Abstract
A new occurrence of buckthorn fossil leaves is reported from the upper Eocene strata of Markam Basin, southeastern Tibet, China. The leaf margin is either entire or slightly sinuous. Secondary veins are regularly spaced, forming eucamptodromous venation. These secondaries exist as straight lines from midvein to near margin and then arch abruptly upward and enter into a margin vein. The tertiary veins are densely spaced and parallel, and are percurrent to secondary veins. This leaf architecture conforms with Berhamniphyllum Jones and Dilcher, an extinct fossil genus reported from America. Our fossils are characterized by their dense secondaries, with secondary veins on the upper half portion of the blade accounting for over 40% of all secondaries. A new species, Berhamniphyllum junrongii Z. K. Zhou, T. X. Wang et J. Huang sp. nov., is proposed. Further analysis shows that confident assignment among Rhamnidium, Berchemia, and Karwinskia cannot be made based on leaf characters alone. Berhamniphyllum might represent an extinct common ancestor of these genera. In this study, several fossil Berchemia from Yunnan and Shandong are emended and reassigned to Berhamniphyllum. A new complex, namely the Berchemia Complex, is proposed based on morphology, molecular evidence, and the fossil record. This complex contains the fossil leaves of Rhamnidium, Karwinskia, Berchemia, and Berhamniphyllum. The historical biogeography of the Berchemia Complex is also discussed in this paper. This complex might have originated in the late Cretaceous in Colombia, South America, and dispersed to North America via Central America during the Eocene. Subsequently, the complex moved from North America to East Asia via the Bering Land Bridge no later than the late Eocene. Besides, the complex migrated from North America to Europe via the North Atlantic Land Bridge and then migrated further to Africa. In East Asia, it first appeared in Markam on the Qinghai-Tibetan Plateau, and then dispersed to other regions of Asia.
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References
Ai K K, Shi G L, Zhang K X, Ji J L, Song B W, Shen T Y, Guo S X. 2019. The uppermost Oligocene Kailas flora from southern Tibetan Plateau and its implications for the uplift history of the southern Lhasa terrane. Palaeogeogr Palaeoclimatol Palaeoecol, 515: 143–151
Basinger J F, Dilcher D L. 1984. Ancient bisexual flowers. Science, 224: 511–513
Becker H F. 1969. Fossil plants of the Tertiary Beaverhead Basins in souothwestern Montana. Palaeontogr Abt B, 127: 1–142
Berry E W. 1916a. The lower Eocene floras of southeastern North America. US Geol Surv Prof Pap, 91: 1–149
Berry E W. 1916b. The physical conditions indicated by the flora of the Calvert formation. US Geol Surv Prof Pap, 98: 61–73
Bozukov V. 2000. Miocene macroflora of the Satovcha Graben (Western Rhodopes). Phytol Balcan, 5: 15–30
Bozukov V, Palamarev E, Petkova A. 2008. The fossil macroflora of the Vulche Pole Molasse formation (SE Bulgaria). Phytol Balcan, 14: 173–184
Büchler W. 1990. Eine fossile Flora aus dem oberen Oligozän von Ebnat-Kappel. Bot Helv, 100: 133–166
Chaney R W, Hu H H. 1940. A Miocene Flora from Shantung Province, China. Washington: Publication of Carnegie Institute. 1–507
Chen Y, Schirarend C. 2007. Rhamnaceae. In: Wu Z Y, Raven P H, Hong D Y, eds. Flora of China. Beijing: Science Press. St. Louis: Missouri Botanical Garden Press. 12: 115–168
Collinson M E, Andrews P, Bamford M K. 2009. Taphonomy of the early miocene flora, Hiwegi formation, Rusinga Island, Kenya. J Human Evol, 57: 149–162
