Leaves and fruits of Bauhinia (Leguminosae,
Caesalpinioideae, Cercideae) from the Oligocene
Ningming Formation of Guangxi, South China
and their biogeographic implications
Wang et al.
Wang et al. BMC Evolutionary Biology 2014, 14:88
R E S E A R C H A R T I C L E Open Access
Leaves and fruits of Bauhinia (Leguminosae,
Caesalpinioideae, Cercideae) from the Oligocene
Ningming Formation of Guangxi, South China
and their biogeographic implications
, Zhuqiu Song
, Yunfa Chen
, Si Shen
and Zhenyu Li
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,
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.
Keywords: Bauhinia, Bifoliolate leaf, Bilobate leaf, Biogeography, Cercideae, Cercis, Eocene, Evolution, Fruits, Legumes,
Leguminosae, Low latitude, Ningming Formation, Oligocene, Pulvinus, Tethys Seaway origin, Unifoliolate leaf
* Correspondence: firstname.lastname@example.org;email@example.com;firstname.lastname@example.org
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
© 2014 Wang et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain
Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article,
unless otherwise stated.
Wang et al. BMC Evolutionary Biology 2014, 14:88
Bauhinia L. (Leguminosae Juss., Caesalpinioideae DC.)
is a pantropical legume genus with ca.150—300 species,
the number of which depends on the demarcation of
of Bauhinia is especially complicated, and it has been
recognized either as a large genus [1-3,5,7-9], or as 8-9
distinct genera [4,6,10] (Figure 1). Although a taxonomical
consensus has not been achieved, recent studies on pollen
morphology and molecular systematics of Bauhinia have
suggested that Bauhinia sensu lato is not monophyletic
and should be subdivided into Bauhinia sensu stricto and
other independent genera [6,10-13] (Figure 1). Bauhinia is
well known for its ornamental shrubs and trees, such as B.
blakeana Dunn being first chosen as the city flower of
Hong Kong, China in 1965. In addition, seeds of B.
petersiana Bolle are used as a coffee substitute ; some
species, e.g., B. championii (Benth.) Benth., B. purpurea L.,
B. tomentosa L., have local pharmacological uses [14-16].
Bauhinia was named after two Swiss botanists, the
brothers Jean Bauhin (1541–1613) and Gaspard Bauhin
(1560–1624), suggesting a brotherly relationship in its
commonly bilobate leaves . Bauhinia, along with a
northern temperate genus Cercis L. and several tropical
genera, bear bilobate, bifoliolate, or sometimes unifoliolate
leaves, which constitute the tribe Cercideae Bronn as sister
to the remaining legumes in the molecular phylogenetic
trees [17-24]. Bilobate, bifoliolate, or unifoliolate pulvinate
leaves with basal actinodromous or acrodromous venations
are characteristic for Cercideae [25-27], whereas leaves of
other legumes are usually pinnately compound, occasion-
ally trifoliolate or palmate (Figure 1). Hence, well-preserved
bilobate, bifoliolate, or unifoliolate pulvinate leaves are
easily recognizable in the fossil record and can provide an
instrumental evidence for understanding the early evolu-
tion and biogeographic history of the Cercideae and the
The goals of this paper are to (1) investigate and evaluate
the fossil record of Bauhinia, with special reference to
that of Cercis, by comparing both extinct and extant
angiosperms with the similar lobed leaf forms, (2) describe
the foliage and fruit fossils from the Oligocene Ningming
Formation of Guangxi, South China, and discuss their
The fossil foliage and fruits studied in this paper were
collected from the Ningming Formation at 22°07.690’N,
107°02.434’E in the western region of Ningming County,
Guangxi Zhuang Autonomous Region, South China
(Figure 2). The Ningming Formation is primarily shallow
lacustrine deposits consisting of gray to dark gray mud-
stone, light yellow shaly siltstone, and finely grained sand-
stone. No volcanic rocks and mammals are hitherto found
in the Ningming Formation , and an absolute age for
this formation is therefore unavailable. The Ningming Basin
is among the late Palaeogene basins (e.g., mammal-bearing
Figure 1 A simplified phylogenetic tree of the Leguminosae,with special reference to the phylogeny of the tribe Cercideae (after
[10,17]) and iconic leaf forms enhanced. The purple taxa belong to Bauhinia sensu lato.
Wang et al. BMC Evolutionary Biology 2014, 14:88 Page 2 of 16
Na Duong and Bose basins) [29,30] in southern Guangxi
and northern Vietnam that experienced a generally similar
geological history, so it is inferred that the Ningming For-
mation is likely to be late Eocene—Oligocene in age. The
previous studies on plant macrofossils (e.g., Palaeocarya
ningmingensis H.M. Li et Y.F. Chen, P. guangxiensis H.M.
Li et Y.F. Chen, Bauhinia larsenii D.X. Zhang et Y.F. Chen,
Cephalotaxus ningmingensis G.L. Shi et al., Cupressus
guangxiensis G.L. Shi et al., and Calocedrus huashanensis
G.L. Shi et al.), sporo-pollen assemblages (e.g., Quercoidites
microhenrici (Potonié) Potonié), and fishes (e.g., Ecocarpia
ningmingensis G.J. Chen et al., Huashancyprinus robustispi-
nus G.J. Chen et M.M. Chang) from the same locality indi-
cate the Ningming Formation most possibly an Oligocene
age [31-39], which is adopted in this paper.
