ORIGINAL ARTICLE
Pollen morphology of some species of the genus Quercus L. (Fagaceae) in the Southern Caucasus and adjacent areas
 
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1
Institute of Botany after A. Takhtajan, National Academy of Sciences of the Republic of Armenia, Yerevan, Armenia
2
ROCEEH Research Centre ‘The role of culture in early expansions of humans’ of the Heidelberg Academy of Sciences, Senckenberg Research Institute, Senckenberganlage 25, 60325 Frankfurt am Main, Germany
Submission date: 2019-08-12
Online publication date: 2020-06-29
Publication date: 2020-06-29
 
Acta Palaeobotanica 2020; 60(1): 1–42
 
KEYWORDS
ABSTRACT
The palynomorphology of 19 modern species of the genus Quercus L. native to Armenia and adjacent regions, including the Caucasus and Transcaucasia, the Mediterranean region (especially Turkey), as well as Iran, Iraq and Afghanistan, was studied using light microscopy (LM) and scanning electron microscopy (SEM). The work revealed two main types of apertures (3-zonocolpate, 3-zonocolp-porate) as well as six morphological types of pollen based on three main types of exine ornamentation (tuberculate, verrucate, rugulate). We suggest that two main groups of exine ornamentation developed from a common initial type. The first group covers all species of the subgenus Quercus and also Q. suber and Q. alnifolia of the subgenus Heterobalanus. The second group is limited to the morphological type Q. ilex (species Q. ilex, Q. coccifera, subgenus Heterobalanus). On the other hand, the presence of widespread interspecific and introgressive hybridization within the genus Quercus indicates an ongoing process of speciation. This also has an effect on pollen features, which are very similar in a number of species but also vary in individual samples even within the same species. The morphological uniformity of the pollen surface (especially for the subgenus Quercus), the presence of islets of secondary sporopollenin on the surface of pollen grains, as well as orbicules in anthers, do not indicate general primitiveness of representatives of this genus but most likely denote a relatively high degree of speciation activity within this group.
 
REFERENCES (92)
1.
Avetisyan, E.M., 1950. Uproshchenny atsetolizny metod obrabotki pil’tsi. Botanicheskii Zhurnal 35(4), 385−387 (in Russian).
 
2.
Avetisyan, E.M., Hayrapetyan, A.M., 2002. K terminologii slozhnikh apertur (summary: On the terminology of compound apertures of pollen grains). Flora, rastitel’nost’ i rastitel’nie resursy Armenii 14, 64−67 (in Russian).
 
3.
Avetisyan, E.M., Manukyan, L.K., 1962. Opisanie pil’tsi semeystva Fagaceae. Flora Armenii, 4. Akademiya Nauk ArmSSR, Yerevan (in Russian).
 
4.
Barrón, E., Averyanova, A., Kvaček, Z., Momohara, A., Pigg, K.B., Popova, S., Postigo-Mijarra, J.M., Tiffney, B.H., Utescher, T., Zhou, Z.K., 2017. The fossil history of Quercus. In: Gil-Pelegrín, E., Peguero- Pina, J.J., Sancho-Knapik, D. (eds), Oaks physiological ecology. Exploring the functional diversity of genus Quercus L. Tree physiology, 7. Springer, Heidelberg, New York, pp. 39–105. https://doi.org/10.1007/978-3-....
 
5.
Blackmore, S., Barnes, S.H., 1986. Harmomegatic mechanisms in pollen grains. In: Blackmore, S., Ferguson, I.K. (eds), Pollen and spores: form and function. Linnean Society Symposium Series, 12. Linnean Society, London, pp. 137−150.
 
6.
Blanco, M.A.F., Barrera, R.M.V., Gonzalez, D.F., Merino, A.P., 1996. Estudio polínico de Quercus robur L. en el noroeste de la península Ibérica. Botánica Macaronésica 23, 25−33.
 
7.
Cao, M., Zhou, Z.K., 2002. Pollen morphology and its systematic significance of the Quercus from China. Guihaia 22, 14–18.
 
8.
Colombo, P.M., Lorenzoni, F.C., Grigoletto, F., 1983. Pollen grain morphology supports the taxonomical discrimination of Mediterraneae oaks (Quercus, Fagaceae). Plant Systematics and Evolution 141, 273−284. https://doi.org/10.1007/bf0098....
 
