Bilobate leaves of Bauhinia (Leguminosae, Caesalpinioideae, Cercideae) from the middle Miocene of Fujian Province, southeastern China and their biogeographic implications
© Lin et al. 2015
Received: 11 August 2015
Accepted: 10 November 2015
Published: 16 November 2015
Morphological and molecular phylogenetic studies suggest that the pantropical genus Bauhinia L. s.l. (Bauhiniinae, Cercideae, Leguminosae) is paraphyletic and may as well be subdivided into nine genera, including Bauhinia L. s.s. and its allies. Their leaves are usually characteristic bilobate and are thus easily recognized in the fossil record. This provides the opportunity to understand the early evolution, diversification, and biogeographic history of orchid trees from an historical perspective under the framework of morphological and molecular studies.
The taxonomy, distribution, and leaf architecture of Bauhinia and its allies across the world are summarized in detail, which formed the basis for classifying the bilobate leaf fossils and evaluating the fossil record and biogeography of Bauhinia. Two species of Bauhinia are described from the middle Miocene Fotan Group of Fujian Province, southeastern China. Bauhinia ungulatoides sp. nov. is characterized by shallowly to moderately bilobate, pulvinate leaves with shallowly cordate bases and acute apices on each lobe, as well as paracytic stomatal complexes. Bauhinia fotana F.M.B. Jacques et al. emend. possesses moderately bilobate, pulvinate leaves with moderately to deeply cordate bases and acute or slightly obtuse apices on each lobe.
Bilobate leaf fossils Bauhinia ungulatoides and B. fotana together with other late Paleogene – early Neogene Chinese record of the genus suggest that Bauhinia had been diverse in South China by the late Paleogene. Their great similarities to some species from South America and South Asia respectively imply that Bauhinia might have undergone extensive dispersals and diversification during or before the Miocene. The fossil record, extant species diversity, as well as molecular phylogenetic analyses demonstrate that the Bauhiniinae might have originated in the Paleogene of low-latitudes along the eastern Tethys Seaway. They dispersed southwards into Africa, migrated from Eurasia to North America via the North Atlantic Land Bridge or floating islands during the Oligocene. Then the genus spread into South America probably via the Isthmus of Panama since the Miocene onward, and underwent regional extinctions in the Boreotropics of mid-high-latitudes during the Neogene climatic cooling. Hence, Bauhinia presently exhibits a pantropical intercontinental disjunct distribution.
Bauhinia L. s.s.
Barklya F. Muell.
Lasiobema (Korth.) Miq.
Lysiphyllum (Benth.) de Wit
Tylosema (Schweinf.) Torre et Hillc.
Bauhinia divaricata L.
Barklya syringifolia F. Muell.
Gigasiphon humblotianum (Baill.) Drake
Lasiobema scandens (L.) de Wit
Lysiphyllum cunninghamii (Benth.) de Wit
Phanera coccinea Lour.
Piliostigma reticulatum (DC.) Hochst.
Schnella macrostachya Raddi
Tylosema fassoglense (Schweinf.) Torre et Hillc.
Trees, shrubs (rarely semi-scandent), sometimes with intrastipular spines, rarely with thorns, without tendrils
Trees (unarmed, up to 18 m tall)
Mostly trees, occasionally large shrubs or climbers, without tendrils
Tendrilled lianas, scandent shrubs, without intrastipular spines or thorns
Trees, semi-scandent shrubs, tendrilled lianas, without intrastipular spines or thorns
Tendrilled lianas, scandent shrubs, rarely trees, without intrastipular spines or thorns