In China, all the land belongs to our country. Our
fossil-collecting fieldwork was done in non-National
Nature Reserves (NNR) and non-private areas and has
been allowed by the local government. We did not violate
the Chinese fossil collection and mining laws and manage-
The macrofossils are preserved as compressions/im-
pressions only with a little organic material remaining in
mudstone. Cuticle preparations were unsuccessful because
organic material has been greatly weathered. All the mar-
cofossil specimens used herein are deposited at Natural
History Museum of Guangxi (NHMG), Nanning, P.R.
China (see Additional file 2).
The exsiccatae examined in this study are kept at the
following herbaria: Chengdu Institute of Biology, Chinese
Academy of Sciences, Chengdu (CDBI), Guangxi Institute
of Botany, Chinese Academy of Sciences, Guilin (IBK),
South China Botanical Garden, Chinese Academy of
Sciences, Guangzhou (IBSC), the Herbarium of Northeast
China, Shenyang (IFP), Kunming Institute of Botany,
Chinese Academy of Sciences, Kunming (KUN), and the
Chinese National Herbarium, Beijing (PE) (see Additional
(1) eFloras.org . Bauhinia and other living taxa con-
cerned here were consulted (Figure 3; see Additional file 3).
(2) Chinese Virtual Herbarium (CVH) . The images
of herbarium specimens were browsed. (3) ILDIS (Inter-
national Legume Database & Information Service) .
The geographic distribution of living species in Bauhinia
is compiled by ILDIS, with a few newly published records
(Figure 4; see Additional file 1). (4) Hunt Institute for Bo-
tanical Documentation . Standardized abbreviations of
plant-family names and periodical titles in this paper were
consulted and applied (see References; Additional file 3).
Terms used in the specimen descriptions for leaves and
fruits follow Ellis et al. . As for the foliage of the
Cercideae, the lower pulvinus has been interpreted as a
primary pulvinus at the base of the leaf while the upper
pulvinus as a secondary pulvinus homologous with the
pulvinus on the leaflet petiolule, consisting of an apical
common joint with two distal laminar joints, one for
each half of the lamina [25,27,59]. Anatomically, laminar
joints are resulted from the tertiary pulvini at the base of
Figure 2 Fossil locality showing Ningming of Guangxi, South China (after ).
Wang et al. BMC Evolutionary Biology 2014, 14:88 Page 3 of 16
each primary vein . Van der Pijl  classified the
leaves of Bauhinia into three basic types: unifoliolate,
bilobate, and bifoliolate. Cusset  subdivided the leaves
of the tribe Bauhinieae Benth. into seven types, but
unifoliolate, bilobate, and bifoliolate types epitomize in
the foliage of living and fossil species of Bauhinia.
Figure 3 Similar leaf forms in Bauhinia and other angiospermous taxa. (a) Ipomoea pes-caprae (L.) R. Br. Specimen: PE12054. (b) Hoya kerrii
Craib. Specimen: IBSC199290. (c) Oxalis corymbosa DC. Specimen: PE1688774. (d) Liriodendrites bradacii K.R. Johnson . (e) Liriophyllum kansense
Dilcher et P.R. Crane . (f) Passiflora cupiformis Masters. Specimen: KUN0368045. (g) Zygophyllum fabago L. . (h) Brenierea insignis Humbert
. (i) Hymenaea courbaril L. . (j) Guibourtia coleosperma (Benth.) J. Léonard . (k) Aphanocalyx richardsiae (J. Léonard) Wieringa [48,49]. (l)
Bauhinia didyma L. . (m) Bauhinia variegata L. Cultivated at NHMG, Nanning and photographed by Qi Wang on October 17
2013, also see
the Cover Image of this paper. (n) Cercis chinensis Bunge. Cultivated at the Institute of Botany, Beijing. Scale bars = 2 cm.
Wang et al. BMC Evolutionary Biology 2014, 14:88 Page 4 of 16
Hence, unifoliolate, bilobate, and bifoliolate leaves are
adopted herein for the description of Bauhinia foliage.
Time calibrations refer to the latest Geologic Time Scale
. The global palaeogeographic maps for the Late
Cretaceous, Palaeocene, Eocene, and Oligocene were
Both fossil and extant taxa bearing similar unifolioate,
bilobate, and bifoliolate leaves in Leguminosae and other
families (Figure 3; see Additional file 3) were compared
to evaluate the fossil record and biogeographic history of
Bauhinia. Based upon an extensive review on the litera-
ture and specimens of previously reported Bauhinia and
other similar foliage from the Cretaceous and Cenozoic,
we summarized the reliable fossil record of Bauhinia
(see Additional file 4).
