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Phytogeographical Implication of Bridelia Will.(Phyllanthaceae) Fossil Leaf from the Late Oligocene ofIndiaGaurav Srivastava*, R.C. Mehrotra
Birbal Sahni Institute of Palaeobotany, Lucknow, India
Abstract
Background: The family Phyllanthaceae has a predominantly pantropical distribution. Of its several genera, Bridelia Willd. isof a special interest because it has disjunct equally distributed species in Africa and tropical Asia i.e. 18–20 species in Africa-Madagascar (all endemic) and 18 species in tropical Asia (some shared with Australia). On the basis of molecularphylogenetic study on Bridelia, it has been suggested that the genus evolved in Southeast Asia around 3365 Ma, whilespeciation and migration to other parts of the world occurred at 1062 Ma. Fossil records of Bridelia are equally important tosupport the molecular phylogenetic studies and plate tectonic models.
Results: We describe a new fossil leaf of Bridelia from the late Oligocene (Chattian, 28.4–23 Ma) sediments of Assam, India.The detailed venation pattern of the fossil suggests its affinities with the extant B. ovata, B. retusa and B. stipularis. Based onthe present fossil evidence and the known fossil records of Bridelia from the Tertiary sediments of Nepal and India, we inferthat the genus evolved in India during the late Oligocene (Chattian, 28.4–23 Ma) and speciation occurred during theMiocene. The stem lineage of the genus migrated to Africa via ‘‘Iranian route’’ and again speciosed in Africa-Madagascarduring the late Neogene resulting in the emergence of African endemic clades. Similarly, the genus also migrated toSoutheast Asia via Myanmar after the complete suturing of Indian and Eurasian plates. The emergence and speciation of thegenus in Asia and Africa is the result of climate change during the Cenozoic.
Conclusions: On the basis of present and known fossil records of Bridelia, we have concluded that the genus evolved duringthe late Oligocene in northeast India. During the Neogene, the genus diversified and migrated to Southeast Asia viaMyanmar and Africa via ‘‘Iranian Route’’.
Citation: Srivastava G, Mehrotra RC (2014) Phytogeographical Implication of Bridelia Will. (Phyllanthaceae) Fossil Leaf from the Late Oligocene of India. PLoSONE 9(10): e111140. doi:10.1371/journal.pone.0111140
Editor: Navnith K.P. Kumaran, Agharkar Research Institute, India
Received June 16, 2014; Accepted September 10, 2014; Published October 29, 2014
Copyright: � 2014 Srivastava, Mehrotra. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper.
Funding: These authors have no support or funding to report.
Competing Interests: The authors have declared that no competing interests exist.
* Email: [email protected]
Introduction
The family Phyllanthaceae has a predominantly pantropical
distribution (with a few temperate elements) [1] (Figure 1)
consisting of morphologically diverse, ,60 genera and 2000
species. The family was separated from the Euphorbiaceae s.l.(sensu lato) on the basis of molecular data [2]. The pollen evidence
indicates that the family became well diversified by the Eocene
[3,4]. Of its several genera, Bridelia Willd. is of a special interest
because it has disjunct equally distributed species in Africa and
tropical Asia i.e. 18–20 species in Africa and Madagascar (all
endemic) and 18 species in tropical Asia (some shared with
Australia) [5–7]. On the basis of molecular phylogenetic study on
Bridelia, it has been suggested that the genus evolved around
3365 Ma (i.e. the stem age) and radiated by the 1062 Ma (i.e. the
crown group) [8]. Fossil records of such taxon are equally
important to support the molecular phylogenetic studies.
In the present paper we describe a new leaf impression/
compression of Bridelia from the late Oligocene (Chattian, 28.4–
23 Ma; [9]) sediments of Makum Coalfield (27u159–27u 259 N),
Assam, India (Figure 2) which was located at low palaeolatitude
(i.e. 10u–15u N) during the period [10]. The suturing of the Indian
plate with the Eurasian plate, during the aforesaid period, was not
complete to facilitate the plant migration (Figure 3) [11–13]. An
attempt has also been made to discuss its origin and dispersal.