Collinson M E, Manchester S R, Wilde V. 2012. Fossil fruits and seeds of the Middle Eocene Messel biota, Germany. Abh Senckenb Ges Naturforsch, 570: 1–251
Correa E, Jaramillo C, Manchester S, Gutierrez M. 2010. A fruit and leaves of Rhamnaceous affinities from the late Cretaceous (Maastrichtian) of Colombia. Am J Bot, 97: 71–79
Davis C C, Bell C D, Mathews S, Donoghue M J. 2002. Laurasian migration explains Gondwanan disjunctions: Evidence from Malpighiaceae. Proc Natl Acad Sci USA, 99: 6833–6837
Denk T, Grímsson F, Zetter R. 2010. Episodic migration of oaks to Iceland: Evidence for a North Atlantic “land bridge” in the latest Miocene. Am J Bot, 97: 276–287
Deng T, Wang X, Wu F, Wang Y, Li Q, Wang S, Hou S. 2019. Review: Implications of vertebrate fossils for paleo-elevations of the Tibetan Plateau. Glob Planet Change, 174: 58–69
Dilcher D L, Lott T A. 2005. A middle Eocene fossil plant assemblage (Powers Clay Pit) from western Tennessee. Bull Florida Museum Nat Hist, 45: 1–43
Ding L, Spicer R A, Yang J, Xu Q, Cai F, Li S, Lai Q, Wang H, Spicer T E V, Yue Y, Shukla A, Srivastava G, Khan M A, Bera S, Mehrotra R. 2017. Quantifying the rise of the Himalaya orogen and implications for the South Asian monsoon. Geology, 45: 215–218
Dong W, Qi G. 2013. Hominoid-producing localities and biostratigraphy in Yunnan. In: Wang X M, Flynn L J, Fortelius M, eds. Fossil Mammals of Asia—Neogene Biostratigraphy and Chronology. New York: Colombia University Press. 293–313
Donoghue M J, Smith S A. 2004. Patterns in the assembly of temperate forest around the Northern Hemisphere. Phil Trans R Soc Lond B, 359: 1633–1644
Ellis B, Daly D C, Hickey L J, Johnson K R, Mitchell J D, Wilf P, Wing S L. 2009. Manual of Leaf Architecture. Ithaca: Cornell University Press
Flora of North America Editorial Committee, eds. 1993+. Flora of North America North of Mexico. 19+ vols. New York: Oxford University Press
Givulescu R. 1996. Flora Oligocena Superioara din Bazinul Petrosani. Casa Cartii de Stiinta, Cluj-Napoca, 1–177
Guo S X. 2011. The late Miocene Bangmai flora from Lincang county of Yunnan, southwestern China (in Chinese with English Abstract). Acta Palaeontol Sin, 50: 353–408
Guo Z T, Sun B, Zhang Z S, Peng S Z, Xiao G Q, Ge J Y, Hao Q Z, Qiao Y S, Liang M Y, Liu J F, Yin Q Z, Wei J J. 2008. A major reorganization of Asian climate by the early Miocene. Clim Past, 4: 153–174
Hauenschild F, Favre A, Michalak I, Muellner-Riehl A N. 2018. The influence of the Gondwanan breakup on the biogeographic history of the ziziphoids (Rhamnaceae). J Biogeogr, 45: 2669–2677
Hantke R. 1954. Die fossile Flora der obermiozänen Oehninger-Fundstelle Schrotzburg (Schienerberg, Süd-Baden). Doctoral Dissertation. Zürich: ETH Zürich
Heer O. 1855–1859. Flora Tertiaria Helveticae. Die Tertiäre flora der Schweiz. Winterthur: J. Wurster and Compagnie
Huang J. 2017. The middle Miocene Wenshan flora, Yunnan, southwestern China and its palaeoenvironment reconstruction. Doctoral Dissertation (in Chinese). Xishuangbanna: Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences
Ishida S. 1970. The Noroshi Flora of Noto Peninsula, Central Japan. Memoirs of the Faculty of Science Kyoto University, Series of Geology and Mineralogy, 37: 1–112
Iturralde-Vinent M A, MacPhee R D E. 1999. Paleogeography of the Caribbean region: Implications for Cenozoic biogeography. Bull Am Mus Nat Hist, 238: 1–95
Jia L B, Manchester S R, Su T, Xing Y W, Chen W Y, Huang Y J, Zhou Z K. 2015. First occurrence of Cedrelospermum (Ulmaceae) in Asia and its biogeographic implications. J Plant Res, 128: 747–761