Photographs of specimens were taken with digital cam-
eras (Panasonic DMC-FZ30 and Nikon D90). A simplified
phylogenetic tree (Figure 1) of the Cercideae within Legu-
minosae was partially adapted from the literature [10,17],
with the iconic leaf forms enhanced. A map for the
fossil locality (Figure 2) was partially adapted from the
literature . Line drawings of leaf specimens for
fossil and living taxa as well as of distributional map of
Bauhinia were drawn (Figures 3,4,5,6,7 and 8) and ar-
ranged using CorelDRAW 10.0 (Corel, Ottawa, Ontario,
Canada) and Adobe Photoshop 6.0 (San Jose, California,
plants, the author citation of plant names in this paper and
journal titles in References follow Brummitt and Powell
 as well as Botanico-Periodicum-Huntianum (BPH),
its supplement (BPH/S), and BPH-2 , respectively.
The herbarium codes refer to Index Herbariorum .
Similar leaf architectural comparisons
A leaf lamina partially or fully divided into two lobes is
not very common but remarkable among angiosperms.
Such leaf forms can be traced back to the Late Cretaceous,
for example extinct Liriodendron-like angiosperms Lirio-
dendrites bradacii K.R. Johnson  and Liriophyllum
kansense Dilcher et P.R. Crane  (Figure 3d,e), but
some of them have been erroneously identified as Bau-
hinia fossils (see Additional file 4). Overall, both extinct
and extant taxa bearing bilobate and bifoliolate foliage
occur in Leguminosae, Apocynaceae Juss., Convolvulaceae
Juss., Liriodendraceae sensu M.S. Romanov et Dilcher,
Oxalidaceae Bercht. et J. Presl, Passifloraceae Juss.
ex Roussel, Proteaceae Juss., and Zygophyllaceae R. Br.. In
order to determine the reliable fossils of Bauhinia,com-
parisons are made among both extinct and extant taxa
with similar lobed leaf forms (Figure 3; see Additional
The taxonomy of Bauhinia L.
The systematics of living Bauhinia L. is primarily based
upon growth habit, inflorescence, flower, calyx, hypan-
thium, petal, fertile stamen number, stamen filament,
Figure 4 Distributions of modern and fossil Bauhinia L. (The base map drawn by Mr. Sun Yingbao, Institute of Botany, CAS, Beijing). Green
dots indicate modern distributions . Red symbols show fossils from the Oligocene–Miocene of China , this paper, Ecuador , India
[51-54], Nepal , Thailand , and Uganda .
Wang et al. BMC Evolutionary Biology 2014, 14:88 Page 5 of 16
gynophore, stigma, pollen, fruit, seed, and leaf morphology
[1-8,12,13], as well as molecular data [9,11]. Species of
Bauhinia sensu stricto are usually trees or shrubs, rarely
semi-scandent plants, whereas those of Lysiphyll um (Benth.)
De Wit, Schnella Raddi, Tyl osem a (Schweinf.) Torre et
Hillc., and Phanera Lour. (all belonging to Bauhinia sensu
lato) are lianas, herbaceous vines or rarely shrubs. Differ-
ent character combinations in reproductive and vegetative
organs have been used to classify Bauhinia sensu lato into
Bauhinia sensu stricto and other 7-8 genera, with refer-
ence to the molecular phylogenetics of Cercideae [4,6,10]
(Figure 1). Bauhinia sensu stricto as one of the first
Figure 5 Bauhinia ningmingensis sp. nov. from the Oligocene of Ningming, Guangxi, South China. (a) NHMG 011655. The foliage apex is
not preserved. (b-c) Holotype: NHMG 011654, and its line-drawing, showing the leaf architectural detail. (d) The apex of holotype, showing the
higher-order veins. (e) The base of holotype, showing the pulvinate tissue. Scale bars = 1 cm.
Wang et al. BMC Evolutionary Biology 2014, 14:88 Page 6 of 16
Figure 6 Bauhinia cheniae sp. nov. from the Oligocene of Ningming, Guangxi, South China. (a-b) Holotype: NHMG 011656a, b. Red arrow
indicates the position of the sinus. (c) Line-drawing of holotype, showing the leaf architectural detail. (d) NHMG 011657. Red arrow indicates the
position of the sinus. Green arrow shows a folded leaf base. (e) Enlargement of the petiole in d, showing thickened upper and lower pulvini as
well as dense, spreading hairs. (f) NHMG 011658. Red arrow indicates the position of the sinus. Green arrows indicate partially overlapped primary
veins, implying this leaf is folded. (g) NHMG 011659, with the higher-order veins. Red arrow indicates a short spine in the sinus. Green arrow
shows a semicircular laminar joint at the leaf base. Scale bars = 1 cm.
Wang et al. BMC Evolutionary Biology 2014, 14:88 Page 7 of 16
branching lineages is the only pantropical genus in the
subtribe Bauhiniinae (Benth.) Walp. of Cercideae, so it
may boast an earlier origin and evolutionary history
than other relatives within the Bauhiniinae.