9.
Czerepanov, S.K., 1995. Vascular plants of Russia and adjacent states (the former USSR). Cambridge University Press, New York, pp. 1–516.
 
10.
Denk, T., Grimm, G.W., 2009. Significance of pollen characteristics for infrageneric classification and phylogeny in Quercus (Fagaceae). International Journal of Plant Sciences 170(7), 926–940. https://doi.org/10.1086/600134.
 
11.
Denk, T., Grimm, G.W., 2010. The oaks of western Eurasia: traditional classifications and evidence from two nuclear markers. Taxon 59(2), 351–366. https://doi.org/10.1002/tax.59....
 
12.
Denk, T., Tekleva, M.V., 2014. Pollen morphology and ultrastructure of Quercus with focus on Group Ilex (= Quercus subgenus Heterobalanus (Oerst.) Menitsky): implications for oak systematics and evolution. Grana 53(4), 255–282. https://doi.org/10.1080/001731....
 
13.
Denk, T., Grímsson, F., Zetter, R., 2012. Fagaceae from the early Oligocene of Central Europe: persisting new world and emerging old world biogeographic links. Review of Palaeobotany and Palynology 169, 7−20. https://doi.org/10.1016/j.revp....
 
14.
Denk, T., Grimm, G.W., Manos, P.S., Deng, M., Hipp, A.L., 2017. An updated infrageneric classification of the oaks: review of previous taxonomic schemes and synthesis of evolutionary patterns. In: Gil- Pelegrín, E., Peguero-Pina, J.J., Sancho-Knapik, D. (eds), Oaks Physiological Ecology. Exploring the Functional Diversity of Genus Quercus L., Tree Physiology, 7. Springer, Heidelberg, New York, pp. 13–38. https://doi.org/10.1007/978-3-....
 
15.
Docturoski, V.S., Kudriaschow, V.V., 1923. Pil’tsa v torfe. Izvestiya Nauchno-experimental’nogo torfyanogo instituta (Moskwa) 5, 33–44 (in Russian).
 
16.
Dupont, P., Dupont, S., 1972. Etude de pollens de chênes (genre Quercus L.) en microscopie électronique à balayage. Comptes rendus de l’Académie des Sciences Paris 274(17), 2503−2506. Erdtman, G., 1923. Beitrag zur Kenntnis der Mikrofossilen in Torf und Sedimenten. Arkiv för Botanik 18(14), 1−9.
 
17.
Erdtman, G., 1943. An introduction to pollen analysis. Chronica Botanica Company, Waltham.
 
18.
Erdtman, G., 1952. Pollen morphology and plant taxonomy. Angiosperms. Almqvist et Wiksell, Stockholm.
 
19.
Erdtman, G., Berglund, B., Praglowski, J., 1961. An introduction to a Scandinavian pollen flora. Almqvist et Wiksell, Stockholm. https://doi.org/10.1080/001731....
 
20.
Fortini, P., Antonecchia, G., Di Marzio, P., Maiuro, L., Viscosi, V., 2015. Role of micromorphological leaf traits and molecular data in taxonomy of three sympatric white oak species and their hybrids (Quercus L.). Plant Biosystems 149, 546−558. https://doi.org/10.1080/112635....
 
21.
Greenfield, E.K., 1962. Proiskhozhdenie antofilii u nasekomikh. Leningradski Gosudarsvenni Universitet, Leningrad (in Russian).
 
22.
Grímsson, F., Zetter, R., Grimm, G.W., Krarup Pedersen, G., Pedersen, A.K., Denk, T., 2015. Fagaceae pollen from the early Cenozoic of West Greenland: revisiting Engler’s and Chaney’s Arcto-Tertiary hypotheses. Plant Systematics and Evolution 301, 809–832. https://doi.org/10.1007/s00606....
 
23.
Grímsson, F., Grimm, G.W., Zetter, R., Denk, T., 2016. Cretaceous and paleogene Fagaceae from North America and Greenland: evidence for a Late Cretaceous split between Fagus and the remaining Fagaceae. Acta Palaeobotanica 56, 247–305. https://doi.org/10.1515/acpa-2....
 
24.
Grossheim, A.A., 1949. Opredelitel’ rasteni Kavkaza. Sovetskaja Nauka, Moskva (in Russian).
 
25.
Hayrapetyan, A., 2013. Palynomorphological investigation of the genus Quercus L. In: Abstracts of the conference «The Role of the Southern Caucasus on Early Human Evolution and Expansion – Refuge, Hub or Source Area?». Tbilisi, Georgia, 73−74. http://www.roceeh.net/fileadmi... program_abstract_Tbilisi.pdf Heslop-.
 
