Phytogeographical Implication of Will. () Fossil from the Late Oligocene of

Gaurav 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. is of a special interest because it has disjunct equally distributed in and tropical i.e. 18–20 species in Africa- Madagascar (all endemic) and 18 species in tropical Asia (some shared with Australia). On the basis of molecular phylogenetic study on Bridelia, it has been suggested that the evolved in Southeast Asia around 3365 Ma, while speciation and migration to other parts of the world occurred at 1062 Ma. Fossil records of Bridelia are equally important to support 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 on the present fossil evidence and the known fossil records of Bridelia from the Tertiary sediments of and India, we infer that the genus evolved in India during the late Oligocene (Chattian, 28.4–23 Ma) and speciation occurred during the Miocene. The stem lineage of the genus migrated to Africa via ‘‘Iranian route’’ and again speciosed in Africa-Madagascar during the late Neogene resulting in the emergence of African endemic clades. Similarly, the genus also migrated to Southeast Asia via after the complete suturing of Indian and Eurasian plates. The emergence and speciation of the genus 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 during the late Oligocene in northeast India. During the Neogene, the genus diversified and migrated to Southeast Asia via Myanmar 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. PLoS ONE 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: ß 2014 Srivastava, Mehrotra. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted 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 23 Ma; [9]) sediments of Makum Coalfield (27u159–27u 259 N), Assam, India (Figure 2) which was located at low palaeolatitude The family Phyllanthaceae has a predominantly pantropical (i.e. 10u–15u N) during the period [10]. The suturing of the Indian distribution (with a few temperate elements) [1] (Figure 1) plate with the Eurasian plate, during the aforesaid period, was not consisting of morphologically diverse, ,60 genera and 2000 complete to facilitate the migration (Figure 3) [11–13]. An species. The family was separated from the Euphorbiaceae s.l. attempt has also been made to discuss its origin and dispersal. (sensu lato) on the basis of molecular data [2]. The pollen evidence indicates that the family became well diversified by the Eocene Regional geology [3,4]. Of its several genera, Bridelia Willd. is of a special interest The Makum Coalfield is a well known basin having exposure of because it has disjunct equally distributed species in Africa and the late Oligocene sediments. The coalfield is important because (i) tropical Asia i.e. 18–20 species in Africa and Madagascar (all it is one of the largest coal producing basins in northeast India and endemic) and 18 species in tropical Asia (some shared with (ii) it contains a well diversified low latitude palaeoflora [14–22]. Australia) [5–7]. On the basis of molecular phylogenetic study on Infact, there is no other Oligocene sedimentary basin in the Indian Bridelia, it has been suggested that the genus evolved around sub-continent which contains such a rich and diversified assem- 6 6 33 5 Ma (i.e. the stem age) and radiated by the 10 2 Ma (i.e. the blage of fossil . The basin was situated at a low crown group) [8]. Fossil records of such taxon are equally palaeolatitude i.e. ,10u–15u N (Figure 3) [10] and the sediments important to support the molecular phylogenetic studies. were deposited in a deltaic, or lagoonal environment In the present paper we describe a new leaf impression/ [15,23–25]. The coalfield is made up of Baragolai, Ledo, compression of Bridelia from the late Oligocene (Chattian, 28.4– Namdang, Tikak, Tipong and Tirap collieries, lies in between

