phytogeographical implication of brideliawill ...phytogeographical implication of brideliawill....

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


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



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



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



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

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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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http://data.gbif.org/species/3076094/

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