Abstract
A critical analysis of studies addressing fluctuating asymmetry (FA) of plant leaves, published recently in Russia, demonstrated that most of these studies are based on insufficiently substantiated assumptions, employ outdated or inadequate methodology and do not contain sufficient information to support the use of the reported results in further reviews and meta-analyses. Contrary to widespread opinion, the current level of knowledge does not allow practical use of FA for bioindication. This use will only be possible after controlled experiments verify the cause-and-effect relationships between the levels of FA and the impacts of different stressors on plants. An adequate assessment of FA requires repeated, high precision measurements, which should be conducted blindly. In this treatise, I discuss the prospective directions for FA research in plants and provide recommendations on experimental design, data analysis and presentation of the results in publications.
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Albarrán-Lara, A.L., Mendoza-Cuenca, L., Valencia-Avalos, S., et al., Leaf fluctuating asymmetry increases with hybridization and introgression between Quercus magnoliifolia and Quercus resinosa (Fagaceae) through an altitudinal gradient in Mexico, Int. J. Plant Sci., 2010, vol. 171, no. 3, pp. 310–322.
Alexander, A., Barnett-Cowan, M., Bartmess, E., et al., An open, large-scale, collaborative effort to estimate the reproducibility of psychological science, Perspect. Psychol. Sci., 2012, vol. 7, no. 6, pp. 657–660.
Anamthawat-Jónsson, K. and Thórsson, Æ.Th., Natural hybridization in birch: Triploid hybrids between Betula nana and B. pubescens, Plant Cell Tissue Organ Cult., 2003, vol. 75, no. 2, pp. 99–107.
Begley, C.G. and Ellis, L.M., Raise standards for preclinical cancer research, Nature, 2012, vol. 483, no. 7391, pp. 531–533.
Clarke, G.M., Fluctuating asymmetry: A technique for measuring developmental stress of genetic and environmental origin, Acta Zool. Fenn., 1992, vol. 191, no. 1, pp. 31–35.
Freeman, D.C., Graham, J.H., and Emlen, J.M., Developmental stability in plants: Symmetries, stress and epigenesis, Genetica, 1993, vol. 89, nos. 1–3, pp. 97–119.
Graham, J.H., Raz, S., Hel-Or, H., and Nevo, E., Fluctuating asymmetry: methods, theory, and applications, Symmetry, 2010, vol. 2, no. 2, pp. 466–540.
Grime, J.P., Plant Strategies and Vegetation Processes, Chichester: Wiley, 1979.
Hergovich, A., Schott, R., and Burger, C., Biased evaluation of abstracts depending on topic and conclusion: Further evidence of a confirmation bias within scientific psychology, Curr. Psychol., 2010, vol. 29, no. 3, pp. 188–209.
Hume, D., Environmental Monitoring and Fluctuating Asymmetry: Study Design, Wellington: New Zealand Dep. Conserv., 2001.
Klisarić, N.B., Miljković, D., Avramov, S., et al., Fluctuating asymmetry in Robinia pseudoacacia leaves: Possible in situ biomarker? Environ. Sci. Pollut. Res., 2014, vol. 21, no. 22, pp. 12928–12940.
Kolbas, A., Marchand, L., Herzig, R., et al., Phenotypic seedling responses of a metal-tolerant mutant line of sunflower growing on a Cu-contaminated soil series: Potential uses for biomonitoring of Cu exposure and phytoremediation, Plant Soil, 2014, vol. 376, nos. 1–2, pp. 377–397.
Koropachinskii, I.Yu., Natural hybridization and problems in hybridization of birch species in Northern Asia, Sib. Ekol. Zh., 2013, no. 4, pp. 459–479.
Koroteeva, E.V., Veselkin, D.V., Kuyantseva, N.B., and Chashchina, O.E., The size, but not the fluctuating asymmetry of the leaf, of silver birch changes under the gradient influence of emissions of the Karabash Copper Smelter Plant, Dokl. Biol. Sci., 2015, vol. 460, pp. 36–39.
Kozlov, M.V., Pseudoreplication in ecological research: The problem overlooked by Russian scientists, Zh. Obshch. Biol., 2003, vol. 64, no. 4, pp. 292–307.
