Abstract
Leaf shape variations and developmental instability were examined for the first time in natural populations of Prunus avium (L.) L. in the central Balkan region (Bosnia and Herzegovina) at different elevational points, from 230 to 1177 m. above sea level. Geometric morphometric tools were applied to assess the variability of leaf shapes and sizes, while a fluctuating asymmetry leaf index was used as a measure of leaf developmental instability. According to the results of canonical variate analysis for the symmetric component of shape variation and hierarchical analysis of variance for centroid size, the studied populations could be partially differentiated into three groups. The co-variation between leaf form (shape and size) and climate variables was significant, estimated by two-block partial least square analysis. Climate variables (the sum of precipitation in May and the De Martonne aridity index) mostly influenced leaf shape and size. A population situated at the highest elevation had the highest value for fluctuating asymmetry leaf index, which was an indication of developmental instability. High natural variability and interpopulation differences were observed for all studied leaf traits (leaf shape, centroid size, fluctuating asymmetry leaf index, leaf area, leaf length and width, petiole length). For well-known traditional morphometric measures (leaf area, leaf length, leaf width, and petiole length) in accordance with previous studies, intrapopulation variability was greater than interpopulation variability. For centroid size and the fluctuating asymmetry leaf index (measures used in geometric morphometrics) variability was higher among populations than within them. This indicates that geometric morphometrics could give new insights into infra-specific variability.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams DC, Otárola-Castillo E (2013) Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol Evol 4:393–399. https://doi.org/10.1111/2041-210X.12035
Albert CH, Thuiller W, Yoccoz NG, Soudant A, Boucher F, Saccone P, Lavorel S (2010) Intraspecific functional variability: extent, structure and sources of variation. J Ecol 98(3):604–613. https://doi.org/10.1111/j.1365-2745.2010.01651.x
Ballian D, Bogunić F, Čabaravdić A, Pekeč S, Franjić J (2012) Population differentiation in the wild cherry (Prunus avium L.) in Bosnia and Herzegovina. Period Biol 114:43–54. https://hrcak.srce.hr/80897
Baltas EA (2008) Climatic conditions and availability of water resources in Greece. Int J Water Resour D 24(4):635–649. https://doi.org/10.1080/07900620802230129
Bresson CC, Vitasse Y, Kremer A, Delzon S (2011) To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech? Tree Physiol 31(11):1164–1174. https://doi.org/10.1093/treephys/tpr084
Chitwood DH, Headland LR, Ranjan A, Martinez CC, Braybrook SA, Koenig DP, Sinha NR (2012) Leaf asymmetry as a developmental constraint imposed by auxin-dependent phyllotactic patterning. Plant Cell 24(6):2318–2327. https://doi.org/10.1105/tpc.112.098798
Chitwood DH, Rundell SM, Li DY, Woodford QL, Yu TT, Lopez JR, Greenblatt D, Kang J, Londo JP (2016) Climate and developmental plasticity: interannual variability in grapevine leaf morphology. Plant Physiol 170(3):1480–1491. https://doi.org/10.1104/pp.15.01825
Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Pooter H (2003) Handbook of protocols for standardised and easy measurement of plant functional traits worldwide. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51(4):335–380. https://doi.org/10.1071/BT02124
Demesure B, Comps B, Petit RJ (1996) Chloroplast DNA phylogeography of the common 670 beech (Fagus sylvatica L.) in Europe. Evolution 50:2515–2520. https://doi.org/10.1111/j.1558-5646.1996.tb03638.x
Ducci F, De Cuyper B, De Rogatis A, Dufour J, Santi F (2013) Wild Cherry Breeding (Prunus avium L.). In: Pâques LE (ed) Forest tree breeding in Europe, vol 25. Springer, Dordrecht, pp 463–511
Franiel I (2008) Fluctuating asymmetry of Betula pendula Roth leaves: an index of environment quality. Biodiv Res Conserv 9(10):1897–2810
Freeman DC, Brown ML, Duda JJ, Graraham JH, Emlen JM, Krzysik AJ, Balbach H, Kovacic DA, Zak JC (2005) Leaf fluctuating asymmetry, soil disturbance and plant stress: a multiple year comparison using two herbs, Ipomoea pandurate and Cnidoscoluss timulosus. Ecol Indic 5:85–95. https://doi.org/10.1016/j.ecolind.2004.05.002
Gömöry D, Paule L, Gömöryová E (2011) Effects of microsite variation on growth and adaptive traits in a beech provenance trial. J For Sci 57:192–199. https://doi.org/10.17221/88/2010-JFS
