Change of Leaf Trait Asymmetry Type in Tilia cordata Mill. and Betula pendula Roth under Air Pollution
Abstract
:1. Introduction
2. Material and Methods
2.1. Study Area and Study Plots
2.2. Estimation of Traffic Air Pollution
2.3. Leaf Trait Selection and Estimation of FA Integrated Index
2.4. Analysis of Leaf Trait Asymmetry Types
3. Results
3.1. Analysis of Leaf Trait Asymmetry Type in T. cordata under Air Pollution
3.2. Analysis of Leaf Trait Asymmetry Type in B. pendula under Air Pollution
4. Discussion
Author Contributions
Funding
Conflicts of Interest
References
- Palmer, A.R.; Strobeck, C. Fluctuating asymmetry: Measurements, analysis, patterns. Annu. Rev. Ecol. Syst. 1986, 17, 391–421. [Google Scholar] [CrossRef]
- Zakharov, V.M. Asimmetriya Zhivotnykh (The Asymmetry of Animals); Nauka: St. Petersburg, Russia, 1987; pp. 5–30. (In Russian) [Google Scholar]
- Palmer, A.R.; Strobeck, C. Fluctuating asymmetry as a measure of developmental stability: Implications of non-normal distributions and power of statistical tests. Acta Zool. Fennica 1992, 191, 57–72. [Google Scholar]
- Zakharov, V.M.; Zhdanov, N.P.; Kirik, E.F.; Shkil’, F.N. Ontogenesis and population: Evaluation of developmental stability in natural populations. Russ. J. Dev. Biol. 2001, 32, 336–351. [Google Scholar] [CrossRef]
- Shadrina, E.G.; Vol’pert, Y.L. Experience of applying plant and animal fluctuating asymmetry in assessment of environmental quality in terrestrial ecosystems: Results of 20-year studies of wildlife and anthropogenically transformed territories. Russ. J. Dev. Biol. 2018, 49, 23–35. [Google Scholar] [CrossRef]
- Leamy, L.J.; Klingenberg, C.P. The genetics and evolution of fluctuation asymmetry. Annu. Rev. Ecol. Evol. Syst. 2005, 36, 1–21. [Google Scholar] [CrossRef] [Green Version]
- Carter, A.J.R.; Osborne, E.; Houle, D. Heritability of directional asymmetry in Drosophila melanogaster. Int. J. Evol. Biol. 2009, 2009, 1–7. [Google Scholar] [CrossRef] [Green Version]
- Leung, B.; Forbes, M.R.; Houle, D. Fluctuating asymmetry as a bioindicator of stress: Comparing efficacy of analysis involving multiple traits. Am. Nat. 2000, 155, 101–115. [Google Scholar] [CrossRef]
- Hoffman, A.A.; Woods, R.E. Associating environmental stress with developmental stability: Problems and patterns. In Developmental Instability. Causes and Consequences; Polak, M., Ed.; Oxford University Press: New York, NY, USA, 2003; pp. 387–401. [Google Scholar]
- Hagen, S.B.; Ims, R.A.; Yoccoz, N.G. Fluctuating asymmetry as an indicator of elevation stress and distribution limits in mountain birch (Betula pubescens). Plant. Ecol. 2008, 195, 157–163. [Google Scholar] [CrossRef]
- Cornelissen, T.; Stiling, P. Similar responses of insect herbivores to leaf fluctuating asymmetry. Arthrop. Plant. Inter. 2011, 5, 59–69. [Google Scholar] [CrossRef]
- Kozlov, M.V.; Wilsey, B.J.; Koricheva, J.; Haukioja, E. Fluctuating asymmetry of birch leaves increases under pollution impact. J. Appl. Ecol. 1996, 33, 1489–1495. [Google Scholar] [CrossRef]
- Shadrina, E.G.; Vol’pert, Y.L. Developmental instability of the organism as a result of pessimization of environment under anthropogenic transformation of natural landscapes. Russ. J. Dev. Biol. 2014, 45, 117–126. [Google Scholar] [CrossRef]
- Franiel, I. Fluctuating asymmetry of Betula pendula Roth leaves—An index of environment quality. Biodiv. Res. Conserv. 2008, 9, 7–10. [Google Scholar]
- Valkama, J.; Kozlov, M.V. Impact of climatic factors on the developmental stability of mountain birch growing in a contaminated area. J. Appl. Ecol. 2001, 38, 665–673. [Google Scholar]
- Llorens, L.; Peñuelas, J.; Emmett, B. Developmental instability and gas exchange responses of a heathland shrub to experimental drought and warming. Int. J. Plant. Sci. 2002, 163, 959–967. [Google Scholar] [CrossRef] [Green Version]
