Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2022-07-01
Page range: 221-251
Abstract views: 64
PDF downloaded: 2

Taxonomic implications of anatomical characteristics of the genus Tulipa (Liliaceae) in Turkey and their place in the historical subgeneric classifications

Bolu Abant İzzet Baysal University, Faculty of Science & Literature, Department of Biology, 14280, Bolu, Turkey
Bolu Abant İzzet Baysal University, Faculty of Science & Literature, Department of Biology, 14280, Bolu, Turkey
Anatolia anatomy cluster analysis PCA taxonomy tulips Monocots

Abstract

This paper comprehensively discusses anatomical features of the genus Tulipa (Liliaceae) in Turkey. These are compared with the current subgeneric classification.   Anatomical structures, including transverse sections of the root, stem (scape) and leaf, and surface sections of the leaves are illustrated based on the 420 preparations obtained from 42 OTUs (populations) belonging to 18 taxa. Densities of stomata and epidermis cells per unit leaf area (mm2), stomatal index and ratio of stomata index on the leaf surfaces were also calculated. Cluster and principal component analyses (PCA) were employed, and all results were compared at the population level. In this anatomical study, some significant differences were found among Tulipa taxa, especially at the infrageneric and interspecific levels. The results of anatomical investigations are consistent with published results of previous morphological and molecular analyses. The results of cluster analysis and PCA support the classifications of Veldkamp & Zonneveld and Christenhusz et al. including three subgenera, Eriostemones, Tulipa and Clusianae, but subgenus Orithyia was not included in this study because it is absent from Turkey. Subgenus Eriostemones is divided into two sections, Sylvestres and Saxatiles, following treatments by Baker and Eker et al. In subgenus Tulipa, although morphometric analyses partially supported the taxonomic grouping previously proposed as three separate sections, Tulipa, Tulipanum and Eichleres, it also clearly indicates that considering them as a single section (Tulipa) is perhaps a better option.

References

<p>Almeida, M.T. &amp; Bisby, F.A. (1984) A simple method for establishing taxonomic characters from measurement data. <em>Taxon 33</em>: 405–409. https://doi.org/10.2307/1220978</p>
<p>Baker, J.G. (1874) Revision of the genera and species of Tulipeae. <em>Journal of the Linnean Society</em>, <em>Botany</em> 14: 275–296.&nbsp; https://doi.org/10.1111/j.1095-8339.1874.tb00314.x</p>
<p>Baker, J.G. (1883a) The species of <em>Tulipa</em>. <em>Gardener’s Chronicle</em> 19: 626, 668, 691, 788.</p>
<p>Baker, J.G. (1883b) The species of <em>Tulipa</em>. <em>Gardener’s Chronicle</em> 20: 11, 12, 71, 153, 168–169, 233–234, 266.</p>
<p>Baker, J.G. (1891) New or noteworthy plants. <em>Gardeners’ Chronicle</em> (3<sup>rd</sup> series) 9: 330.</p>
<p>Bıçakçı, A. &amp; Malyer, H. (1998) <em>Echinophora</em> L. (Apiaceae) türlerinin yaprak anatomisi. <em>Ot Sistematik Botanik Dergisi</em> 5 1: 31–46.</p>
<p>Boissier, P.E. (1844) <em>Tulipa undulatifolia. Diagnoses Plantarum Orientalium Novarum</em> 5: 57.</p>
<p>Boissier, P.E. (1859) <em>Tulipa armena. Diagnoses Plantarum Orientalium Novarum</em> (series secunda) 4: 99.</p>
