Volume 21(3), 108- 114, 2017 JOURNAL of Horticulture, Forestry and Biotechnology www.journal-hfb.usab-tm.ro

Actual state of knowledge regarding research on lime tree in the world – short review

Manea M. I.1*, Cântar I. C.2

1Banat University of Agricultural Science and Veterinary Medicine “King Michael I of Romania” from Timisoara; 2National Institute for Research and Development for Forestry „Marin Drăcea”, Timişoara Station

*Corresponding author. Email: [email protected]

Abstract Current paper aims to present and discuss on the principal Key words research works regarding lime trees in the word and especially in our country and in Europe. In the first part are presented the methods and materials used lime trees, reseach papers, for the elaboration of this review paper. The results succinctly present the short review, sp. most important research on the field related to lime trees. Firstly are presented relevant research from Romania in the fields of air pollution and usage of trees from Tilia genus as biomonitors and also in forestry terms. In Romania there where done also research regarding morphologichal differentiation of lime trees. At Europen level, research regarding lime tree where structured by the area where field work was done: central, northern, southern, eastern and western Europe. In the last part of the results and discussions were presented some research from outside of Europe, from Central America and Middle East. On conclusions, there are succinctly presented the most relevant aspects regarding lime trees research areas presented above.

Species from Tilia genus are native in forests from oak, oak and other broad-leaved trees: in Banat, in northern hemisphere, both in Europe and Asia but also Romanian Plain, in Dobrogea and in the Moldavian in center and in the East of North America [16]. From Plateau [1]. more than 350 of the Tilliaceae family, only Tilia species grow as mixed forest or four Tilia species are native on our continent: small- disseminated, in oak and sessile oak stands, in broad- leaved lime-Tilia cordata Mill., large-leaved lime-Tilia leaved forests on the plain, in riparian forests and on platyphyllos Scop., Caucasian lime-Tilia dasystyla hills, in sessile oak-beech forests and rarely, in beech Stev. and silver lime-Tilia tomentosa Moench., T. forests. The silver lime is the only species which forms cordata and T. platyphyllos cover the main area of pure stands in which, the small-leaved lime and the Europe, ranging from southern Finland to southern broad-leaved lime, participate only disseminated [1]. Italy and the Caucasus. T. cordata is more abundant A similar situation regarding his distribution is than T. platyphyllos and its core region is Central and also found in the Caransebeş Experimental Base of Eastern Europe. T. platyphyllos has a smaller range, I.N.C.D.S. "Marin Drăcea", where, along with other reaching slightly further south but only reaching species of the genus occupies an important percentage southern Sweden at its northern extent and having a in the hill areas of the experimental base, along with much more patchy occurrence in northern Central oak, sessile oak and beech. Europe. Neither species is present in the far west of Current paper aims to present and discuss on the Europe, with the western extent in North-West Spain principal research works regarding lime trees in the and Wales [26]. The other species of lime which occur word and especially in our country and in Europe. naturally in Europe, have regional distribution: T. tomentosa especially occurs in the Balkans and Material and Methods Hungary, while T. dasystyla is typical for the regions around the Black Sea [17, 23]. In Romania there are The main method used for substantiate and three native lime species: T. cordata Mill. (the most achievement of this study was the bibliographical common), T. tomentosa Moench. (the most drought research and documentation in order to study, to know resistant), and T. platyphyllos Scop. (the most water and to present aspects of researches on lime trees of the demanding) [28]. main areas of the Europe and with a geographical The highest density of lime, especially of silver dispersion as large as possible. lime, exists in four centers of the country, where the The analysis and synthesis were also used in order lime, forms pure stands or mixed forests with sessile to present in a comprehensive mode the principal

