Leaf macro- and micromorphological traits and phenotypic diversity of Quercus petraea subspecies in Eastern Romania
DOI:
https://doi.org/10.15835/nbha52413966Keywords:
leaf descriptors, peripheral populations, Quercus petraea subsp. petraea, Quercus petraea subsp. dalechampii, Quercus petraea subsp. polycarpa, Sessiliflorae Loj., taxonomic classificationAbstract
Sessile oak (Quercus petraea) is a polytypic species comprising three subspecies (Q. petraea subsp. petraea – Qpe, Q. petraea subsp. dalechampii – Qda, and Q. petraea subsp. polycarpa – Qpo) with distinct ecological requirements, posing significant challenges in morphological differentiation. The integration of macro- and micro-morphological analyses plays a crucial role in clarifying the taxonomic uncertainties. This study aimed to characterize phenotypic diversity and identify key leaf descriptors for distinguishing sessile oak subspecies across three peripheral populations, one reference population, and one sessile oak comparative trail from Eastern Romania. A comprehensive analysis was conducted on 227 sampled trees, utilizing multivariate statistical analysis - encompassing 18 macromorphological and 9 micromorphological leaf descriptors. The results revealed distinct traits of Qda and Qpo, including shorter leaves with maximal width in the lower half of the lamina, fewer lobes, ovate shapes, a subcordate basal shape, and a higher intercalary vein frequency compared to Qpe. Furthermore, Qpo could be differentiated from both Qpe and Qda by its shorter lamina lengths, fewer lobes, greater lobe width ratios, and stellate trichomes with shorter rays. The length of rays of stellate trichomes has emerged as a significant micromorphological descriptor. Qda predominated in peripheral populations, likely due to natural selection in drought-affected local ecosystems. This highlights the importance of prioritizing this taxon in breeding programs and conserving it in situ, given its remarkable leaf plasticity and adaptability. Additionally, principal component indicated a fairly high level of morphological similarity among the three subspecies. These findings emphasize the critical importance of comprehensive morphological analyses for precise species classification and deeper understanding of sessile oak taxonomy.
References
Aas G (1993). Taxonomical impact of morphological variation in Quercus robur and Q. petraea: a contribution to the hybrid controversy. Annales des Sciences Forestières 50(1):107s-113s. https://doi.org/10.1051/forest:19930709
Abrams MD (1994). Genotypic and phenotypic variation as stress adaptations in temperate tree species: a review of several case studies. Tree Physiology 14(7-8-9): 833-842. https://doi.org/10.1093/treephys/14.7-8-9.833
Apostol EN, Curtu AL, Daia LM, Apostol B, Dinu CG, Şofletea N (2017). Leaf morphological variability and intraspecific taxonomic units for pedunculate oak and grayish oak (genus Quercus L., series Pedunculatae Schwz.) in Southern Carpathian Region (Romania). Science of The Total Environment 609:497–505.
https://doi.org/10.1016/J.SCITOTENV.2017.05.274
Apostol EN, Curtu AL, Șofletea N (2015). Structura taxonomică intraspecifică într-un complex de cvercinee din estul României, la contactul cu zona silvostepei externe [Intraspecific taxonomic structure in a mixed oak stand from Eastern Romania, at contact with external forest steppe]. Revista de Silvicultură și Cinegetică 37:47-51.
Ashton PMS, Berlyn GP (1994). A comparison of leaf physiology and anatomy of Quercus (section Erythrobalanus ‐Fagaceae) species in different light environments. American Journal of Botany 81(5):589-597. https://doi.org/10.1002/j.1537-2197.1994.tb15489.x
Bacilieri R, Ducousso A, Kremer A (1995). Genetic, morphological, ecological and phenological differentiation between Quercus petraea (Matt.) Liebl. and Quercus robur L. in a mixed stand of Northwest of France. Silvae Genetica 44(1):1–9.
Bacilieri R, Ducousso A, Kremer A (1996). Comparison of morphological characters and molecular markers for the analysis of hybridization in sessile and pedunculate oak. Annales des Sciences Forestières 53(1):79-91. https://doi.org/10.1051/forest:19960106
Beldie A (1952). Genul Quercus [Genus Quercus]. Flora RPR I:224-261.