Gratani L (2014) Plant phenotypic plasticity in response to environmental factors. Adv Bot 2014:1–17. https://doi.org/10.1155/2014/208747
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. https://doi.org/10.1002/joc.1276
Hijmans RJ, Guarino L, Mathur P (2012) Manual of DIVA-GIS version 7.5
Hovenden MJ, Vander Schoor JK (2006) The response of leaf morphology to irradiance depends on altitude of origin in Nothofagus cunninghamii. New Phytol 169:291–297. https://doi.org/10.1111/j.1469-8137.2005.01585.x
Kiełtyk P (2017) Variation of vegetative and floral traits in the alpine plant Solidago minuta: evidence for local optimum along an elevational gradient. Alp Bot 128:47–57. https://doi.org/10.1007/s00035-017-0197-7
Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x
Klingenberg CP (2015) Analyzing fluctuating asymmetry with geometric morphometrics: concepts, methods, and applications. Symmetry 7:843–934. https://doi.org/10.3390/sym7020843
Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22(11):569–574. https://doi.org/10.1016/j.tree.2007.09.006
Kozlov MV, Cornelissen T, Gavrikov DE, Kunavin MA, Lama AD, Milligan JR, Zverev V, Zvereva EL (2017) Reproducibility of fluctuating asymmetry measurements in plants: sources of variation and implications for study design. Ecol Indic 73:733–740. https://doi.org/10.1016/j.ecolind.2016.10.033
Lindgren B, Laurila A (2005) Proximate causes of adaptive growth rates: growth efficiency variation among latitudinal populations of Rana temporaria. J Evol Biol 18(4):820–828. https://doi.org/10.1111/j.1420-9101.2004.00875.x
Liu Y, Li Y, Song J, Zhang R, Yan Y, Wang Y, Du FK (2018) Geometric morphometric analyses of leaf shapes in two sympatric Chinese oaks: Quercus dentata Thunberg and Quercus aliena Blume (Fagaceae). Ann For Sci 75(4):90
Mal TK, Uveges JL, Turk KW (2002) Fluctuating asymmetry as an ecological indicator of heavy metal stress in Lythrum salicaria. Ecol Indic 1(3):189–195. https://doi.org/10.1016/S1470-160X(02)00004-3
Meier IC, Leuschner C (2008) Leaf size and leaf area index in Fagus sylvatica Forests: competing effects of precipitation, temperature and nitrogen availability. Ecosystems 11(5):655–669. https://doi.org/10.1007/s10021-008-9135-2
Miljković D (2012) Developmental stability of Iris pumila flower traits: a common garden experiment. Arch Biol Sci 64:123–133. https://doi.org/10.2298/ABS1201123M
Miljković D, Selaković S, Vujić V, Stanisavljević N, Radović S, Cvetković D (2018) Patterns of herbivore damage, developmental stability, morphological and biochemical traits in female and male Mercurialis perennis in contrasting light habitats. Alp Bot 128:193–206. https://doi.org/10.1007/s00035-018-0203-8
Mratinić E, Fotirić Akšić M, Jovković R (2012) Analysis of wild sweet cherry (Prunus avium L.) germplasm diversity in South-East Serbia. Genetika 44:259–268. https://doi.org/10.2298/GENSR1202259M
Nicotra AB, Leigh A, Boyce CK, Jones CS, Niklas KJ, Royer DL, Tsukaya H (2011) The evolution and functional significance of leaf shape in the angiosperms. Funct Plant Biol 38(7):535–552. https://doi.org/10.1071/FP11057
Palmer AR (1994) Fluctuating asymmetry analyses: a primer. In: Markow TA (ed) Developmental instability: its origins and evolutionary implications. Springer Kluwer, Dordrecht, pp 335–364
Palmer AR, Strobeck C (2003) Fluctuating asymmetry analysis revisited. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, Oxford, pp 279–319
Pescador DS, de Bello F, Valladares F, Escudero A (2015) Plant trait variation along an altitudinal gradient in mediterranean high mountain grasslands: controlling the species turnover effect. PLoS One 10(3):p.e0118876. https://doi.org/10.1371/journal.pone.0118876
Popović V, Kerkez I (2016) Population variability of wild cherry (Prunus avium L.) in Serbia according to the leaf morphology. Šumarski list 140:347–355. https://doi.org/10.31298/sl.140.7-8.3
Rakonjac V, Mratini E, Jovković R, Fotiri M (2014) Analysis of morphological variability in wild cherry (Prunus avium L.) genetic resources from central Serbia. J Agric Sci Technol 16:151–162
Read QD, Moorhead LC, Swenson NG, Bailey JK, Sanders NJ (2014) Convergent effects of elevation on functional leaf traits within and among species. Funct Ecol 28:37–45. https://doi.org/10.1111/1365-2435.12162
Reinhardt D (2005) Regulation of phyllotaxis. Int J Dev Biol 49:539–546. https://doi.org/10.1387/ijdb.041922dr
Rohlf J (2016a) tpsUtil v 1.70 (computer program). Stony Brook University, New York
Rohlf J (2016b) tpsDig2 v 2.26 (computer program). Stony Brook University, New York