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Figure 1. Map showing the modern distribution of the family Phyllanthaceae and Bridelia [1, 64]. doi:10.1371/journal.pone.0111140.g001 the latitudes 27u 159–27u 259 N and longitudes 95u 409–95u 559 E Barail Group (Figure 2). In this group, there is an upward trend of (Figure 2) and is located along the outermost flank of the Patkai marine to non-marine palaeoenvironment which symbolizes the range. On the southern and southeastern sides are the hills which infilling of a linear basin on the eastern edge of the Indian plate. rise abruptly to heights of 300–500 m from the alluvial plains of The detailed sedimentary information of the Tirap mine section the Buri Dihing and Tirap rivers, respectively. was given by Kumar et al. [24]. The fossils collected for the present study belong to the Tikak Parbat Formation being considered to be late Oligocene Materials and Methods (Chattian, 28.4–23 Ma; [9]) in age on the basis of regional lithostratigraphy [26], remote sensing [27] and biostratigraphic Material for the present study was collected from the Tirap controls [24]. colliery of the Makum Coalfield, Tinsukia District, Assam. The The Tikak Parbat Formation constitutes alternations of prior permission was taken from the General Manager, North- sandstone, siltstone, mudstone, shale, carbonaceous shale, clay eastern Coalfield, Margherita, Assam, India for the collection of and coal seams [28]. However, the plant remains are mainly fossil plants. The specimen was first cleared with the help of a fine confined to the grey carbonaceous and sandy shales. The chisel and hammer and then photographed in natural low angled formation is underlain by 300 m of predominantly massive, light using 10 megapixel digital camera (Canon SX110). The micaceous or ferruginous sandstones that incorporate the terminology used in describing the fossil leaf is based on Hickey Baragolai Formation, which is successively underlain by 1100– [30], Dilcher [31] and Ellis et al. [32]. Attempts were made to 1700 m of thin-bedded fine-grained quartzitic sandstones with extract cuticle from the leaf but it did not yield. The permission thin shale and sandy shale partings that constitute the Naogaon was taken from the Directors, Forest Research Institute, Dehradun Formation [29]. Together the three formations represent the 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.

Nomenclature The 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. Figure 2. Simplified geological map of the Makum Coalfield, The online version of this work is archived and available from the Assam, India showing the fossil locality (red circle) [65]. following digital repositories: PubMed Central, LOCKSS. doi:10.1371/journal.pone.0111140.g002

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Figure 3. Map showing the fossil locality (yellow dot) in palaeogeographic map during the Oligocene [66]. doi:10.1371/journal.pone.0111140.g003

Results Affinities. The characteristic features of the fossil leaf such as elliptic shape, crenate margin, craspedodromous to eucampto- Systematic description dromous venation, moderate acute angle of divergence of Order. Juss. (1820) [33] secondary veins, percurrent to recurved tertiary veins and Family. Phyllanthaceae Martinov (1820) [34] fimbriate marginal venation suggest its affinity with Bridelia of the family Phyllanthaceae. A large number of species of Bridelia Subfamily. Phyllanthoideae Asch. (1864) [35] such as B. assamica Hook.f., B. cinnamomea Hook.f., B. glauca Tribe. Bridelieae Mu¨ll. Arg. (1864) [36] Blume, B. insulana Hance, B. ovata Decne. (syn. B. burmanica Genus. Bridelia Willd. (1806) [37] Hook.f.), B. retusa (L.) A. Juss. (syn. B. squamosa), B. stipularis (L.) Species. B. makumensis Srivastava and Mehrotra, sp. nov. Blume (syn. B. scandens), B. tomentosa Blume and the species of its sister genus Hook.f. ex Planch such as Figures. 4A, B, D; 5A, D C. collinus (Roxb.) Benth. ex Hook.f., C. malabaricus Mu¨ll.Arg. and C. Holotype. Specimen No. BSIP 40115 monoicus (Lour.) Mu¨ll.Arg. were studied and compared in the Horizon. Tikak Parbat Formation herbarium of the Forest Research Institute, Dehradun and the Locality. Tirap Colliery, Tinsukia District, Assam (27u 179 200 N; Central National Herbarium, Howrah. 95u 469 150 E) In B. assamica, B. cinnamomea, B. glauca, B. scandens and Age. Late Oligocene (Chattian, 28.4–23 Ma) Cleistanthus monoicus the angle of divergence of secondary veins is narrow-moderate acute which is in contrast to the present fossil. In Number of specimens studied. One. B. insulana, B. tomentosa, and C. malabar- Description. Leaf nearly complete, simple, symmetrical, icus the distance between the two secondary veins is greater than microphyll, elliptic, preserved lamina length 5.2 cm (estimated the present fossil. In the venation pattern the fossil shows lamina length 7.3 cm), maximum width near the middle portion maximum similarity with B. retusa (Figure 4C, E) and B. stipularis 2.4 cm; apex not preserved but seems to be acute-obtuse; base (Figure 5B, C, E) but differs from them in having asymmetrical slightly broken, asymmetrical, acute, normal; margin entire but base. In having asymmetrical base our fossil shows resemblance slightly crenate seen on the distal portion, seemingly wavy; texture with B. ovata where base varies from asymmetrical ([38], Plate 14, appearing chartaceous; attachment with petiole not preserved; Figure 2) to symmetrical (CNH Herbarium sheet no. 400497). venation pinnate, simple craspedodromous to eucamptodromous; However, angle of divergence of secondary veins is more acute in primary vein stout in thickness, curved; secondary veins 11 pairs B. ovata than that of our fossil. It appears that our fossil shows a visible, 0.2–0.4 cm apart, predominantly alternate, angle of combination of characters found in B. ovata, B. retusa and B. divergence moderate acute (48u–62u), smoothly and sometimes stipularis. The comparable species are distributed throughout the abruptly curved up near the margin, attachment with the primary hotter parts of India, along the foot of the Himalaya, south India, vein normal, rarely decurrent; intersecondary veins absent; tertiary Malacca, Malayan Peninsula, Myanmar, Sri Lanka, Philippines veins simple percurrent, recurved, forked, oblique to mid-vein, and tropical Africa [39]. angle of origin AO, AA, AR, predominantly alternate, close; As far as fossil leaf records of Bridelia are concerned they are marginal ultimate venation fimbriate; quaternary veins orthogo- known mainly from Nepal and India. Two fossil species of the nal. genus, namely B. mioretusa and B. siwalica are known from the