Beldie A, Cretzoiu P (1941). Studiu sistematic al gorunului din România [Systematic study of sessile oak in Romania]. Analele ICAS 7(1):38-49.
Biondi E, Casavecchia S, Guerra V, Medagli P, Beccarisi L, Zuccarello V (2004). A contribution towards the knowledge of semideciduous and evergreen woods of Apulia (South-Eastern Italy). Fitosociologia 41(1):3-28.
Boratynski A, Marcysiak K, Lewandowska A, Jasinska A, Iszkulo G, Burczyk J (2008). Differences in leaf morphology between Quercus petraea and Q. robur adult and young individuals. Silva Fennica 42(1):115.
Borazan A, Babaç MT (2003). Morphometric leaf variation in oaks (Quercus) of Bolu, Turkey. Annales Botanici Fennici 233-242.
Brullo S, Guarino R, Siracusa G (1999). Revisione tassonomica delle querce caducifoglie della Sicilia [Taxonomic revision of deciduous oak trees in Sicily]. Webbia 54(1):1-72. https://doi.org/10.1080/00837792.1999.10670670
Bruschi P (2010). Geographical variation in morphology of Quercus petraea (Matt.) Liebl. as related to drought stress. Plant Biosystems 144(2):298-307. https://doi.org/10.1080/11263501003672462
Bruschi P, Grossoni P, Bussotti F (2003). Within- and among-tree variation in leaf morphology of Quercus petraea (Matt.) Liebl. natural populations. Trees - Structure and Function 17(2):164-172. https://doi.org/10.1007/s00468-002-0218-y
Bruschi P, Vendramin GG, Bussotti F, Grossoni P (2000). Morphological and molecular differentiation between Quercus petraea (Matt.) Liebl. and Quercus pubescens Willd. (Fagaceae) in Northern and Central Italy. Annals of Botany 85(3):325-333. https://doi.org/10.1006/anbo.1999.1046
Bussotti F, Grossoni P (1997). European and Mediterranean oaks (Quercus L.; Fagaceae): SEM characterization of the micromorphology of the abaxial leaf surface. Botanical Journal of the Linnean Society 124(2):183-199. https://doi.org/10.1111/j.1095-8339.1997.tb01789.x
Bussotti F, Pollastrini M, Holland V, Brüggemann W (2015). Functional traits and adaptive capacity of European forests to climate change. Environmental and Experimental Botany 111: 91-113. https://doi.org/10.1016/j.envexpbot.2014.11.006
Camus A (1954). 1936–1954. Les chenes monographie du genre Quercus (et Lithocarpus) [Monograph of the Genus Quercus (and Lithocarpus)]. Encyclopédie Economique de Sylviculture 6-8.
Christensen KI (1997). Quercus L. In: Strid A, Tan K (Eds). Flora Hellenica. I. pp 42-50.
Clinovschi F (2005). Dendrologie [Dendrology]. Editura Universităţii din Suceava.
Constantinescu N (1973). Regenerarea arboretelor [The Regeneration of Forests]. Ediţia a II-a, Ed. Ceres, Bucureşti, pp 668.
