Dietary and habitat shifts in relation to climate of Neogene-Quaternary proboscideans and associated mammals of the Indian subcontinent

Quaternary Science Reviews 224 (2019) 105968

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Dietary and habitat shifts in relation to climate of NeogeneQuaternary proboscideans and associated mammals of the Indian subcontinent Rajeev Patnaik a, *, Ningthoujam Premjit Singh a, Debajyoti Paul b, Raman Sukumar c a b c

Center for Advanced Study in Geology, Panjab University, Chandigarh, 160014, India Department of Earth Sciences, Indian Institute of Technology, Kanpur, 208016, India Centre for Ecological Sciences, Indian Institute of Science, Bengaluru, 560012, India

a r t i c l e i n f o

a b s t r a c t

Article history: Received 31 March 2019 Received in revised form 8 September 2019 Accepted 24 September 2019 Available online xxx

Several studies have established that African proboscideans shifted their feeding strategies (browsing vs. grazing) in response to climatic and ecological changes. However, similar studies on their Indian relatives are rare. In this regard, we analysed the stable carbon (d13C) and oxygen (d18O) isotope composition, hypsodonty indices (HI), and lamellae numbers of both newly recovered and existing fossil material (proboscideans and associated mammals) spanning the last ~14 Ma. We also obtained intra-tooth d13C and d18O values of selected extant and extinct proboscideans as well as associated mammals to understand any intra- and inter-annual variation in dietary and water intake behaviour, respectively. Our results reveal that Middle Miocene brachydont deinotheres (ex. Deinotherium indicum) and bunodont gomphotheres (ex. Gomphotherium) with few cusp pairs were browsers living in relatively closed forests under moist conditions. By Late Miocene they continued browsing in relatively open forests. Deinotheres in the subcontinent did not survive the Late Miocene climate change that led to drier conditions and the spread of grasslands. The Late Miocene endemic forms Stegolophodon and Stegodon were browsers while the immigrant Choerolophodon was a mixed feeder. However, Pliocene gomphotheres such as bunodont Anancus and brachydont Stegodon adapted themselves to shrinking forests and spreading grasslands; the former sustained on grazing, whereas the latter showed flexibility in its diet ranging from browsing, mixed-feeding to pure grazing. Associated mammals such as rhinoceratids, giraffids, equids, and bovids responded in a similar manner to this climatic and ecological transition across the Late Miocene to Pliocene by shifting their diets accordingly. The Mid-Pliocene hypsodont elephantid immigrant Elephas planifrons, the Early Pleistocene hypsodont immigrant E. hysudricus, and Elephas platycephalus, with multiple lamellae (10e16) were also essentially grazers. Sometime around Middle Pleistocene, the giant elephantid immigrant Palaeoloxodon namadicus, a pure grazer, appeared on the grasslands of the subcontinent, coinciding with a shift in E. hysudricus diet from pure grazing to browsing. E. hysudricus likely gave rise to the extant E. maximus, a mixed feeder with higher contribution of browse to its diet. © 2019 Elsevier Ltd. All rights reserved.

Keywords: Stable isotopes Hypdodonty index Lamellar counts Proboscideans Neogene Quaternary Diet

1. Introduction Proboscideans are essentially Afrotheres, i.e. they originated in Africa. It is only in the early Miocene ~20 Ma that they arrived in the Indian subcontinent when the Afro-Arabian plate collided with € gl, 1998; Koufos et al., 2003; Harzhauser et al., 2007). Eurasia (Ro Appropriately, this semi-permanent early connection is referred to

* Corresponding author. E-mail address: [email protected] (R. Patnaik). https://doi.org/10.1016/j.quascirev.2019.105968 0277-3791/© 2019 Elsevier Ltd. All rights reserved.

€ gl, 1998) that allowed as the “Gomphotherium Landbridge” (Ro faunal exchange between the continents repeatedly (Patnaik, 2016). Beside Gomphotherium, Deinotherium was an early Miocene immigrant, followed by Zygolophodon and Choerolophodon. Stegolophodon probably evolved in the subcontinent from Gomphotherium in the Middle Miocene and so did Stegodon in the latest Miocene (Van Der Made, 2010; Johnston and Sanders, 2017). