Coryphoid Palm Leaf Fossils from the Maastrichtian–Danian of Central India with Remarks on Phytogeography of the Coryphoideae (Arecaceae)

Premise of research A large number of fossil coryphoid palm wood and fruits have been reported from the Deccan Intertrappean beds of India. We document the oldest well-preserved and very rare costapalmate palm leaves and inflorescence like structures from the same horizon. Methodology A number of specimens were collected from Maastrichtian–Danian sediments of the Deccan Intertrappean beds, Ghughua, near Umaria, Dindori District, Madhya Pradesh, India. The specimens are compared with modern and fossil taxa of the family Arecaceae. Pivotal results Sabalites dindoriensis sp. nov. is described based on fossil leaf specimens including basal to apical parts. These are the oldest coryphoid fossil palm leaves from India as well as, at the time of deposition, from the Gondwana- derived continents. Conclusions The fossil record of coryphoid palm leaves presented here and reported from the Eurasian localities suggests that this is the oldest record of coryphoid palm leaves from India and also from the Gondwana- derived continents suggesting that the coryphoid palms were well established and wide spread on both northern and southern hemispheres by the Maastrichtian–Danian. The coryphoid palms probably dispersed into India from Europe via Africa during the latest Cretaceous long before the Indian Plate collided with the Eurasian Plate.


Introduction
Palms (Arecaceae/Palmae) are considered an important and characteristic component of tropical rainforest ecosystems having a pantropical distribution [1]. The family has been placed within the commelinid clade of the monocotyledons [2,3], and is composed of five subfamilies: Arecoideae, Calamoideae, Ceroxyloideae, Coryphoideae and Nypoideae [4,5]. The family comprises 188 genera and about 2600 species [5,6,7]. Palm species richness is the highest in tropical Asia (.1200 species) and the higher in the Americas (730 species) than in Africa (only 65 species) [5]. It has been suggested that the low diversity of palms in Africa in contrast to Asia and America is due to Neogene aridification in Africa [8]. However, recent studies suggest in situ diversification in other regions like Asia and America etc [9,10]. In Indian subcontinent, palms consist of 20 genera and 88 species [5] with 24 species belonging to 9 genera endemic [11]. Among the five subfamilies of the Arecaceae, Coryphoideae is sister to a clade comprising Arecoideae and Ceroxyloideae. Asmussen et al. [12] considered Coryphoideae as one of the earliest diverging members of Arecaceae from which both pinnate and palmate leaves may have evolved. However, Baker and Couvreur [9,10] on the basis of molecular data suggest that the divergence of Coryphoideae occurred at about 87 Ma (95% HPD [86][87][88] in Laurasia in which Sabalites carolinensis Berry described from the late Coniacianearly Santonian (85.8-83.5 Ma) of South Carolina, USA was used as a calibration point [13]. Kvaček and Herman [14] recorded S. longirachis Kvaček and Herman from the early Campanian of Austria. A large number of fossil records attributed to Coryphoideae in the form of fruit and wood are also reported from the Deccan Intertrappean sediments. These are: Hyphaeneocarpon indicum Bande, Prakash and Ambwani [15], Palmocarpon coryphoidium Shete and Kulkarni [16], Palmocaulon costapalmatum Kulkarni and Patil [17], P. hyphaeneoides Shete and Kulkarni [18], Palmoxylon coryphoides Ambwani and Mehrotra [19] and P. hyphaeneoides Rao and Shete [20].
Here we report very rare and well-preserved costapalmate palm leaves under the organ genus Sabalites (S. dindoriensis sp. nov.) from the Deccan Intertrappean sediments (Maastrichtian-Danian) of Central India. This is the oldest fossil record of costapalmate palm leaves from India and the Gondwana-derived continents. The locality bearing the fossils was situated in a low palaeolatitude ,18.09u S near the equator (Fig. 1) [21] when the leaves were deposited. Attempts have also been made to discuss the origin and phytogeography of the subfamily Coryphoideae in Indian context.

