Leaf architecture and anatomy of eight species of Tilia (Malvaceae)
DOI:
https://doi.org/10.21829/abm131.2024.2332Keywords:
combination of characteristics, midvein, mucilage cavities, primary venation, teeth, trichomesAbstract
Background and Aims: The genus Tilia (Malvaceae) consists of approximately 23 species with unclear boundaries between some of them, especially for the species and subspecies of North America. Although their leaf variation has been recorded, it has not been studied comparatively with other Tilia species present in Europe or Asia. The purpose of this work was to identify leaf morpho-anatomical characters that contribute to Tilia species differentiation. In this work we describe and compare the leaf architecture and anatomy of eight species and four subspecies belonging to the genus Tilia.
Methods: Leaves of eight species and four subspecies were collected or removed from collections. Complete leaves were cleared and stained to describe their architecture, and their anatomy was characterized through transverse and paradermal sections.
Key results: Results showed that leaves are variable in shape, margin dentate with first and second order teeth, secondary venation mostly craspedodromous and well-developed areole. Leaves were hypostomatic heterobaric and with three types of midvein. The combination of characters favored the recognition of species. For example, T. platyphyllos is characterized by teeth with narrower bases, T. mongolica is the only species with a deltoid lamina and without domatia, and T. caroliniana subsp. occidentalis is distinguished by the lamina with three teeth per cm and four-armed stellate trichomes with a length of 332 µm. A key is provided for species and subspecies studied.
Conclusions: The different combinations of leaf characters are promising for the systematics of the genus Tilia.
Downloads
References
Andrés-Hernández, A. R. and T. Terrazas. 2006. Petiole and leaf anatomy of species of the genus Rhus s. str. (Anacardiaceae). Botanical Sciences 78: 95-106. DOI: https://doi.org/10.17129/botsci.1723 DOI: https://doi.org/10.17129/botsci.1723
Andrés-Hernández, A. R. and T. Terrazas. 2009. Leaf architecture of Rhus s.str. (Anacardiaceae). Feddes Repertorium 120(5-6): 293-306. DOI: https://doi.org/10.1002/fedr.200911109 DOI: https://doi.org/10.1002/fedr.200911109
Andrés-Hernández, A. R., D. Espinosa, M. E. Fraile-Ortega and T. Terrazas. 2012. Venation patterns of Bursera species Jacq. ex L. (Burseraceae) and systematic significance. Plant Systematics and Evolution 298(9): 1723-1731. DOI: https://doi.org/10.1007/s00606-012-0673-x DOI: https://doi.org/10.1007/s00606-012-0673-x
Ash, A. W., B. Ellis, L. J. Hickey, K. R. Johnson, P. Wilf and S. L. Wing. 1999. Manual of leaf architecture: Morphological description and categorization of dicotyledonous and net-veined monocotyledonous angiosperms. Smithsonian Institution. Washington, USA. 67 pp.
