf blade of Acer pseudoplatanus L. in conditions of roadside ecosystems of the city of Donetsk. Regulation of growth, development and productivity of plants. Minsk, 228 (in Russian).

Shtirts, Yu.A. (2012). Assessment of the variability of the apex and the base of the leaf blade of Роpulus nigra L. in conditions of industrial dumps. Industrial botany, 12, 31-36 (in Russian).

Shtirts, Yu.A. (2012). Variation of the dimensions of the leaf blade of Роpulus nigra L. in conditions of industrial dumps in the Donetsk region. Biological recultivation and monitoring of disturbed lands. Ekaterinburg, 305-310 (in Russian).

Shtirts, Yu.A. (2013). Morphological diversity of leaf blades of Populus nigra L. in conditions of industrial dumps. Industrial Botany, Donetsk, 13, 116-124 (in Russian).

Shtirts, Yu.A. (2014). Morphological parameters of the leaf blade of Betula pendula Roth in the roadside territories of the motorways of Donetsk. Introduction, conservation and monitoring of plant diversity. Kiev, 217-218 (in Russian).

Shtirts, Yu.A. (2017). Variability of the degree of ruggedness edge of the leaf blade Populus nigra L. in industrial dumps. Acta Biologica Sibirica, 3(2), 46-51, doi:10.14258/abs.v3i2.2731 (in Russian).

Smirnova, O.V., Zaugolnova, L.B., Taronova, N.A., Falikov, L.D. (1976). Criteria for distinguishing age conditions and features of the ontogenesis course in plants of different biomorphs. Moscow, I, 14-43 (in Russian).

Sobchak, R.O., Afanasyeva, T.G., Kopylov, M.A. (2013). Estimation of the ecological state of recreational forests by the method of fluctuating asymmetry of leaves Betula pendula Roth. Bulletin of Tomsk State University, 368, 195-199 (in Russian).

Soldatova, V.Yu. (2006). Fluctuating asymmetry of Betula platyphylla Sukacz. as a criterion of quality of urban environment and territories subject to anthropogenic influence (on the example of Yakutia). Yakutsk (in Russian).

Stakovetskaya, O.K., Kulikova, N.A., Sovetova, E.S. (2012). Estimation of the ecological state of the air environment using bioindication methods. Available from: http://www.rusnauka.com/10_DN_2012/Ecologia/6_106476.doc.htm/ Accessed on 17.01.2018 (in Russian).

Swaddle, J.P. (2003). Fluctuating asymmetry, animal behavior and evolution. Advances in the study of behavior, 32, 169-205.

Thoday, J.M. (1958). Homeostasis in a selection experiment. Heredity, 12(4), 401-415.

Trubina, L.K., Khramova, E.P., Lugovskaya, A.Yu. (2016). Computer analysis of images of leaf blades Potentilla fruticosa for bioindication of urban areas. Ecology and nature management, 4(36), 263-273 (in Russian).

Trubyanov, A.B. (2010). Analysis of the fluctuating asymmetry parameters. Nizhny Novgorod (in Russian).

Velickovica, M., Perisica, S. (2006). Leaf fluctuating asymmetry of common plantain as an indicator of habitat quality. Plant Biosystems, 140(2), 138-145, doi:10.1080/11263500600756322

Vogel, S. (2009). Leaves in the lowest and highest winds: temperature, force and shape. New Phytologist, 183, 13-26.

Waddington, C.H. (1942). Canalization of development and the inheritance of acquired characters. Nature, 150, 563-565.

Wilsey, B.J., Haukioja, E., Koricheva, J., Sulkinoja, M. (1998). Leaf fluctuating asymmetry increases with hybridization and elevation in tree-line birches. Ecology, 79(6), 2092-2099, doi:10.1890/0012-9658(1998)079[2092:LFAIWH]2.0.CO;2

Wilsey, B.J., Saloniemi, I. (1999). Leaf fluctuating asymmetry in tree-line mountain birches, Betula pubescens ssp. tortuosa: genetic or environmentally influenced? Oikos, 87(2), 341-345, doi:10.2307/3546749

Wuytacka, T., Wuytsa, K, van Dongenc, S., Baetenb, L., Kardela, F., Verheyenb, K., Samsona, R. (2011). The effect of air pollution and other environmental stressors on leaf fluctuating asymmetry and specific leaf area of Salix alba L. Environmental Pollution, 159(10), 2405-2411, doi:10.1016/j.envpol.2011.06.037

Zaitseva, I.O. (2012). Bioecological mechanisms of wood introductions adaptation in the steppe zone of Ukraine. Dnepropetrovsk (in Ukrainian).

Zakharov, V.M. (1987). Asymmetry in animals. Moscow (in Russian).

Zakharov, V.M. (2001). Ontogenesis and population (stable development and population variation). Ecology, 3, 177-191 (in Russian).

Zakharov, V.M., Baranov, A.S., Borisov, V.I., et al. (2000). Health of the environment: a methodology for evaluation. Assessment of the state of natural populations for the stability of development: methodological guidance for reserves. Moscow (in Russian).

Zhamurina, N.A., Anhalt, E.M., Volokhina, O.A. (2015). Estimation of the condition of plantations in the tract Kachkarsky Mar. Actual problems of the forestry complex, 41, 22-26 (in Russian).

Zhuchenko, A.A. (1988). Adaptive potential of cultivated plants (ecological and genetic basis). Kishinev (in Russian).

Zhukov, A.V., Shtirts, Yu.A., Zhukov, S.P. (2011). Evaluation of morphological variability of Betula pendula Roth leaflets in ecosystems with different degree of anthropogenic transformation by methods of geometric morphometry. Problems of ecology and nature protection of the technogenic region, 1(11), 128-134 (in Russian).

Zorina, A.A. (2010). Fluctuating asymmetry of animals and plants. Saarbrucken (in Russian).

Zorina, A.A. (2012). Methods of statistical analysis of fluctuating asymmetry. Principles of ecology, 1(3), 24-47 (in Russian).

Zorina, A.A. (2013). The estimation of the fluctuating asymmetry on the basis of the normalized deviation. Principles of ecology, 1, 69-72, doi:10.15393/j1.art.2013.2361 (in Russian).

Zorina, A.A. (2014). Formation of fluctuating asymmetry in the process of individual development of Betula pendula. Principles of ecology, 4, 31-52, doi:10.15393/j1.art.2014.3901 (in Russian).

Zorina, A.A., Korosov, A.V. (2007). Evaluation of fluctuating asymmetry. Special methods of biometrics. Petrozavodsk, 79-88 (in Russian).

Zorina, A.A., Korosov, A.V. (2009). Variability of indices and indices of asymmetry of sheet features in the crown Betula pendula (Betulaceae). Botanical Journal, 94(8), 1172-1192 (in Russian).




DOI: http://dx.doi.org/10.15421/2018_204

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