The Deccan Traps: a brief review
The Deccan Traps (Continental Flood Basalt) are one of the largest igneous provinces of the world. The area occupied by the Deccan Traps today is about 500,000 sq km in peninsular India which includes Andhra Pradesh, Gujarat, Karnataka, Madhya Pradesh and Maharashtra ( Fig. 2A). The original stretch may have been over 1.5 million sq km including sediments found in the Arabian Sea to the west of Mumbai [22]. The outpouring of magma/lava was associated with the northward voyage of the Indian Plate after it was separated from Gondwana during the Early Cretaceous and moved over the Reunion Hot Spot situated east of Madagascar in the Indian Ocean [23,24]. The extensive volcanic eruptions with associated magma and lava outpouring that formed the Deccan Traps and associated sedimentary beds has been difficult to date and thus is an active topic of discussion among geologists and palaeontologists. Recent studies based on 40 Ar/ 39 Ar dating indicate that the duration of the volcanism extended from 69-61 Ma and the major eruptions took place between 67-65 Ma [25,26] rather than a short duration of only one million years [27].
The sedimentary sequences between two successive magma/ lava flows were deposited in lacustrine, fluviatile and palustrine environments during quiescent (inactive) phases of volcanic activity mainly while the Indian Plate was still an isolated land mass moving toward Asia. These are repeated episodic events resulting in the multiple sequences of fossiliferous beds and basalts. The fossiliferous sediments of the intertrappean beds are exposed mainly in Central India, western India and to the south in parts of Andhra Pradesh and Karnataka, including Rajahmundry ( Fig. 2A). The age of the Deccan Intertrappean beds was previously thought to be early Palaeogene due to the abundance of angiospermous remains [28,29]. However, microfloral studies and faunal assemblages suggest a Maastrichtian age for most of the intertrappean exposures but there are a few Palaeocene indicators [30][31][32][33]. Currently, based on radiometric dating and planktonic foraminifera, the age of the intertrappean sediments is considered to be upper Maastrichtian-Danian [34][35][36][37].
Recent studies of the sedimentary sequences associated with the Deccan Traps (both Infratrappean and Intertrappean) have been conducted to resolve their role in mass extinction at the K-Pg boundary. Cripps et al. [38] working on Mumbai Intertrappeans concluded that volcanic activity had hardly any effect on the floristic elements. However, pollen analysis shows distinct floral changes at different stratigraphic levels [32,33].
The flora reported from Deccan Intertrappean beds is unique and one of the richest fossil plant assemblages in India. The fossil plant assemblage includes all the plant groups ranging from algae to angiosperms [39]. Most of the fossil flora (mainly angiosperms) from intertrappean beds is reported from Central India (Madhya Pradesh and Maharashtra) with only a few elements of the flora reported from western India [40][41][42]. The majority of the plant macrofossils reported from the Deccan Traps are permineralized woods, fruits with only a few leaf impressions [39], however, microfossils have also been recorded [33].

Materials and Methods
The fossil palm leaves were collected from Umaria near Ghughua (23u 7' N; 80u 37' E), in the premises of Ghughua Fossil National Park, Dindori District, Madhya Pradesh. The fossil site is situated about 76 km east of Jabalpur and spreads over an area of 27.34 ha in Ghughua and Umaria villages (Fig. 2B). The locality is very rich in permineralized angiospermous woods (both palms and eudicots), but leaves and other plant organs are rarely preserved and thus very rarely found. The studied fossil leaf specimens were first cleaned with a chisel and hammer and then photographed in natural low angled light using a 10 megapixel digital camera (Canon SX110). All the figured fossil specimens (Specimen nos 40073-40077) are housed in the repository of Birbal Sahni Institute of Palaeobotany, Lucknow, India. The fossil leaves were compared with the nearest living relatives in the herbaria of the Central National Herbarium, Howrah, Forest Research Institute, Dehradun, National Botanical Research Read and Hickey [43] gave five basic characters of palm leaves that can be used alone, or in various combinations to differentiate fossil palm leaves. We followed their classification and placed our specimens in the genus Sabalites G. Saporta [44] emended Read and Hickey [43], which they proposed for costapalmate fossil palm leaves.