Morphological characters are the features that ultimately
support the distinctiveness of real biological entities, so
integral studies mutually illuminating between morphology
and molecular systematics will be key in the discrimination
of elusive relationships within Bauhinia sensu lato. How-
ever, considerable convergence, parallelism or evolutionary
conservativeness in the organs (especially leaves) of
Bauhinia sensu stricto and its relatives often place
palaeobotanists in a predicament. Without reproductive
organs (especially the calyces, fertile stamens, and petals),
bilobate leaves of some species in Bauhinia sensu stricto,
Phanera,andSchnella would not be distinguished from
each other even by neobotanists. Hence, bilobate or
bifoliolate leaf fossils in Cercideae were often assigned
to Bauhinia sensu lato (see Additional file 4).
The fossil record of Bauhinia and other bilobate leafed taxa
Overall, Bauhinia bears mostly bilobate, bifoliolate, or
sometimes unifoliolate leaves having characteristic upper
and lower pulvini, basal actinodromous or acrodromous
primary veins (3-13 in number per leaf), brochidodromous,
eucamptodromous or craspedodromous secondary veins,
and alternate or opposite percurrent tertiary veins, charac-
ter combinations of which are noticeably different from
the lobed foliage of genera in the tribe Detarieae sensu
lato Polhill of Leguminosae, as well as in Apocynaceae,
Convolvulaceae, Liriodendraceae, Oxalidaceae, Passiflora-
ceae, Proteaceae Juss., and Zygophyllaceae (see Figure 3;
Figure 7 Additional leaves of Bauhinia cheniae sp. nov. from Ningming. (a-b) NHMG 011670, and its line-drawing, showing the leaf architectural
detail. (c) NHMG 011671. Red arrow indicates a long spine in the sinus of folded leaf. (d-e) NHMG 011672, 011673, showing two deeply bilobate leaves.
Green arrow shows a semicircular laminar joint at the leaf base. Scale bars = 1 cm.
Wang et al. BMC Evolutionary Biology 2014, 14:88 Page 8 of 16
Figure 8 (See legend on next page.)
Wang et al. BMC Evolutionary Biology 2014, 14:88 Page 9 of 16
Additional file 3). The simple, unlobed leaves of Bauhinia
also differ from those of Cercis in the tribe Cercideae in
the former usually bearing fewer and weaker secondary
veins along the distal third of the midvein and a mucro or
spine at the leaf tip . Based upon an extensive review
on the previously reported Bauhinia and other similar
foliage from the Cretaceous and Cenozoic, those pre-
Oligocene reports regarding Bauhinia across the world are
either questionable or have been rejected (see Additional
file 4). Besides the reliable fossils from Ningming of China,
foliage and/or wood of Bauhinia have been described from
the Miocene-Pliocene of Thailand, India, Nepal, Uganda,
Key to the fossil species of Bauhinia from Ningming
1. Lateral primary veins approach to the margin; secondary
cheniae sp. nov.
1. Lateral primary veins do not approach to the margin;
secondary veins brochidodromous–———2
2. Bilobate, bifid to ca. 1/2 to 3/5 of laminar
length–—————————Bauhinia larsenii D.X. Zhang
et Y.F. Chen emend.
2. Bifoliolate, bifid to laminar base–Bauhinia ningmin-
gensis sp. nov.
Family Leguminosae Juss.
Subfamily Caesalpinioideae DC.
Tribe Cercideae Bronn
Subtribe Bauhiniinae (Benth.) Walp.
Genus Bauhinia L.
Type Bauhinia divaricata L.
Three fossil species of Bauhinia are described as follows.
All the voucher specimens were collected from the same
locality and stratigraphy, and they are deposited at the
Ningming County, Guangxi Zhuang Autonomous Region,
South China (Figure 2).
Stratigraphic horizon and age
Ningming Formation, Oligocene.
Natural History Museum of Guangxi (NHMG), Nanning,
Bauhinia ningmingensis QiWang,Z.Q.Song,Y.F.
The specific epithet is derived from Ningming County,
where the fossils were collected.
NHMG 011654 (Figure 5b-e) (designated here).
NHMG 011655 (Figure 5a) (designated here).
Small, bifoliolate leaves. Leaflets pulvinate and laminae
strongly asymmetrical, obliquely ovate or slightly falcate.
Leaflet apexes obtuse. Bases wide cuneate or slightly
concave. Margin entire. Primary veins basal acrodro-
mous (3-4 in number) and curved on the exmedial
side, not reaching the leaflet margin. Secondary veins
brochidodromous. Tertiary veins percurrent or ramified,
straight, convex or sinuous. Quaternary veins forming ir-
regular polygons. Aerolation well developed. Freely ending
veinlets mostly branching once. Marginal ultimate veins
looped and fimbriate.
Bifoliolate leaves inferred from the symmetry of individual
leaflets. Leaflet laminae strongly asymmetrical, obliquely
ovate or slightly falcate (Figure 5a-c), ca. 4.0-5.3 cm long
and 2.0-2.6 cm wide, with partially preserved pulvinate tis-
sue, ca. 2.5 mm long, showing some horizontal striations
(Figure 5c,e). The petiole not preserved. Texture appar-
ently membranous to chartaceous. Leaflet apexes obtuse
(Figure 5b,d). Bases wide cuneate or slightly concave
(Figure 5a-c,e). Margin entire. Primary veins basal acro-
dromous, 3-4 in number. Innermost primary veins
straight or curved, extremely approaching to the leaflet
veins on the exmedial side curved, connecting with second-
ary veins to form a series of arches and loops, not reaching
the leaflet margin (Figure 5a-c). Outermost primary veins
shorter and weaker. Secondary veins brochidodromous,
(See figure on previous page.)