Trees, shrubs, without tendrils
Tendrilled lianas, scandent shrubs, without intrastipular spines or thorns
Trailing or climbing herbs, lianas, without intrastipular spines or thorns
Spathaceous, splitting along one side or into 2 unequal lobes
Shortly lobed in the upper part, campanulate with obtuse teeth
Lobed, forming a very long hypanthium
Lobed or truncate
Lobed or split, broadly campanulate, ribbed, rusty-velvety
Lobed, forming 4 or 5 approximately equal lobes
Lobed in the upper part, dentate
Lobed or truncate, five-veined or inconspicuously veined
Lobed, forming a short hypanthium
3, rarely 2
West and East Africa, Malesia
Australia, Southeast Asia
South and Southeast Asia
Africa, Asia, Australia
The leaf fossil record of Bauhinia previously reported and used in this study
Illustration and notes
Ca. 2.2 × 2.0 cm
Mahenge Site, Singida Town, Tanzania
B. cheniae Q. Wang et al.
Ca. 2.0–6.0 × 2.2–6.5 cm
Fig. 2CIII here
Ningming County, Guangxi Zhuang Autonomous Region, China
Possibly late Eocene or Oligocene
B. larsenii D.X. Zhang et Y.F. Chen
Ca. 2.1–4.5 × 1.8–4.8 cm
Fig. 2CV here
B. ningmingensis Q. Wang et al.
Ca. 4.0–5.3 × 4.0–5.2 cm
Fig. 2CIV here
Bauhcis moranii Calvillo-Canadell et Cevallos-Ferriz
4.3–4.5 × 5.8–6.4 cm
Fig. 2CX; attributed to Bauhinia by some authors
Los Ahuehuetes, Tepexi de Rodríguez, Puebla, Mexico
Bauhinia krishnanunnii A.K. Mathur et al.
6.0 × 5.0 cm
Fig. 2CIX here
Dagshai Cantonment and Daghota, Kalka-Shimla Highway, Solan District, Himachal Pradesh, India
B. kachchhensis R.N. Lakh. et Guleria
Ca. 6.2–8 cm wide, at least 3.5–5 cm long
Khari Nadi Bed, near Goyela-Mokra; Thingdawl, Mizoram; Kachchh, India
Bauhinia sp. 2
7.0 cm wide, at least 3.0 cm long
Mae Sot, Changwat Tak, Thailand
Late Early Miocene–early Middle Miocene
B. ungulatoides sp. nov.
7.5–9.5 × 5.4–6.0 cm
Lindai Village, Fotan Town, Zhangpu County, Zhangzhou City, Fujian Province, Southeast China
[37, this study]
B. fotana F.M.B. Jacques et al. emend.
Ca. 4.5–7.5 × 4.0–6.0 cm
Fig. 6 here
B. ramthiensis Antal et N. Awasthi
Ca. 9.0 × 8.6 cm
Right bank of upsteam of Ramthi River near Oodlabari, Darjeeling District, West Bengal, India
B. siwalika R.N. Lakh. et N. Awasthi
1.5–4.0 × 2.0–6.0 cm
Fig. 2CXIII here
Siwalik, Bhikhnathoree, West Champaran District, Bihar; Cherrapunji, West Khasi Hills District, Meghalaya, India
Middle Miocene–middle Pleistocene
B. ecuadorensis E.W. Berry
5.25 × 5.0 cm
Fig. 2CXI here
Loja Basin, Ecuador
B. wenshanensis H.H. Meng et Z.K. Zhou
Ca. 6.0–7.0 × 3.0–4.0 cm
Fig. 2CVI here
Dashidong Town, Wenshan County, Southeast Yunnan Province, China
B. nepalensis N. Awasthi et N. Prasad
4.5–7.5 × 5.6–11.4 cm
Fig. 2CVII here
Surai Khola beds, near Surai Khola bridge, Surai Khola, Nepal
Late Miocene–late Pleistocene
B. waylandii R.W. Chaney
2.5 × 2.5 cm
Fig. 2CXII here
Busano, Bugishu District, Eastern Province, Uganda
Bauhinia sp. 3
5.5 × 7.0 cm
Fig. 2CVIII here
Mahuadanr Valley, Palamu District, Bihar, India
In this article, we comprehensively investigate the leaf architecture of extant Bauhinia and its allies, describe two bilobate leafed fossil-species of Bauhinia from the middle Miocene Fotan Group of Fujian Province, southeastern China, and discuss their biogeographic implications.
The studied fossil leaves were examined and photographed using digital cameras (Panasonic DMC-FZ30 and Nikon D90). The cuticles were macerated using Schulze’s solution followed by diluted Ammonia (for a detailed procedure see ), and then mounted on slides, examined and photographed on a Zeiss AxioScope A1 microscope. Both the figured macrofossil specimens and cuticle slides (prefixed “PB”) are deposited at Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, P.R. China.