<p>Boissier, P.E. (1882) <em>Flora orientalis</em>, vol. 5. H. Georg, Geneva &amp; Basel. pp. 191–201.</p>
<p>Botschantzeva, Z.P. (1982) <em>Tulips: taxonomy, morphology, cytology, phytogeography and physiology</em>. Translated and edited by H.Q. Varekamp, Balkema, Rotterdam, 640 pp.</p>
<p>Brummitt, R.K. &amp; Powell, C.E. (1992) <em>Authors of plant names</em>. Royal Botanic Gardens, Kew.</p>
<p>Christenhusz, M.J.M., Govaerts, R., David, J.C., Hall, T., Borland, K., Roberts, P.S., Tuomisto, A., Buerki, S., Chase, M.W. &amp; Fay, M.F. (2013) Tiptoe through the tulips-cultural history, molecular phylogenetics and classification of <em>Tulipa</em> (Liliaceae). <em>Botanical Journal of the Linnean Society</em> 172: 280–328. https://doi.org/10.1111/boj.12061</p>
<p>Coşkunçelebi, K., Terzioğlu, S., Türkmen, Z., Makbul, S. &amp; Usta, A. (2008) A comparative study on two closely relative <em>Tulipa</em> L. taxa from NE Anatolia. <em>Plant Systematics and Evolution</em> 276: 191–198. https://doi.org/10.1007/s00606-008-0094-z</p>
<p>Çakır, T. &amp; Bağcı, E. (2006) <em>Verbascum euphraticum</em> Bentham ve <em>V. melitenense</em> Boiss. (Scrophulariaceae) türleri üzerinde taksonomik bir çalışma. <em>Fırat Üniversitesi Fen ve Mühendislik Bilimleri Dergisi</em> 18: 445–458.</p>
<p>De Reboul, E. (1822) <em>Nonnullarum specierum Tuliparum in agro Florentino sponte nascentium propriae notae</em>. Archiepiscopali, Florence, pp. 1–7.</p>
<p>De Reboul, E. (1847) Sulla divisione del genere <em>Tulipa</em> in sezioni naturali. <em>Giornale Botanico Italiano </em>2: 57–61.</p>
<p>Dekhkonov, D., Tojibaev, K., Yusupov, Z., Makhmudjanov, D. &amp; Asatulloev, T. (2022) Morphology of tulips (<em>Tulipa</em>, Liliaceae) in its primary centre of diversity. <em>Plant Diversity of Central Asia</em> 1: 52–70. https://doi.org/10.54981/PDCA/vol1_iss1/a3</p>
<p>Don, D. (1836) <em>Orithyia uniflora</em>. <em>In</em>: Sweet, R. (Ed.) <em>The British flower garden</em>, ser. 2, 4. Ridgway, London. t. 336.</p>
<p>Eker, İ. (2010) <em>Revision of the genus </em>Tulipa<em> L. (Liliaceae) in Turkey</em>. PhD thesis. Abant İzzet Baysal Üniversitesi, Fen Bilimleri Enstitüsü, Bolu, 294 pp.</p>
<p>Eker, İ. &amp; Babaç, M.T. (2010) <em>Tulipa koyuncui</em> Eker &amp; Babaç sp. nov. (Liliaceae) from east Anatolia. <em>Nordic Journal of Botany</em> 28: 324–328. https://doi.org/10.1111/j.1756-1051.2009.00591.x</p>
<p>Eker, İ. (2012) <em>Tulipa. In</em>: Güner, A., Aslan, S., Ekim, T., Vural, M. &amp; Babaç, M.T. (Eds.) <em>Türkiye Bitkileri Listesi (Damarlı Bitkiler)</em>. Nezahat Gökyiğit Botanik Bahçesi ve Flora Araştırmaları Derneği Yayını, İstanbul, pp. 610–612. [in Turkish]</p>
<p>Eker, İ., Babaç, M.T. &amp; Koyuncu, M. (2014) Revision of the genus <em>Tulipa</em> L. (Liliaceae) in Turkey. <em>Phytotaxa</em> 1: 1–112. https://doi.org/10.11646/phytotaxa.157.1.1</p>
<p>Eker, İ., Yıldırım, H. &amp; Altıoğlu, Y. (2016) <em>Tulipa cinnabarina</em> subsp. <em>toprakii</em> (Liliaceae), a new subspecies from southwestern Anatolia. <em>PhytoKeys</em> 69: 65–70. https://doi.org/10.3897/phytokeys.69.9302</p>
<p>Eker, İ. (2018) <em>Tulipa</em> L. <em>In:</em> Güner A, Kandemir A, Menemen Y, Yıldırım H, Aslan S, Ekşi G, Güner I, Çimen AÖ (Eds.) <em>Resimli Türkiye Florası</em> 2, ANG Vakfı Nezahat Gökyiğit Botanik Bahçesi Yayınları, İstanbul, pp. 880–926. [in Turkish]</p>