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Figure 4. Bridelia . A. Fossil leaf of Bridelia makumensis sp. nov. showing shape, size and venation pattern. B. Text diagram of the fossil leaf showing craspedodromous and eucamptodromous venation (yellow and green arrows), secondary veins (red arrows) and percurrent, recurved and forked tertiary veins (blue, orange and black arrows). C. Modern leaf of 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 of the fossil leaf showing secondary veins (pink arrows), percurrent, recurved and forked tertiary veins (yellow, white and red arrows); predominantly alternate tertiary veins (orange arrow). E. Modern leaf of Bridelia retusa showing secondary veins (pink arrows); percurrent, recurved and forked tertiary veins (yellow, white and red arrows) Scale bar = 1 cm, unless mentioned. doi:10.1371/journal.pone.0111140.g004

Siwalik sediments (late Miocene) of Surai Khola, western Nepal Assam [15]. All the aforesaid fossils are different from the present [38]. Three more fossil species of Bridelia, namely B. stipularis fossil in a combination of characters (Table 1). Under such and B. verucosa have been described from the Middle Siwalik circumstances a new species, B. makumensis Srivastava and sediments of Darjeeling, West Bengal [40], while another species Mehrotra, sp. nov. is created and the specific epithet is after the viz., B. oligocenica is known from the late Oligocene sediments of fossil locality.

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Figure 5. Bridelia leaves. A. Enlarged apical portion of the fossil leaf showing craspedodromous and eucamptodromous venation (orange and blue arrows), secondary veins (yellow arrows) and percurrent tertiary veins (red arrows). B. Apical portion of the modern leaf of B. stipularis showing similar craspedodromous and eucamptodromous venation (orange and blue arrows) as found in the fossil and secondary veins (yellow arrows). C. Modern leaf 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

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Discussion

veins Fossil wood record of Bridelia 0 As 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

veins 3 central South Asia, temperate Asia, tropical Africa, Northern 0 Moderate acute Percurrent Narrow acute Percurrent 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 eucamptodromous eucamptodromous families. Ramanujam [44] instituted the genus Bischofioxylon for the fossil woods resembling Bischofia and described Bischofioxylon miocenicum from south India. Ma¨del [45] had suggested its affinities with Bridelia and merged it into another organ genus Bridelioxylon Ma¨del. Therefore, Bande [46] established Bischofi- nium for the fossil woods resembling Bischofia. Awasthi [47] suggested that neither B. miocenicum Ramanujam nor Biscofinium Bande 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 Elliptic Symmetrical Craspedodromous- other genera of the Euphorbiaceae.