In addition, we examined the previously reported Bauhinia leaf fossils from the Oligocene Ningming Formation of Guangxi, South China [29, 30] and the Neogene of India and Nepal [38, 39, 42, 44]. The specimens are housed at Natural History Museum of Guangxi, Nanning (NHMG) and Birbal Sahni Institute of Palaeobotany, Lucknow (BSIP) (see Additional file 3).
The exsiccatae used in this study are from the following Herbaria: Harvard University, Cambridge (A), The Natural History Museum, London (BM), National Botanic Garden of Belgium, Meise (BR), Queensland Herbarium, Brisbane (BRI), Royal Botanic Garden Edinburgh, Edinburgh (E), Field Museum of Natural History, Chicago (F), Centro Studi Erbario Tropicale Università degli Studi di Firenze, Firenze (FT), Conservatoire et Jardin Botaniques de la Ville de Genève, Genève (G), Royal Botanic Gardens, Kew (K), National Herbarium Nederland, Leiden University Branch, Leiden (L), Botanische Staatssammlung München, München (M), Real Jardín Botánico, Madrid (MA), National Herbarium of Victoria, Melbourne (MEL), Missouri Botanical Garden, Missouri (MO), The New York Botanical Garden, Bronx (NY), Muséum National d’Histoire Naturelle, Paris (P), The Chinese National Herbarium, Beijing (PE), the Swedish Museum of Natural History, Stockholm (S), Trinity College, Dublin (TCD), Smithsonian Institution, Washington (US), and Wageningen University, Wageningen (WAG) (see Additional file 3).
(1) ILDIS (International Legume Database & Information Service) . The species and distribution of Bauhinia and its allies have been compiled by ILDIS, with special reference to some recently published taxonomic articles (Table 1; see Additional file 1). (2) eFloras.org . Morphological descriptions and illustrations of Bauhinia and its allies concerned here were checked. (3) Chinese Virtual Herbarium (CVH) . Online images of herbarium specimens of Bauhinia and its allies were browsed. (4) Index Herbarium . The standardized Herbarium codes were adopted. (5) The International Plant Names Index . The standardized abbreviations for authors of plant-names and journal titles in References were consulted and adopted in this paper.
The gross morphology, venation, and cuticle of modern and fossil leaves were described on the basis of the standard terminology [56, 57]. The morphological interpretation and terms specifically for leaves of the Cercideae follow the literature [24, 27, 30]. Time calibrations and geological terms referred to the latest International Chronostratigraphic Chart .
Leaf morphological analyses
Leaf morphological variables are measured and calculated using CorelDRAW 12.0 on the basis of leaf images (Fig. 2) from illustrated species, including the length-to-width/2 ratio, dissection index, and sinus (see Additional file 4). The dissection index (DI) is the ratio of an outline’s perimeter to the square root of its area [59–61], i.e., DI = Perimeter/[2sqrt (π × Area)], which is a standardized metric to determine shape complexity, especially regarding the complex degree of bilobate leaves studied here.
Leaf morphology of Bauhinia and its allies
Bauhinia L. s.s. outside America
Bauhinia L. s.s. in America
Bauhinia ungulatoides Y.X. Lin et al.
Bauhinia fotana F.M.B. Jacques et al.
Barklya F. Muell.
Lasiobema (Korth.) Miq.
Lysiphyllum (Benth.) de Wit
Tylosema (Schweinf.) Torre et Hillc.