Curtu AL, Gailing O, Finkeldey R (2007). Evidence for hybridization and introgression within a species-rich oak (Quercus spp.) community. BMC Evolutionary Biology 7:1-15. https://doi.org/10.1186/1471-2148-7-218
Curtu AL, Sofletea N, Toader AV, Enescu MC (2011). Leaf morphological and genetic differentiation between Quercus robur L. and its closest relative, the drought-tolerant Quercus pedunculiflora K. Koch. Annals of Forest Science 68:1163-1172. https://doi.org/10.1007/s13595-011-0105-z
de Boer HJ, Drake PL, Wendt E, Price CA, Schulze E-D, Turner NC, Nicolle D, Veneklaas EJ (2016). Apparent overinvestment in leaf venation relaxes leaf morphological constraints on photosynthesis in arid habitats. Plant Physiology 172(4):2286-2299. https://doi.org/10.1104/pp.16.01313
Demeter Z, Kanalas P, Máthé C, Cseke K, Szollosi E, M-Hamvas M, Jámbrik K, Kiss Z, Mészáros I (2014). Osmotic stress responses of individual white oak (Quercus section, Quercus subgenus) genotypes cultured in vitro. Journal of Plant Physiology 171(2):16-24. https://doi.org/10.1016/J.JPLPH.2013.09.013
Deng M, Jiang XL, Song YG, Coombes A, Yang XR, Xiong YS, Li QS (2017). Leaf epidermal features of Quercus Group Ilex (Fagaceae) and their application to species identification. Review of Palaeobotany and Palynology 237:10-36. https://doi.org/10.1016/J.REVPALBO.2016.11.006
Di Pietro R, Conte AL, Di Marzio P, Fortini P, Farris E, Gianguzzi L, Müller M, Rosati L, Spampinato G, Gailing O (2021). Does the genetic diversity among pubescent white oaks in southern Italy, Sicily and Sardinia islands support the current taxonomic classification? European Journal of Forest Research 140(2):355-371. https://doi.org/10.1007/s10342-020-01334-z
Di Pietro R, Conte AL, Di Marzio P, Gianguzzi L, Spampinato G, Caldarella O, Fortini P (2020a). A multivariate morphometric analysis of diagnostic traits in southern Italy and Sicily pubescent oaks. Folia Geobotanica 55(3):163-183. https://doi.org/10.1007/s12224-020-09378-0
Di Pietro R, Di Marzio P, Antonecchia G, Conte AL, Fortini P (2020b). Preliminary characterization of the Quercus pubescens complex in southern Italy using molecular markers. Acta Botanica Croatica 79(1):0. https://doi.org/10.37427/botcro-2020-002
Di Pietro R, Di Marzio P, Medagli P, Misano G, Silletti GN, Wagensommer RP, Fortini P (2016). Evidence from multivariate morphometric study of the Quercus pubescens complex in Southeast Italy. Botanica Serbica 40(1):83-100. https://doi.org/10.5281/zenodo.48865
Di Pietro R, Viscosi V, Peruzzi L, Fortini P (2012). A review of the application of the name Quercus dalechampii. Taxon 61(6):1311-1316. https://doi.org/10.1002/tax.616012
Du B, Zhu Y, Kang H, Liu C (2021). Spatial variations in stomatal traits and their coordination with leaf traits in Quercus variabilis across Eastern Asia. Science of The Total Environment 789:147757. https://doi.org/10.1016/J.SCITOTENV.2021.147757
Dupouey J-L, Badeau V (1993). Morphological variability of oaks (Quercus robur L, Quercus petraea (Matt) Liebl, Quercus pubescens Willd) in Northeastern France: preliminary results, 35s-40s. In: Annales des sciences forestières. EDP Sciences. https://doi.org/10.1051/forest:19930702
Enescu CM, Curtu AL, Şofletea N (2013). Is Quercus virgiliana a distinct morphological and genetic entity among European white oaks? Turkish Journal of Agriculture and Forestry 37(5):632-641. https://doi.org/10.3906/tar-1210-28
Enescu CM, Sofletea N, Curtu AL (2012). A multivariate approach to differentiate three Romanian oak species: a case study. Bulletin of the Transilvania University of Brasov. Series II: Forestry• Wood Industry• Agricultural Food Engineering 29-34.
Filipova E, Asenov A (2016). Review on Quercus dalechampii Ten. and Quercus petraea (Mattuschka) Liebl. in the vegetation of Bulgaria. Annual of Sofia University “St. Kliment Ohridski” Faculty of Biology, BOOK 2 – BOTANY 100.