108 aspect and results for each paper and research work characteristic for each settlements and suggested some studied. important pollution factors. Was found a correlation The materials used are represented by the between dust chemical composition and the size of the international databases, studies, articles and books cities (characterized by the number of his residents). from specific literature, studied to achieve the proposed The method of sampeling was relatively simple and objectives, the results of this survey being presented on chemical analysis and also statistical evaluation can be below. extende to the geographical area of the focal settlements. By the inclusion of a further background Results and Discussions (e.g. meteorologic, economic,epidemiologic) variables, the model can be enhanced for a more realistic The results of bibliographical research conducted description for observing the differences[27]. are structured on European areas and countries being Regarding research on forestry field about lime presented geographical grouped as follows. trees, PURCELEAN et al. (1970), in the paper "Typological research in lime tree stand and mixed Research on lime trees in Romania stands with the participation of lime trees"(" Cercetări Species from Tilia genus (linden trees) in terms of tipologice în teişuri şi arborete amestecate cu ornamental trees own an important position on participarea teiului ") shows that in linden stands, the European history, mythology, traditions and culture productivity of the derived type in few cases and this may be a cause of their abundance on urban corresponds to the productivity class of the basic type, areas. In general, lime trees are very resistant species to but is usually lower. Another phenomenon that become biotic and abiotic stress, but some sanitary problems, at evident during the typological researches on lime trees the same time may occur (different pests). Also, lime stand and lime mixed stands is the hornbeam tendency trees are good accumulator and also bioindicator, of to gradually replace the lime, because of possessing heavy metals (Alina Tenche, Tilia spp. – Urban Trees greater seed regeneration capacity and better support for Future, 2014). Accumulations of heavy metals Pb, for reduced consistency in derived linden stands. Cr, Ni, Cu, Mn, Fe in leaves of lime trees in green Another significant fact is the localization of the areas (urban and periurban) of West part of Romania, derived types in the south and south-east of Romania considering different conditions of traffic, were studied and to a lesser extent in the Central Moldavian Plateau by ȚENCHE-COSNTANTINESCU Alina et al. and in the Banat and Crişana Hills. The thermophilia of (2014), using the method of atomic absorption linden species is the primary cause of this situation spectrophotometry. The study confirmed the strong [22]. correlation between intensity of the trafic and the CAMBIR et al. (1970), in the paper "Researches accumulation of Pb in lime leaves. By mitigating the about suitable seasons for lime culture" ("Cercetări effects of air pollution and especially regarding heavy privind staţiunile apte pentru cultura teiului ") shows metals, Tilia spp. should promoted in the future as that the lime species in our country have the widest urban trees[28]. spread in the forest area of the plain and the hills, In the same direction, of foliar response reactions partly in the forest steppe zone and quite rarely in the induced by atmospheric pollutants, ŞOLTUZU, B. D. mountain area. The same author concludes that all lime et al. (2012), present the foliar response reaction species achieve superior productivity on smooth or induced by atmospheric pollutants on the Aesculus slightly sloping terrains, high non-flooded plains, hippocastanum L. and T. tomentosa species situated narrow valleys and shady bases, the lower part of the around Iaşi city`s air quality monitoring stations. They shaded slopes; on brown-evolved alluvial soils, emphasized that the large amount of dry leaves is not reddish-brown, brown-rusty, or brown forest soil [2]. always related to necrotic leaf surface. It was found In Romania, T. tomentosa grows, where the that the amount of chlorophyll a and b and the intensity species reaches the northern most limit of its European of photosynthesis aren`t always correlated, as already range (on southern and western slopes) up to 1,000 m known from literature[25]. elevation as in the south of the country. In Romania the Also, regarding the monitoring of the optimum elevation for silver lime forests is between environment, a pilot study from Transilvania, 150-450 m (RADOGLOU, K. et al. citing Haralamb, Romania, using lime tree leaves, as natural traps for 1967; Stanescu et al., 1997). T. tomentosa is a average atmospheric deposition,was conducted by TOTH M. intolerant and climax species, that can be found in even B., et al. (2007). A study including 16 locations from age stands of eitherpure lime trees (like in south- Romania was made in order to establish the main eastern Romania) or in mixed stands together with characteristics and the main sources of air pollutants. other broadleaved tree species as Carpinus betulus, Linden leaves Quercus robur, Acer campestris, Ulmus campestris, (T. cordata, T. platyphyllos, T. tomentosa) were etc. It can be also found in mixed stands from the forest collected and after that, were used for the analyzes.The steppe together with Fraxinus ornus, Quercus analysis of data regarding the concentration of heavy pubescens, etc. It can prosper on compact soils, as the metal, suggests that the composition of dust is soils found on terraces, where it grows together with