Dissection index (Perimeter/[2sqrt (π × Area)])
Obtuse, acuminate or acute
Acuminate or acute, rarely obtuse
Acute or slightly obtuse
Acuminate, with a drip tip
Acuminate or acute, rarely obtuse
Obtuse or rounded
Obtuse, acuminate or acute
Acuminate or acute
Cuneate, truncate, or Slightly to deeply cordate
Cuneate, truncate or slightly cordate, rarely deeply cordate
Slightly or shallowly cordate
Moderately to deeply cordate
Slightly to deeply cordate or cuneate, rarely truncate
Slightly to deeply cordate
Slightly to deeply cordate, raely cuneate
Slightly to deeply cordate
Bilobate or bifoliolate, rarely unifoliolate
Bilobate or unifoliolate, rarely bifoliolate
Bilobate or unifoliolate
Bilobate, bifoliolate or unifoliolate
Bilobate, rarely bifoliolate
Chartaceous to coriaceous
Chartaceous to coriaceous
No or < 120°
No or < 80°
No or < 130°
No or < 75°
No or < 25°
Actinodromous or acrodromous
Actinodromous or acrodromous
Actinodromous or acrodromous
Actinodromous or acrodromous
Actinodromous or acrodromous
5–13 in number Not branched to frequently branched
5–9 Not branched or less branched, frequently branched rarely
7–9 Less branched
7 Frequently branched
5–9 Not branched to frequently branched
8–10 Frequently branched
5–13 Not branched to frequently branched
11 Frequently branched
7–11 Not branched to frequently branched
9 Frequently branched
Craspedodromous, eucamptodromous or brochidodromous
Craspedodromous, eucamptodromous, rarely brochidodromous
Brochidodromous or eucamptodromous
Craspedodromous or eucamptodromous
Brochidodromous craspedodromous, 1 or eucamptodromous
Craspedodromous, eucamptodromous or brochidodromous
Epidermal walls straight, wavy or sinuate; stomata paracytic, anomocytic, anisocytic or tetracytic; trichomes multicellular, uniseriate, unicellular or no; glands present or not
Epidermal walls straight or wavy; stomata anomocytic or paracytic, trichomes uniseriate or multiseriate, glandular; glands present or not
Epidermal walls straight or slightly curved; stomata paracytic; no trichome; no gland
Trichomes sometimes sparse, caducous; minute intrastipular trichomes
Subglabrous or almost glabrous, with minute trichomes on the veins
Epidermal walls straight; stomata tetracytic; no trichome
Epidermal walls wavy or sinuate; stomata tetracytic; no trichome
Epidermal walls wavy or sinuate; stomata anisocytic, tetracytic, anomocytic or paracytic; trichomes on both surfaces; no gland
Epidermal walls straight; stomata anomocytic or anisocytic; trichomes multicellular, unicellular, uniseriate and hooked; no gland
Epidermal walls undulate or sinuate; trichomes glandular, multicellular, uniseriate; no gland
Trichomes linear, canaliculate, with a ring and conical base or not; no gland
Family Leguminosae Juss.
Subfamily Caesalpinioideae DC.
Tribe Cercideae Bronn
Subtribe Bauhiniinae (Benth.) Walp.
Genus Bauhinia L. s.s.
Type Bauhinia divaricata L.
Two fossil-species of Bauhinia are described as follows. All the voucher specimens were collected from the same locality and stratigraphy and are deposited at the same institute.
Lindai Village, Zhangpu County, Zhangzhou City, Fujian Province, P. R. China (Fig. 3a).
Stratigraphic horizon and age
The middle part of the Fotan Group, Langhian Stage (middle Miocene) (Fig. 3b, c).
Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, P.R. China.
The specific epithet is derived from the Latin “ungulatus” (hoof-shaped) suffixed by “oides” (resembling), implying the striking similarities between leaves of studied fossils and extant Bauhinia ungulata L. (Fig. 2XXIII).
Lamina ovate-elliptical or elliptical in outline, shallowly to moderately bilobate, with pulvinate petiole and untoothed margin. Laminar base slightly or shallowly cordate, lobe apex acute. Primary venation basal actinodromous with 7–9 basal veins. Midvein terminated at the bottom of a narrow sinus. Lateral primaries straight or curved, and the innermost pairs reaching the lobe apex and outer pairs approaching to the laminar margin. Secondary veins craspedodromous. Intersecondary veins present. Tertiary veins opposite and alternate percurrent. Quaternary veins forming irregular polygons. Areolation well developed. Freely ending veinlets unbranched. Marginal ultimate veins absent; leaves hypostomatic. Epidermal cells on both surfaces, similarly quadrangular or pentagonal, with straight or slightly curved anticlinal walls. Stomatal complexes paracytic, randomly oriented.