Disjunct distribution pattern and possible migratory path of Bridelia from India to Africa-Madagascar and Southeast crenate Entire Obovate Asymmetrical Eucamptodromous Wide acuteAsia Percurrent 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

from the Cenozoic sediments. Cleistanthus at 3365 Ma and suggested that the genus evolved in Southeast Asia and later migrated westward to India and Africa Acute, asymmetrical Entire-slightly asymmetrical and eastward to Australia. However, this hypothesis didn’t get

Bridelia 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 Acute-ObtuseObtuse Round Obtuse Entire Entire Elliptic Symmetrical Elliptic Symmetrical Eucamptodromous Eucamptodromous Wide acute NG Narrow acute NG Seemingly acute- obtuse NP Obtuse, Lamina NPAcute Acute NP Entire Entire Elliptic Elliptic Symmetricalthe Symmetrical plant Eucamptodromous migration Craspedodromous- Narrow acute between ?Percurrent 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 and 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 B. stipularis B. verucosa B. ovata, B. retusa B. stipularis B.ovata Modern Comparable Forms Apex Base Margin Shape Balance Venation pattern 2 B. retusa B. retusa 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 Prasad

Srivastava conditions also favoured in the evolution of Bridelia because the Awasthi and Comparative chart of the known fossil leaves of Pathak 31] Pathak 31] late Oligocene was the time of last significant globally warm Prasad and 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 NP = Not preserved; NG = Not given. doi:10.1371/journal.pone.0111140.t001 B. stipularis B. verucosa B. makumensis and Mehrotra Table 1. B. siwalika Pandey [30] Fossil taxa B.oligocenica Mehrotra [15] Bridelia mioretusa and Pandey 30] (MMCO) [50]. All the above facts indicate that Bridelia evolved