Figure 8 Bauhinia larsenii D.X. Zhang et Y.F. Chen emend. from the Oligocene of Ningming,Guangxi,South China.(a-b) Holotype:
NHMG 45003. (b) Partial enlargement of holotype. White arrows show an organic connection of the leafy shoot and fruit. (c-d) NHMG 45004 and
its line-drawing, showing the leaf architectural detail. (e) NHMG 45019, showing a detached fruit. Red arrow refers to a thin, long stipe. (f) NHMG
45012. Red arrow indicates a short spine in the sinus of folded leaf. (g) NHMG 011676. Yellow arrow refers to a thickened upper pulvinus. (h)
NHMG 011678. Red arrow indicates the position of the sinus of folded leaf. (i) NHMG 011677. Green arrows indicate partially overlapped primary
veins, implying this leaf is folded. Scale bars = 1 cm.
Wang et al. BMC Evolutionary Biology 2014, 14:88 Page 10 of 16
diverging at ca. 60°-90° from the primary veins on the
exmedial side. Tertiary veins alternate and opposite percur-
rent or ramified, straight, convex or sinuous (Figure 5a-c).
Quaternary veins forming irregular polygons. Aerolation
well developed. Freely ending veinlets mostly branch-
ing once. Marginal ultimate veins looped and fimbriate
This fossil new species B. ningmingensis is very similar
to living B. madagascariensis subsp. meridionalis Du
PuyetR.Rabev.andB. didyma L. Chen [3,5,41]
(Figure 3l; see Additional file 3), which are distributed
in southeastern Madagascar and southern China,
Myanmar, northern Thailand, respectively. However, it
noticeably bears much larger leaflets (ca. 4.0-5.3×2.0-
2.6 cm) than those of the two living species (ca. 0.7-3 ×
04-1.7 cm and 1.2-2.4 × 0.9-1.6 cm). In addition, B.
ningmingensis sp. nov. is different from the previously
reported bifoliolate fossil species B. ecuadorensis E.W.
Berry  and B. siwalika U. Lakh. et N. Awasthi 
from the Miocene of India and Ecuador in the leaf
architectural detail (see Additional files 3 and 4).
Bauhinia cheniae Qi Wang, Z. Q. Song, Y. F. Chen, S.
Shen et Z. Y. Li, sp. nov. (Figures 6a-g, 7a-e).
The specific epithet is dedicated to Prof. Chen Dezhao
(Chen Te-chao) (South China Botanical Garden, CAS) for
her important contribution to the taxonomy of Cercideae.
NHMG 011656a, b (Figure 6a-c) (designated here; part
and counterpart specimens).
NHMG 011657, 011658, 011659 (Figure 6d-g), 011670
(Figure 7a,b), 011671, 011672, 011673 (Figure 7c-e),
011674, 011675, 011660, 011661, 011662, 011663,
011664, 011665, 011666, 011667, 011668, and 011669
Small, broadly ovate or suborbicular, moderately or deeply
bilobate leaves. Petioles glabrescent or hairy, bearing
thicken upper and lower pulvini. Lobe apexes slightly
acuminate, obtuse or rounded. Laminar bases shallowly
to deeply cordate. Margin entire. Primary veins basal
actinodromous, 7-9 in number. The midvein terminated
in a short or long spine within a narrow or flaring sinus.
Lateral primary veins straight or curved, branched or
unbranched, approaching to the margin. Secondary veins
eucamptodromous. Intersecondary veins present. Tertiary
veins percurrent or ramified, mostly convex, sinuous or
rarely straight. Quaternary veins percurrent, forming
irregular polygons. Aerolation well developed. Freely
ending veinlets mostly unbranched. Marginal ultimate
Bilobate leaves, wide ovate or suborbicular, ca. 2.0-6.0 cm
long and 2.2-6.5 cm wide, often folded along the midvein
(Figures 6a-c, 7a-e). The petiole glabrescent or covered
with dense, spreading hairs (Figure 6d,e).The petiole stout,
ca. 1.6-2.0 cm long, bearing thickened, upper and lower
pulvini (Figures 6d,e 7c). The upper pulvinus connecting
the laminar base via a tiny, semicircular laminar joint. Bifid
to ca. 2/3-4/5 of laminar length or almost to the laminar
base, forming a narrow or flaring sinus. Two lobes symmet-
rical or slightly asymmetrical. Lobe apex slightly acuminate,
obtuse or rounded (Figures 6a-d,f and 7a-e). Laminar base
symmetrical, shallowly to deeply cordate (Figures 6a-d,f,g,
7a-e). Margin entire. Texture apparently chartaceous. Pri-
mary veins basal actinodromous, 7-9 in number, the out-
most pair and midvein being weaker than the inner pairs.