The leaf attachment is petiolate. Petioles are partially preserved, at least 1.5 cm long, with a tiny, semicircular upper pulvinus impression connecting the laminar base (Fig. 4a-c). Laminae are bilobate, ovate-elliptical or elliptical in outline (Fig. 4a-e), ca. 7.5–9.5 cm long and 5.4–6.0 cm wide. The apex is bifid to ca. 1/3–2/5 of laminar length, with a reflex apex angle at ca. 20°–30° (Fig. 4a, b, d, e). Two lobes are symmetrical or slightly asymmetrical. Lobe apices are acute. Laminar bases are slightly or shallowly cordate (Fig. 4a-f). The margin is entire. The texture appears coriaceous. Primary venation is basal actinodromous with 7–9 basal veins. The midvein is straight, moderate in thickness, terminated at the bottom of the sinus. Lateral primaries are straight or curved, extremely ascending and rarely branched, and the innermost pairs reaching the lobe apex and outer pairs approaching to the laminar margin (Fig. 4a-f). Secondary veins are less prominent, craspedodromous, diverging at ca. 40°–80° from the innermost and outmost lateral primaries and approaching to the laminar margin (Fig. 4a, b, d, e). Intersecondary veins are approximately parallel to neighboring secondary veins, radiating out about 1/3–1/2 of distance from the primaries to laminar margin. Tertiary veins are opposite and alternate percurrent, slightly curved to sinuous, connecting the neighboring primary veins or between the primary veins and the secondary veins (or the margin). Quaternary veins are linked with other higher veins, forming irregular polygons (Fig. 4d, e). The areolation is well developed. Freely ending veinlets are unbranched. Marginal ultimate veins are absent.
Leaves are hypostomatic. The adaxial cuticle consists of isodiametric to slightly elongated epidermal cells. These cells are usually quadrangular or pentagonal, rarely hexagonal or heptagonal, with straight to slightly curved anticlinal walls and smooth periclinal walls (Fig. 5a). Epidermal cells in abaxial cuticles are similar in form and size to those in adaxial cuticles. Stomata are evenly distributed in the non-venous region of abaxial cuticles and randomly oriented (Fig. 5b). Stomatal complexes are paracytic, commonly asymmetrical, ovate, elliptical to oblong in outline. Subsidiary cells are crescent or irregularly shaped. Guard cells are not sunken (Fig. 5c, d). Trichomes or trichome bases are not observed.
The bilobate leaves described here are obviously different from five small genera, i.e., Lysiphyllum, Piliostigma, Tylosema, Barklya and Gigasiphon (Fig. 2I-VII; Table 3). Leaves of extant Tylosema, Barklya and Gigasiphon are unlobed or only very slightly bilobate; Lysiphyllum are bifoliolate. Piliostigma has bilobate leaves like our fossil leaves, but differs in having more basal veins (11) and bigger reflex apex angle (80°–90°). Following comparison with extant Bauhinia, Lasiobema, Phanera and Schnella (Fig. 2VIII-CII; Table 3), the present leaf fossils are attribute to Bauhinia in the light of character combinations such as very similar leaf architecture and dissection index. Leaves of Schnella have cordate, even auriculate bases (Fig. 2XCVII-C). In Phanera, leaves are usually broader than [lower in L/(W/2) ratio] than B. ungulatoides (Table 3; see Additional file 4), and the widest part is near the base (Fig. 2LXXXVII-XCIII). Bauhinia ungulatoides are similar to Phanera coccinea Lour. (Fig. 2LXXVIII), but are more shallowly bilobate. It can also be easily distinguished from the bilobate leaves of Lasiobema by reflex apex angles at ca. 20°–30°. The reflex apex angles of leaves in Lasiobema are either very wide (>40°) (Fig. 2LVIII, LX, LXIV-LXVII) or extremely narrow (<10°) sinus (Fig. 2LIX, LXI, LXXI, LXXII) (see Additional file 4). Bauhinia ungulatoides is characterized by shallowly cordate bases and acute apices on each lobe. It is more or less distinguishable from the bilobate leaves of Bauhinia’s allies in Bauhiniinae (Table 3). Although it is possible that these similarities are result of convergent evolution it is worth noting that Bauhinia ungulatoides is most similar to two South American species, i.e., B. ungulata (Fig. 2XXIII) and B. forficata Link [26, 63] (Fig. 2XXII), among the investigated extant species. They all bear extremely ascending and rarely branched lateral primary veins. However, since the reproductive organs of B. ungulatoides are unknown, it is more appropriate to assign it to a new fossil-species rather than to any extant species. Regarding fossil-species (Table 2), B. ungulatoides is similar to B. wenshanensis H.H. Meng et Z.K. Zhou from the late Miocene of Yunnan, southwestern China  (Fig. 2CVI), but the latter bears more secondary veins.