Regional geologyThe Makum Coalfield is a well known basin having exposure of
the late Oligocene sediments. The coalfield is important because (i)
it is one of the largest coal producing basins in northeast India and
(ii) it contains a well diversified low latitude palaeoflora [14–22].
Infact, there is no other Oligocene sedimentary basin in the Indian
sub-continent which contains such a rich and diversified assem-
blage of fossil plants. The basin was situated at a low
palaeolatitude i.e. ,10u–15u N (Figure 3) [10] and the sediments
were deposited in a deltaic, mangrove or lagoonal environment
[15,23–25]. The coalfield is made up of Baragolai, Ledo,
Namdang, Tikak, Tipong and Tirap collieries, lies in between
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the latitudes 27u 159–27u 259 N and longitudes 95u 409–95u 559 E
(Figure 2) and is located along the outermost flank of the Patkai
range. On the southern and southeastern sides are the hills which
rise abruptly to heights of 300–500 m from the alluvial plains of
the Buri Dihing and Tirap rivers, respectively.
The fossils collected for the present study belong to the Tikak
Parbat Formation being considered to be late Oligocene
(Chattian, 28.4–23 Ma; [9]) in age on the basis of regional
lithostratigraphy [26], remote sensing [27] and biostratigraphic
controls [24].
The Tikak Parbat Formation constitutes alternations of
sandstone, siltstone, mudstone, shale, carbonaceous shale, clay
and coal seams [28]. However, the plant remains are mainly
confined to the grey carbonaceous and sandy shales. The
formation is underlain by 300 m of predominantly massive,
micaceous or ferruginous sandstones that incorporate the
Baragolai Formation, which is successively underlain by 1100–
1700 m of thin-bedded fine-grained quartzitic sandstones with
thin shale and sandy shale partings that constitute the Naogaon
Formation [29]. Together the three formations represent the
Barail Group (Figure 2). In this group, there is an upward trend of
marine to non-marine palaeoenvironment which symbolizes the
infilling of a linear basin on the eastern edge of the Indian plate.
The detailed sedimentary information of the Tirap mine section
was given by Kumar et al. [24].
Materials and Methods
Material for the present study was collected from the Tirap
colliery of the Makum Coalfield, Tinsukia District, Assam. The
prior permission was taken from the General Manager, North-
eastern Coalfield, Margherita, Assam, India for the collection of
fossil plants. The specimen was first cleared with the help of a fine
chisel and hammer and then photographed in natural low angled
light using 10 megapixel digital camera (Canon SX110). The
terminology used in describing the fossil leaf is based on Hickey
[30], Dilcher [31] and Ellis et al. [32]. Attempts were made to
extract cuticle from the leaf but it did not yield. The permission
was taken from the Directors, Forest Research Institute, Dehradun
and the Botanical Survey of India, Kolkata for the herbarium
consultation. The fossil plant was identified with the help of
herbarium sheets of the extant plant available there. The type
specimen (no. BSIP 40115) is housed in the museum of the Birbal
Sahni Institute of Palaeobotany, Lucknow, India.
NomenclatureThe electronic version of this article in Portable Document
Format (PDF) in a work with an ISSN or ISBN will represent a
published work according to the International Code of Nomen-
clature for algae, fungi, and plants, and hence the new names
contained in the electronic publication of a PLOS ONE article are
effectively published under that Code from the electronic edition
alone, so there is no longer any need to provide printed copies.
The online version of this work is archived and available from the
following digital repositories: PubMed Central, LOCKSS.