Midvein terminated in a short or long spine within the
sinus (Figures 6g, 7c). Lateral primary veins straight or
curved, branched or unbranched, and the innermost pair
reaching the lobe apex and outer pairs approaching to the
margin. Secondary veins eucamptodromous, diverging at
ca. 30°-80° mainly from the innermost and outmost lateral
primary veins and arching upward along the margin
(Figures 6a-c,f,g, 7a,b). A pair of secondary veins usually
emitting from the midvein near the sinus and approaching
to the inner margin of lobes (Figure 6b-d, f). Intersecond-
ary veins sometimes present, parallel to subjacent second-
ary veins. Tertiary veins alternate and opposite
percurrent or ramified, mostly convex, sinuous or rarely
straight. Quaternary veins alternate and opposite percur-
rent, forming irregular polygons (Figures 6b,c,g, 7a,b).
Aerolation well developed. Freely ending veinlets mostly
unbranched. Marginal ultimate veins absent.
This fossil new species B. cheniae is very similar to living
B. variegata L. (Figure 3m) and B. purpurea L. [3,5,41]
in having deeply bilobate leaves and eucamptodromous
secondary veins, but it differs from the extant species in
having the fewer primary veins and a densely hairy peti-
ole (see Additional file 3). In these respects, B. cheniae
sp. nov. is also different from the previously reported,
bilobate leafed fossil species B. larsenii D.X. Zhang et Y.
F. Chen , B. krishnanunnii A.K. Mathur et al. , B.
ramthiensis Antal et N. Awasthi , B. nepalensis N.
Awasthi et N. Prasad , Bauhinia sp. 1 , Bauhinia
sp. 2 , and B. waylandii R.W. Chaney  from the
Miocene–Pliocene of India, Nepal, Thailand, and
Uganda (see Additional files 3 and 4).
Wang et al. BMC Evolutionary Biology 2014, 14:88 Page 11 of 16
Bauhinia larsenii D.X.ZhangetY.F.Chenemend.
Bauhinia larsenii D.X. Zhang et Y. F. Chen, see Chen
and Zhang in Bot. J. Linn. Soc. 147: 439, Figures 1, 2, 3,
5 and 6, 2005.
NHMG 45003 (Figure 8a,b herein) (first designated and
illustrated by Chen and Zhang : Figure 1]).
NHMG 45004 (counterpart specimen of holotype; first
figured herein, Figure 8c,d), 45012 and 45019 (first desig-
nated and illustrated by Chen and Zhang : Figures 2
and 6; Figure 8f,e herein).
Other specimens examined herein
NHMG 011676, 011678, 011677 (Figure 8g-i), and
Leaves suborbicular or slightly ovate to wide ovate, ca.
2.1-4.5 cm long and 1.8-4.8 cm wide, usually folded
along the midvein (Figure 8a-d, f-i). Bifid to ca.1/2-3/5
of laminar length, forming a narrow sinus. Two lobes
symmetrical or slightly asymmetrical. Lobe apex rounded
to obtuse (Figure 8a,c,d,f ). Laminar base symmetrical,
rounded or shallowly cordate (Figure 8a,c,d,g). Margin
entire. Texture apparently chartaceous to coriaceous.
Primary veins basal actinodromous, 5-9 in number, the
outmost pair being weaker than the midvein and inner
sinus. Lateral primary veins branched or unbranched, and
the innermost pair reaching the lobe apex. Major second-
ary veins brochidodromous, diverging at ca. 45°—60° from
the lateral primary veins mainly on the exmedial side and
sporadically on the admedial side (Figure 8d). A pair of
minor secondary veins emitting from the midvein near
the sinus and approaching to the inner margin of lobes
(Figure 8d). Secondary veins fused with each other or the
branches of primary veins to form loops near the leaf
margin, or arcs between the primary veins. Tertiary veins
alternate and opposite percurrent or ramified, convex or
sinuous. Quaternary veins alternate percurrent. Marginal
ultimate veins looped and fimbriate (Figure 8d). Other
higher-order veins invisible. The petiole, ca. 1.0-2.2 cm
long, with an upper pulvinus and a lower pulvinus
(Figure 8a,c,d,f-i). The upper pulvinus thickened,
connecting the laminar base via a tiny, semicircular
laminar joint. The lower pulvinus slightly thickened,
attached at a curved vegetative shoot at ca. 45°. Not far
from the lower pulvinus, a fruit attached on the shoot
(Figure 8a-c). The pedicel, ca. 0.2 cm long, with an
inferior perianth scar and a fruit, indicating the flower
of its parent plant hypogynous (Figure 8a). The fruit
elliptic, ca. 2.8-3.5 cm long and 1.0-1.1 cm wide, with
a slightly curved, acuminate base and an acute apex
(Figure 8a-c,e). The fruit base bearing a thin stipe, ca.