Bauhinia fotana F.M.B.Jacques, G.L.Shi et Z.K.Zhou emend. Y.X.Lin, W.O.Wong, G.L.Shi, S.Shen et Z.Y.Li (Fig. 6).
Paratype (first designated and illustrated by Jacques et al. ).
Other specimens examined here
The leaf attachment is petiolate. Petioles are partially preserved, at least ca. 1/2 of laminar length, with a tiny, semicircular upper pulvinus impression connecting the laminar base (Fig. 6a, b, e, f). Laminae are bilobate, broadly ovate to suborbicular in outline (Fig. 6a-f), ca. 4.5–7.5 cm long and 4.0–6.0 cm wide. The apex is bifid to ca. 1/3 of laminar length, with a reflex apex angle at ca. 30°–45° (Fig. 6b, d). Two lobes are symmetrical or slightly asymmetrical. Lobe apices are acute or slightly obtuse. Laminar bases are moderately to deeply cordate (Fig. 6a-f). The margin is entire. The texture appears chartaceous. Primary venation is basal actinodromous with 9–11 basal veins. The midvein is stout in thickness, terminated at the bottom of the sinus. The outmost pairs are weaker than the midvein and inner pairs. Lateral primaries are curved, branched or unbranched, and the innermost pairs reach the lobe apex and outer pairs approaching to the laminar margin (Fig. 6a-f). Secondary veins are eucamptodromous, diverging at ca. 45°–80° from the innermost and outmost lateral primary veins and approaching to the laminar margin (Fig. 6a-b). Tertiary veins are opposite and alternate percurrent, mostly sinuous and convex, rarely straight, connecting the neighboring primary veins or between the primary veins and the secondary veins (or the margin), as well as forming agrophic veins to the margin at the laminar base (Fig. 6a-b). Quaternary veins are linked with other higher veins, forming irregular polygons (Fig. 6b). The areolation is well developed. Freely ending veinlets are unbranched. Marginal ultimate veins are absent. Cuticles are unavailable.
Bauhinia fotana was originally described on the basis of two fossil leaves , but the initial description is very simple without characters of high order veins known. Here, we emended it based upon its types and newly collected specimens from the same locality. Its leaves are broader [smaller in L/(W/2) ratio] than Schnella (Fig. 2XCVIII-C) and most Phanera species (Fig. 2LXXVIII, LXXXVI-LXXXVIII) (Table 3, see Additional file 4). Bauhinia fotana is somewhat similar to Phanera ornata (Kurz) Thoth. (Fig. 2XC), but bears more deeply bilobate leaves with much less secondary veins. It is different from Lasiobema, which usually has an obvious caudate apex (Fig. 2LVIII, LXIV, LXV). Except for the size (4.5–7.5 × 4.0–6.0 cm), B. fotana shows great similarities with the extant B. acuminata L. (9–12 × 8–12.5 cm) (Fig. 2XIII) in bearing broadly ovate or suborbicular bilobate leaves with an acute apex, a moderately to deeply cordate base as well as similar venation. Among the fossil species (Table 2), B. fotana closely resembles Bauhinia sp. 3 (Fig. 2CVIII) from the Neogene of India , but the latter bears weak primary veins and larger L/(W/2) ratio of leaves.
The pantropical genus Bauhinia and its allies have similarly bilobate, bifoliolate, or unifoliolate leaves. They along with the northern temperate to subtropical genus Cercis L. constitute the tribe Cercideae as sister to the remaining legumes in the molecular phylogenetic trees [1–5, 10–13] (Fig. 1). Recently, strictly east-to-west vicariances for the biogeographic evolution of Cercis and Bauhinia have been suggested through molecular analyses [41, 71]. The earliest diverging clades in the Bauhiniinae were inferred to make their debut most possibly in Asia during the middle Paleocene (ca. 62.7 Ma) . The fossil record of Cercis and Bauhinia can provide key points of reference for deciphering the early evolution and biogeographic history of the Cercideae.