Figure 1. Map showing the modern distribution of the family Phyllanthaceae and Bridelia [1, 64].doi:10.1371/journal.pone.0111140.g001
Figure 2. Simplified geological map of the Makum Coalfield,Assam, India showing the fossil locality (red circle) [65].doi:10.1371/journal.pone.0111140.g002
Bridelia Fossil Leaf from Assam, India
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Results
Systematic description
Order. Malpighiales Juss. (1820) [33]
Family. Phyllanthaceae Martinov (1820) [34]
Subfamily. Phyllanthoideae Asch. (1864) [35]
Tribe. Bridelieae Mull. Arg. (1864) [36]
Genus. Bridelia Willd. (1806) [37]
Species. B. makumensis Srivastava and Mehrotra, sp. nov.
Figures. 4A, B, D; 5A, D
Holotype. Specimen No. BSIP 40115
Horizon. Tikak Parbat Formation
Locality. Tirap Colliery, Tinsukia District, Assam (27u 179 200 N;
95u 469 150 E)
Age. Late Oligocene (Chattian, 28.4–23 Ma)
Number of specimens studied. One.
Description. Leaf nearly complete, simple, symmetrical,
microphyll, elliptic, preserved lamina length 5.2 cm (estimated
lamina length 7.3 cm), maximum width near the middle portion
2.4 cm; apex not preserved but seems to be acute-obtuse; base
slightly broken, asymmetrical, acute, normal; margin entire but
slightly crenate seen on the distal portion, seemingly wavy; texture
appearing chartaceous; attachment with petiole not preserved;
venation pinnate, simple craspedodromous to eucamptodromous;
primary vein stout in thickness, curved; secondary veins 11 pairs
visible, 0.2–0.4 cm apart, predominantly alternate, angle of
divergence moderate acute (48u–62u), smoothly and sometimes
abruptly curved up near the margin, attachment with the primary
vein normal, rarely decurrent; intersecondary veins absent; tertiary
veins simple percurrent, recurved, forked, oblique to mid-vein,
angle of origin AO, AA, AR, predominantly alternate, close;
marginal ultimate venation fimbriate; quaternary veins orthogo-
nal.
Affinities. The characteristic features of the fossil leaf such as
elliptic shape, crenate margin, craspedodromous to eucampto-
dromous venation, moderate acute angle of divergence of
secondary veins, percurrent to recurved tertiary veins and
fimbriate marginal venation suggest its affinity with Bridelia of
the family Phyllanthaceae. A large number of species of Brideliasuch as B. assamica Hook.f., B. cinnamomea Hook.f., B. glaucaBlume, B. insulana Hance, B. ovata Decne. (syn. B. burmanicaHook.f.), B. retusa (L.) A. Juss. (syn. B. squamosa), B. stipularis (L.)
Blume (syn. B. scandens), B. tomentosa Blume and the species of its
sister genus Cleistanthus Hook.f. ex Planch such as C. collinus(Roxb.) Benth. ex Hook.f., C. malabaricus Mull.Arg. and C.monoicus (Lour.) Mull.Arg. were studied and compared in the
herbarium of the Forest Research Institute, Dehradun and the
Central National Herbarium, Howrah.
In B. assamica, B. cinnamomea, B. glauca, B. scandens and
Cleistanthus monoicus the angle of divergence of secondary veins is
narrow-moderate acute which is in contrast to the present fossil. In
B. insulana, B. tomentosa, Cleistanthus collinus and C. malabar-icus the distance between the two secondary veins is greater than
the present fossil. In the venation pattern the fossil shows
maximum similarity with B. retusa (Figure 4C, E) and B. stipularis(Figure 5B, C, E) but differs from them in having asymmetrical
base. In having asymmetrical base our fossil shows resemblance
with B. ovata where base varies from asymmetrical ([38], Plate 14,
Figure 2) to symmetrical (CNH Herbarium sheet no. 400497).
However, angle of divergence of secondary veins is more acute in
B. ovata than that of our fossil. It appears that our fossil shows a
combination of characters found in B. ovata, B. retusa and B.stipularis. The comparable species are distributed throughout the
hotter parts of India, along the foot of the Himalaya, south India,
Malacca, Malayan Peninsula, Myanmar, Sri Lanka, Philippines
and tropical Africa [39].