Kozlov, M.V., Planirovanie ekologicheskikh issledovanii: teoriya i prakticheskie rekomendatsii (Planning of Ecological Research: Theory and Practical Recommendations), Moscow: KMK, 2015a, 2nd ed.
Kozlov, M.V., How reproducible are the measurements of leaf fluctuating asymmetry? Peer J, 2015b, vol. 3, e1027.
Kozlov, M.V. and Hurlbert, S.H., Pseudoreplication, chatter, and the international nature of science: A reply to D.V. Tatarnikov, Zh. Obshch. Biol., 2006, vol. 67, no. 2, pp. 145–152.
Kozlov, M.V. and Niemelä, P., Drought is more stressful for northern populations of Scots pine than low summer temperatures, Silva Fenn., 2003, vol. 37, no. 2, pp. 175–180.
Kozlov, M.V. and Vorobeichik, E.L., Impact of point polluters on terrestrial ecosystems: Presentation of results in publications, Russ. J. Ecol., 2012, vol. 43, no. 4, pp. 265–272.
Kozlov, M.V. and Zvereva, E.L., A second life for old data: Global patterns in pollution ecology revealed from published observational studies, Environ. Pollut., 2011, vol. 159, no. 5, pp. 1067–1075.
Kozlov, M.V. and Zvereva, E.L., Confirmation bias in studies of fluctuating asymmetry, Ecol. Indicat., 2015, vol. 57, pp. 293–297.
Kozlov, M.V., Zvereva, E.L., and Zverev, V.E., Impact of Point Polluters on Terrestrial Biota: Comparative Analysis of 18 Contaminated Areas, Dordrecht: Springer-Verlag, 2009.
Kozlov M.V., Cornelissen T., Gavrikov D.E. et al. Reproducibility of fluctuating asymmetry measurements in plants: Sources of variation and implications for study design, Ecol. Indicat., 2016. doi 10.1016/j.ecolind.2016.10.033
Kryazheva, N.G., Chistyakova, E.K., and Zakharov, V.M., Analysis of development stability of Betula pendula under conditions of chemical pollution, Russ. J. Ecol., 1996, vol. 27, no. 6, pp. 422–424.
Laius, D.L., Grem, D.Kh., Katolikova, M.V., and Yurtseva, A.O., Fluctuating asymmetry and random phenotypic variation in population research: History, achievements, problems, and prospects, Vestn. S.-Peterb. Gos. Univ., Ser. 3: Biol., 2009, no. 3, pp. 98–110.
Malafeeva, E.F. and Marina, A.V., Bioindication of the state of the environment: A method based on fluctuating asymmetry, Biol. Shkole, 2010, no. 6, pp. 39–46.
McNutt, M., Reproducibility, Science, 2014, vol. 343, no. 6168, p. 231.
Merilä, J. and Björklund, M., Fluctuating asymmetry and measurement error, Syst. Biol., 1995, vol. 44, no. 1, pp. 97–101.
Metodicheskie rekomendatsii po vypolneniyu otsenki kachestva sredy po sostoyaniyu zhivykh sushchestv (otsenka stabil’nosti razvitiya zhivykh organizmov po urovnyu asimmetrii morfologicheskikh struktur. Rasporyazhenie MPR no. 460-r ot 16.10.2003) (Guidelines for Evaluation of Environmental Quality Using the State of Living Beings: Evaluation of Developmental Stability of Organisms by Studying Asymmetry of Morphological Structures. Administrative Directive no. 460-r of the RF Ministry of Natural Resources and Environment, October 16, 2003), Moscow, 2003.
Møller, A.P. and Swaddle, J.P., Asymmetry, Developmental Stability, and Evolution, Oxford: Oxford Univ. Press, 1997.
Nickerson, R.S., Confirmation bias: A ubiquitous phenomenon in many guises, Rev. Gen. Psychol., 1998, vol. 2, no. 2, pp. 175–220.
Palmer, A.R. and Strobeck, C., Fluctuating asymmetry: Measurement, analysis, patterns, Ann. Rev. Ecol. Syst., 1986, vol. 17, pp. 391–421.