Fortini P, Antonecchia G, Di Marzio P, Maiuro L, Viscosi V (2013). Role of micromorphological leaf traits and molecular data in taxonomy of three sympatric white oak species and their hybrids (Quercus L.). Plant Biosystems 149(3):546-558. https://doi.org/10.1080/11263504.2013.868374
Fortini P, Di Marzio P, Di Pietro R (2015). Differentiation and hybridization of Quercus frainetto, Q. petraea, and Q. pubescens (Fagaceae): insights from macro-morphological leaf traits and molecular data. Plant Systematics and Evolution 301(1):375-385. https://doi.org/10.1007/s00606-014-1080-2
Fortini P, Viscosi V, Maiuro L, Fineschi S, Vendramin GG (2009). Comparative leaf surface morphology and molecular data of five oaks of the subgenus Quercus oerst (Fagaceae). Plant Biosystems 143(3):543-554. https://doi.org/10.1080/11263500902722980
Franjić J, Liber Z, Škvorc Ž, Idžojtić M, Šoštarić R, Stančić Z (2006). Morphological and molecular differentiation of the Croatian populations of Quercus pubescens Willd. (Fagaceae). Acta Societatis Botanicorum Poloniae 75(2):123-130. https://doi.org/10.5586/asbp.2006.015
Gafenco IM (2023). Phenological structure and phenotypic analysis for leaf descriptors in peripheral populations of sessile oak (Quercus petraea (Matt.) Liebl.) from Eastern Romania. PhD Thesis, Transilvania University of Brasov, Brasov.
Gafenco IM, Pleșca BI, Șofletea N (2023). The taxonomic structure of sessile oak (Quercus petraea (Matt.) Liebl.) in marginal populations from Eastern Romania–a bibliographic study. Revista de Silvicultură şi Cinegetică 27(52): 39-45.
Gancz V, Doniţă N, Bândiu C, Biriş IA, Apostol J, Marcu C (2008). Harta pădurilor pe unităţi ecosistemice [Forest ecosistem units map], Scalea 1: 100.000. Editura Silvică.
Gellini R, Bussotti F, Bettini D, Grossoni P, Bottacci A (1992). Species of the genus Quercus in Italy: characterization by means of leaf surface observation. Plant Biosystem 126(3-4):481-504.
Georgescu C, Ciobanu R (1965). Consideraţii geografico-ecologice asupra speciilor de Quercus din seriile Lanuginosae Simk. și Sessiliflorae [Geographic-ecological considerations about Quercus species from Lanuginosae Simk. and Sessiliflorae series]. Locaj. din R.P.R. Studii și Cercetări de Biologie, Seria Botanică 18(4):299-301.
Georgescu CC, Morariu I (1948). Monografia Stejarilor Din România [Monography of Oaks from Romania]. Tip." Universul" SA.
Govaerts R, Frodin DG (1998). World Checklist and Bibliography of Fagales. Kew: Royal Botanic Gardens.
Grossoni P, Bruschi P, Bussotti F, Pollastrini M, Selvi F (2021). The taxonomic interpretation of Mediterranean oaks of Quercus sect. Quercus (Fagaceae): uncertainties and diverging concepts. Flora Mediterranea 31:271-278. https://doi.org/10.7320/FlMedit31SI.271
Hernandez JO, Park BB (2022). The leaf trichome, venation, and mesophyll structural traits play important roles in the physiological responses of oak seedlings to water-deficit stress. International Journal of Molecular Sciences 23(15):8640. https://doi.org/10.3390/ijms23158640
Hetherington AM, Woodward FI (2003). The role of stomata in sensing and driving environmental change. Nature 424(6951):901-908. https://doi.org/10.1038/nature01843
Jerše M, Batič F (2007). Morfološka analiza puhastega hrasta (Quercus pubescens Willd.) v Sloveniji [Morphological analysis of pubescent oak (Quercus pubescens Willd.) in Slovenia]. Zbornik gozdarstva in lesarstva 83:35-45.
Jovanović M, Janković IK, Milovanović J, Nonić M, Šijačić-Nikolić M (2023). Intraspecific variability of the sessile oak (Quercus petraea Matt. Liebl.) leaf traits from the Mount Kosmaj (Serbia). Biology Bulletin 50(6):1223-1233. https://doi.org/10.1134/S1062359023602471
Jovanovic M, Tucovic A (1975). Genetics of common and sessile oak (Quercus robur L. and Q. petraea Liebl.). Annales Forestales 7(2):23-53.
Jurkšiene G, Baliuckas V (2014). Leaf morphological variation of sessile oak (Quercus petraea [Matt.] Liebl.) and pedunculate oak (Quercus robur L.) in Lithuania. Research for Rural Development 2:63-69.
Kissling P (1977). Les poils des quatre espéces de chénes du Jura (Quercus pubescens, Q. petraea, Q. robur et Q. cerris). Ber. Schweiz. Berichte der Schweizerischen Botanischen Gesellschaft 87:1-18.