As far as fossil leaf records of Bridelia are concerned they are
known mainly from Nepal and India. Two fossil species of the
genus, namely B. mioretusa and B. siwalica are known from the
Figure 3. Map showing the fossil locality (yellow dot) in palaeogeographic map during the Oligocene [66].doi:10.1371/journal.pone.0111140.g003
Bridelia Fossil Leaf from Assam, India
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Siwalik sediments (late Miocene) of Surai Khola, western Nepal
[38]. Three more fossil species of Bridelia, namely B. stipularisand B. verucosa have been described from the Middle Siwalik
sediments of Darjeeling, West Bengal [40], while another species
viz., B. oligocenica is known from the late Oligocene sediments of
Assam [15]. All the aforesaid fossils are different from the present
fossil in a combination of characters (Table 1). Under such
circumstances a new species, B. makumensis Srivastava and
Mehrotra, sp. nov. is created and the specific epithet is after the
fossil locality.
Figure 4. Bridelia leaves. A. Fossil leaf of Bridelia makumensis sp. nov. showing shape, size and venation pattern. B. Text diagram of the fossil leafshowing craspedodromous and eucamptodromous venation (yellow and green arrows), secondary veins (red arrows) and percurrent, recurved andforked tertiary veins (blue, orange and black arrows). C. Modern leaf of Bridelia retusa showing craspedodromous and eucamptodromous venation(yellow and green arrows), secondary veins (red arrows) and percurrent and recurved tertiary veins (blue and orange arrows). D. Enlarged portion ofthe fossil leaf showing secondary veins (pink arrows), percurrent, recurved and forked tertiary veins (yellow, white and red arrows); predominantlyalternate tertiary veins (orange arrow). E. Modern leaf of Bridelia retusa showing secondary veins (pink arrows); percurrent, recurved and forkedtertiary veins (yellow, white and red arrows) Scale bar = 1 cm, unless mentioned.doi:10.1371/journal.pone.0111140.g004
Bridelia Fossil Leaf from Assam, India
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Figure 5. Bridelia leaves. A. Enlarged apical portion of the fossil leaf showing craspedodromous and eucamptodromous venation (orange and bluearrows), secondary veins (yellow arrows) and percurrent tertiary veins (red arrows). B. Apical portion of the modern leaf of B. stipularis showing similarcraspedodromous and eucamptodromous venation (orange and blue arrows) as found in the fossil and secondary veins (yellow arrows). C. Modernleaf of B. stipularis showing shape, size and venation pattern. D. Basal portion of the fossil leaf showing course of secondary veins (yellow arrows). E.Basal portion of the modern leaf of B. stipularis showing similar course of secondary veins as found in the fossil (yellow arrows).doi:10.1371/journal.pone.0111140.g005
Bridelia Fossil Leaf from Assam, India
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Discussion
Fossil wood record of BrideliaAs far as the fossil records of Bridelia are concerned, they are
known in the form of leaves and woods. The leaf fossil records
have been discussed in the affinities (see section affinities). Fossil
woods of Bridelia are known from various Tertiary sediments of
central South Asia, temperate Asia, tropical Africa, Northern
Africa, Europe, America and Australia [41] but their affinities with
modern Bridelia are uncertain because of the homogeneity in
wood characters of various genera of Euphorbiaceae s.l.Bailey [42] instituted the genus Paraphyllanthoxylon for the
fossil woods resembling Phyllanthoid Euphorbiaceae that includes
the genus Bridelia also. However, he was not sure of its affinities.
Wheeler et al. [43] after studying various species of Paraphyl-lanthoxylon concluded that the genus can not be assigned with
certainty to the Euphorbiaceae because of its similarities to other
families.