109 mixtures with Quercus Frainetto and Quercus Cerris zymograms of 10 spontaneous T. cordata, T. (RADOGLOU, K. et al. citing Stanescu et al., 1997) platyphyllos hybrids showed different banding patterns [23]. In terms of morphologichal differentiation of lime with species and specific alleles at 13 of the 14 trees from Romania, IVANOV et al. (2014), highlight described gene loci. Therefore, differentiation between the morphological traits which differentiate the three studied species and their naturally occurring hybrid (T. species ( T. cordata, T. platyphyllos and T. tomentosa) europaea) is easily feasible with allozyme studies[7]. by using Discriminant Analysis. Sampels from 150 The phenology of flowering of lime and pollen lime trees and eleven twig and leaf descriptors were release for four species of lime was studied by Elżbieta made. The results of statistical analysis confirmed a WERYSZKO-CHMIELEWSKA, Dagmara Anna high discriminating power of certain features. To SADOWSK in 2010. Their study shows that in the year separate the three lime species lamina length, abaxial 2010 the duration of flowering of three lime species (T. laminal pubescence and bud pubescence were the platyphyllos, T. x europaea, T. cordata) was 16 days, variables, used to develop three discriminant where as T. tomentosa flowered just 12 days. The functions[11]. entire duration of flowering for four lime species, with different flowering dates, was 38 days. They concluded Research on lime trees on central Europe that this period is in agreement with data from In Europe were made research regarding lime literature, showing that lime species bloming at tress in different fields not just in pollution and different times and it can provide pollen for bees over a silvicultural research fields. GÜLZ, P. G. (1988) et al. total period of six weeks[30]. studied epicuticular leaf waxes of T. tomentosa RADOGLOU, K.(2009), published a review on Moench. and T. X europaea L. Quantity and the silviculture and ecology of lime trees (T. cordata composition of epicuticular leaf wax of T. tomentosa Mill., T. platyphyllos Scop. and T. tomentosa Moench.) Moench. and T. x europaea L. were examined and in Europe. The aime of this review was to synthesise showed similar wax compositions. The waxes of these on the existing literature, different aspects for Tilia sp. two Tilia species contained homologous series of n- growth which is relevant for the practical silviculture. alkanes, wax esters, aldehydes, acetates, primary The authors intend to describe and establish the growth alcohols and fatty acids. In addition to these common pattern of linden trees, in order to identify some epicuticular wax constituents, the triterpenol ß-amyrin factors that influence lime variability and in order to was found free as well as esterified with long chain obtain conclusions for a better forest management [23]. fatty acids and in very high amounts with acetic acid in GLENZ, C. et al. (2006) analyzed the growth both Tilia species [9]. response of tree seedlings of 22 mainly European Similar research were made by Olga Karolina species, following a 120-day flood. For T. cordata, the KOSAKOWSKA et al. (2015), regarding variability on study revealed an extremely high reduction of height intraspecific terms, in phenolic compounds content, grown [8]. mucilage and essential oil from small-leaved lime (T. cordata Mill.) in Poland. The objective of the study Research on lime trees on northern Europe was to find out the chemical variability for small- In Great Britain, MYLETT, A. (2007) use RAPD leaved lime native in the eastern part of Poland, markers in assessing genetic variability in T. cordata to regarding the content and also the composition of facilitate appropriate reestablishment of native trees. phenolic compounds (flavonoids and phenolic acids), The genetic diversity of small leaved lime (T. cordata) essential oil composition and mucilage in flowers was investigated using RAPD markers to estimate the content. The studied populations show considerable genetic relationships between trees. Initial results of differences regarding the accumulation of the RAPD analysis indicate that the trees from two biologically active compounds[12]. separate woodland areas although largely similar show Regarding the european range of T. tomentosa, two separate clusters [15]. Mirosława KUPRYJANOWICZ et al. (2015) HANSEN et al. (2014), shows that genetic reconstructed European range of this species during the diversity of common lime that is planted in Danish last interglacial, basis on new finds of Eemian T. historical areas is very low, and the same clones were tomentosa Moench macroremais in NE Poland [13]. produced for decades/centuries by private nurseries In terms of systematic Tilia genus, Liesebach H., from Netherlands and Germany . They also provide Sinkó Z. (2008) , published a contribution to Tilia evidence, that it is very possible to have the same genus systematics, considering some hybrids for using genetic material as the originally planted when dead RAPD analysis. lime trees need to be replaced in the historical gardens. Also in genetics of genus Tilia, hybridization and Furthermore, they demonstrated the utility of DNA inheritance of allozymes in two European Tilia species markers for the management of replant material in ( T. cordata and T. platyphyllos) was studied by M historical gardens[10]. FROMM and HH HATTEMER (2003). Inheritance PRATTANA PHUEKVILAI and KIRSTEN analysis was done utilizing lime trees and open- WOLFF (2013), from Newcastle, United Kingdom, pollinated progenies. In comparison with T. cordata, studied microsatellite markers in the genus Tilia,