Cervantes, A., T. Terrazas and H. M. Hernández. 2009. Foliar architecture and anatomy of Bernardia and other genera of Acalyphoideae (Euphorbiaceae). Brittonia 61(4): 375-391. DOI: https://doi.org/10.1007/s12228-009-9084-x DOI: https://doi.org/10.1007/s12228-009-9084-x
Corney, D. P., H. L. Tang, J. Y. Clark, Y. Hu and J. Jin. 2012. Automating digital leaf measurement: the tooth, the whole tooth, and nothing but the tooth. PloS one 7(8): e42112. DOI: https://doi.org/10.1371/journal.pone.0042112 DOI: https://doi.org/10.1371/journal.pone.0042112
da Silva-Luz, C. L., J. R. Pirani, J. D. Mitchell, D. Daly, C. N. Do Valle Capelli, D. Demarco, S. K. Pell and G. M. Plunkett. 2019. Phylogeny of Schinus L. (Anacardiaceae) with a new infrageneric classification and insights into evolution of spinescence and floral traits. Molecular Phylogenetics and Evolution 133: 302-351. DOI: https://doi.org/10.1016/j.ympev.2018.10.013 DOI: https://doi.org/10.1016/j.ympev.2018.10.013
de Meneses Silva, P. C., M. I. Gallão and E. C. Pereira de Arruda. 2023. Comparative anatomical study of two Malvaceae species from a seasonally dry forest. Flora 303: 152290. DOI: https://doi.org/10.1016/j.flora.2023.152290 DOI: https://doi.org/10.1016/j.flora.2023.152290
do Carmo, A., R. Pacifico, R. Gonçales-Silva, P. Gonçales Sbais, K. Fidanza and L. A. de Souza. 2019. Epidermal micromorphology and venation patterns of Microlicieae (Melastomataceae) leaves: Looking for new characters for the taxonomy of this neotropical tribe. Flora 261: 151-494. DOI: https://doi.org/10.1016/j.flora.2019.151494 DOI: https://doi.org/10.1016/j.flora.2019.151494
Downing, T. L., P. Y. Ladiges and M. F. Duretto. 2008. Trichome morphology provides phylogenetically informative characters for Tremandra, Platytheca and Tetratheca (former Tremandraceae). Plant Systematics and Evolution 271(3-4): 199-221. DOI: https://doi.org/10.1007/s00606-007-0622-2 DOI: https://doi.org/10.1007/s00606-007-0622-2
Garcia, T. B., R. C. V. Potiguara, T. Y. S. Kikuchi, D. Demarco and A. C. A. Aguiar-Dias. 2014. Leaf anatomical features of three Theobroma species (Malvaceae s.l.) native to the Brazilian Amazon. Acta Amazonica 44(3): 291-300. DOI: https://doi.org/10.1590/1809-4392201300653 DOI: https://doi.org/10.1590/1809-4392201300653
Hanson, H. C. 1917. Leaf‐structure as related to environment. American Journal of Botany 4(9): 533-560. DOI: https://doi.org/10.1002/j.1537-2197.1917.tb05471.x DOI: https://doi.org/10.1002/j.1537-2197.1917.tb05471.x
Hardin, J. 1990. Variation patterns and recognition of varieties of Tilia americana s.l. Systematic Botany 15(1): 33-48. DOI: https://doi.org/10.2307/2419014 DOI: https://doi.org/10.2307/2419014
Hetterscheid, W. L. A. and E. P. Hennipman. 1984. Venation patterns, soral characteristics and shape of the fronds of the microsorioid Polypodiaceae. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 540(1): 11-47.
Hickey, L. J. 1973. Classification of the architecture of dicotyledonous leaves. American Journal of Botany 60(1): 17-33. DOI: https://doi.org/10.1002/j.1537-2197.1973.tb10192.x DOI: https://doi.org/10.1002/j.1537-2197.1973.tb10192.x
Hickey, L. J. 1979. A revised classification of the architecture of dicotyledonous leaves. Anatomy of the Dicotyledons. Vol. 1. Systematic Anatomy of Leaf and Stem, with a Brief History of the Subject. Clarendon Press. Oxford, UK. 25-39 pp.
Hussin, K. H. and Z. M. Sani. 1998. Comparative leaf anatomical studies of some Sterculia L. species (Sterculiaceae). Botanical Journal of the Linnean Society 127(2): 159-174. DOI: https://doi.org/10.1111/j.1095-8339.1998.tb02094.x DOI: https://doi.org/10.1111/j.1095-8339.1998.tb02094.x
Johansen, D. A. 1940. Plant microtechnique. McGraw-Hill Book Company Inc. London, UK. 523 pp.