Ramanujam [44] instituted the genus Bischofioxylon for the
fossil woods resembling Bischofia and described Bischofioxylonmiocenicum from south India. Madel [45] had suggested its
affinities with Bridelia and merged it into another organ genus
Bridelioxylon Madel. Therefore, Bande [46] established Bischofi-nium for the fossil woods resembling Bischofia. Awasthi [47]
suggested that neither B. miocenicum Ramanujam nor BiscofiniumBande belongs to Bischofia or Bridelia. The generic diagnosis of
Bridelioxylon is within the range of generic diagnosis of
Paraphyllanthoxylon Bailey. In our opinion due to the homoge-
neity in wood characters, it is difficult to separate Bridelia from
other genera of the Euphorbiaceae.
Disjunct distribution pattern and possible migratory pathof Bridelia from India to Africa-Madagascar and SoutheastAsia
The disjunct phytogeography of Bridelia with equal distribution
of species in Africa and tropical Asia and endemism in the African-
Madagascar species are interesting. Based on the molecular data,
Li et al. [8] inferred that Bridelia separated from its sister genus
Cleistanthus at 3365 Ma and suggested that the genus evolved in
Southeast Asia and later migrated westward to India and Africa
and eastward to Australia. However, this hypothesis didn’t get
support from the fossil records of the genus. The present fossil
record from the late Oligocene sediments of northeast India is
important because during the late Oligocene, suturing of the
Indian plate with the Eurasian plate was not complete to facilitate
the plant migration between India and Southeast Asia (Figure 3)
[11–13]. In the light of the oldest fossil evidence of Bridelia from
northeast India we suggest that the genus evolved most likely
during the late Oligocene in northeast India, while the speciation
must have occurred during the Miocene followed by the dispersal
of the genus from India to Southeast Asia via Myanmar as the
suturing of both the aforesaid plates completed during the early
Miocene [48,49]. Our fossil shows affinity with three species of
Bridelia, namely B. ovata, B. retusa and B. stipularis; this again
suggests that the speciation must have occurred after the late
Oligocene and most likely during the Miocene as suggested by the
molecular data [8] and supported by the diversity in fossil records
from the Siwalik of Nepal and India [38,40]. The climatic
conditions also favoured in the evolution of Bridelia because the
late Oligocene was the time of last significant globally warm
climate during the Cenozoic [50] under which the genus evolved
and the speciation of the genus in Asia most likely to have
occurred during the Middle Miocene Climatic Optimum
(MMCO) [50]. All the above facts indicate that Bridelia evolved
Ta
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Bridelia Fossil Leaf from Assam, India
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in India during the late Oligocene and after the complete suturing
of Indian and Eurasian plates the genus migrated to Southeast
Asia via Myanmar and then to Australia, along with several other
plant taxa such as Alphonsea of the family Annonaceae [20],
Mangifera [51] and Semecarpus of the family Anacardiaceae [18]
(Figure 1). Similarly, the stem lineage of Bridelia also migrated to
Africa via ‘‘Iranian Route’’ [52] during the late Miocene to early
Pleistocene and this can be explained on the basis of plate tectonic
model. Africa was isolated from Eurasia during the mid-
Cretaceous to early Miocene [53]. By the early Miocene, Africa
made land connections with east Eurasia via ‘‘Iranian Route’’
(Iranian and Arabian block) [52], and Bridelia most likely to have
migrated through this route during the Miocene (Figure 1). After
reaching to Africa, the stem lineage of the genus speciosed locally
due to the availability of free niche and less competition which
resulted in the local endemism of the genus in Africa. The
speciation of stem lineage of Bridelia in Africa again coincides with
the climatic condition in Africa i.e. occurrence of aridity in Africa
during the late Neogene [54–56]. The aforesaid view also gets
supports from the molecular phylogenetic study which suggests
that the African clade speciosed at ca 361 Ma [8].
The corridor via ‘‘Iranian Route’’ was not only for Bridelia but
also common for faunal exchange [52,57] and several other
African plant taxa reported from the Pliocene of western India
[58]; this suggests that the migration was in between Africa and
east Eurasia.
The migration of Bridelia from India to Africa and Southeast
Asia again supports the ‘‘Out of India’’ hypothesis [59].