Kleiman D, Aarssen LW (2007). The leaf size/number trade‐off in trees. Journal of Ecology 95(2):376-382. https://doi.org/10.1111/j.1365-2745.2006.01205.x
Kleinschmit J (1993). Intraspecific variation of growth and adaptive traits in European oak species. In: Annales des sciences forestières. EDP Sciences. Pp 166-185.
Kremer A, Dupouey JL, Deans JD, Cottrell J, Csaikl U, Finkeldey R, Espinel S, Jensen J, Kleinschmit J, Van Dam B (2002). Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Annals of Forest Science 59(7):777-787. https://doi.org/10.1051/forest:2002065
Kučera P (2018). New name for Central Europaean oak formerly labelled as Quercus dalechampii. Biologia 73(4):313-317. https://doi.org/10.2478/s11756-018-0048-z
López de Heredia U, Valbuena-Carabaña M, Córdoba M, Gil L (2009). Variation components in leaf morphology of recruits of two hybridising oaks (Q. petraea [Matt.] Liebl. and Q. pyrenaica Willd.) at small spatial scale. European journal of forest research 128:543-554. https://doi.org/10.1007/s10342-009-0302-6
Manos PS, Doyle JJ, Nixon KC (1999). Phylogeny, biogeography, and processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae). Molecular Phylogenetics and Evolution 12(3):333-349. https://doi.org/10.1006/mpev.1999.0614
Matula R (2009). Analysis of ecology of a little-known white oak schur, using geobiocoenological typology. Journal of Landscape Ecology 2(2):30-40.
Mátyás V (1971). Short taxonomic review of the Oaks of Hungary. Erdészeti Kutatások 67(2):55-68.
Mediavilla S, Escudero A (2004). Stomatal responses to drought of mature trees and seedlings of two co-occurring Mediterranean oaks Forest Ecology and Management 187(2-3):281-294.
Mediavilla S, Martín I, Babiano J, Escudero A (2019). Foliar plasticity related to gradients of heat and drought stress across crown orientations in three Mediterranean Quercus species. PLoS One 14(10):e0224462. https://doi.org/10.1371/journal.pone.0224462
Meng Y, Wang J-J, Nie Z-L (2016). Comparative morphology of leaf epidermis in 34 species of Maianthemum (Asparagaceae, Polygonateae) and their systematic significance. Phytotaxa 275(2):81-96. https://doi.org/10.11646/phytotaxa.275.2.1
Milletti N, Paoli P, Moggi G (1982). Ricerche sulle querce caducifoglie italiane. 6. Analisi numerica della morfologia fogliare in un popolamento di Quercus petraea [Matt.] Liebl. delle Alpi orientali. Webbia 36(1):101-133.
Morales F, Abadía A, Abadía J, Montserrat G, Gil-Pelegrín E (2002). Trichomes and photosynthetic pigment composition changes: Responses of Quercus ilex subsp. ballota (Desf.) Samp. and Quercus coccifera L. to Mediterranean stress conditions. Trees - Structure and Function 16(7):504-510. https://doi.org/10.1007/s00468-002-0195-1
Nixon KC (1993). Infrageneric classification of Quercus (Fagaceae) and typification of sectional names. Annales des Sciences Forestières 50:25s-34s. https://doi.org/10.1051/forest:19930701
Nyman CF (1884). Conspectus Florae Europaeae: Seu Enumeratio Methodica Plantarum Phanerogamarum Europae Indigenarum, Indicatio Distributionis Geographicae Singularium Etc. Supplementum I. typis officinae Bohlinianae.
Ogaya R, Peñuelas J (2007). Leaf mass per area ratio in Quercus ilex leaves under a wide range of climatic conditions. The importance of low temperatures. Acta Oecologica 31(2):168-173. https://doi.org/10.1016/J.ACTAO.2006.07.004
Owusu SA, Sullivan AR, Weber JA, Hipp AL, Gailing O (2015). Taxonomic relationships and gene flow in four North American Quercus species (Quercus section Lobatae). Systematic Botany 40(2):510-521. https://doi.org/10.1600/036364415X688754
Panahi P, Jamzad Z, Pourmajidian M, Fallah A, Pourhashemi M, Sohrabi H (2012). Taxonomic revision of the Quercus brantii complex (Fagaceae) in Iran with emphasis on leaf and pollen micromorphology. Acta Botanica Hungarica 54(3-4):355-375.