110 developed to investigate the genetic variation in T. was evident for V, Cr, Fe, Ni, As, and Pb, and it was platyphyllos and its relationship with T. cordata. more regular for A. hippocastanum. They conclude that Fifteen microsatellite markers were developed using a leaves of Tilia spp. and A. hippocastanum could be microsatellite enrichment protocol. Most loci show a used to monitor concentrations and seasonal variations high level of polymorphism in two T. platyphyllos of these radionuclides in air in urban areas [21]. populations from France. The number of alleles ranged In Serbia also, SERBULA et al. (2013) study the from one to 15, with a mean of 8.96. The mean heavy metal air pollution and he used Tilia spp. and observed and expected heterozygosities were 0.71 and Pinus spp. The influences of airborne pollution 0.70, respectively. Cross-amplification results originating from the Mining–Metallurgical Complex indicated that 12 out of 15 loci amplified polymorphic Bor (Serbia) on the concentrations of Cu, Pb, Zn and loci in 23 species in the genus. They conclude that Mn in the samples of Tilia spp. and Pinus spp. were these markers will be useful tools for investigating the examined. According to the results of the enrichment phylogeography and hybridization of Tilia species factors, branches were the parts most enriched [20]. with Cu and Pb. According to the bioconcentration factor, translocation factor and translocation index, Research on lime trees on southern Europe high concentrations of Cu and Pb in aerial parts of pine Regarding Tilia species and atmospheric polution and linden are mostly a consequence of airborne in Italy, PELLEGRINI et al. (2013), , studied the pollution [24]. ecophysiology of Tilia americana exposed to ozone The reduced developmental stability in T. cordata fumigation. In natural conditions lime trees do not have leaves, as effects of disturbed environment, was foliar injudy produced by ozone . In the present study, studied by MIROSLAVA V. VELIKOVIC (2010). the effects of ozone was investigated, on Developmental stability (DS) or homeostasis, it refers ecophysiological and also biochemical parameters of to a ability of an individual to produce a different and Tilia americana saplings that were exposed to a consistent phenotype in a different and given fumigation (120 ppb for a period of 45 consecutive environment. Obtained data shown that T. cordata days and 5 h/day). After this treatment, even if leaves can be a trustworthy indicator for developmental samplings did not showed visible foliar injury, some stability and evaluation studies based on an test using a parameters were affected in a significant way: stomatal combination of end-points. Moreover, the results conductance of water vapor (decrease with 15% in highlighted the differences on ability of morphometric comparison with control), photosynthesis ( decrease characters of leaf to buffer their development, under with 39%), intercellular concentration of CO2 and also variable environmental conditions [29]. chlorophyll fluorescence indexes ( increase with 30%). After 45 days of fumigation neo–, viola– and Research on lime trees on westhern Europe anteraxanthin content decrease significantly (25%, In western Europe, Fineschi et al. studied 34% and 63%, compared with controls). It was chloroplast DNA variation at T. cordata. Haplotypic observed that zeaxanthin induction was not detected, diversity Error! Hyperlink reference not suggesting that by exposure, the xanthopyll cycle was valid.distribution for 17 populations of T. cordata was not activate. In accordance with this results, this researched by PCR–RFLP markers of the chloroplast species should be considered as “middle genomes.The analysis showed a high total genetic tolerant/sensitive” [18]. diversity (hT = 0.881) and high number of haplotypes (14). The distribution of the chloroplast DNA Research on lime trees on easthern Europe haplotypes revealed a reduced geographic structure of FILIZ et al. (2015), studied the genetic variations genetic diversity. Relatively low genetic differentiation of silver lime (T. tomentosa Moench.) by RAPD among T. cordata populations can be explained mainly markers in urban and forest ecosystems in Turkey. The as a consequence of the human impact on this genetic diversity analysis of T. tomentosa trees was species[6]. done using random amplified polymorphic DNA (RAPD) primers. In the study, were used 28 trees Research on lime trees on other parts of the word samples, from 25 urban landscape and 3 forest PEREZ-ORTEGA G. et al. (2008) studied ecosystems, were used. Sampels from forest sedative and anxiolytic efficacy of T. americana var. ecosystems and urban landscape showed a wery high Mexicana inflorescences used traditionally by genetic similarity (from 28% to 92%) and they have communities of State of Michoacan, Mexico. All formed a common UPGMA ( unweighted pair group samples tested produced a lengthening in the time of method, with arithmetic mean) tree [5]. SP (induced hypnosis potentiation). Moreover, a Moss and tree leaves, including lime tree leaves significant attenuation in the anxiety-response in the used as biomonitors in Serbia, was studied by Popović plus-maze test and a diminution in both the head et al.(2010). Seasonal accumulation of the examined dipping response and ambulatory activity were trace elements in leaves of Aesculus hippocastanum L. observed resembling the response to diazepam (0.3 and Tilia spp. (T. tomentosa L. and T. cordata Mill.) mg/kg, i.p.). The results demonstrate that