- Zakharov, V.M.; Kryazheva, N.G.; Dmitriev, S.G.; Trofimov, I.E. Evaluation of possible changes in population state due to climate change (with particular references to the study of developmental stability of the European white birch). Biol. Bull. Rev. 2012, 2, 190–193. [Google Scholar] [CrossRef]
- Xu, Z.; Hu, T.; Zhang, Y. Effects of experimental warming on phenology, growth and gas exchange of tree line birch (Betula utilis) saplings, Eastern Tibetan Plateau, China. Eur. J. For. Res. 2012, 131, 811–819. [Google Scholar] [CrossRef]
- Nuche, P.; Komas, B.; Camarero, J.J.; Alados, C.L. Developmental instability as an index of adaptation to drought stress in a Mediterranean oak. Ecol. Indic. 2014, 40, 68–75. [Google Scholar] [CrossRef] [Green Version]
- Zvereva, E.L.; Kozlov, M.V.; Niemelä, P.; Haukioja, E. Delayed induced resistance and increase in leaf fluctuating asymmetry as responses of Salix borealis to insect herbivory. Oecologia 1997, 109, 368–373. [Google Scholar] [CrossRef]
- Møller, A.P.; Shykoff, J.A. Morphological developmental stability in plants: Patterns and causes. Int. J. Plant. Sci. 1999, 160, 135–146. [Google Scholar] [CrossRef]
- Ribeiro, V.A.; da Silva, R.N.; Sousa-Souto, L.; de Siqueira Neves, F. Fluctuating asymmetry of and herbivory on Poincianella pyramidalis (Tul.) L.P. Queiroz (Fabaceae) in pasture and secondary tropical dry forest. Acta Bot. Bras. 2013, 27, 21–25. [Google Scholar] [CrossRef] [Green Version]
- McKenzie, J.A.; Clarke, G.M. Diazanon resistance, fluctuating asymmetry and fitness in Australian sheep blowfly, Lucilia curpina. Genetics 1988, 120, 213–220. [Google Scholar] [PubMed]
- Graham, J.H.; Roe, K.E.; West, T.V. Effects of lead and benzene on developmental stability of Drosophila melanogaster. Ecotoxicology 1993, 2, 185–195. [Google Scholar] [CrossRef] [PubMed]
- Leamy, L.J.; Doster, M.J.; Huet-Hudson, Y.M. Effects of methoxychlor on directional and fluctuating asymmetry of mandible characters in mice. Ecotoxicology 1999, 8, 63–71. [Google Scholar] [CrossRef]
- Lens, L.; Van Dongen, S. Fluctuating and directional asymmetry in natural bird populations exposed to different levels of habitat disturbance, as reveal by mixture analysis. Ecol. Lett. 2000, 3, 516–522. [Google Scholar] [CrossRef]
- Mohan, D.; Tiwari, G. Mobility, environment and safety in megacities. IATSS Res. 2000, 24, 39–46. [Google Scholar] [CrossRef] [Green Version]
- Molina, M.J.; Molina, L.T. Megacities and atmospheric pollution. J. Air Waste Manag. Assoc. 2004, 54, 644–680. [Google Scholar] [CrossRef]
- Kosiba, P. Variability of morphometric leaf traits in small-leaved linden (Tilia cordata Mill.) under the influence of air pollution. Acta Societatis Botanicorum Poloniae 2008, 77, 125–137. [Google Scholar] [CrossRef] [Green Version]
- Veliĉković, M. Reduced developmental stability in Tilia cordata leaves: Effects of disturbed environment. Periodicum Biologorum 2010, 112, 273–281. [Google Scholar]
- Baranov, S.G. Use of morphogeometric method for study fluctuating asymmetry in leaves Tilia cordata under industrial pollution. Advan. Environ. Biol. 2014, 8, 2391–2398. [Google Scholar]
- Freer-Smith, P.H. The responses of six broadleaved trees during long-term exposure to SO2 and NO2. New Phytol. 1984, 97, 49–61. [Google Scholar] [CrossRef]
- Maksimović, T.; Ilić, P.; Bajić, S. Air pollution on vegetation in Banja Luka. Qual. Life 2018, 9, 33–37. [Google Scholar] [CrossRef]
- Erofeeva, E.A. Hormesis and paradoxical effects of drooping birch (Betula pendula Roth) parameters under motor traffic pollution. Dose Response 2015, 13, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Bartell, S.M. Biomarkers, bioindicators, and ecological risk assessment. Environ. Bioindic. 2006, 1, 39–52. [Google Scholar] [CrossRef]