26.
Harrison, J., 1979. An interpretation of the hydrodynamics of pollen. American Journal of Botany 66, 737−743. https://doi.org/10.1002/j.1537....
 
27.
Hesse, M., Halbritter, H., Zetter, R., Weber, M., Buchner, R., Frosch-Radivo, A., Ulrich, S., 2009. Pollen terminology. An illustrated handbook. Springer, Wien. https://doi.org/10.1007/978-3-....
 
28.
Hill, R.S., Jordan, G.J., 1993. The evolutionary history of Nothofagus (Nothofagaceae). Australian Systematic Botany 6, 111–126. https://doi.org/10.1071/sb9930....
 
29.
Hill, R.S., Read, J., 1991. A revised infrageneric classification of Nothofagus (Fagaceae). Botanical Journal of the Linnean Society 105, 37–72. https://doi.org/10.1111/j.1095....
 
30.
Hipp, A.L., Manos, P., Mcvay, J.D., Cavender-Bare Rodriguez, A., Romero-Severson, J., Hahn, M., Budaitis, B., Deng, M., Grimm, G.W., Fitzek, E.C., Jennings, T.L., Avishai, M., Simeone, M.C., 2015. A phylogeny of the world’s oaks. Botany 2015. Edmonton, Kanada, 25−29 July 2015, abstract ID 1305. http://2015.botanyconference.o... search/index.php?func=detail&aid=1305.
 
31.
Hubert, F., Grimm, G.W., Jousselin, E., Berry, V., Franc, A., Kremer, A., 2014. Multiple nuclear genes stabilize the phylogenetic backbone of the genus Quercus. Systematics and Biodiversity 12, 405–423. https://doi.org/10.1080/147720....
 
32.
Hyde, H.A., 1955. Oncus, a new term in pollen morphology. New Phytologist 54, 255−256. https://doi.org/10.1111/j.1469....
 
33.
Jarvis, D.I., Leopold, E.B., Liu, Y., 1992. Distinguishing the pollen of deciduous oaks, evergreen oaks and certain rosaceous species of southwestern Sichuan Province, China. Review of Palaeobotany and Palynology 75, 259−271. https://doi.org/10.1016/0034-6....
 
34.
Jones, J.H., 1986. Evolution of the Fagaceae: The implications of foliar features. Annals of the Missouri Botanical Garden 73, 228–275. https://doi.org/10.2307/239911....
 
35.
Kosmath, L., 1927. Studie über das Antherentapetum. Österreichische Botanische Zeitschrift 76, 235–241. https://doi.org/10.1007/bf0124....
 
36.
Kremer, A., Abbott, A.G., Carlson, J.E., Manos, P.S., Plomion, C., Sisco, P., Staton, M.E., Ueno, S., Vendramin, G.G., 2012. Genomics of Fagaceae. Tree Genetics & Genomes 8, 583–610. https://doi.org/10.1007/s11295....
 
37.
Kubitzki, K., 1993. Fagaceae. In: Kubitzki, K. (ed.), The families and genera of vascular plants, 2. Springer, Berlin, Heidelberg, New York, pp. 301–309. https://doi.org/10.1007/978-3-....
 
38.
Kuprianova, L.A., 1965. Palinologiya serezhkotsvetnikh (Palynology of Amentiferae). Nauka, Moscow, Leningrad (in Russian). Kuprianova, L.A., Alyoshina, L.A., 1967. Palinologicheskaya terminologiya pokritosemennikh rasteni. Nauka, Leningrad (in Russian).
 
39.
Kuprianova, L.A., Alyoshina, L.A., 1972. Pyl’tsa i spory rasteni flori Yevropeyskoy chasti SSSR (Pollen and spores of plants of the flora of the European part of USSR), I. Akademiya Nauk SSSR, BIN, Leningrad (in Russian).
 
40.
Litt, T., Pickarski, N., Heumann, G., Stockhecke, M., Tzedakis, P.C., 2014. A 600,000 year long continental pollen record from Lake Van, eastern Anatolia (Turkey). Quaternary Science Reviews 104, 30−41. https://doi.org/10.1016/j.quas....
 