Etymology. The specific epithet is named after the fossil locality. Holotype

Diagnosis
Leaves costapalmate. Costa/petiole very thick at the basal portion and gradually tapers towards apex, petiole robust, unarmed; a number of longitudinal fibre like structures seen on the petiole/costa. Leaf segments plicate, emerging at an acute angle from costa; fused at emerging point. Mid-veins of each segment thick; two orders of veins on either side of mid-vein, segments near the petiole narrow becoming broader away from the petiole; transverse veins rarely preserved, very fine, perpendicular or obliquely oriented to parallel veins.
Description. The species is described based on the five specimens shown in The specimen in Figure 3C shows the middle portion with a preserved length of about 42.5 cm and a width of 14.5 cm. The costa is about 3.3 cm broad at the base and tapers to 0.7 cm distally. Leaf segments are preserved along both sides of costa but their terminal portions are broken. The segments are inserted on the costa and their maximum length is about 20 cm. The specimen illustrated in Figure 4C contains only plicate leaf segments with a few segments flattened on the rock surface. The detached segments have a maximum width of about 5.4 cm.   These leaf segments clearly show a distinct mid-vein with about 16 major parallel veins on either side of mid-vein, each with a minor vein between them (Fig. 4D).
Specimens (BSIP No. 40076 and 40077) are incomplete and broken. The preserved length is about 30 cm and the width is 7 cm each. The costa tapers gradually from 0.9 cm to 0.3 cm along the apex (Fig. 5A). All the leaf segments are preserved incompletely near the costa; numerous 2u veins run parallel on either side of the midrib.
Also present in this specimen is a poorly preserved impression of a rachilla-like structure (Figs 5A-C) with a preserved length of 9 cm and a width of 1.4 cm. This axis is reminiscent of an inflorescence after the spirally arranged flowers were abscised with striated bracts probably adanate to axis. A spatulate rachillar bract of preserved length 6.6 cm and width 1.4 cm is present adjacent to the floral axis having numerous parallel veins (Figs 5A-C).
Affinities. The diagnostic features of the fossil leaves include: palmate, plicate leaves with long costa (costapalmate) and unarmed petiole. These characters suggest that the fossil leaves have affinities with the subfamily Coryphoideae in the Arecaceae [5]. A number of palm taxa were examined at the Central National Herbarium, Howrah, Forest Research Institute, Dehradun, National Botanical Research Institute, Lucknow and the website of Royal Botanic Gardens, Kew [45] to find species with similar characters. The fossil leaves show resemblance with a number of coryphoid palms with costapalmate leaves in gross morphology such as Bismarckia nobilis Hildebr. & Wendl., Borassus aethiopum Mart., B. flabellifer L., Corypha taliera Roxb., Hyphaene coriacea Gaertn. (Fig. 6) from the present fossil. The inflorescence like structure of the fossil shows a close resemblance with the Hyphaene Gaertn. by having characteristic shape, striated bracteoles and spatulate large bract associated with floral axis which also gets support from the previous fossil records of Hyphaene from the same horizon [15,18,20]. However, due to the lack of spines on the petiole of fossil it cannot be assigned exactly to the modern taxa. As Read and Hickey [43] stated that ''Since it is very difficult to identify specimens of modern palms accurately from their leaves alone, no attempt should be made to place fossil palm fragments in genera of modern palms unless unquestionably identifiable with them''. Under these circumstances the fossils are placed in the organ genus Sabalites G. Saporta [44] proposed for costapalmate fossil leaves.
A number of palm leaves have been described from Upper Cretaceous-Neogene deposits of India under various fossil taxa (table 1) . The species attributed to Amesoneuron (Goeppert) Read and Hickey [47][48][49][50][51][52][53] cannot be compared with the leaves under consideration as they are isolated fragments of lamina with parallel veins but the fragments are not attached to main rachis making it impossible to determine whether they belong to pinnate or palmate leaves. Malpophyllum dakshinens [58] is based on anatomical features and Malpophyllum sp. [58] is based on a very fragmentary specimen in which costa and other characteristic features are not preserved.