Jones, G. N. 1968. Taxonomy of American species of linden (Tilia). University of Illinois Press. Urbana, IL, USA. 156 pp. DOI: https://doi.org/10.5962/bhl.title.50274
Judd, W. S. and S. R. Manchester. 1997. Circumscription of Malvaceae (Malvales) as determined by a preliminary cladistic analysis of morphological, anatomical, palynological, and chemical characters. Brittonia 49(3): 384-405. DOI: https://doi.org/10.2307/2807839 DOI: https://doi.org/10.2307/2807839
Karabourniotis, G., G. Liakopoulos, P. Bresta and D. Nikolopoulos. 2021. The optical properties of leaf structural elements and their contribution to photosynthetic performance and photoprotection. Plants 10(7): 1455. DOI: https://doi.org/10.3390/plants10071455 DOI: https://doi.org/10.3390/plants10071455
Koch, K., B. Bhushan and W. Barthlott. 2009. Multifunctional surface structures of plants: an inspiration for biomimetics. Progress in Materials Science 54(2): 137-178. DOI: https://doi.org/10.1016/j.pmatsci.2008.07.003 DOI: https://doi.org/10.1016/j.pmatsci.2008.07.003
Loria, M. C. 1967. Sistematicheskii obzor lip Kavkaz. Botanicheskly Zhurnal SSSR 52: 1789-1791.
Lu, H. F., B. Jiang, Z. G. Shen, J. B. Shen, Q. F. Peng and C. G. Cheng. 2008. Comparative leaf anatomy, FTIR discrimination and biogeographical analysis of Camellia section Tuberculata (Theaceae) with a discussion of its taxonomic treatments. Plant Systematics and Evolution 274(3-4): 223-235. DOI: https://doi.org/10.1007/s00606-008-0047-6 DOI: https://doi.org/10.1007/s00606-008-0047-6
Maleev, V. P. 1949. Tilia. Flora of the USSR 15: 3-25.
Martínez-Cabrera, D., T. Terrazas and H. Ochoterena. 2007. Leaf architecture of Hamelieae (Rubiaceae). Feddes Repertorium 118(7-8): 286-310. DOI: https://doi.org/10.1002/fedr.200711140 DOI: https://doi.org/10.1002/fedr.200711140
Martínez-Millán, M. and S. R. S. Cevallos-Ferriz. 2005. Leaf architecture of Anacardiaceae. Revista Mexicana de Biodiversidad 76(2): 137-190. DOI: https://doi.org/10.22201/ib.20078706e.2005.002.308 DOI: https://doi.org/10.22201/ib.20078706e.2005.002.308
Martínez-Quezada, D. M., P. Rivera, A. Rojas-Leal, J. L. Villaseñor and T. Terrazas. 2022. Leaf secretory structures in Asteraceae: a synthesis of their diversity and evolution. Botanical Review 89(1): 59-90. DOI: https://doi.org/10.1007/s12229-022-09276-4 DOI: https://doi.org/10.1007/s12229-022-09276-4
McCarthy, D. M. and R. J. Mason-Gamer. 2016. Chloroplast DNA-based phylogeography of Tilia americana (Malvaceae). Systematic Botany 41(4): 865-880. DOI: https://doi.org/10.1600/036364416X693964 DOI: https://doi.org/10.1600/036364416X693964
McCarthy, D. M. and R. J. Mason-Gamer. 2020. Morphological variation in North American Tilia and its value in species delineation. International Journal of Plant Sciences 181(2): 175-195. DOI: https://doi.org/10.1086/706781 DOI: https://doi.org/10.1086/706781
Metcalfe, C. R. and L. Chalk. 1950. Anatomy of the dicotyledons: Leaves, stems and wood in relation to taxonomy with notes on economics uses (Vol. I). Clarendon Press. Oxford, UK. 276 pp.
Pacheco-Trejo, J., T. Terrazas and H. Ochoterena. 2009. Leaf architecture of the genus Didymaea Hook. F. (Rubiaceae). Plant Systematics and Evolution 281(1-4): 137-149. DOI: https://doi.org/10.1007/s00606-009-0195-3 DOI: https://doi.org/10.1007/s00606-009-0195-3
Peng, L., X. Xia, A. Wang and L. Zhao. 2019. Comparative study on development and structural characteristics of bracts and leaves of Tilia japonica Simonk. Plant Science Journal 37(6): 719-725. DOI: https://doi.org/10.11913/PSJ.2095-0837.2019.60719
Perrotta, V. G., S. A. Stenglein and A. M. Arambarri. 2007. Leaf anatomy of Ceiba chodatii and C. speciosa (Bombacaceae). Kurtziana 33(2): 17-25.