111 inflorescences of stored specimens obtained from In terms of morphologichal differentiation of lime popular local markets show the same effectiveness trees from Romania, IVANOV et al. (2014), highlight with regard to sedative and anxiolytic-like actions than the morphological features that distinguish the three freshly collected samples. Since no toxicity was species (T. cordata, T. platyphyllos and T. observed through this route of administration (up to tomentosa)by using Discriminant Analysis. 5000 mg/kg); therefore, it suggests that this plant is In Europe were made research regarding lime secure when used as tranquilizer in folk medicine [19]. tress in different fields not just in pollution and In Middle East, HOSSEINZADEH COLAGAR et silvicultural research fields. GÜLZ, P. G. (1988) et al. al. (2013) studied the analasys of genetic diversity for studied epicuticular leaf waxes of T. tomentosa Tilia rubra dc. by using RAPD analysis methods for Moench. and T.X europaea L. samples from Hyrcanian forests, from the North of Similar research were made by Olga Karolina Iran. Genetic variability and differentiation of six KOSAKOWSKA et al. (2015), regarding variability on populations of T. rubra from iranian forests were intraspecific terms, in phenolic compounds content, examined with the help of RAPD markers.In this study mucilage and essential oil from small-leaved lime (T. the results does not match with the origin of cordata Mill.) in Poland. populations. Low inter-population differentiation and Regarding the european range of T. tomentosa, lack of significant correlation between geographic and Mirosława KUPRYJANOWICZ et al. (2015) genetic distances shown an intensive gene flow among reconstructed European range of this species during the populations of T. rubra [4]. last interglacial, basis on new finds of Eemian T. tomentosa Moench macroremais in NE Poland. Conclusions In terms of systematic Tilia genus, Liesebach H., Sinkó Z. (2008) , published a contribution to Tilia In Romania, research regarding environmental genus systematics, considering some hybrids for using monitoring capacity of Tilia species were done. The RAPD analysis. study confirmed a direct correlation between intensity The phenology of flowering of lime and pollen of the traffic and the accumulation in lime trees leaves release for four species of lime was studied by Elżbieta of Pb [28]The large amount of dry leaves is not always WERYSZKO-CHMIELEWSKA, Dagmara Anna related to necrotic leaf surface. It was found that the SADOWSK in 2010. amount of chlorophyll a and b and the intensity of GLENZ, C. et al. (2006) analyzed the growth photosynthesis aren`t always correlated, as already response of tree seedlings of 22 mainly European known from literature [25]. Discriminant analysis of species, following a 120-day flood. For T. cordata, the heavy metal concentration on lime leaves revealed that study revealed an extremely high reduction of height the composition of dust is a characteristic of the city grown. and also suggested some pollution factors that are In Great Britain, MYLETT, A. (2007) use RAPD in relevant [27]. assessing genetic variability in T. cordata to facilitate Regarding research on forestry field about lime appropriate reestablishment of native trees. trees, PURCELEAN et al. (1970) shows that in linden HANSEN et al. (2014), shows that genetic stands, the productivity of the derived type in few cases diversity of common lime that is planted in Danish corresponds to the productivity class of the basic type, historical areas is very low, and the same clones were but is usually lower. Another phenomenon that become produced for decades/centuries by private nurseries evident during the typological researches on lime trees from Netherlands and Germany .PRATTANA stand and lime mixed stands is the hornbeam tendency PHUEKVILAI and KIRSTEN WOLFF (2013), from to gradually replace the lime. Another significant fact Newcastle, United Kingdom, studied microsatellite is the localization of the derived types in the in the markers in the genus Tilia, developed to investigate the south and south-east of Romania and to a lesser extent genetic variation in T. platyphyllos and its relationship in the Central Moldavian Plateau and in the Banat and with T. cordata. Crişana Hills. The thermophilia of linden species is the Regarding Tilia species and atmospheric polution primary cause of this situation. CAMBIR et al. (1970) in Italy, PELLEGRINI et al. (2013), studied the shows that the lime species in our country have the ecophysiology of T. americana under ozone widest spread in the forest area of the plain and the fumigation. hills, partly in the forest steppe zone and quite rarely in FILIZ et al. (2015), studied the genetic variations the mountain area. RADOGLU et al. (2009) say that in of silver lime (T. tomentosa Moench.) by RAPD Romania, T. tomentosa grows, where this species markers in urban landscape and forest ecosystems fom reaches the northern limit of itsEuropean range (on Turkey. western and southern slopes) up to elevation of 1000 Moss and tree leaves, including lime tree leaves m, as in the south of Romania. In Romania the used as biomonitors in Serbia, was studied by Popović optimum elevation for silver lime forests is between et al.(2010). 150-450m.