41.
Liu, Y.S., Zetter, R., Ferguson, D.K., Mohr, B.A.R., 2007. Discriminating fossil evergreen and deciduous Quercus pollen: a case study from the Miocene of Eastern China. Review of Palaeobotany and Palynology 145, 289−303. https://doi.org/10.1016/j.revp....
 
42.
Makino, M., Hayashi, R., Takahara, H., 2009. Pollen morphology of the genus Quercus by scanning electron microscope. Scientific Reports of Kyoto Prefectural University, Life and Environmental Sciences 61, 53–81.
 
43.
Manos, P.S., Zhou, Z.K., Cannon, C.H., 2001. Systematics of Fagaceae: phylogenetic tests of reproductive trait evolution. International Journal of Plant Sciences 162, 1361–1379. https://doi.org/10.1086/322949.
 
44.
Marquez, J., Seoane-Camba, J., Suarez-Cervera, M., 1997. The role of the intine and cytoplasm in the activation and germination processes of Poaceae pollen grains. Grana 36, 328−342. https://doi.org/10.1080/001731....
 
45.
Meduz, J., Gonzales Flores, G., 1984. Pollen morphology of some Mexican oaks. Grana 23, 77−84. https://doi.org/10.1080/001731....
 
46.
Meinke, H., 1927. Atlas und Bestimmungsschlüssel zur Pollenanalyse. Bot. Archiv. 19, 380−449. Menitsky, Y.L., 1980. Fagaceae. In: Zhizn’ rasteni, 5(1). Prosveshchenie, Moskva, pp. 293−311 (in Russian).
 
47.
Menitsky, Y.L., 1982. Obzor vidov roda Quercus L. Yevrazii (Conspectus specierum generis Quercus L. Gerontogeae). Nauka, Leningrad (in Russian).
 
48.
Menitsky, Y.L., 1984. Duby Asii. Nauka, Leningrad (in Russian). Menitsky, Y.L., 2005. Oaks of Asia. Science Publishers, Enfield, USA.
 
49.
Menitsky, Y.L., 2012. Fagaceae Dumort. In: Kudryashova, G.L., Tatanov, I.V. (eds), Konspekt flory Kavkaza (Caucasian flora conspectus), 3(2). Association of Scientific Publications KMK, St. Petersburg, Moscow, pp. 286–292 (in Russian). https:// www.binran.ru/resursy/informat... tekuschie-proekty/caucasian-flora/contentkav/ allpdf/tom32.php.
 
50.
Meyer, N.R., 1980. Veroyatnie napravleniya evolyutsii sporodermy golosemennikh i nekotorikh pokrytosemennihh. In: Sistematika i evolyutsiya vishikh rasteni. Nauka, Leningrad, pp. 86–92 (in Russian).
 
51.
Monoszon, M., 1954. Morfologicheskoe opisanie pil’tsi glavneyshikh vidov duba, proizrastayushchikh na territorii SSSR. Trudi Instituta geografii AN SSSR 61, 93−118 (in Russian).
 
52.
Monoszon, M., 1961. O variatsiyakh morfologicheskikh priznakov pil’tsi nekotorikh vidov duba. Dokladi Academii Nauk SSSR 140(6), 1456−1459 (in Russian).
 
53.
Mühlenthaler, K., 1955. Die Struktur einiger Pollenmembranen. Planta 46(1), 1−13. https://doi.org/10.1007/bf0194....
 
54.
Mulkidzhanyan, YA.I., 1962. Fagaceae. Flora Armenii, 4. Akademiya Nauk ArmSSR, Yerevan, pp. 374– 391 (in Russian).
 
55.
Nakagava, T., Yasuda, Y., Tabata, H., 1996. Pollen morphology of Himalayan Pinus and Quercus and its importance in palynological studies in Himalayan area. Review of Palaeobotany and Palynology 91(14), 317−329. https://doi.org/10.1016/0034-6....
 
56.
Naryshkina, N.N., 2013. Morfologia sovremennoy i iskopaemoy pil’tsi nekotorikh vidov roda Quercus L. Synopsis of master’s thesis. Biologo-pochvenni institut DVO RAN, Vladivostok (in Russian).
 
57.
Olsson, U., 1975. A morphological analysis of phenotypes in populations of Quercus (Fagaceae) in Sweden. Botaniska Notiser 128, 55−68.
 
58.
Pacini, E., Franchi, G.G., Hesse, M., 1985. The tapetum: its form, function and possible phylogeny in embryophyta. Plant Systematics and Evolution 149, 155−185. https://doi.org/10.1007/bf0098....
 
