Leaves and fruits of Bauhinia (Leguminosae, Caesalpinioideae, Cercideae) from the Oligocene Ningming Formation of Guangxi, South China and their biogeographic implications

BMC Evolutionary Biology

Zhenyu Li¹  Si Shen¹  Yunfa Chen²  Zhuqiu Song²  Qi Wang¹ 

[1] State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, P.R. China;Natural History Museum of Guangxi, Nanning 530012, P.R. China

关键词: Unifoliolate leaf;    Tethys Seaway origin;    Pulvinus;    Oligocene;    Ningming Formation;    Low latitude;    Leguminosae;    Legumes;    Fruits;    Evolution;    Eocene;    Cercis;    Cercideae;    Biogeography;    Bilobate leaf;    Bifoliolate leaf;    Bauhinia;   

Others  :  856658
DOI  :  10.1186/1471-2148-14-88

 received in 2014-01-19, accepted in 2014-04-13,  发布年份 2014

【 摘 要 】

Background

The pantropical genus Bauhinia, along with the northern temperate Cercis and several tropical genera, bear bilobate, bifoliolate, or sometimes unifoliolate leaves, which constitute the tribe Cercideae as sister to the rest of the family Leguminosae based on molecular phylogenetics. Hence, the fossil record of Cercideae is pivotal to understand the early evolution and biogeographic history of legumes.

Results

Three fossil species of Bauhinia were described from the Oligocene Ningming Formation of Guangxi, South China. Bauhinia ningmingensis sp. nov. is characterized by its bifoliolate, pulvinate leaves bearing basal acrodromous primary veins and brochidodromous secondary veins. B. cheniae sp. nov. bears moderately or deeply bilobate, pulvinate leaves, with basal actinodromous primary veins and eucamptodromous secondary veins. B. larsenii D.X. Zhang et Y.F. Chen emend. possesses shallowly or moderately bilobate, pulvinate leaves bearing basal actinodromous primary veins and brochidodromous secondary veins, as well as elliptic, stipitate, non-winged, and oligo-seeded fruits. Meanwhile, previously reported Bauhinia fossils were reviewed, and those pre-Oligocene foliage across the world are either questionable or have been rejected due to lacking of reliable evidence for their pulvini or/and basal actinodromous or acrodromous venations. Besides Oligocene leaves and fruits presented here, foliage and/or wood of Bauhinia have been documented from the Miocene–Pliocene of Thailand, India, Nepal, Uganda, and Ecuador.

Conclusions

Bauhinia has exhibited a certain diversity with bifoliolate- and bilobate-leafed species in a low-latitude locality–Ningming since at least the Oligocene, implying that the tropical zone of South China may represent one of the centres for early diversification of the genus. The reliable macrofossils of Bauhinia and Cercis have made their debut in the Eocene–Oligocene floras from mid-low latitudes and appeared to lack in the coeval floras at high latitudes, implying a possible Tethys Seaway origin and spread of legumes. However, detailed scenarios for the historical biogeography of Bauhinia and its relatives still need more robust dataset from palaeobotany and molecular phylogeny in future research.