Bilobate fossil leaves that are attributed to or closely compared with Bauhinia are also reported from the late Eocene of Vietnam , the late Eocene-early Miocene of Brazil , and the latest Oligocene-mid-late Miocene of Australia . These records, however, have been either rejected or questioned due to lack of evidence for the pulvinus and/or basal actinodromous or acrodromous venation . Paleobotanical evidence indicates that Cercis  and Bauhinia  (Table 2) had first appeared in the Eocene to Oligocene of mid-low latitudes in the Northern Hemisphere. This may more or less support a tropical Tethys Seaway (Laurasian) origin [4, 5, 13] or an “Out of Tropical Asia” dispersal [25, 41] of the Cercideae and the Leguminosae as previously hypothesized. In contrast, the West Gondwana hypothesis or “Out of Africa” hypothesis for the origin of legumes [76–78] has been recently rejected by biome supertree and molecular analyses [4, 5]. In this article, bilobate leafed fossil-species, i.e., B. ungulatoides and B. fotana, from the middle Miocene of Fujian, southeastern China provide some new insights into the biogeography of Bauhinia and its allies.
Floristic exchanges between East Asia and South Asia
Major collision of India with Asia in the early Cenozoic enlarged the land-area linked to Eurasia, and subsequent connection with Australasia during the Neogene led to more connections between Eurasia and Oceania [79–82], which have greatly facilitated the floristic exchanges between East Asia, South Asia, Southeast Asia and Oceania. Recent paleobotanical studies have suggested that the Sino-Indian floristic affinities have begun to be established between the tropical flora of India and (sub) tropical floras of southwestern and southeastern China during the Miocene [37, 83–85]. Our present study on the Miocene Bauhinia further supports this viewpoint.
Bilobate leaves of Bauhinia from the Miocene of southeastern China show considerable similarities with the congeneric fossil-species [41, 44] from the Neogene of southwestern China and India, implying that the expansion of Bauhinia from (sub) tropical East Asia to tropical South Asia might have taken place since the Miocene with the northward drift and collision of southern landmasses into Eurasia, as well as the closure of the eastern Tethys Seaway . The fossils presented here further support the previous viewpoint  that the tropical zone  of South China may represent one of the centers for early diversification of Bauhinia. The bilobate and bifoliolate leaves from the Oligocene (or possibly late Eocene) Ningming Formation of Guangxi, South China  are the earliest, well-documented, reliable fossils of Bauhinia.
Floristic exchanges between Eurasia and Africa
Africa has been connected with Europe by the collision between the Afro-Arabian and Eurasian plates since the late Late Cretaceous , which facilitated floristic exchange such as the pantropical palms (Arecaceae Schultz Sch.) [78, 89]. Bauhinia and Bauhinia-like fossils previously reported from the early Paleocene to Miocene of Europe [90–95] have been either rejected or transferred to other groups . Instead, some other bilobate leaf fossils that had been described as Cassia L. and Mimosa L. from the Oligocene of Germany and France [96–100] (Fig. 2CXIV-CXVII) are far more likely to represent Bauhinia. Cassia rottensis Weyland, Mimosa weberi Schimp., M. deperdita Saporta, and M. ayamadi Marion closely resemble the extant Bauhinia in their basal actinodromous or acrodromous venations. Specifically, C. rottensis and M. weberi from Germany bear great similarities with the extant African species Bauhinia morondavensis Du Puy et R. Rabev. (Fig. 2XXVIII), B. natalensis Hook. (Fig. 2XXX), and B. kalantha Harms. (Fig. 2XXXI).
Under such circumstances, Bauhinia and Bauhinia-like bilobate leaf fossils from the Oligocene of Germany (Fig. 2CXIV, CXV) as well as from the middle Eocene of Tanzania  imply that the Bauhiniinae might have begun to exchange between Europe and Africa across the western Tethys Seaway. Bauhinia might have become depauperate and finally extinct in Europe after the Oligocene with the uplift of the Himalayan-Tibetan plateau , the desertification in the Asian interior , the establishment of the Asian monsoon system , and the desiccation of the Mediterranean Sea .