Pigott, D. 2012. Lime-trees and basswoods: a biological monograph of the genus Tilia. Cambridge University Press.UK. 395 pp. DOI: https://doi.org/10.1086/670573 DOI: https://doi.org/10.1017/CBO9781139033275
Pizzolato, T. D. 1977. Staining of Tilia mucilages with Mayer’s tannic acid-ferric chloride. Bulletin of the Torrey Botanical Club 104(3): 277-279. DOI: https://doi.org/10.2307/2484311 DOI: https://doi.org/10.2307/2484311
Ramayya, N. and S. R. S. Rao. 1976. Morphology, phylesis and biology of the peltate scale, stellate and tufted hairs in Malvaceae. Journal of Indian Botanical Society 55(1): 75-79.
Ramírez-Díaz, M., T. Terrazas, S. Aguilar-Rodríguez, A. Rojas-Leal and D. Martínez-Cabrera. 2019. Ontogenia de los tricomas foliares de Tilia caroliniana subsp. floridana (Malvaceae). Revista Mexicana de Biodiversidad 90(2). DOI: https://doi.org/10.22201/ib.20078706e.2019.90.2779 DOI: https://doi.org/10.22201/ib.20078706e.2019.90.2779
Rao, S. R. S. and N. Ramayya. 1987. Trichome types and their taxonomic importance in the Tiliaceae. Journal of Indian Botanical Society 10(1): 65-73.
Rodrigues, T. M., A. C. Esteves Amaro, C. S. Fernandes Boaro, K. Reis Mendes, S. de Melo Silva, C. Ferreira Jr. and S. Rodrigues Machado. 2017. Four distinct leaf types in the Brazilian Cerrado, based on bundle sheath extension morphology. Botany 95(12): 1171-178. DOI: https://doi.org/10.1139/cjb-2017-0073 DOI: https://doi.org/10.1139/cjb-2017-0073
Ruzin, S. E. 1999. Plant Microtechnique and Microscopy. Oxford University Press. New York, USA. 322 pp.
Sajo, M. G. and P. J Rudall. 2002. Leaf and stem anatomy of Vochysiaceae in relation to subfamilial and suprafamilial systematics. Botanical Journal of the Linnean Society 138(3): 339-364. DOI: https://doi.org/10.1046/j.1095-8339.2002.00025.x DOI: https://doi.org/10.1046/j.1095-8339.2002.00025.x
Sharma, R. 1990. Trichomes in some Tiliaceae. Journal of Indian Botanical Society 69: 11-14.
Silva Araújo, J. S., A. Alves Azevedo, L. Campos Sila and R. M. Strozi Alves Meira. 2010. Leaf anatomy as an additional taxonomy tool for 16 species of Malpighiaceae found in the Cerrado area (Brazil). Plant Systematics and Evolution 286(1-2): 117-131. DOI: https://doi.org/10.1007/s00606-010-0268-3 DOI: https://doi.org/10.1007/s00606-010-0268-3
Solano, E., T. Terrazas, J. Reyes-Rivera and H. Serrano-Casas. 2017. Anatomía comparativa de raíz, tallo, hoja y base del pedúnculo de Manfreda (Asparagaceae: Agavoideae). Revista Mexicana de Biodiversidad 88(4): 899-911. DOI: https://doi.org/10.1016/j.rmb.2017.10.019 DOI: https://doi.org/10.1016/j.rmb.2017.10.019
Solis-Montero, L., T. Terrazas and M. Ishiki-Ishihara. 2013. Leaf architecture and anatomy of eleven species of Mortoniodendron (Malvaceae s.l.). Plant Systematics and Evolution 299(3): 553-566. DOI: https://doi.org/10.1007/s00606-012-0742-1 DOI: https://doi.org/10.1007/s00606-012-0742-1
Solís-Montero, L., N. Rendón-Carmona, T. Terrazas and M. Ishiki. 2009. Los domacios de Mortoniodendron (Malvaceae s.l.). Brittonia 61(1): 71-84. DOI: https://doi.org/10.1007/s12228-008-9059-3 DOI: https://doi.org/10.1007/s12228-008-9059-3
Tejero-Diez, D., S. Aguilar-Rodríguez, T. Terrazas and L. Pacheco. 2010. Arquitectura y anatomía foliar del complejo Polypodium plesiosorum sensu Moran (Polypodiaceae). Revista de Biología Tropical 58(3): 955-976. DOI: https://doi.org/10.15517/rbt.v58i2.5257 DOI: https://doi.org/10.15517/rbt.v58i2.5257
Thiers, B. 2023. Index Herbariorum: a global directory of public herbaria and associated staff. http://sweetgum.nybg.org/ih/ (consulted September 2023).