【 授权许可】

   
2014 Wang et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Wunderlin RP, Larsen K, Larsen SS: Cercideae Bronn (1822). In Advances in legume systematics, part 1. Edited by Polhill RM, Raven PH. Kew: The Royal Botanic Gardens; 1981:107-116.
• [2]Wunderlin RP, Larsen K, Larsen SS: Reorganization of the Cercideae (Fabaceae: Caesalpinioideae). Biol Skr 1987, 28:1-40.
• [3]Chen TC: Bauhinia Linn. In Flora Reipublicae Popularis Sinicae, Tomus 39. Edited by Wu TL, Chen PY, Wei CF, Chen TC. Beijing: Science Press; 1988:145-203.
• [4]Lewis G, Forest F: Tribe Cercideae. In Legumes of the world. Edited by Lewis G, Schrire B, Mackinder B, Lock M. Kew: The Royal Botanic Gardens; 2005:57-68.
• [5]Chen TC, Zhang DX, Larsen K, Larsen SS: Bauhinia Linnaeus. In Flora of China, vol. 10. Edited by Wu ZY, Raven PH, Hong DY. Beijing: Science Press & St. Louis: Missouri Botanical Garden Press; 2010:6-21.
• [6]Wunderlin RP: Reorganization of the Cercideae (Fabaceae: Caesalpinioideae). Phytoneuron 2010, 48:1-5.
• [7]Zhang DX: Leaf venation of Cercideae (Leguminosae). J Trop Subtrop Bot 1994, 2:45-57.
• [8]Zhang DX: A cladistic analysis of Bauhinia L. (Leguminosae). Chin J Bot 1995, 7:52-64.
• [9]Hao G, Zhang DX, Zhang MY, Guo LX, Li SJ: Phylogenetics of Bauhinia subgenus Phanera (Leguminosae: Caesalpinioideae) based on ITS sequences of nuclear ribosomal DNA. Bot Bull Acad Sin 2003, 44:223-228.
• [10]LPWG (the Legume Phylogeny Working Group): Legume phylogeny and classification in the 21st century: Progress, prospects and lessons for other species-rich clades. Taxon 2013, 62:217-248.
• [11]Sinou C, Forest F, Lewis GP, Bruneau A: The genus Bauhinia s. l. (Leguminosae): a phylogeny based on the plastid trnL–trnF region. Botany 2009, 87:947-960.
• [12]Santos FDARD, Novaes DDM, Queiroz LPD: Pollen of Bauhinia L. and Phanera Lour. (Leguminosae–Caesalpinioideae) from the Brazilian Caatinga. Amer J Pl Sci 2012, 3:909-920.
• [13]Banks H, Forest F, Lewis G: Palynological contribution to the systematics and taxonomy of Bauhinia s. l. (Leguminosae: Cercideae). S African J Bot 2013, 89:219-226.
• [14]Anju J, Manodeep C, Jagdish K: Bauhinia tomentosa: a phytopharmacological review. Int Res J Pharm 2011, 2:128-131.
• [15]Kumar T, Chandrashekar KS: Bauhinia purpurea Linn.: A review of its ethnobotany, phytochemical and pharmacological profile. Res J Med Pl 2011, 5:420-431.
• [16]Zhang YQ, Xu W, Li H, Chen LD, Chu KD: Some progress in Bauhinia championi (Benth.) Benth. of Chinese herbal medicines. Asia-Pacific Tradit Med 2012, 8:207-209.
• [17]LPWG (the Legume Phylogeny Working Group): Towards a new classification system for legumes: Progress report from the 6th International Legume Conference. S African J Bot 2013, 89:3-9.
• [18]Bruneau A, Forest F, Herendeen PS, Klitgaard BB, Lewis GP: Phylogenetic relationships in the Caesalpinioideae (Leguminosae) as inferred from chloroplast trnL intron sequences. Syst Bot 2001, 26:487-514.
• [19]Bruneau A, Mercure M, Lewis GP, Herendeen PS: Phylogenetic patterns and diversification in the caesalpinioid legumes. Botany 2008, 86:697-718.
• [20]Doyle JJ, Luckow MA: The rest of iceberg: legume diversity and evolution in a phylogenetic context. Pl Physiol 2003, 131:900-910.
• [21]Wojciechowski MF, Lavin M, Sanderson MJ: A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Amer J Bot 2004, 91:1846-1862.
• [22]Lewis G, Schrire B, Mackinder B, Lock M: Legumes of the world. Kew: The Royal Botanic Gardens; 2005:1-577.
• [23]Schrire BD, Lavin M, Lewis GP: Global distribution patterns of the Leguminosae: insights from recent phylogenies. Biol Skr 2005, 55:375-422.
• [24]Lavin M, Herendeen PS, Wojciechowski MF: Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary. Syst Biol 2005, 54:575-594.
• [25]Van der Pijl L: The leaf of Bauhinia. Acta Bot Neerl 1952, 1:287-309.
• [26]Cusset G: Essai d’une Taxinomie Foliaire dans la Tribu des Bauhinieae. Adansonia, N S 1966, 6:251-280.