- Connon, R.E.; Geist, J.; Werner, I. Effect-Based tools for monitoring and predicting the ecotoxicological effects of chemicals in the aquatic environment. Sensors 2012, 12, 12741–12771. [Google Scholar] [CrossRef] [Green Version]
- Cedergreen, N.; Streibig, J.C.; Kudsk, P.; Mathiassen, K.; Duke, S.O. The occurrence of hormesis in plants and algae. Dose Response 2007, 5, 150–162. [Google Scholar] [CrossRef]
- Calabrese, E.J. Hormesis: Why it is important to toxicology and toxicologists. Environ. Toxicol. Chem. 2008, 27, 1451–1474. [Google Scholar] [CrossRef]
- Agathokleous, E.; Kitao, M.; Calabrese, E.J. Environmental hormesis and its fundamental biological basis: Rewriting the history of toxicology. Environ. Res. 2018, 165, 274–278. [Google Scholar] [CrossRef]
- Schatz, A. More on paradoxical effects. Fluoride 1999, 32, 43–44. [Google Scholar]
- Smith, S.W.; Hauben, M.; Aronson, J.K. Paradoxical and bidirectional drug effects. Drug Saf. 2012, 35, 173–189. [Google Scholar] [CrossRef]
- Calabrese, E.J.; Blain, R.B. Hormesis and plant biology. Environ. Poll. 2009, 157, 42–48. [Google Scholar] [CrossRef]
- Erofeeva, E.A. Hormesis and paradoxical effects of wheat seedling (Triticum aestivum L.) parameters upon exposure to different pollutants in a wide range of doses. Dose Response 2014, 12, 121–135. [Google Scholar] [CrossRef] [PubMed]
- Erofeeva, E.A. Hormesis and paradoxical effects of pea (Pisum sativum L.) parameters upon exposure to formaldehyde in a wide range of doses. Ecotoxicology 2018, 27, 569–577. [Google Scholar] [CrossRef] [PubMed]
- Agathokleous, E.; Kitao, M.; Calabrese, E.J. Human and veterinary antibiotics induce hormesis in plants: Scientific and regulatory issues and an environmental perspective. Environ. Int. 2018, 120, 489–495. [Google Scholar] [CrossRef] [PubMed]
- Agathokleous, E.; Belz, R.G.; Calatayud, V.; De Marco, A.; Hoshika, Y.; Kitao, M.; Saitanis, C.; Sicard, P.; Paoletti, E.; Calabrese, E.J. Predicting the effect of ozone on vegetation via linear non-threshold (LNT), threshold and hormetic dose-response models. Sci. Total Environ. 2019, 649, 61–74. [Google Scholar] [CrossRef]
- Agathokleous, E.; Kitao, M.; Calabrese, E.J. Hormetic dose responses induced by lanthanum in plants. Environ. Pollut. 2019, 244, 332–341. [Google Scholar] [CrossRef]
- Calabrese, E.J. Hormetic mechanisms. Crit. Rev. Toxicol. 2013, 43, 580–606. [Google Scholar] [CrossRef]
- Agathokleous, E. Environmental hormesis, a fundamental non-monotonic biological phenomenon with implications in ecotoxicology and environmental safety. Ecotoxicol. Environ. Saf. 2018, 148, 1042–1053. [Google Scholar] [CrossRef] [Green Version]
- Wagener, J.; Loiko, V. Recent insights into the paradoxical effect of echinocandins. J. Fungi 2018, 4, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Gelashvili, D.B.; Koposov, E.V.; Laptev, L.A. Ekologiya Nizhnego Novgoroda (Ecology of Nizhni Novgorod); Business Polygraphy: Nizhni Novgorod, Russia, 2007; pp. 102–103. (In Russian) [Google Scholar]
- Erofeeva, E.A. Dependence of guaiacol peroxidase activity and lipid peroxidation rate in drooping birch (Betula pendula Roth) and tillet (Tilia cordata Mill.) leaf on motor traffic pollution intensity. Dose Response 2015, 13, 1–6. [Google Scholar] [CrossRef] [Green Version]
- Kozlov, M.V.; Zvereva, E.L. Confirmation bias in studies of fluctuating asymmetry. Ecol. Indic. 2015, 57, 293–297. [Google Scholar] [CrossRef]
- Illowsky, B.; Dean, S. Introductory Statistics. Available online: https://opentextbc.ca/introstatopenstax/chapter/outliers/ (accessed on 29 July 2019).