<p>Eker, İ. (2019) Tunika Tüylerinin Yerleşimi ve Çiçek Rengi Varyasyon Aralıklarının <em>Tulipa</em> L. Cinsinin Taksonomisindeki Önemi. <em>Bağbahçe Bilim Dergisi</em> 6: 1–9. [in Turkish]</p>
<p>Fahn, A. (1982) <em>Plant anatomy</em>, 3rd Ed. Pergamon, Oxford, 588 pp.</p>
<p>Fay, M.F., Borland, K., Stranc, P., Chase, M.W. (2001) Phylogenetics of the genus <em>Tulipa</em> (Liliaceae): evidence from five plastid DNA regions.<em> In:</em> <em>Botany 2001 Abstracts </em>165. Botanical Society of America, St. Louis.</p>
<p>Freyn, J.F. (1896) Über neue und bemerkenswerthe orientalische Pflanzenarten<em>. Bulletin de l’Herbier Boissier</em> 4: 178–200.</p>
<p>Hall, A.D. (1940) <em>The genus Tulipa</em>. Royal Horticultural Society, London, 171 pp.</p>
<p>Herbert, W. (1844) <em>Tulipa humilis</em>. <em>Edwards’s Botanical Register</em> 30 (Misc.): 30.</p>
<p>Honda, M. (1935) <em>Amana</em>, a new genus of Liliaceae. <em>Bulletin of the Biogeographical Society of Japan</em> 6: 19–21.</p>
<p>IPNI (2022) <em>The international plant names index</em>. Available from: http://www.ipni.org, (accessed 24 February 2022).</p>
<p>IUCN (2016) Red List guidance documents-IUCN standards and petitions subcommittee.<em> In:</em> <em>Guidelines for using the IUCN Red List categories and criteria</em>, version 12. Available from: http://www.iucnredlist.org/ (Accessed 1 June 2019)</p>
<p>Jensen, W.A. (1962) <em>Botanical histochemistry: principles and practice</em>. Freeman, San Francisco and London, 408 pp.</p>
<p>Kandemir, N. &amp; Özkan, M. (2000) Liliaceae familyasına ait iki endemik takson üzerinde morfolojik ve anatomik çalışmalar. <em>Fırat Üniversitesi Fen ve Mühendislik Bilimleri Dergisi</em> 12: 1–17.</p>
<p>Koch, K.H.E. (1849) Beiträge zu einer Flora des Orientes. <em>Linnaea</em> 22: 177–338.</p>
<p>Kosenko, V.N. (1991) Pollen morphology of the family Liliaceae. <em>Botanicheskij Zhurnal (Leningrad)</em> 76: 1696–1706. [in Russian]</p>
<p>Kosenko, V.N. (1992) Pollen morphology and systematic problems of the Liliaceae family. <em>Botanicheskij Zhurnal (Leningrad)</em> 77: 1–15 (in Russian).</p>
<p>Levesque, R. (2007) <em>SPSS programming and data management: a guide for SPSS and SAS users</em>, fourth edition. SPSS, Chicago, 522 pp.</p>
<p>Link, J.H.F. (1799) Nachricht von einer Reise nach Portugal nebst botanischen Bemerkungen. <em>Journal für die Botanik</em> 2: 297–326.</p>
<p>Linnaeus, C. (1753) <em>Tulipa</em>. <em>Species plantarum,</em> 1. Salvius, Stockholm, pp. 305–306.</p>
<p>Marais, W. (1980) Notes on<em> Tulipa</em>. <em>Kew Bulletin</em> 35: 257–259. https://doi.org/10.2307/4114569</p>
<p>Marais, W. (1984) <em>Tulipa</em>. <em>In:</em> Davis, P.H., Mill, R.R. &amp; Tan, K. (Eds.) <em>Flora of Turkey and the east Aegean islands</em>, 8. Edinburgh University Press, Edinburgh, pp. 245–263.</p>
<p>Massart, D.L., Smeyers-Verbeke, J., Capron, X. &amp; Schlesrer, K. (2005) Visual presentation of data by means of box plots. <em>LC-GC Europe</em> 18: 215–218.</p>
<p>Meidner, H. &amp; Mansfield, T.A. (1968) <em>Physiology of stomata</em>. McGraw-Hill, London.</p>