• [27]Owens SA: Secondary and tertiary pulvini in the unifoliate leaf of Cercis canadensis L. (Fabaceae) with comparison to Bauhinia purpurea L. Int J Pl Sci 2000, 161:583-597.
• [28]Kuang GD, Chen GJ, Chen YF, Huang ZT: New information on the Tertiary biostratigraphy of the Ningming Basin, Guangxi. J Stratigr 2004, 28:362-367.
• [29]Liu GW, Yang RY: Pollen assemblages of the Late Eocene Nadu Formation from the Bose Basin of Guangxi, Southern China. Palynology 1999, 23:97-114.
• [30]Böhme M, Aiglstorfer M, Antoine P-O, Appel E, Havlik P, Métais G, Phuc LT, Schneider S, Setzer F, Tappert R, Tran DN, Uhl D, Prieto J: Na Duong (northern Vietnam)–an exceptional window into Eocene ecosystems from Southeast Asia. Zitteliana A 2013, 53:121-167.
• [31]Li HM, Chen YF, Chen GJ, Kuang GD, Huang ZT: Tertiary fossil winged fruits of Palaeocarya from Ningming of Guangxi. S China Acta Palaeontol Sin 2003, 42:537-547.
• [32]Wang WM, Chen GJ, Chen YF, Kuang GD: Tertiary palynostratigraphy of the Ningming basin, Guangxi. J Stratigr 2003, 27:324-327.
• [33]Chen YF, Zhang DX: Bauhinia larsenii, a fossil legume from Guangxi, China. Bot J Linn Soc 2005, 147:437-440.
• [34]Chen GJ, Fang F, Chang MM: A new cyprinid closely related to cultrins + xenocyprinins from the Mid-Tertiary of South China. J Vertebr Paleontol 2005, 25:492-501.
• [35]Chen GJ, Chang MM: A new cyprinin from Oligocene of South China. Sci China Earth Sci 2011, 54:481-492.
• [36]Shi GL: Fossil plants from the Oligocene Ningming Formation of Guangxi, and a preliminary palaeoclimatic reconstruction of the flora. Nanjing, China: Ph.D. thesis. Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences; 2010:1-218.
• [37]Shi GL, Zhou ZY, Xie ZM: A new Cephalotaxus and associated epiphyllous fungi from the Oligocene of Guangxi, South China. Rev Palaeobot Palynol 2010, 161:179-195.
• [38]Shi GL, Zhou ZY, Xie ZM: Cupressus foliage shoots and associated seed cones from the Oligocene Ningming Formation of Guangxi, South China. Rev Palaeobot Palynol 2011, 166:325-334.
• [39]Shi GL, Zhou ZY, Xie ZM: A new Oligocene Calocedrus from South China and its implications for transpacific floristic exchanges. Amer J Bot 2012, 99:108-120.
• [40]eFloras.org. St. Louis: Missouri Botanical Garden & Cambridge: Harvard University Herbaria; Published on the Internet [http://www.efloras.org/ webcite] (accessed 9 May 2014).
• [41]Chinese Virtual Herbarium(CVH): A National Taxonomic Database. Beijing: Institute of Botany, Chinese Academy of Sciences; Published on the Internet [http://v5.cvh.org.cn/ webcite] (accessed 15 April 2014).
• [42]International Legume Database & Information Service (ILDIS. Cardiff: Cardiff School of Computer Science & Informatics; Published on the Internet [http://www.ildis.org/ webcite] (accessed 15 April 2014)
• [43]Hunt Institute for Botanical Documentation. Pittsburgh: Hunt Library Carnegie Mellon University; Published on the internet [http://huntbot.andrew.cmu.edu/HIBD/Departments/Databases.shtml webcite] (accessed 15 April 2014)
• [44]Johnson KR: Description of seven common fossil leaf species from the Hell Creek Formation (Upper Cretaceous: Upper Maastrichtian), North Dakota, South Dakota, and Montana. Proc Denver Mus Nat Hist, Ser 3 1996, 12:1-47.
• [45]Dilcher DL, Crane PR: Archaeanthus: An early angiosperm from the Cenomanian of the western Interior of North America. Ann Missouri Bot Gard 1984, 71:351-384.
• [46]Du Puy DJ, Labat JN, Rabevohitra R, Villiers JF, Bosser J, Moat J: The Leguminosae of Madagascar. Kew: The Royal Botanic Gardens; 2002:1-737.
• [47]Palmer E, Pitman N: Trees of southern Africa, vol. 2. Cape Town A. A: Balkema; 1972:705-1497.
• [48]Brenan JPM: Leguminosae subfamily Caesalpinioideae. In Flora of Tropical East Africa. Edited by Milne-Redhead E, Polhill RM. London: Crown Agents for Oversea Governments and Administrations; 1967:1-230.
• [49]Wieringa JJ: Monopetalanthus exit. A systematic study of Aphanocalyx, Bikinia, Icuria, Michelsonia and Tetraberlinia (Leguminosae, Caesalpinioideae). Wageningen Agric Univ Pap 1999, 99(4):1-320.