Russell K (2003) EUFORGEN Technical Guidelines for genetic conservation and use for wild cherry (Prunus avium). Drawings: Prunus avium.. International Plant Genetic Resources Institute, Rome
Santi F, Muranty H, Dufour J, Paques LE (1998) Genetic parameters and selection in a multisite wild cherry clonal test. Silvae Genet 47(2–3):61–67
SAS Institute, Inc. (2011) The SAS System for Windows, release 9.3. SAS Institute, Cary
Seguí J, Lázaro A, Traveset A, Salgado-Luarte C, Gianoli E (2017) Phenotypic and reproductive responses of an Andean violet to environmental variation across an elevational gradient. Alp Bot 128:59–69. https://doi.org/10.1007/s00035-017-0195-9
Sheets HD, Zelditch M, Swiderski D (2002) Morphometrics software: IMP-Integrated morphometrics package. https://www3.canisus.edu/~sheets/morphsoft.html
Šilić Č (2005) Atlas of Dendroflora (trees and shrubs) in Bosnia and Herzegovina. Franjevacka kuca Masna Luka, Matica hrvatska Citluk, Citluk
Sørensen JG, Norry FM, Scannapieco AC, Loeschcke V (2005) Altitudinal variation for stress resistance traits and thermal adaptation in adult Drosophila buzzatiifrom the new world. J Evol Biol 18:829–837. https://doi.org/10.1111/j.1420-9101.2004.00876.x
Souza GM, Viana JDOF, Oliveira RFD (2005) Asymmetrical leaves induced by water deficit show asymmetric photosynthesis in common bean. Braz J Plant Physiol 17(2):223–227. https://doi.org/10.1590/S1677-04202005000200005
Stefanović M, Nikolić B, Matić R, Popović Z, Vidaković V, Bojović S (2017) Exploration of sexual dimorphism of Taxus baccata L. needles in natural populations. Trees 31:1697–1710. https://doi.org/10.1007/s00468-017-1579-6
Teeling C, Maxted N, Ford-Lloyd BV (2012) The challenges of modelling species distribution: a case study of wild cherry (Prunus avium L.) in Europe. In: Maxted M, Dulloo E, Ford-Lloyd BV, Frese L, Iriondo JM, Pinheiro de Carvalho MAA (eds) Agrobiodiversity conservation: securing the diversity of crop wild relatives and landraces. CABI, London, pp 29–35
Telhado C, Fernando AO, Silveira G, Fernandes W, Cornelissen T (2017) Fluctuating asymmetry in leaves and flowers of sympatric species in a tropical montane environment. Plant Spec Biol 32:3–12. https://doi.org/10.1111/1442-1984.12122
Temel F (2018) Leaf size variation in natural wild cherry (Prunus avium) populations in Turkey. Int J Agric Biol. https://doi.org/10.17957/IJAB/15.0722
Tucić B, Miljković D (2010) Fluctuating asymmetry of floral organ traits in natural populations of Iris pumilafrom contrasting light habitats. Plant Spec Biol. 25:173–184. https://doi.org/10.1111/j.1442-1984.2010.00284.x
Viscosi V, Fortini P, Slice DE, Loy A, Blasi C (2009) Geometric morphometric analyses of leaf variation in four oak species of subgenus Quercus (Fagaceae). Plant Biosyst 143:575–587. https://doi.org/10.1080/11263500902775277
Welk E, De Rigo D, Caudullo G (2016) Prunus avium in Europe: distribution, habitat, usage and threats. In: Mubareka S, Jonsson R, Rinaldi F, Azevedo J, de Rigo D, Sikkema R (eds) European Atlas of forest tree species. Publication Office of the European Union, Luxembourg, pp 140–141
Wright IJ, Dong N, Maire V, Prentice IC, Westoby M, Díaz S et al (2017) Global climatic drivers of leaf size. Science 357(6354):917–921. https://doi.org/10.1126/science.aal4760
Acknowledgements
This paper was achieved as part of the project “Biosensing Technologies and Global System for Long-Term Research and Integrated Management of Ecosystems” (III-43002) and “Evolution in heterogeneous environments: mechanisms of adaptation, biodiversity conservation and biomonitoring” (OI-173025) financed by the Ministry of Education and Science of the Republic of Serbia. We thank the anonymous reviewers for their careful reading of our manuscript and their valuable comments and suggestions. The authors wish to thank the English language editor, native speaker and teacher of English Mrs Esther Grace Helajzen for proofreading and revised text correction,.
Author information
Authors and Affiliations
Contributions
DM, SO and SS designed the research. MSN and LK collected and scanned the specimens. DM performed digitalization of specimens and analysis of fluctuating asymmetry. MS conducted analysis of leaf size and shape. DM and MS wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Miljković, D., Stefanović, M., Orlović, S. et al. Wild cherry (Prunus avium (L.) L.) leaf shape and size variations in natural populations at different elevations. Alp Botany 129, 163–174 (2019). https://doi.org/10.1007/s00035-019-00227-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00035-019-00227-1