Jia L B, Su T, Huang Y J, Wu F X, Deng T, Zhou Z K. 2019. First fossil record of Cedrelospermum (Ulmaceae) from the Qinghai-Tibetan Plateau: Implications for morphological evolution and biogeography. Jnl Sytemat Evol, 57: 94–104
Jiang H, Su T, Wong W O, Wu F, Huang J, Shi G. 2019. Oligocene Koelreuteria (Sapindaceae) from the Lunpola Basin in central Tibet and its implication for early diversification of the genus. J Asian Earth Sci, 175: 99–108
Jones J H, Dilcher D L. 1980. Investigations of angiosperms from the Eocene of North America: Rhamnus marginatus (Rhamnaceae) reexamined. Am J Bot, 67: 959–967
Jung W. 1968. Pflanzenreste aus dem Jungtertiär Nieder-und Oberbayerns und deren lokalstratigraphische Bedeutung. Ber Naturwiss Ver Langshut, 25: 43–71
Köecke V, Uhl D. 2015. The leaf assemblage from the Early-Middle Miocene locality Sulzigtobel near Werthenstein (Canton Lucerne, Switzerland). Phytol Balcan, 21: 99–109
Kovar-Eder J. 2016. Early Oligocene plant diversity along the Upper Rhine Graben: The fossil flora of Rauenberg, Germany. Acta Palaeobot, 56: 329–440
Kubitzki K. 2004. The Families and Genera of Vascular Plants. Vol. 6. Flowering Plants—Dicotyledons: Celastrales, Oxalidales, Rosales, Cornales, Ericales. Berlin: Springer
Lazarević Z, Milivojević J, Bogićević K, Nenadić D. 2013. Early Miocene flora from the Valjevo-Mionica Basin (Western Serbia). N J Geol Pal A, 267: 297–307
Lebreton-Anberrée J, Li S, Li S F, Spicer R A, Zhang S T, Su T, Deng C, Zhou Z K. 2016. Lake geochemistry reveals marked environmental change in Southwest China during the Mid Miocene Climatic Optimum. Chin Sci Bull, 61: 897–910
de León P V, Cevallos-Ferriz S R, Silva-Pineda A. 1998. Leaves of Karwinskia axamilpense sp. nov. (Rhamnaceae) from Oligocene sediments, near Tepexi de Rodríguez, Puebla, Mexico. Can J Bot, 76: 410–419
Li S F, Mao L M, Spicer R A, Lebreton-Anberrée J, Su T, Sun M, Zhou Z K. 2015. Late Miocene vegetation dynamics under monsoonal climate in southwestern China. Palaeogeogr Palaeoclimatol Palaeoecol, 425: 14–40
Li S H, Deng C L, Dong W, Sun L, Liu S Z, Qin H F, Yin J Y, Ji X P, Zhu R X. 2015. Magnetostratigraphy of the Xiaolongtan Formation bearing Lufengpithecus keiyuanensis in Yunnan, southwestern China: Constraint on the initiation time of the southern segment of the Xianshuihe-Xiaojiang fault. Tectonophysics, 655: 213–226
Liu J, Su T, Spicer R A, Tang H, Deng W Y D, Wu F X, Srivastava G, Spicer T, Van Do T, Deng T, Zhou Z K. 2019. Biotic interchange through lowlands of Tibetan Plateau suture zones during Paleogene. Palaeogeogr Palaeoclimatol Palaeoecol, 524: 33–40
Macaluso L, Martinetto E, Vigna B, Bertini A, Cilia A, Teodoridis V, Kvaček Z. 2018. Palaeofloral and stratigraphic context of a new fossil forest from the Pliocene of NW Italy. Rev Palaeobot Palynol, 248: 15–33
MacPhee R D E, Iturralde-Vinent M A. 1995. Origin of the Great Antillean land mammals, 1: New Tertiary fossils from Cuba and Puerto Rico. Am Mus Novitates, 3141: 1–31
Manchester S R. 2000. Late Eocene fossil plants of the John Day Formation, Wheeler County, Oregon. Oregon Geol, 62: 51–63
Myers J A, Kester P R, Retallack G J. 2002. Paleobotanical record of Eocene-Oligocene climate and vegetational change near Eugene, Oregon. Oregon Dep Geol Min Ind Spec Pap, 36: 145–154
Myers N, Mittermeier R A, Mittermeier C G, da Fonseca G A B, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature, 403: 853–858
Ozaki K. 1980. Late Miocene Tatsumitoge flora of Tottori Prefecture, Southwest Honshu, Japan (III). Sci Rep Yokohama Natl Univ, 27: 19–45