59.
Panahi, P., Pourmajidian, M.R., Fallah, A., Pourhashemi, M., 2012. Pollen morphology of Quercus (subgenus Quercus, section Quercus) in Iran and its systematic implication. Acta Societatis Botanicorum Poloniae 81, 33−41. https://doi.org/10.5586/asbp.2....
 
60.
Papini, A., Simeone, M.C., Bellarosa, R., Spada, F., Schirone, B., 2011. Quercus macranthera Fisch. & Mey. ex Hohen. and Quercus iberica M. Bieb. Taxonomic definition and systematic relationships with European oaks inferred from nuclear internal transcribed spacer (ITS) data. Plant Biosystems 145(1), 37−49. https://doi.org/10.1080/112635....
 
61.
Pilcher, J.R., 1968. Some application of scanning electron microscopy to the study of modern and fossil pollen. Ulster Journal of Archeology (UJA) 31, 87−91.
 
62.
Potonié, R., 1934. Zur Morphologie der fossilen Pollen und Sporen. Arbeiten des Instituts für Paläobotanik und Petrographie der Brennsteine 4, 5−24.
 
63.
Praglowski, J., 1982. Fagaceae L.: Fagoideae. World pollen and spore flora, 11. Almqvist & Wiksell, Stockholm.
 
64.
Punt, W., Hoen, P.P., Blackmore, S., Nilsson, S., Le Thomas, A., 2007. Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology 143, 1−81. https://doi.org/10.1016/j.revp....
 
65.
Rowley, J.R., Gabaraeva, N.I., 2004. Microspore development in Quercus robur (Fagaceae). Review of Palaeobotany and Palynology 132, 115−132. https://doi.org/10.1016/j.revp....
 
66.
Sadori, L., Koutsodendris, A., Panagiotopoulos, K., Masi, A., Bertini, A., Combourieu-Nebout, N., Francke, A., Kouli, K., Joannin, S., Mercuri, A.M., Peyron, O., Torri, P., Wagner, B., Zanchetta, G., Sinopoli, G., Donders, T.H., 2016. Pollen-based paleoenvironmental and paleoclimatic change at Lake Ohrid (south-eastern Europe) during the past 500 ka. Biogeosciences 13, 1423−1437. https://doi.org/10.5194/bg-13-....
 
67.
Samoilovich, S., 1950. Rod Quercus L. – Dub. In: Krishtofovich, A.N. (ed.), Pil’tsevoy analiz. Gosgeolizdat, Moskva, 226–231 (in Russian).
 
68.
Schottky, E., 1912. Die Eichen des extratropischen Ostasiens und ihre pflanzengeographische Bedeutung. Botanische Jahrbücher für Systematik 47, 617–708.
 
69.
Schwarz, O., 1936a. Über die Typologie des Eichenblattes und ihre Anwendung in der Paläobotanik. Feddes Repertorium 86(13), 60−70.
 
70.
Schwarz, O., 1936b–1939. Monographie der Eichen Europas und des Mittelmeergebietes. Repertorium specierum novarum regni vegetabilis, Sonderbeiheft D, I(1−5), II(1−4). F. Fedde, Berlin.
 
71.
Schwarz, O., 1964. Quercus L. In: Tutin, T.G., Heywood, V.H., Burges, N.A., Valentine, D.H., Walters, S.M., Webb, D.A. (eds), Flora Europaea, vol. 1: Lycopodiaceae to Platanaceae. Cambridge University Press, Cambridge, pp. 61−64.
 
72.
Shtepa, I.S., 1942. Stroenie pol’tsi kavkazskikh predstaviteley sem. Fagaceae Soobshcheniya Akademii Nauk Gruzinskoy SSR 3(5), 451−457 (in Russian).
 
73.
Smit, A., 1973. A scanning electron microscopical study of the pollen morphology in the genus Quercus. Acta Botanica Neerlandica 22(6), 655−665. https://doi.org/10.1111/j.1438....
 
74.
Smolyaninova, L.A., Golubkova, V.F., 1950. K metodike issledovaniya pil’tsi. Dokladi Akademii Nauk SSSR 75(1), 125−126 (in Russian).
 
75.
Solomon, A.M., 1983a. Pollen morphology and plant taxonomy of white oaks in eastern North America. American Journal of Botany 70(4), 481−494. https://doi.org/10.1002/j.1537....
 