PLOS ONE | www.plosone.org 6 October 2014 | Volume 9 | Issue 10 | e111140 Bridelia Fossil Leaf from Assam, India in India during the late Oligocene and after the complete suturing dance of palms like Nypa [23] provides clear evidence of a coastal of Indian and Eurasian plates the genus migrated to Southeast plain environment where both temperature and humidity remain Asia via Myanmar and then to Australia, along with several other high throughout the year [62]. Quantitative palaeoclimate plant taxa such as Alphonsea of the family Annonaceae [20], reconstruction based on CLAMP analysis on the Makum Coalfield Mangifera [51] and Semecarpus of the family Anacardiaceae [18] palaeoflora was made by Srivastava et al. [25]. They have used 80 (Figure 1). Similarly, the stem lineage of Bridelia also migrated to different leaf morphotypes, from the Tirap colliery of the Makum Africa via ‘‘Iranian Route’’ [52] during the late Miocene to early Coalfield, which were analysed by following standard protocol of Pleistocene and this can be explained on the basis of plate tectonic CLAMP analysis [63]. The CLAMP analysis indicates mean model. Africa was isolated from Eurasia during the mid- annual temperature (MAT) 28.363.7uC, warm month mean Cretaceous to early Miocene [53]. By the early Miocene, Africa temperature (WMMT) 34.265.2uC and cold month mean made land connections with east Eurasia via ‘‘Iranian Route’’ temperature (CMMT) 23.665.5uC. The precipitation estimates (Iranian and Arabian block) [52], and Bridelia most likely to have suggest a marked seasonality in the rainfall pattern showing a wet migrated through this route during the Miocene (Figure 1). After season with 20 times the rainfall of the dry season. The similar reaching to Africa, the stem lineage of the genus speciosed locally pattern can be seen in Sunderbans lying in the modern Ganges/ due to the availability of free niche and less competition which Brahmaputra/Meghna delta. Therefore, it is suggested that the resulted in the local endemism of the genus in Africa. The South Asian Monsoon was already established by the late speciation of stem lineage of Bridelia in Africa again coincides with Oligocene time at an intensity similar to that of today [25]. the climatic condition in Africa i.e. occurrence of aridity in Africa during the late Neogene [54–56]. The aforesaid view also gets Conclusions supports from the molecular phylogenetic study which suggests that the African clade speciosed at ca 361 Ma [8]. Fossil evidences, along with the molecular data are important in The corridor via ‘‘Iranian Route’’ was not only for Bridelia but studying the evolution and speciation of an organism. In the also common for faunal exchange [52,57] and several other present paper we have reported fossil leaf of Bridelia from the late African plant taxa reported from the Pliocene of western India Oligocene sediments of northeast India and suggested its affinity [58]; this suggests that the migration was in between Africa and with B. ovata, B. retusa and B. stipularis. Our fossil data, along east Eurasia. with the known fossil records of Bridelia from the Neogene The migration of Bridelia from India to Africa and Southeast sediments of Nepal and India suggests that the genus evolved Asia again supports the ‘‘Out of India’’ hypothesis [59]. during the late Oligocene and migration and speciation occurred from India to Southeast Asia via Myanmar and from India to Palaeofloristics and Palaeoclimate of the Makum Africa via ‘‘Iranian Route’’ during the Miocene. The present Coalfield, Assam finding fits well with the molecular phylogenetic analysis and plate The Makum Coalfield is important in view of its high diversity tectonic models. of plant fossils. The late Oligocene was the time of last significant globally warm period during the Cenozoic and the fossil locality Acknowledgments was situated at 10u–15u N palaeolatitude [10]. The known floristic diversity indicates that the family Fabaceae was the most dominant The authors are thankful to the authorities of the Coal India Limited followed by Anacardiaceae, Clusiaceae, Combretaceae, Areca- (Northeastern Region), Margherita for permission to collect plant fossils from the Makum Coalfield. Thanks are also due to the Directors, Botanical ceae, Annonaceae, Lauraceae and Sapindaceae etc. Most of the Survey of India, Kolkata and the Forest Research Institute, Dehradun for aforesaid families have pantropical distribution, while the abun- permitting us to consult the herbarium. The authors are also thankful to dance of palms indicates high water availability. Prof. Sunil Bajpai, Director, Birbal Sahni Institute of Palaeobotany, The families like Annonaceae, Burseraceae, Clusiaceae, Com- Lucknow for providing necessary facilities and permission to carry out this bretaceae, Lecythidaceae, Myristicaceae and Rhizophoraceae are work. They are thankful to Prof. E.A. Wheeler of North Carolina State typical pantropical megatherm families [60] whose presence in the University, USA for sending her valuable reprints. The authors are also palaeoflora provides an evidence that the CMT (mean tempera- grateful to Prof. Khum Paudiyal, one anonymous reviewer and Prof. ture of the coldest month) was at least not less than 18uC [25]. Navnith K.P. Kumaran for their valuable suggestions in improving the Similarly, the presence of most dominant family Fabaceae [17] manuscript. whose abundance and richness covary with the temperature [61], indicates warm climate. The occurrence of families Avicenniaceae Author Contributions and Rhizophoraceae is also very significant in terms of the Conceived and designed the experiments: GS RCM. Performed the depositional environment. These families are highly indicative of experiments: GS RCM. Analyzed the data: GS RCM. Contributed deltaic, mangrove or lacustrine deposition of coal seams and reagents/materials/analysis tools: GS RCM. Contributed to the writing of associated sediments in the Makum Coalfield [15]. The abun- the manuscript: GS RCM.

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