Ozaki K. 1991. Late Miocene and Pliocene Floras in Central Honshu, Japan. Bulletin of Kanagawa Prefectural Museum Natural Science Special Issue. Yokohama: Kanagawa Prefectural Museum. 1–244
Palgrave K C. 2015. Palgrave’s Trees of Southern Africa. 3rd ed. Cape Town: Struik Publishers
Prasad M, Dwivedi H D. 2007. Systematic study of the leaf impressions from the Churia Formation of Koilabas area, Nepal and their significance. Palaeobotanist, 56: 139–154
Retallack G J. 1992. Middle Miocene fossil plants from Fort Ternan (Kenya) and evolution of African grasslands. Paleobiology, 18: 383–400
Richardson J E, Fay M F, Cronk Q C B, Chase M W. 2000. A revision of the tribal classification of rhamnaceae. Kew Bull, 55: 311–340
Sakala J. 2000. Flora and vegetation of the roof of the main lignite seam in the Bilina Mine (Most Basin, Lower Miocene). Acta Mus Nat Pragae Ser B Hist Nat, 56: 49–84
Singh S K, Prasad M. 2007. Late Tertiary leaf flora of mahuadanr valley, Jharkhand. J Palaeontol Soc India, 52: 175–194
Smiley C J, Gray J, Huggins L M. 1975. Preservation of Miocene fossils in unoxidized lake deposits, Clarkia, Idaho. J Paleontol, 49: 833–844
Spicer R A. 2017. Tibet, the Himalaya, Asian monsoons and biodiversity—In what ways are they related? Plant Divers, 39: 233–244
Spitzelberger V G. 1989. Die Miozänfundstelle Goldern bei Landshut (Niederbayern). Geol Bavarica, 94: 371–407
Su T, Wilf P, Xu H, Zhou Z K. 2014. Miocene leaves of Elaeagnus (Elaeagnaceae) from the Qinghai-Tibet Plateau, its modern center of diversity and endemism. Am J Bot, 101: 1350–1361
Su T, Li S F, Tang H, Huang Y J, Li S H, Deng C L, Zhou Z K. 2018. Hemitrapa Miki (Lythraceae) from the earliest Oligocene of southeastern Qinghai-Tibetan Plateau and its phytogeographic implications. Rev Palaeobot Palynol, 257: 57–63
Su T, Farnsworth A, Spicer R A, Huang J, Wu F X, Liu J, Li S F, Xing Y W, Huang Y J, Deng W Y D, Tang H, Xu C L, Zhao F, Srivastava G, Valdes P J, Deng T, Zhou Z K. 2019a. No high Tibetan Plateau until the Neogene. Sci Adv, 5: eaav2189
Su T, Spicer R A, Li S H, Xu H, Huang J, Sherlock S, Huang Y J, Li S F, Wang L, Jia L B, Deng W Y D, Liu J, Deng C L, Zhang S T, Valdes P J, Zhou Z K. 2019b. Uplift, climate and biotic changes at the Eocene-Oligocene transition in south-eastern Tibet. Natl Sci Rev, 6: 495–504
Suessenguth K. 1953. Rhamnaceae. In: Engler A, Prantl K, eds. Die natürlichen Pflanzenfamilien. 2nd ed. Berlin: Dunker et Humboldt
Sun X J, Wang P X. 2005. How old is the Asian monsoon system?—Palaeobotanical records from China. Palaeogeogr Palaeoclimatol Palaeoecol, 222: 181–222
Tang H, Liu J, Wu F X, Spicer T, Spicer R A, Deng W Y D, Xu C L, Zhao F, Huang J, Li S F, Su T, Zhou Z K. 2019. Extinct genus Lagokarpos reveals a biogeographic connection between Tibet and other regions in the Northern Hemisphere during the Paleogene. J Syt Evol, 18: jse.12505
Tao J R, Chen M H. 1983. Cenozoic flora of southern Hengduan Mountain-Lincang, Yunnan. In: The CAS Scientific Expedition to the Tibetan Plateau, eds. Hengduan Mountain Investigation Collection (I) (in Chinese). Kunming: Yunnan People’s Publishing House. 74–89
Taylor T N, Taylor E L, Krings M. 2008. Paleobotany: The Biology and Evolution of Fossil Plants. 2nd ed. New York: Academic Press. 1230
Teodoridis V. 2007. Revision of Potamogeton fossils from the Most Basin and their palaeoecological significance (Early Miocene, Czech Republic). Bull Geosci, 82: 409–418
Tiffney B H, Manchester S R. 2001. The use of geological and paleontological evidence in evaluating plant phylogeographic hypotheses in the Northern hemisphere tertiary. Int J Plant Sci, 162: S3–S17