76.
Solomon, A.M., 1983b. Pollen morphology and plant taxonomy of red oaks in eastern North America. American Journal of Botany 70(4), 495−507. https://doi.org/10.1002/j.1537....
 
77.
Sporne, K.R., 1973. A note on the evolutionary status of tapetal types in dicotyledons. New Phytologist 72, 1173−1174. https://doi.org/10.1111/j.1469....
 
78.
Takhtajan, A.L., 1966. Sistema i filogeniya tsvekovikh rasteni (Systema et Phylogenia Magnoliophytorum). Nauka, Moskva, Leningrad (in Russian).
 
79.
Takhtajan, A., 1987. Sistema Magnoliofitov (Systema Magnoliophytorum). Nauka, Leningrad (in Russian).
 
80.
Takhtajan, A., 1997. Diversity and classification of flowering plants. Columbia University Press, New York.
 
81.
Takhtajan, A., 2009. Flowering Plants. Springer, Netherlands. Tekleva, M.V., 2012. Skritoe raznoobrazie, ili elektronni mikroskop speshit na pomoshch (Reports of popular science articles of winners of The Russian Foundation for Basic Research of 2012 competition). Biologia i meditsinskie nauki. ITZC Molnet, pp. 158−167 (in Russian).
 
82.
Tekleva, M.V., Polevova, S.V., 2014. Morfologia i ul’trastruktura sporodermi v sistematike roda Quercus L. Semicentenary after Konstantin Meyer: XIII Moskow Symposium on plant phylogeny, Moskva, Rossia (2−6 February 2015), 295−299 (in Russian). The Plant List. http://www.theplantlist.org/.
 
83.
Trelease, W., 1924. The American oaks. Memoirs of the National Academy of Sciences 20, 1−255.
 
84.
Tzedakis, P.C., Hooghiemstra, H., Pälike, H., 2006. The last 1.35 million years at Tenaghi Philippon: revised chronostratigraphy and long-term vegetation trends. Quaternary Science Reviews 25, 3416−3430. https://doi.org/10.1016/j.quas....
 
85.
Valdes, B., Diez, M.J., Fernandez, I., 1987. Atlas Polinico de Andalucia Occidental. Instituto de Dessarrollo Regional N 43, Universidad de Sevilla, Sevilla, Spain.
 
86.
Van Benthem, F., Clarke, G.C.S., Punt, W., 1984. Fagaceae. Review of Palaeobotany and Palynology 42, 87−110. https://doi.org/10.1016/0034-6....
 
87.
Wang, P.L., Chang, K.T., 1991. The pollen morphology in relation to the taxonomy and phylogeny of Fagaceae. Acta Phytotaxonomica Sinica 29, 60–66.
 
88.
Wang, P.L., Pu, F.T., Zheng, Z.H., 2000. Pollen morphology of the genus Nothofagus and its taxonomic significance. Acta Phytotaxonomica Sinica 38, 452–461.
 
89.
Wodehouse, R.P., 1935. Pollen grains. McGraw-Hill, New York, London. Wodehouse, R.P., 1936. Evolution of pollen grains. The Botanical Review 2, 67−84. https://doi.org/10.1007/bf0286....
 
90.
Wronska-Pilarek, D., Danielewicz, W., Bocianowski, J., Malinski, T., Janyszek, M., 2016. Comparative pollen morphological analysis and its systematic implications on three european Oak (Quercus L., Fagaceae) species and their spontaneous hybrids. PLOSone 11(8), 1–19. https://doi.org/10.1371/journa....
 
91.
Xiang, X.-G., Wang, W., Li, R.-Q., Lin, L., Liu, Y., Zhou, Z.-K., Li, Z.-Y., Chen, Z.-D., 2014. Largescale phylogenetic analyses reveal fagalean diversification promoted by the interplay of diaspores and environments in the Paleogene. Perspectives in Plant Ecology, Evolution and Systematics 16(3), 101–110. https://doi.org/10.1016/j.ppee....
 
92.
Xing, Y.-W., Hu, J.-J., Jacques, F.M.B., Wang, L., Su, T., Huang, Y.-J., Liu, Y.-S., Zhou, Z.-K., 2013. A new Quercus species from the upper Miocene of southwestern China and its ecological significance. Review of Palaeobotany and Palynology 193, 99–109. https://doi.org/10.1016/j.revp....
 
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