Migration from Eurasia to America via the North Atlantic Land Bridge
In America Bauhinia and Bauhinia-like bilobate leaves (Fig. 2CX, CXI) are only known from the Oligocene of Mexico  and the Miocene of Ecuador . The Bauhina leaf from late Eocene-early Miocene of Brazil is questionable since it lacks pulvinus and the primary venation is not distinctly basal actinodromous . Brazil that occupies highly diversified Bauhinia species today has been suggested as the center for origin of orchid trees . However, recent molecular phylogenetic study resolved Asian species as the basalmost lineage in the genus Bauhinia whereas the neotropical species diverged during the middle Miocene . The relatively extensive fossil record of Bauhinia from the late Paleogene – early Neogene of South China also supports that South China is one of the centers for early diversification of the genus.
Given that the Bauhiniinae originated in the Paleogene of low-latitudes along the eastern Tethys Seaway as we hypothesize here, it is most likely that Bauhinia and its allies migrated into North and Central America from Europe via the North Atlantic Land Bridge (NALB) [105–108]. During the early Paleogene, with the epicontinental seaways around North America and Eurasia receding, barriers between these two continents were reduced, allowing floristic exchanges of thermophilous plants to develop into a more uniform and continuous Boreotropical flora [78, 105, 106, 109]. The NALB lay at lower latitude in the Paleogene-early Neogene than the Bering Land Bridge (BLB), and it may have been more favorable for tropical, subtropical or even temperate plants to migrate [107–110]. So far, Bauhinia fossils are unknown in mid-high latitudes from East Asia and North America, supporting that the BLB, situated at higher latitudes, seems not to have witnessed the migration of Bauhinia. Hence, the NALB may have been the most feasible route for migration of Bauhinia from Eurasia to North America since the late Paleogene. An alternative migration route from Eurasia to North America for (sub) tropical lineages that have recently been suggested for Smilax Havanensis group  might also apply to the presumable trans-Atlantic dispersal of Bauhinia. These authors suggested trans-Atlantic crossings at lower latitudes via “floating islands” as has also been suggested for numerous angiosperm lineages  and for animals (e.g., platyrrhine monkeys) .
It is of great interest that bilobate leaves of Bauhinia presented here from the middle Miocene of southeastern China exhibit great similarities with some extant Bauhinia species (Fig. 2XXII, XXIII) from South America, implying extensive dispersals of Bauhinia populations from Eurasia to America in or by the Miocene, during which the Isthmus of Panama was formed, facilitating the Great American Biotic Interchange [114, 115]. This inference is also consistent with the result based on molecular phylogenetic study , which suggests that South American Bauhinia diverged during the middle Miocene.
Bilobate leaf fossils, i.e., B. ungulatoides and B. fotana presented here, from the middle Miocene of southeastern China are consistent with the viewpoint that the tropical zone of South China is one of the centres for early diversification of Bauhinia, and their great similarities to some species from South Asia and South America imply that Bauhinia might have undergone extensive dispersals and diversification during the Miocene.
The reliable fossil record, extant species diversity, as well as molecular phylogenetic analyses suggest that the Bauhiniinae might have originated in the Paleogene of low-latitudes along the eastern Tethys Seaway. They dispersed southwards into Africa, migrated from Eurasia to North America via the North Atlantic Land Bridge or floating islands in southern North Atlantic during the Oligocene. Then they spread into South America via the Isthmus of Panama since the Miocene onward, and underwent regional extinctions in the Boreotropics of mid-high-latitudes by the Neogene climatic cooling, so Bauhinia presently exhibits a pantropical intercontinental disjunct distribution.
We would like to thank Dr. Rashmi Srivastava, Birbal Sahni Institute of Palaeobotany, Lucknow, Mr. Yuan Daojun, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, and Dr. Chen Yunfa, Song Zhuqiu, Natural History Museum of Guangxi, Nanning for access to specimen collections. Dr. Susy Albert, The MS University of Baroda, Vadodara and Dr. Ruth P. Clark, Royal Botanic Gardens, Kew for helpful discussions. Academic Editor Toshihiro Yamada and two anonymous reviewers are thanked for their helpful comments. This work was supported by the National Natural Science Foundation of China (grant nos. 41372029 and 41206173) to WOW and GLS.
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