Palmate leaf fossil taxa reported from Indian Upper Cretaceous-Neogene sediments includes Palmacites, a taxon for leaves lacking primary costa. Costapalmate forms referred to Sabalites and Sabalophyllum and two specimens placed in the modern genera, Livistona and Trachycarpus. The Palmacites species (Palmacites sp. [50], P. makumensis Srivastava, Mehrotra and Bauer [57], P. khariensis Lakhanpal and Guleria [61], P. tsokarensis Paul et al. [62]) lack a costa and therefore differ from Sabalites dindoriensis. Sabalophyllum livistonoides Bonde [68] is based on a petrified leaf with anatomical features and therefore it could not be compared with S. dindoriensis. Sabalites microphylla Sahni [66] and Sabalites sp. [67] are fragmentary palmate leaves not attached to petiole, so it is not clear whether they are costapalmate. Trachycarpus ladakhensis Lakhanpal et al. [69,70] lacks primary costa. Livistona wadiai Lakhanpal et al. [56] is the only costapalmate leaf reported from late Eocene-Oligocene sediments of Ladakh Himalaya, it is a smaller leaf with thin costa and narrower leaf segments.
In a detailed work on coryphoid palms from the Eocene of Texas, Daghlian [72] reported a number of fossil palm leaves under various fossil taxa, namely, Costapalma, Palmacites, Palustrapalma, Sabal and Sabalites based on cuticular features. But none of them show morphological resemblance with the leaves of Sabalites dindoriensis. Recently, Zhou et al. [73] reported many coryphoid palm leaves from the Eocene of southern China. But all the specimens are much smaller in size, with intact cuticular structures and short costa. Besides, the fossil records of palms are abundant worldwide and it is not possible to explore all of them here. Therefore, we compare Sabalites dindoriensis with those fossil costapalmate leaves that are most similar. Sabal chinensis (Endo) Huzioka and Takahashi [74] from the Eocene of Northeast China, Japan and Russia is similar to the basal part of one specimen (Fig. 3A, BSIP Museum no. 40073) in having a thick stout unarmed petiole extending into the lamina (costapalmate) and leaf segments fused at their emerging point. It differs from the present species by having a shorter costa with narrower segments. The specimens of the middle and apical portions of Sabilites dindoriensis (Figs 3C, 4A-D and 5A BSIP Museum nos 40074-40077) show a close resemblance to S. longirachis [14] reported from the early Campanian of Austria and Maastrichtian of the Pyrénées [75] in having a thick long costa and segments with a similar angle of attachment. However, this species is based on cuticular features and fine venation, none of which are preserved in S. dindoriensis leaves. Therefore, in the absence of any similar leaves we propose the new species, Sabalites dindoriensis R. Srivastava, G. Srivastava and D. L. Dilcher sp. nov.

Modern distribution of palms and their ecology
Palms are largely distributed and diversified in tropical areas [5,76] with 90% of the species diversity restricted to tropical rainforest [1]. They are much less prominent and diverse in temperate regions [5,77,78], thus showing very restricted frost tolerance [77]. The low frost tolerance of palms is considered to be an evolutionarily conserved trait. Their architecture and more notably a crown composed of large evergreen leaves [79], which has limited frost resistance [80] and unique stem physiology doesn't allow dormancy [81]. Palms also exhibit a strong latitudinal diversity gradient [82] and need water accessibility for their survival [5,83]. Palms grow mainly under the top canopy of tropical rain forests along low hills and streams in warm and humid conditions, while a few grow in open areas. They are also dominant in coastal swamps and mangrove forests [8,84]. Studies of new world palms indicate that solar radiation as related to absolute latitude and water is the main factor that determines the richness of palms species [85]. However, the subfamily Coryphoideae is distributed in a wider range of habitats such as pantropical to warm temperate areas of the world (Fig. 7). It is also found in climatic extremes such as cold and arid regions [5].