0.4-0.8 cm long (Figure 8e). The suture slightly thickened
and non-winged. Carbonaceous remnants with an oblique
orientation on the valve surface (Figure 8e) implying the
fruit unilocular, possibly coriaceous in texture, and tardily
dehiscent. Seeds, about 2-4 in number in a fruit, grossly
elliptic or oblong in contour (Figure 8a-c), ca. 0.3-0.6 cm
long and 0.2-0.3 cm wide, oriented with their length
perpendicular to the fruit length.
This fossil species B. larsenii was first described by Chen
and Zhang  on the basis of four specimens. Here, we
emended this species, especially regarding the leaf
architecture and fruit morphology, based upon the
type specimens and newly collected materials. It is very
similar to living B. viridescens Desv. and B. brachycarpa
Wall. ex Benth. [3,5,41] in bearing shallowly or moderately
bilobate leaves, brochidodromous secondary vein, and el-
liptic fruits (see Additional file 3). However, no adequate
characters guarantee the fossils to belong to any living
species. In addition, B. larsenii is different from B. cheniae
sp. nov. and other fossil species [33,50-57] in the leaf
architectural detail (see Additional files 3 and 4). In
particular, B. larsenii represents the first recognition of
Bauhinia fruit and foliage organically connected in the
The Leguminosae is the third largest angiosperm family
only after Orchidaceae Juss. and Asteraceae Bercht. et J.
Presl, varying in habit from herbs to shrubs, vines, lianas,
and trees, with an extremely high diversity of ca. 751 living
genera and ca. 19,500 species [10,17] across different habi-
tats of the world. Meanwhile, this family has an abundant
and diverse fossil record, and its characteristic fruits,
flowers, pollen, foliage, and wood have been well recog-
nized from numerous Cenozoic localities around the
world [65,66]. However, an outstanding incongruence
between the palaeobotanical finds and molecular system-
atics of legumes is that the earliest fossil record of the
tribe Cercideae as sister to all other lineages in the
molecular phylogenetic trees of Leguminosae [9-14,20-24]
has so far occurred later than that of some derived tribes
bearing compound leaves such as Sophoreae Spreng. ex
DC. in the subfamily Papilionoideae L. ex DC. . Such
an incongruence implies that the extant Cercideae bearing
the simple, entire or bilobate to bifoliolate foliage is
unlikely to be the most primitive in Leguminosae, but
the derived as some authors formerly suggested from
Wang et al. BMC Evolutionary Biology 2014, 14:88 Page 12 of 16
an extinct legume ancestor possibly with palmately com-
pound leaves  or pinnately compound leaves [27,69].
The fossil record of the Cercideae lacking or being fewer
than those derived tribes in the early Palaeogene of middle
latitudes is because either the early distribution of the
Cercideae might be restricted to low latitudes, or palaeo-
botanical studies on the coeval legumes from low latitudes
are relatively inadequate . Hence, the Cercideae fossils,
especially from low latitudes, can provide an historical
perspective for their early evolution, adaptive radiation,
and biogeographic history.
Leaves of Cercis have been reported from Late Cret-
aceous and Cenozoic sediments, but the overwhelming
majority of these reports have been rejected, questioned,
revised [59,71], or in need of confirmation by reinvesti-
gation of the original materials and discovery of better
preserved materials  (see Additional file 4). The
oldest reliable fossils of Cercis are represented by the
foliage and/or fruits (i.e., C. parvifolia Lesq., C. herbmeyeri
H. Jia et Manchester) from the Late Eocene Florissant
Formation, Colorado and John Day Formation, Oregon,
western USA [71,72]. In contrast, the foliage fossils of
Bauhinia have been previously reported from the Late
Cretaceous and Palaeogene of North America and Eurasia
[73-88], but these identifications are erroneous or unreli-
able  (see Additional file 4). Although Bauhinia or
Bauhinia-like bilobate foliage have been recently reported
from the middle Eocene of Tanzania , the late Eocene
of Vietnam , the late Eocene-early Miocene of Brazil
, and possibly the latest Oligocene–mid-late Miocene
of Australia , the preservation of these pre-Miocene
fossils, which are observed from the originally published
figures, appears too poor to reliably assign these leaf fossils
to either Bauhinia or even Cercideae, because neither
the pulvinus nor basal actinodromous or acrodromous
venations can be confirmed (see Additional file 4). Instead,
the oldest reliable evidence of Bauhinia and Bauhinia-like
foliage are provided from the Oligocene Ningming Forma-
tion, Guangxi, South China (i.e., Bauhinia ningmingensis
sp. nov., B. cheniae sp. nov., and B. larsenii D. X. Zhang
et Y. F. Chen , this paper) and Coatzingo Formation,
Puebla, Mexico (i.e., Bauhcis moranii Calvillo-Canadell
et Cevallos-Ferriz ). By the Miocene–Pliocene, various
species of Bauhinia have existed in Thailand, India, Nepal,
Uganda, and Ecuador (Figure 4) while those of Cercis have
become widespread in mid-latitudes of the northern
In addition, some other unifoliolate or bilobate foliage
or fruit fossils from the Oligocene—Miocene of Jinggu
(Yunnan), Zhangpu (Fujian), and Ningming (Guangxi) in
South China have been reliably described [93-95] or pre-
liminarily identified as Cercis and Bauhinia (Unpublished
observation by Qi Wang, Institute of Botany, Beijing,
, 2013). Also, the bilobate foliage extremely
similar to Bauhinia has been discovered from the Eocene -
Oligocene coals of West Sumatra, western Indonesia (vide
the image of this leaf fossil and information provided by
Drs. Yahdi Zaim, Institute of Technology, Bandung,
Indonesia, Peter Wilf, Pennsylvania State University,
and Gregg F. Gunnell, Duke University Lemur Center,
2014). Hence, more Cercideae fossil will be
studied and reported from low-latitude tropical zone 
of East and Southeast Asia. Recently, a strictly east-to-
west vicariance for the historical biogeography of Cercis
has been postulated by molecular data . The Cercideae
macrofossils occurring in the Eocene to Oligocene of
mid-low latitudes and apparently lacking in the coeval
sediments at high-latitudes appear to partially support a
tropical Tethys Seaway origin and spread [11,22,23] or an
“Out-of-Tropical Asia”dispersal  of the Cercideae and
the Leguminosae as formerly hypothesized by some
authors. However, detailed historical biogeography of
Cercideae still need more palaeobotanical and molecular
Bauhinia has exhibited a certain diversity with three species
(i.e., B. ningmingensis, B. cheniae,andB. larsenii) bearing
bifoliolate or bilobate leaves in a low-latitude locality—
Ningming since at least the Oligocene, implying 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.