• [50]Berry EW: Fossil floras from southern Ecuador. Johns Hopkins Univ Stud Geol 1945, 14:93-150.
• [51]Lakhanpal RN, Awasthi N: A late Tertiary forule from near Bhikhnathoree in West Champaran District, Bihar. In Proceedings of the symposium on evolutionary botany and biostratigraphy. Current Trends in Life Sciences 10 (A. K. Ghosh Commemoration Volume). Edited by Sharma AK, Mitra GC, Banerjee M. New Delhi: Today and Tomorrow’s Printers & Publishers; 1984:587-596.
• [52]Mathur AK, Mishra VP, Mehra S: Systematic study of plant fossils from Dagshai, Kasauli and Dharmsala formations of Himachal Pradesh. Geol Surv India, Palaeontol Indica, N S 1996, 50:1-121.
• [53]Antal JS, Awasthi N: Fossil flora from the Himalayan foot-hills of Darjeeling District, West Bengal, India and its palaeoecological and phytogeographical significance. Palaeobotanist 1993, 42:14-60.
• [54]Bande MB, Srivastava GP: Late Cenozoic plant-impressions from Mahuadnar Valley, Palamu District, Bihar. Palaeobotanist 1990, 37:331-366.
• [55]Awasthi N, Prasad M: Siwalik plant fossils from Surai Khola area, western Nepal. Palaeobotanist 1990, 38:298-318.
• [56]Endo S, Fujiyama I: Some Late Mesozoic and Late Tertiary plants and a fossil insect from Thailand. In Contributions to the geology and palaeontology of Southeast Asia 31, geology and palaeontology of Southeast Asia, volume 2. Edited by Kobayashi T, Toriyama R. Tokyo: University of Tokyo Press; 1966:191-197.
• [57]Chaney RW: A Tertiary flora from Uganda. J Geol 1933, 41:702-709.
• [58]Ellis B, Daly DC, Hickey LJ, Johnson KR, Mitchell JD, Wilf P, Wing SL: Manual of leaf architecture. Ithaca & New York: Cornell University Press; 2009:1-190.
• [59]Owens SA, Fields PF, Ewers FW: Degradation of the upper pulvinus in modern and fossil leaves of Cercis (Fabaceae). Amer J Bot 1998, 85:273-284.
• [60]Walker JD, Geissman JW, Bowring SA, Babcock LE: The Geological Society of America Geologic Time Scale. Geol Soc Amer Bull 2013, 125:259-272.
• [61]Scotese CR: A continental drift flipbook. J Geol 2004, 112:729-741.
• [62]Brummitt RK, Powell CE: Authors of plant names. Kew: The Royal Botanic Gardens; 1992:1-732.
• [63]Botanico-Periodicum-Huntianum (BPH). Pittsburgh: Hunt Library Carnegie Mellon University; Published on the internet [http://fmhibd.library.cmu.edu/fmi/iwp/cgi?-db=BPH_Online&-loadframes webcite] (accessed 15 April 2014)
• [64]Index Herbariorum. Bronx: The New York Botanical Garden; Published on the internet [http://sweetgum.nybg.org/ih/ webcite] (accessed 15 April 2014)
• [65]Herendeen PS, Dilcher DL: Advances in legume systematics, part 4, the fossil record. Kew: The Royal Botanic Gardens; 1992:1-326.
• [66]Wang Q: Nomenclatural notes on Leguminosites and several taxonomically relevant names (fossil Leguminosae). Taxon 2012, 61:871-877.
• [67]Crepet WL, Herendeen PS: Papilionoid flowers from the Early Eocene of southeastern North America. Edited by Herendeen PS, Dilcher DL. In Advances in Legume Systematics: 4. The Fossil Record. Kew: The Royal Botanic Gardens; 1992:43-55.
• [68]Watari S: Anatomical studies on some leguminous leaves with special reference to the vascular system in petioles and rachises. J Fac Sci Imp Univ Tokyo, Sect 3 Bot 1934, 4:225-365.
• [69]Wang Q: Pulvini of Cercis leaves from the Miocene Shanwang Formation of Shandong Province and the early evolution of the pulvinus in Leguminosae. Acta Palaeontol Sin 2012, 51:1-13.
• [70]Herendeen PS, Crepet WL, Dilcher DL: The fossil history of the Leguminosae: phylogenetic and biogeographic implications. In Advances in legume systematics, part 4, the fossil record. Edited by Herendeen PS, Dilcher DL. Kew: The Royal Botanic Gardens; 1992:303-316.
• [71]Jia H, Manchester SR: Fossil leaves and fruits of Cercis (Leguminosae) from the Eocene of western North America. Int J Pl Sci 2014, 175. in press (DOI: 10.1086/675693)