Palaeofloristics and Palaeoclimate of the MakumCoalfield, Assam
The Makum Coalfield is important in view of its high diversity
of plant fossils. The late Oligocene was the time of last significant
globally warm period during the Cenozoic and the fossil locality
was situated at 10u–15u N palaeolatitude [10]. The known floristic
diversity indicates that the family Fabaceae was the most dominant
followed by Anacardiaceae, Clusiaceae, Combretaceae, Areca-
ceae, Annonaceae, Lauraceae and Sapindaceae etc. Most of the
aforesaid families have pantropical distribution, while the abun-
dance of palms indicates high water availability.
The families like Annonaceae, Burseraceae, Clusiaceae, Com-
bretaceae, Lecythidaceae, Myristicaceae and Rhizophoraceae are
typical pantropical megatherm families [60] whose presence in the
palaeoflora provides an evidence that the CMT (mean tempera-
ture of the coldest month) was at least not less than 18uC [25].
Similarly, the presence of most dominant family Fabaceae [17]
whose abundance and richness covary with the temperature [61],
indicates warm climate. The occurrence of families Avicenniaceae
and Rhizophoraceae is also very significant in terms of the
depositional environment. These families are highly indicative of
deltaic, mangrove or lacustrine deposition of coal seams and
associated sediments in the Makum Coalfield [15]. The abun-
dance of palms like Nypa [23] provides clear evidence of a coastal
plain environment where both temperature and humidity remain
high throughout the year [62]. Quantitative palaeoclimate
reconstruction based on CLAMP analysis on the Makum Coalfield
palaeoflora was made by Srivastava et al. [25]. They have used 80
different leaf morphotypes, from the Tirap colliery of the Makum
Coalfield, which were analysed by following standard protocol of
CLAMP analysis [63]. The CLAMP analysis indicates mean
annual temperature (MAT) 28.363.7uC, warm month mean
temperature (WMMT) 34.265.2uC and cold month mean
temperature (CMMT) 23.665.5uC. The precipitation estimates
suggest a marked seasonality in the rainfall pattern showing a wet
season with 20 times the rainfall of the dry season. The similar
pattern can be seen in Sunderbans lying in the modern Ganges/
Brahmaputra/Meghna delta. Therefore, it is suggested that the
South Asian Monsoon was already established by the late
Oligocene time at an intensity similar to that of today [25].
Conclusions
Fossil evidences, along with the molecular data are important in
studying the evolution and speciation of an organism. In the
present paper we have reported fossil leaf of Bridelia from the late
Oligocene sediments of northeast India and suggested its affinity
with B. ovata, B. retusa and B. stipularis. Our fossil data, along
with the known fossil records of Bridelia from the Neogene
sediments of Nepal and India suggests that the genus evolved
during the late Oligocene and migration and speciation occurred
from India to Southeast Asia via Myanmar and from India to
Africa via ‘‘Iranian Route’’ during the Miocene. The present
finding fits well with the molecular phylogenetic analysis and plate
tectonic models.
Acknowledgments
The authors are thankful to the authorities of the Coal India Limited
(Northeastern Region), Margherita for permission to collect plant fossils
from the Makum Coalfield. Thanks are also due to the Directors, Botanical
Survey of India, Kolkata and the Forest Research Institute, Dehradun for
permitting us to consult the herbarium. The authors are also thankful to
Prof. Sunil Bajpai, Director, Birbal Sahni Institute of Palaeobotany,
Lucknow for providing necessary facilities and permission to carry out this
work. They are thankful to Prof. E.A. Wheeler of North Carolina State
University, USA for sending her valuable reprints. The authors are also
grateful to Prof. Khum Paudiyal, one anonymous reviewer and Prof.
Navnith K.P. Kumaran for their valuable suggestions in improving the
manuscript.
Author Contributions
Conceived and designed the experiments: GS RCM. Performed the
experiments: GS RCM. Analyzed the data: GS RCM. Contributed
reagents/materials/analysis tools: GS RCM. Contributed to the writing of
the manuscript: GS RCM.
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