By the Miocene–Pliocene, various species of Bauhinia
have existed in Thailand, India, Nepal, Uganda, and
Ecuador while those of Cercis have become widespread
in mid-latitudes of the northern hemisphere. Such a
biogeographic pattern implies a possible Tethys Seaway
origin and spread for legumes. However, detailed scenarios
for the historical biogeography of Bauhinia and its rela-
tives still need more robust dataset from palaeobotany
and molecular phylogeny in future research.
Additional file 1: The distribution of living species in Bauhinia L.
Additional file 2: Information on voucher specimens used in this
Additional file 3: Comparisons between Bauhinia species and other
taxa with similar foliage.
Additional file 4: Previously described fossils assignable or similar
to Bauhinia L.
The authors declare that they have no competing interests.
Wang et al. BMC Evolutionary Biology 2014, 14:88 Page 13 of 16
ZYL, YFC, QW, and SS conducted data analyses, taxonomic treatments, and
evolutionary and biogeographic interpretations. QW and ZQS photographed
specimens, illustrated the line-drawings, and arranged the figures. QW wrote
the manuscript and formatted the text. All authors read and approved the
We greatly thank two anonymous reviewers for their useful comments and
suggestions. Dr. Chen Gengjiao, Mr. Xie Zhiming and other colleagues,
Natural History Museum of Guangxi, Nanning for assistance in the field.
Dr. Shi Gongle, Nanjing Institute of Geology and Palaeontology, CAS, Nanjing,
Dr. Steven R. Manchester, Florida Museum of Natural History, Gainesville,
Dr. Yahdi Zaim, Institute of Technology, Bandung, Dr. Peter Wilf, Pennsylvania
State University, and Dr. Gregg F. Gunnell, Duke University Lemur Center,
Durham for providing us with unpublished images, manuscripts, and thesis.
Mrs. Anna Pavlova, National Institute of Carpology, Moscow, Dr. Yulia V.
Mosseichik, Geological Institute of the Russian Academy of Sciences, Moscow,
Dr. Boris I. Pavlyutkin, Far East Geological Institute, Vladivostok, Prof. Martin
Pickford, Muséum National d’Histoire Naturelle, Paris, Dr. Mike Pole, University of
Tasmania, Hobart, Prof. Rakesh C. Mehrotra, Birbal Sahni Institute of
Palaeobotany, Lucknow, Prof. Subir Bera, University of Calcutta, Kolkata, Dr. Silvia
N. Césari, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”,
Buenos Aires, Prof. Vladan Radulović, University of Belgrade, Belgrade, Dr. Huang
Junhua, Xinjiang Agricultural University, Urumqi, Dr. Yang Yong, Institute of
Botany, CAS, Beijing, and Dr. Xue Jinzhuang, Peking University, Beijing for
providing us with some key references. Mr. Zong Ruiwen, China University of
Geosciences, Wuhan for graphing Figure 2. Mr. Sun Yingbao, Institute of Botany,
CAS for offering a world base map in Figure 4. This work was supported by the
National Natural Science Foundation of China (nos. 41372029 and 41162002),
the State Key Laboratory of Systematic and Evolutionary Botany, CAS (no.
56176G1044), and the State Key Laboratory of Palaeobiology and Stratigraphy,
Nanjing Institute of Geology and Palaeontology, CAS (no. 123106) to QW, ZYL
Received: 19 January 2014 Accepted: 13 April 2014
Published: 24 April 2014
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Cite this article as: Wang et al.:Leaves and fruits of Bauhinia
(Legu mi no sa e, Caesalpinioideae, Cercideae) from the Oligocene Ningm ing
Formation of Guangxi, South China and their biogeographic
implications. BMC Evolutionary Biology 2014 14:88.
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