• [72]MacGinitie HD: Fossil plants of the Florissant beds, Colorado. Publ Carnegie Inst Washington 1953, 599:1-198.
• [73]Newberry JS: Description of a species of Bauhinia from the Cretaceous clays of New Jersey. Bull Torrey Bot Club 1886, 13:77-78.
• [74]Newberry JS: The flora of the Amboy Clays. Monogr U S Geol Surv 1895, 26:1-260.
• [75]Berry EW: A new Cretaceous Bauhinia. Torreya 1908, 8:218-219.
• [76]Berry EW: A new Cretaceous Bauhinia from Alabama. Amer J Sci, Ser 4 1910, 29:256-258.
• [77]Berry EW: The flora of the Raritan Formation. Bull Geol Surv New Jersey 1911, 3:1-233.
• [78]Berry EW: Contributions to the Mesozoic flora of the Atlantic Coastal Plain, XI. Tennessee. Bull Torrey Bot Club 1916, 43:283-304.
• [79]Berry EW: Upper Cretaceous floras of the eastern gulf region in Tennesse, Mississippi, Alabama, and Georgia. U S Geol Surv Profess Pap 1919, 112:1-177.
• [80]Kryshtofovich AN: On the Cretaceous flora of Russian Sakhalin. J Coll Sci Imp Univ Tokyo 1918, 40:1-73.
• [81]Kryshtofovich AN: Cretaceous flora of Sakhalin, Mgach and Polovinka. In A. N. Kryshtofovich selected works, tom 2, 1962 (reprinted). Moscow & Leningrad: Izdatel’stvo Academii Nauk SSSR; 1937:211-289.
• [82]Brown RW: New items in Cretaceous and Tertiary floras of the western United States. J Washington Acad Sci 1956, 46:104-108.
• [83]Brown RW: Paleocene flora of the Rocky Mountains and Great Plains. U S Geol Surv Profess Pap 1962, 375:1-119.
• [84]Shilin PV: On the age of plant-bearing deposits of Taldysaj. Vestnik Akad Nauk Kazakh SSR 1970, 1:57-59.
• [85]Shilin PV: Late Cretaceous flora of the Beleuty River. Mater Istorii Fauny Fl Kazakhstana 1977, 7:126-139.
• [86]Shilin PV, Romanova EV: Senonskie flory Kazakhstana (=Senonian flora of Kazakhstan). Alma-Ata: Nauka; 1978:1-176.
• [87]Tao JR, Xiong XZ: The latest Cretaceous flora of Heilongjiang Province and the floristic relationship between East Asia and North America. Acta Phytotax Sin 1986, 24:1-15.
• [88]Tao JR, Zhou ZK, Liu YS: The evolution of the Late Cretaceous–Cenozoic floras in China. Beijing: Science Press; 2000:1-282.
• [89]Jacobs BF, Herendeen PS: Eocene dry climate and woodland vegetation in tropical Africa reconstructed from fossil leaves from northern Tanzania. Palaeogeogr Palaeoclimatol Palaeoecol 2004, 213:115-123.
• [90]Biagolini CH, Bernardes-de-Oliveira MEC, Caramês AG: Itaquaquecetuba Formation, São Paulo basin, Brazil: new angiosperm components of Paleogene taphoflora. Brazil J Geol 2013, 43:639-652.
• [91]Carpenter RJ, Goodwin MP, Hill RS, Kanold K: Silcrete plant fossils from Lightning Ridge, New South Wales: new evidence for climate change and monsoon elements in the Australian Cenozoic. Austral J Bot 2011, 59:399-425.
• [92]Calvillo-Canadell L, Cevallos-Ferriz SRS: Bauhcis moranii gen. et sp. nov. (Cercideae, Caesalpinioideae), an Oligocene plant from Tepexi de Rodríguez, Puebla, Mexico, with leaf architecture similar to Bauhinia and Cercis. Rev Palaeobot Palynol 2002, 122:171-184.
• [93]Wang Q, Shen S: Fossil fruits and leaves of Cercis (Leguminosae, Caesalpinioideae) from the Cenozoic of China and their biogeographic implications. Jap J Palynol 2012, 58(Spec Issue):252.
• [94]WGCPC [abbreviation for “Cenozoic plants from China” Writing Group of Institute of Botany and Nanjing Institute of Geology and Palaeontology, Academia Sinica]: Fossil Plants of China, 3 Cenozoic Plants from China. Beijing: Science Press; 1978:1-232.
• [95]Guo SX, Zhou ZK: The megafossil legumes from China. In Advances in legume systematics, part 4: the fossil record. Edited by Herendeen PS, Dilcher DL. Kew: The Royal Botanic Gardens; 1992:207-223.
• [96]Zhu H: Geographical elements of seed plants suggest the boundary of the tropical zone in China. Palaeogeogr Palaeoclimatol Palaeoecol 2013, 386:16-22.
• [97]Fritsch PW, Cruz BC: Phylogeny of Cercis based on DNA sequences of nuclear ITS and four plastid regions: Implications for transatlantic historical biogeography. Molec Phylogen Evol 2012, 60:816-825.