- Van Dongen, S.; Lens, L.; Molenbergh, G. Mixture analysis of asymmetry: Modelling directional asymmetry, antisymmetry and heterogeneity in fluctuating asymmetry. Ecol. Lett. 1999, 2, 387–396. [Google Scholar]
- Erofeeva, E.A. Dependence of leaf fluctuating asymmetry of Betula pendula (Betulacea) on motor traffic pollution intensity. Rastitelnye Resursy (Plant. Resour.) 2015, 51, 366–383. [Google Scholar]
- Erofeeva, E.A. Dependence of dandelion (Taraxacum officinale Wigg.) seed reproduction indices on intensity of motor traffic pollution. Dose Response 2014, 12, 540–550. [Google Scholar] [CrossRef] [PubMed]
- Erofeeva, E.A. Developmental stability of a leaf of Pisum sativum L. under the influence of formaldehyde in a wide range of doses. Rus. J. Dev. Biol. 2012, 42, 259–263. [Google Scholar] [CrossRef]
- Steimer, A.; Schöb, H.; Grossniklaus, U. Epigenetic control of plant development: New layers of complexity. Curr. Opin. Plant. Biol. 2004, 7, 11–19. [Google Scholar] [CrossRef]
- Herrera, C.M.; Bazaga, P. Epigenetic correlates of plant phenotypic plasticity: DNA methylation differs between prickly and nonprickly leaves in heterophyllous Ilex aquifolium (Aquifoliaceae) trees. Bot. J. Linn. Soc. 2013, 171, 441–452. [Google Scholar] [CrossRef] [Green Version]
- Lodha, M.; Marco, C.F.; Timmermans, M.C. The ASYMMETRIC LEAVES complex maintains repression of KNOX homeobox genes via direct recruitment of Polycomb-repressive complex2. Genes Dev. 2013, 27, 596–601. [Google Scholar] [CrossRef] [Green Version]
- Ahmad, A.; Zhang, Y.; Cao, X.-F. Decoding the epigenetic language of plant development. Mol. Plant. 2010, 3, 719–728. [Google Scholar] [CrossRef] [Green Version]
- Pascual, J.; Cañal, M.J.; Correia, B.; Escandón, M.; Hasbún, R.; Meijón, M.; Pinto, G.; Valledor, V. Can epigenetics help forest plants to adapt to climate change. In Epigenetics in Plants of Agronomic Importance: Fundamentals and Applications; Alvarez-Venegas, R., De la Peña, C., Casas-Mollano, J.A., Eds.; Springer: Berlin/Heidelberg, Germany, 2014; pp. 125–146. [Google Scholar]
- Warren, J.M.; Norby, R.J.; Wullschleger, S.D. Elevated CO2 enhances leaf senescence during extreme drought in a temperate forest. Tree Physiol. 2011, 31, 117–130. [Google Scholar] [CrossRef]
- Gonzalez, E. Seasonal patterns of litterfall in the floodplain forest of a large Mediterranean river. Limnetica 2012, 31, 173–185. [Google Scholar]
- Estiarte, M.; Peñuelas, J. Alteration of the phenology of leaf senescence and fall in winter deciduous species by climate change: Effects on nutrient proficiency. Glob. Chang. Biol. 2015, 21, 1005–1017. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vainio, E.J.; Velmala, S.M.; Salo, P.; Huhtinen, S.; Müller, M.M. Defoliation of Tilia cordata trees associated with Apiognomonia errabunda infection in Finland. Silva Fenn. 2017, 51, 1–10. [Google Scholar] [CrossRef] [Green Version]