Wang W M. 1996. A palynological survey of Neogene strata in Xiaolongtan Basin, Yunnan Province of south China (in Chinese with English Abstract). Bull Bot, 38: 743–748
Writing Group of Cenozoic Plants of China (WGCPC). 1978. Cenozoic plants from China, Fossil Plants of China (in Chinese). Vol. 3. Beijing: Science Press
Wu F X, Miao D S, Chang M M, Shi G L, Wang N. 2017. Fossil climbing perch and associated plant megafossils indicate a warm and wet central Tibet during the late Oligocene. Sci Rep, 7: 878
Wu J Y. 2009. The Pliocene Tuantian flora of Tengchong, Yunnan Province and its paleoenvironmental analysis (in Chinese). Doctoral Dissertation. Lanzhou: Lanzhou University
Wu Z Y, Zhou Z K, Sun H, Li D Z, Peng H. 2006. The Areal-Types of Seed Plants and Their Origin and Differentiation (in Chinese). Kunming: Yunnan Science and Technology Press. 566
Xu C L, Su T, Huang J, Huang Y J, Li S F, Zhao Y S, Zhou Z K. 2019. Occurrence of Christella (Thelypteridaceae) in Southwest China and its indications of the paleoenvironment of the Qinghai-Tibetan Plateau and adjacent areas. J Syt Evol, 57: 169–179
Xu H, Su T, Zhang S T, Deng M, Zhou Z K. 2016. The first fossil record of ring-cupped oak (Quercus L. subgenus Cyclobalanopsis (Oersted) Schneider) in Tibet and its paleoenvironmental implications. Palaeogeogr Palaeoclimatol Palaeoecol, 442: 61–71
Xu H, Su T, Zhou Z K. 2019. Leaf and infructescence fossils of Alnus (Betulaceae) from the late Eocene of the southeastern Qinghai-Tibetan Plateau. J Syt Evol, 57: 105–113
Yabe A. 2008. Early Miocene terrestrial climate inferred from plant megafossil assemblages of the Joban and Soma areas, Northeast Honshu, Japan. Bull Geol Surv Jpn, 59: 397–413
Zhou Z K. 1985. The Miocene Xiaolongtan fossil flora in Kaiyuan, Yunnan, China (in Chinese). Master Dissertation. Nanjing: Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences
Zhou Z K, Yang X F, Yang Q S. 2006. Land bridge and long-distance dispersal—Old views, new evidence. Chin Sci Bull, 51: 1030–1038
Acknowledgements
We thank colleagues from Xishuangbanna Tropical Botanical Garden (XTBG), Chinese Academy of Sciences (CAS), and Kunming Institute of Botany, CAS for field work; Tibetan villagers from Kajun village for their kind help during field work; Dr. Gongle Shi for photographing fossil from Xiaolongtan flora; Prof. Lutz Kunzmann, Ms. Yuqing Wang and Prof. Steven Manchester for providing literature; Dr. Linbo Jia and Prof. Steven Manchester for discussion and comments; the Public Technology Service Center, XTBG, CAS for providing microscopes and experimental facilities; Teresa Spicer for improving the English manuscript. We are also grateful to two anonymous reviewers for their constructive advices. This study was supported by the Strategic Priority Research Program of CAS (Grant Nos. XDA2007030102 & XDB26000000), the NSFC (the National Natural Science Foundation of China)-NERC (Natural Environment Research Council of the United Kingdom) joint research program (Grant Nos. 41661134049 & NE/P013805/1); The Second Tibetan Plateau Scientific Expedition and Research Program (STEP), CAS (GrantNo. 2019QZKK0705), Youth Innovation Promotion Association, CAS (Grant No. 2017439) and Key Research Program of Frontier Sciences, CAS (Grant No. QYZDB-SSW-SMC016).
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Zhou, Z., Wang, T., Huang, J. et al. Fossil leaves of Berhamniphyllum (Rhamnaceae) from Markam, Tibet and their biogeographic implications. Sci. China Earth Sci. 63, 224–234 (2020). https://doi.org/10.1007/s11430-019-9477-8
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DOI: https://doi.org/10.1007/s11430-019-9477-8