Origin and possible migratory path of the Coryphoideae from the Northern Hemisphere to Indian subcontinent Phylogenetic and molecular clock studies indicate that the palms originated and diversified in Laurasia around 100 Ma [1,10] while the coryphoids diverged at about 87 Ma (95% HPD [86][87][88] which was constrained by the calibration point from a Sabalites fossil [9,10] and diversified during the Late Cretaceous to Cenozoic in boreotropical regions [5,86]. The subfamily Coryphoideae includes four major clades including (1) New world thatch palm  (4) tribe Trachycarpeae [5,87]. Based on molecular phylogenetic analysis, Baker and Couvreur [9] suggested that the New world thatch palm clade diverged at 55 Ma (95% HPD  in North America. The Syncarpous clade diverged in Eurasia at 66 Ma (95% HPD . The tribe Phoeniaceae diverged from Trachycarpeae around 49 Ma (95% HPD  in Eurasia. Out of the four aforesaid clades, the syncarpous clade is the earliest diverging clade (66 Ma) that also corresponds to the age of Deccan Intertrappean beds to which our fossils belong. In syncarpous clade, the Caryoteae can be differentiated from the present fossil by having pinnate or bipinnate leaves while amongst Chuniophoeniceae, Coryphae and Borasseae the fossil probably shows near resemblance with floral axis of Hyphaene (Borasseae) by having the characteristic shape and striate bractioles which also corroborate with the previous fossil records of Hyphaene from the same horizon [15,18,20]. In the subsequent study Baker and Couvreur [10] suggested that only one dispersal event occurred from Indian Ocean into India (including Sri Lanka) during the Miocene but the palm fossils reported from the Maastrichtian-Danian sediments of Deccan Intertrappean beds [39] opens a new dispersal route (Fig. 8).
The oldest fossil records of Coryphoideae are reported from the Northern Hemisphere, such as: Sabalites carolinensis [13] from late Coniacian-early Santonian of South Carolina and Sabal bigbendense Manchester, Lehman and Wheeler [88] from Maastrichtian of Texas, USA. Sabalites longirhachis [14] were reported from the lower Campanian of Austria and from the Maastrichtian of the Pyrénées [75].
The fossil records show that the continent of Africa and India possessed much richer palm flora in the past than at present. In Africa, there are definite evidences of palm pollen from the Campanian (83.5-70.6 Ma) and they became much abundant and more diverse during the Maastrichtian (70-65.5 Ma). This period is referred as 'Late Cretaceous Palm Province' [8,89]. The subfamilies such as Nypoideae and Calamoideae have been recorded from the Maastrichtian [90,91], the Coryphoideae in the form of seed has been recorded from the Danian (65.5-61.7 Ma) sediments of Egypt [92]. A large number of fossils attributed to Coryphoideae have been reported from the Deccan Intertrappean sediments such as: Hyphaeneocarpon indicum [15], Palmocarpon coryphoidium [16], Palmocaulon costapalmatum [17], P. hyphaeneoides [18], Palmoxylon coryphoides [19] and P. hyphaeneoides [20]. It is interesting to note that several of the Palmoxylon species reported from the Upper Cretaceous sediments of the Indian subcontinent [66] have also been reported from the late Eocene to early Miocene sediments of Egypt [93]. All the above fossil records and the similarity in coryphoid fossil palm records between India and Africa suggest that the coryphoid palms probably dispersed into India from Europe via Africa. During the Early Cretaceous the Indian plate was separated from the other Gondwana continents and moved northward. It collided with the Kohistan-Ladakh arc at ,85 Ma (an island like structure) re-establishing the land connection between India and Africa ,70 Ma [24]. This facilitated the interchange of various plants and also several Maastrichtian dinosaurs [24]. During the Campanian-Maastrichtian, Africa was also connected with Europe by land [94], which most likely facilitated the entry of coryphoid palms from Europe to Africa. Thus, the migration model of coryphoid palms we propose (Fig. 8) fits well with the plate tectonic models. However, with the aforesaid model, long distance oceanic dispersal cannot be ruled out [9,10]. In future better preserved palm fossils assignable to modern genera are needed to further strengthen the proposed model.