Form of Asymmetry | Median (L-R) | Shape of L-R Distribution | Differences between the Left (L) and Right (R) Traits |
---|---|---|---|
Ideal fluctuating asymmetry (FA) | 0 | Normal | L = R |
Directional asymmetry (DA) | ≠0 | Normal | L ≠ R |
Antisymmetry (AS) | 0 | Platykurtic or bimodal (negative kurtosis) | L = R |
Studied Plots, Their Numbers and Traffic Intensity | Trait Number | |||
---|---|---|---|---|
1 | 2 | 3 | 4 | |
1. Forest Park Shchelkovsky (control plot) (0 veh/h) | FA | FA | FA | FA |
2. Nizhni Novgorod Kremlin (63 veh/h) | FA | FA | DA | DA |
3. Nevzorovyh Street (375 veh/h) | FA | 0.39AS; 0.11DA; 0.50FA | FA | FA |
4. Meditsinskaya Street (690 veh/h) | FA | FA | FA | FA |
5. Timiryazeva Street (1302 veh/h) | DA | FA | FA | DA |
6. Genkinoy Street (1233 veh/h) | FA | FA | FA | FA |
7. Belinskogo Street (no data) | – | – | – | – |
8. Gagarina Prospect (Lebedeva Street bus stop) (3768 veh/h) | DA | FA | FA | FA |
9. Gagarina Prospect (University bus stop) (4050 veh/h) | FA | DA | FA | FA |
10. Lyadov Square (5586 veh/h) | FA | DA | FA | FA |
Studied Plots, Their Numbers and Traffic Intensity | Trait Number | |||
---|---|---|---|---|
1 | 2 | 3 | 4 | |
1. Forest Park Shchelkovsky (control plot) (0 veh/h) | FA | FA | FA | DA |
2. Nizhni Novgorod Kremlin (60 veh/h) | FA | FA | DA | DA |
3. Nevzorovyh Street (291 veh/h) | FA | ? | ? | ? |
4. Meditsinskaya Street (801 veh/h) | FA | FA | FA | DA |
5. Timiryazeva Street (1167 veh/h) | FA | 0.88FA; 0.12DA | FA | FA |
6. Genkinoy Street (1221 veh/h) | FA | 0.54FA; 0.46DA | FA | FA |
7. Belinskogo Street (2103 veh/h) | FA | FA | FA | 0.76FA; 0.24DA |
8. Gagarina Prospect (Lebedeva Street bus stop) (3552 veh/h) | FA | 0.84FA; 0.16DA | 0.69FA; 0.28DA | DA |
9. Gagarina Prospect (University bus stop) (4455 veh/h) | DA | FA | DA | FA |
10. Lyadova Square (5082 veh/h) | DA | FA | AS | DA |
Studied Plots, Their Numbers and Traffic Intensity | Trait Number | ||||||
---|---|---|---|---|---|---|---|
1 | 2 | 3 | 4 | 5 | 6 | 7 | |
1. Forest Park Shchelkovsky (control plot) (0 veh/h) | DA | 0.77FA 0.23AS | FA | FA | FA | FA | FA |
2. Nizhni Novgorod Kremlin (89 veh/h) | ? | FA | FA | DA | 0.83DA 0.17AS | DA | FA |
3. Nevzorovyh Street (336 veh/h) | FA | FA | FA | FA | DA | FA | FA |
4. Meditsinskaya Street (750 veh/h) | FA | FA | FA | DA | FA | FA | FA |
5. Timiryazeva Street (876 veh/h) | FA | 0.72FA 0.28AS | FA | FA | FA | FA | DA |
6. Genkinoy Street (1410 veh/h) | DA | 0.92FA 0.08DA | DA | 0.91FA 0.09DA | AS | 0.60DA 0.40AS | FA |
7. Belinskogo Street (2145 veh/h) | FA | 0.58FA 0.42AS | DA | DA | FA | 0.90FA 0.01AS | 0.60DA 0.40AS |