<p>Meyer, R.K. &amp; Krueger, D.D. (2004) <em>A minitab guide to statistics</em> (3rd editon). Prentice-Hall, New Jersey, 448 pp.</p>
<p>Millar, N. (2001) Biology statistics made simple using Excel. <em>School Science Review</em> 83: 303.</p>
<p>Ocak, A., Alan, S. &amp; Ataşlar, E. (2004) Morphological, anatomical and ecological studies on <em>Tulipa armena</em> Boiss. var. <em>lycica </em>(Baker) Marais (Liliaceae). <em>Turkish Journal of Botany </em>28: 427–434.</p>
<p>Pallas, P.S. von (1776) <em>Tulipa biflora. Reise</em> 3: 727.</p>
<p>Pampanini, R. (1914) Tulipani della Tripolitania. <em>Bullettino della Società Botanica Italiana</em> 21: 110–117.</p>
<p>Persson, K. (2000) Two new bulbous species from the central Taurus Mountains of Turkey. <em>New Plantsman</em> 7: 200–208.</p>
<p>Redouté, P.J. (1803) <em>Tulipa clusiana</em>. <em>Les Liliacées</em> 1. Paris, t. 37.</p>
<p>Redouté, P.J. (1804) <em>Tulipa agenensis</em>. <em>Les Liliacées</em> 1. Paris, t. 60.</p>
<p>Regel, E. (1873) Enumeratio specierum hucusque cognitarum generis Tulipae. <em>Acta Horti Petropolitani</em> 2: 432–457.</p>
<p>Satıl, F. &amp; Akan, H. (2006) Liliaceae familyasından bazı endemik ve nadir geofitler üzerinde anatomik araştırmalar. <em>Ekoloji</em> 58: 21–27.</p>
<p>Soykan, A. &amp; Meriç, Ç. (2012) Morphological and anatomical studies of <em>Tulipa orphanidea</em> (Liliaceae).<em> Phytologia Balcanica</em> 1: 43–48.</p>
<p>Sprengel, C.P.J. (1825) <em>Tulipa saxatilis</em>. <em>In:</em> <em>Systema vegetabilium</em> 2. Dieterich, Göttingen, pp. 63.</p>
<p>Tenore, M. (1811) <em>Flora Napolitana, </em>1. Stamperia francese, Naples, pp. 170–172.</p>
<p>Terzioğlu, S. &amp; Coşkunçelebi, K. (2002) <em>Tulipa gumusanica</em> (Liliaceae), a new species from Turkey. <em>Annales Botanici Fennici</em> 39: 149–151.</p>
<p>Tiwari, S.P., Kumar, P., Yadav, D. &amp; Chauhan, D.K. (2012) Comparative morphological, epidermal, and anatomical studies of <em>Pinus roxburghii</em> needles at different altitudes in the north-west Indian Himalayas. <em>Turkish Journal of Botany</em> 37: 65–73.</p>
<p>Van Raamsdonk, L.W.D. &amp; De Vries, T. (1992) Biosystematic studies in <em>Tulipa</em> sect. <em>Eriostemones</em> (Liliaceae). <em>Plant Systematics and Evolution</em> 179: 27–41. https://doi.org/10.1007/BF00938017</p>
<p>Van Raamsdonk, L.W.D. &amp; De Vries, T. (1995) Species relationships and taxonomy in <em>Tulipa</em> subg. <em>Tulipa</em> (Liliaceae). <em>Plant Systematics and Evolution</em> 195: 13–44. https://doi.org/10.1007/BF00982313</p>
<p>Veldkamp, J.F. &amp; Zonneveld, B.J.M. (2012) The infrageneric nomenclature of <em>Tulipa</em> (Liliaceae). <em>Plant Systematics and Evolution</em> 298: 87–92. https://doi.org/10.1007/s00606-011-0525-0</p>
<p>Von Heldreich, T.H.H. (1862) <em>Tulipa orphanidea. Gartenflora</em> 11: 309, t. 373.</p>
<p>Vvedensky, A.I. (1935) <em>Tulipa</em>. <em>In</em>: Komarov, V.L. (Ed.) <em>Flora of the USSR</em>, vol. 4. An USSR, Leningrad, pp. 246–280.</p>
<p>Wilford, R. (2006) <em>Tulips—species and hybrids for the gardener</em>. Timber Press, Portland, 211 pp.</p>
<p>Zonneveld, B.J.M. (2009) The systematic value of nuclear genome size for “all” species of <em>Tulipa</em> L. (Liliaceae). <em>Plant Systematics and Evolution</em> 281: 217–245. https://doi.org/10.1007/s00606-009-0203-7</p>