Palmer, A.R. and Strobeck, C., Fluctuating asymmetry analyses revisited, in Developmental Instability: Causes and Consequences, Polak, M., Ed., Oxford: Oxford Univ. Press, 2003, pp. 279–319.
Parsons, P.A., Fluctuating asymmetry: A biological monitor of environmental and genomic stress, Heredity, 1992, vol. 68, no. 4, pp. 361–364.
Prinz, F., Schlange, T., and Asadullah, K., Believe it or not: How much can we rely on published data on potential drug targets?, Nat. Rev. Drug Discov., 2011, vol. 10, no. 9. p. 712.
Rosenthal, R., Experimenter Effects in Behavioral Research, New York: Wiley, 1976.
Savelyeva, N.A., Belova, E.E., Pervova, N.E., and Kolontsov, A.A., Estimation of the effect of lead and cadmium ions on fluctuating asymmetry in leaves of the common bean (Phaseolus vulgaris L.), Moscow Univ. Soil Sci. Bull., 2013, vol. 68, no. 4, pp. 192–194.
Valkama, J. and Kozlov, M.V., Impact of climatic factors on the developmental stability of mountain birch growing in a contaminated area, J. Appl. Ecol., 2001, vol. 38, no. 3, pp. 665–673.
Vasil’ev, A.G., Vasil’eva, I.A., and Marin, Yu.F., Phenogenetic monitoring of the weeping birch (Betula pendula Roth.) in the Middle Urals: Testing a new method for assessing developmental instability in higher plants, Russ. J. Ecol., 2008, vol. 39, no. 7, pp. 483–489.
Vaupel, A. and Matthies, D., Abundance, reproduction, and seed predation of an alpine plant decrease from the center toward the range limit, Ecology, 2012, vol. 93, no. 10, pp. 2253–2262.
van Wilgenburg, E. and Elgar, M.A., Confirmation bias in studies of nestmate recognition: A cautionary note for research into the behaviour of animals, PLoS One, 2013, vol. 8, p. e53548.
Wilsey, B.J., Haukioja, E., Koricheva, J., and Sulkinoja, M., Leaf fluctuating asymmetry increases with hybridization and elevation in tree-line birches, Ecology, 1998, vol. 79, no. 6, pp. 2092–2099.
Wuytack, T., Samson, R., Wuyts, K., et al., Do leaf characteristics of white willow (Salix alba L.), northern red oak (Quercus rubra L.), and Scots pine (Pinus sylvestris L.) respond differently to ambient air pollution and other environmental stressors? Water Air Soil Pollut., 2013, vol. 224, no. 1635, pp. 1–14.
Zakharov, V.M., Asimmetriya zhivotnykh (populyatsionnofenogeneticheskii podkhod) (Asymmetry in Animals: A Population-Genetic Approach), Moscow: Nauka, 1987.
Zakharov, V.M., Analysis of fluctuating asymmetry as a method of biomonitoring at the population level, in Bioindication of Chemical and Radioactive Pollution, Krivolutsky, D., Ed., Boca Raton: CRC Press, 1990, pp. 187–198.
Zakharov, V.M. and Clarke, G.M., Biotest. Integral’naya otsenka zdorov’ya ekosistem I otdel’nykh vidov (Biotest: An Integral Assessment of the State of Ecosystems and Individual Species), Moscow: Biotest, 1993.
Zakharov, V.M., Baranov, A.S., Borisov, V.I., et al., Zdorov’e sredy: praktika otsenki (The Health of the Environment: Practical Assessment), Moscow: Tsentr Ekologicheskoi Politiki Rossii, 2000.
Zorina, A.A. and Korosov, A.V., Variation in parameters and indices of asymmetry in leaf characters in the crown of Betula pendula (Betulaceae), Bot. Zh., 2009, vol. 94, no. 8, pp. 1172–1192.
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Original Russian Text © M.V. Kozlov, 2017, published in Ekologiya, 2017, No. 1, pp. 3–12.
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Kozlov, M.V. Plant studies on fluctuating asymmetry in Russia: Mythology and methodology. Russ J Ecol 48, 1–9 (2017). https://doi.org/10.1134/S1067413617010106
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DOI: https://doi.org/10.1134/S1067413617010106