8. Gagarina Prospect (Lebedeva Street bus stop) (3642 veh/h) | FA | 0.93FA 0.07DA | 0.22DA0.78AS | DA | DA | 0.45DA0.55AS | 0.81FA0.19AS |
9. Gagarina Prospect (University bus stop) (4869 veh/h) | FA | 0.60FA 0.40AS | FA | DA | FA | FA | DA |
10. Lyadov Square (3888 veh/h) | ? | ? | FA | FA | AS | FA | FA |
Studied Plots, Their Numbers and Traffic Intensity | Trait Number | ||||
---|---|---|---|---|---|
1 | 2 | 3 | 4 | 5 | |
1. Kiselikha Village (control) (0 veh/h) | FA | AS | AS | AS | FA |
2. Krilova Street (59 veh/h) | DA | FA | FA | FA | 0.9FA 0.1DA |
3. Nizhni Novgorod Kremlin (108 veh/h) | 0.71FA 0.29DA | FA | AS | AS | FA |
4. Lomonosova Street (137 veh/h) | DA | FA | FA | FA | FA |
5. Nesterova Street (303 veh/h) | FA | DA | FA | DA | DA |
6. Nartova Street (399 veh/h) | FA | FA | FA | FA | 0.73FA 0.27DA |
7. Meditsinskaya Street (973 veh/h) | FA | FA | FA | FA | FA |
8. Belinskogo Street (2204 veh/h) | FA | 0.77FA 0.23AS | FA | FA | FA |
9. Gagarina Prospect (Lebedeva bus stop) (3564 veh/h) | FA | FA | FA | FA | DA |
10. Gagarina Prospect (University bus stop) (3964 veh/h) | FA | FA | FA | AS | FA |
Studied Plots, Their Numbers and Traffic Intensity | Trait Number | ||||
---|---|---|---|---|---|
1 | 2 | 3 | 4 | 5 | |
1. Kiselikha Village (control) (0 veh/h) | DA | FA | FA | FA | DA |
2. Melnikova-Pecherskogo Street (4 veh/h) | FA | FA | FA | ? | FA |
3. Nizhni Novgorod Kremlin (72 veh/h) | FA | FA | FA | FA | DA |
4. Lomonosova Street (162 veh/h) | FA | FA | FA | FA | DA |
5. Hevzorovyh Street (293 veh/h) | DA | DA | FA | FA | DA |
6. Nartova Street (477 veh/h) | FA | FA | DA | FA | DA |
7. Meditsinskaya Street (989 veh/h) | FA | FA | DA | DA | DA |
8. Timiryazeva Street (1434 veh/h) | ? | DA | FA | FA | DA |
8. Belinskogo Street (2333 veh/h) | FA | FA | ? | FA | FA |
9. Gagarina Prospect (Lebedeva bus stop) (3135 veh/h) | FA | FA | FA | FA | DA |
10. Gagarina Prospect (University bus stop) (3784 veh/h) | DA | DA | FA | FA | DA |
Studied Plots, Their Numbers and Traffic Intensity | Trait Number | ||||
---|---|---|---|---|---|
1 | 2 | 3 | 4 | 5 | |
1. Kiselikha Village (control) (0 veh/h) | FA | FA | AS | AS | FA |
2. Melnikova-Pecherskogo Street (51 veh/h) | FA | FA | AS | AS | FA |
3. Nizhni Novgorod Kremlin (63 veh/h) | DA | AS | FA | FA | DA |
4. Lomonosova Street (153 veh/h) | AS | DA | AS | FA | FA |
5. Nevzorovih Street (282 veh/h) | FA | FA | 0.33 FA 0.67 DA | FA | FA |
6. Nartova Street (573 veh/h) | ФА | АС | АС | АС | ФА |
7. Meditsinskaya Street (618 veh/h) | DA | FA | FA | DA | DA |
8. Timiryazeva Street (1239 veh/h) | AS | FA | FA | DA | DA |
8. Belinskogo Street (2706 veh/h) | FA | FA | FA | FA | AS |
9. Gagarina Prospect (Lebedeva bus stop) (3291 veh/h) | AS | FA | AS | FA | AS |