Petit RJ, Bodénès C, Ducousso A, Roussel G, Kremer A (2003). Hybridization as a mechanism of invasion in oaks. New Phytologist 161(1):151-164. https://doi.org/10.1046/j.1469-8137.2003.00944.x
Ponton S, Dupouey J-L, Dreyer E (2004). Leaf morphology as species indicator in seedlings of Quercus robur L. and Q. petraea [Matt.] Liebl.: modulation by irradiance and growth flush. Annals of Forest Science 61:73-80. https://doi.org/10.1051/forest:2003086
Požgaj J, Horváthová J (1986). Variabilita a Ekológia Druhov Rodu Quercus L. Na Slovensku. Veda, vydavatel̕stvo Slovenskej akadémie vied.
Proietti E, Filesi L, Di Marzio P, Di Pietro R, Masin R, Conte AL, Fortini P (2021). Morphology, geometric morphometrics, and taxonomy in relict deciduous oaks woods in Northern Italy. Rendiconti Lincei. Scienze Fisiche e Naturali 32(3):549-564. https://doi.org/10.1007/s12210-021-01001-4
Qiu J, Lin M, Tan D (2023). Taxonomic implications of leaf morphology and epidermal anatomy for 14 species of Gagea (Liliaceae) from Xinjiang, China. Botanical Studies 64(1):33. https://doi.org/10.1186/s40529-023-00405-9
Raab-Straube E Von, Raus T (2013). Euro+ Med-Checklist Notulae, 1. Willdenowia 43(1):151-164.
Roleček J (2005). Vegetation types of dry-mesic oak forests in Slovakia. Preslia 77(3):241-261.
Roussel M, Le Thiec D, Montpied P, Ningre N, Guehl J-M, Brendel O (2009). Diversity of water use efficiency among Quercus robur genotypes: contribution of related leaf traits. Annals of Forest Science 66(4):1-10. https://doi.org/10.1051/forest/2009010
Rushton BS (1993). Natural hybridization within the genus Quercus L. Annales des Sciences Forestières 50(EDP Sciences):73s-90s. https://doi.org/10.1051/forest:19930707
Sack L, Scoffoni C (2013). Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytologist 198(4):983-1000. https://doi.org/10.1111/nph.12253
Sanda V, Barabaş N, Ştefănuţ S (2004). Atlas Florae Romaniae. III-Genul Quercus. Editura “Ion Borcea”, Bacău.
Schwarz O (1936). Entwurf zu einem natürlichen System der Cupuliferen und der Gattung Quercus L. Notizblatt des Botanischen Gartens und Museums zu Berlin-Dahlem 13(166):1-22.
Schwarz O (1993). Quercus L. In: Tutin TG, Burges NA, Chater AO, Edmondson JR, Heywood VH, Moore DM, Valentine DH, Walters SM, Webb DA (Eds). Flora Europaea. Cambridge Universita Press, pp 72-76.
Scoffoni C, Rawls M, McKown A, Cochard H, Sack L (2011). Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture. Plant Physiology 156(2):83-843. https://doi.org/10.1104/pp.111.173856
Scotti-Saintagne C, Mariette S, Porth I, Goicoechea PG, Barreneche T, Bodénes C, Burg K, Kremer A (2004). Genome scanning for interspecific differentiation between two closely related oak species (Quercus robur L. and Q. petraea [Matt.] Liebl.). Genetics 168(3):1615-1626. https://doi.org/10.1534/genetics.104.026849
Sheskin DJ (2003). Handbook of Parametric and Nonparametric Statistical Procedures. Chapman and hall/CRC.
Şofletea N (2005). Genetică și Ameliorarea Arborilor [Genetics and tree breeding]. Ed. Pentru Viaţă.
Şofletea N, Curtu L (2007). Dendrologie [Dendrology]. Editura Universităţii Transilvania Braşov, pp 418.