Tölke, E. D., M. C. Medina, A. Lopes Souto, J. P. Rodrigues Marques, G. Gomes Nogueira Alves and R. Laino Gama, J. Rubens Pirani and D. Demarco. 2022. Diversity and evolution of secretory structures in Sapindales. Brazilian Journal of Botany 45(1): 251-279. DOI: https://doi.org/10.1007/s40415-021-00778-w DOI: https://doi.org/10.1007/s40415-021-00778-w
Turner, G. W., A. M. Berry and E. M. Gifford. 1998. Schizogenous secretory cavities of Citrus limon (L.) Burm. F. and a reevaluation of the lysigenous gland concept. International Journal of Plant Sciences 159(1): 75-88. DOI: https://doi.org/10.1086/297523 DOI: https://doi.org/10.1086/297523
Ventrella, M. C., A. L. Almeida, L. A. Nery and V. D. M. Coelho. 2013. Métodos histoquímicos aplicados às sementes. Universidade Federal de Viçosa. Viçosa, Brasil. 40 pp.
Wilkinson, H. P. 1979. The plant surface (mainly leaf) Part IV: Domacio. In. Metcalfe, C. R. and L. Chalk (eds.). Anatomy of the Dicotyledons, 2 ed. Clarendon Press. Oxford, UK. 97-165 pp.
Xie, J., P. Del Tredici, M. LaPorte, A. Bekmetjev, A. R. Lemmon, E. M. Lemmon, W. Gong, Y. Tang, and J. Li. 2023. Phylogenetic relationships of Tilia (Malvaceae) inferred from multiple nuclear loci and plastid genomes. International Journal of Plant Sciences 184(1): 56-67. DOI: https://doi.org/10.1086/722474 DOI: https://doi.org/10.1086/722474
Zhu, G. 1991. Revision of Tilia from Yunnan. Journal of Southwest Forestry College 11(1): 1-7.
Published
How to Cite
-
Abstract3033
-
PDF716
-
XML (Español)35
-
EPUB105
Issue
Section
License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Authors who publish in this journal accept the following conditions:
In accordance with copyright legislation, Acta Botanica Mexicana recognizes and respects the moral rights of authors, as well as the ownership of the patrimonial right, which will be assigned to the journal for its dissemination in open access. Acta Botanica Mexicana does not charge authors for sending and processing articles for publication.
All the texts published by Acta Botanica Mexicana - without exception- are distributed under the Creative Commons 4.0 Attribution-Non Commercial License (CC BY-NC 4.0 International), which allows third parties to use what is published whenever they mention the authorship of the work and the first publication in this journal.
The authors can make other independent and additional contractual agreements for the non-exclusive distribution of the version of the article published in Acta Botanica Mexicana (for example, include it in an institutional repository or publish it in a book) as long as they clearly indicate that the work was published for the first time in Acta Botanica Mexicana
As a consequence, the copyeditors will request you, together with the galley review, to issue your Letter-Transfer of Ownership of Copyright form of the first publication duly completed and signed by the author(s). This letter should be sent by email in pdf file to the email: acta.botanica@inecol.mx (Letter-Transfer of Ownership of Copyright).