10. Gagarina Prospect (University bus stop) (3990 veh/h) | FA | FA | FA | DA | FA |
Studied Plots, Their Numbers and Traffic Intensity | Trait Number | ||||
---|---|---|---|---|---|
1 | 2 | 3 | 4 | 5 | |
1. Kiselikha Village (control) (0 veh/h) | FA | FA | AS | AS | FA |
2. Nizhni Novgorod Kremlin (60 veh/h) | FA | DA | FA | AS | FA |
3. Melnikova-Pecherskogo Street (84 veh/h) | FA | FA | FA | DA | FA |
4. Lomonosova Street (120 veh/h) | FA | DA | DA | DA | AS |
5. Nevzorovih Street (186 veh/h) | FA | DA | DA | DA | AS |
6. Nartova Street (591 veh/h) | DA | FA | FA | FA | AS |
7. Meditsinskaya Street (915 veh/h) | DA | AS | AS | AS | FA |
8. Tmiryazeva Street (1167 veh/h) | DA | FA | FA | FA | DA |
8. Belinskogo Street (2103 veh/h) | FA | 0.81 FA; 0.19 DA | 0.80 FA; 0.20 DA | FA | FA |
9. Gagarina Prospect (Lebedeva bus stop) (3552 veh/h) | FA | DA | FA | FA | AS |
10. Gagarina Prospect (University bus stop) (4455 veh/h) | FA | FA | DA | FA | FA |
Studied Plots, Their Numbers and Traffic Intensity | Trait Number | ||||
---|---|---|---|---|---|
1 | 2 | 3 | 4 | 5 | |
1. Kiselikha Village (control) (0 veh/h) | DA | DA | ? | FA | DA |
2. Campus of Lobachevski University (6 veh/h) | DA | AS | FA | DA | DA |
3. Nizhni Novgorod Kremlin (102 veh/h) | 0.60 FA 0.40 DA | AS | FA | FA | DA |
4. Nevzorovih Street (285 veh/h) | FA | DA | FA | FA | DA |
5. Nartova Street (663 veh/h) | FA | AS | FA | FA | FA |
6. Meditsinskaya Street (915 veh/h) | DA | DA | FA | FA | DA |
7. Tmiryazeva Street (1308 veh/h) | FA | FA | FA | FA | DA |
8. Belinskogo Street (2487 veh/h) | 0.71 FA 0.29 DA | FA | FA | FA | DA |
9. Gagarina Prospect (Lebedeva bus stop) (3762 veh/h) | ? | FA | DA | FA | 0.80 FA 0.20 DA |
10. Gagarina Prospect (University bus stop) (4245 veh/h) | FA | DA | DA | FA | 0.90 FA 0.10 DA |
Plant Species, Sample Size | Asymmetry Type | ||||
---|---|---|---|---|---|
FA | DA | AS | Any Types of Mixed Asymmetry | Any Deviations from FA | |
B. pendula (n = 65) | 0.56 ± 0.06 | 0.17 ± 0.05 | 0.25 ± 0.05 | 0.03 ± 0.02 | 0.45 ± 0.06 |
T. cordata (n = 56) | 0.68 ± 0.06 | 0.20 ± 0.05 | 0 * | 0.13 * ± 0.05 | 0.32 ± 0.06 |
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Erofeeva, E.A.; Yakimov, B.N. Change of Leaf Trait Asymmetry Type in Tilia cordata Mill. and Betula pendula Roth under Air Pollution. Symmetry 2020, 12, 727. https://doi.org/10.3390/sym12050727
Erofeeva EA, Yakimov BN. Change of Leaf Trait Asymmetry Type in Tilia cordata Mill. and Betula pendula Roth under Air Pollution. Symmetry. 2020; 12(5):727. https://doi.org/10.3390/sym12050727
Chicago/Turabian StyleErofeeva, Elena A., and Basil N. Yakimov. 2020. "Change of Leaf Trait Asymmetry Type in Tilia cordata Mill. and Betula pendula Roth under Air Pollution" Symmetry 12, no. 5: 727. https://doi.org/10.3390/sym12050727