112 In Serbia also, SERBULA et al. (2013) study the 10.Hansen, O. K., Thomsen, P., & Rasmussen, C. W. – assessment of airborne heavy metal pollution using 2014 – DNA markers provide insight about common Pinus spp. and Tilia spp. lime in historical plantings–An example from the The reduced developmental stability in T. cordata Royal Danish Gardens. Urban forestry & urban leaves, as effects of disturbed environment, was greening, 13(3), 543-552; studied by MIROSLAVA V. VELIKOVIC (2010). 11.Ivanov, P., Loghin, C., & Enescu, C. M. – 2014 – In western Europe, Fineschi et al. studied Morphological differentiation between Romanian lime chloroplast DNA variation at T. cordata. Haplotypic species (Tilia spp.): A case study. Bulletin of the diversity Error! Hyperlink reference not Transilvania University of Brasov. Forestry, Wood valid.distribution for 17 populations of T. cordata Mill. Industry, Agricultural Food Engineering. Series II, was researched by PCR–RFLP markers of the 7(1), 21; chloroplast genomes. 12.Kosakowska, O. K., Bączek, K., Przybył, J. L., PEREZ-ORTEGA G. et al. (2008) studied Ejdys, M., Kuźma, P., Obiedziński, M., & Węglarz, Z. dedative and anxiolytic efficacy of T. americana var. – 2015 – Intraspecific variability in the content of Mexicana inflorescences used traditionally by phenolic compounds, essential oil and mucilage of communities of State of Michoacan, Mexico. small-leaved lime (Tilia cordata Mill.) from Poland. In Middle East, HOSSEINZADEH COLAGAR et Industrial Crops and Products, 78, 58-65; al. (2013) studied the analasys of genetic diversity for 13.Kupryjanowicz, M., Granoszewski, W., & Fiłoc, M. T. rubra dc. by using RAPD analysis methods for – 2016 – New finds of Eemian Tilia tomentosa samples from Hyrcanian forests, from the North of Moench macroremais in NE Poland, and the Iran. reconstructed European range of this species during the last interglacial. 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