Șofletea N, Moldovan IC, Enescu MC, Crăciunesc I, Curtu AL (2011). Considerații privind identificarea hibrizilor între speciile autohtone de cvercinee [Considerations about identifing hybrids between autochtonous Quercus species]. Revista pădurilor 126(1):6-11.
Șofletea N, Târziu D, Spârchez G, Curtu AL (2001). Research regarding the sessile oak high-altitude ecotype from Poiana Brașov. Analele ICAS 44(1):17-22.
Soheili F, Heydari M, Woodward S, Naji HR (2023). Adaptive mechanism in Quercus brantii Lindl. leaves under climatic differentiation: morphological and anatomical traits. Scientific Reports 13(1):1-12. https://doi.org/10.1038/s41598-023-30762-1
Stănescu V, Şofletea N, Popescu OC (1997). Flora forestieră lemnoasă a României [Romanian wood flora]. București: Ceres.
Stuparu E, Guiman G, Scărlătescu V (2003). Cercetări privind diversitatea genetică a gorunului din populaţii naturale din subregiunea Făgăraş Sud [Research on the genetic diversity of the oak from natural populations in the Fagaras Sud subregion]. Analele ICAS 45:39-46.
Ullah F, Zafar M, Amhad M, Sultana S, Ullah A, Shah SN, Butt MA, Mir S (2018). Taxonomic implications of foliar epidermal characteristics in subfamily Alsinoideae (Caryophyllaceae). Flora 242:31-44. https://doi.org/10.1016/J.FLORA.2018.02.003
Uribe-Salas D, Sáenz-Romero C, González-Rodríguez A, Téllez-Valdéz O, Oyama K (2008). Foliar morphological variation in the white oak Quercus rugosa Née (Fagaceae) along a latitudinal gradient in Mexico: potential implications for management and conservation. Forest ecology and Management 256(12):2121-2126.
https://doi.org/10.1016/j.foreco.2008.08.002
Viscosi V, Lepais O, Gerber S, Fortini P (2009). Leaf morphological analyses in four European oak species (Quercus) and their hybrids: A comparison of traditional and geometric morphometric methods. Plant Biosystems 143(3):564-574. https://doi.org/10.1080/11263500902723129
Wang R, Yu G, He N, Wang Q, Xia F, Zhao N, Xu Z, Ge J (2014). Elevation-related variation in leaf stomatal traits as a function of plant functional type: evidence from Changbai Mountain, China. PLoS One 9(12):e115395. https://doi.org/10.1371/journal.pone.0115395
Wigston DL (1975). The distribution of Quercus robur L., Q. petraea [Matt.] Liebl. and their hybrids in south-western England 1. The Assessment of the taxonomic status of populations from leaf characters. Watsonia 10:345-369.
WinFOLIA PRO (2020). Regent Instruments Inc., Canada.
Yücedaǧ C, Gailing O (2013). Morphological and genetic variation within and among four Quercus petraea and Q. robur natural populations. Turkish Journal of Botany 37(4):619-629. https://doi.org/10.3906/bot-1205-18
Yücedağ C, Müller M, Gailing O (2021). Morphological and genetic variation in natural populations of Quercus vulcanica and Q. frainetto. Plant Systematics and Evolution 307(1):1-15. https://doi.org/10.1007/s00606-020-01737-w
Yücedağ C, Sanders J, Musah M, Gailing O (2019). Stomatal density in Quercus petraea and Q. robur natural populations in Northern Turkey. Dendrobiology 81:58-64. http://dx.doi.org/10.12657/denbio.081.007
Zar JH (2010). Biostatistical Analysis. Prentice Hall:Upper Saddle River, NJ, USA.
Zhu Y, Kang H, Xie Q, Wang Z, Yin S, Liu C (2012). Pattern of leaf vein density and climate relationship of Quercus variabilis populations remains unchanged with environmental changes. Trees 26:597-607. https://doi.org/10.1007/s00468-011-0624-0
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Ioana M. GAFENCO (PLEȘCA), Ecaterina N. APOSTOL, Bogdan I. PLEȘCA, Elena CIOCÎRLAN, Dr. Dan Marian Gurean, Neculae ȘOFLETEA
This work is licensed under a Creative Commons Attribution 4.0 International License.
License:
Open Access Journal:
The journal allows the author(s) to retain publishing rights without restriction. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author.
.png)
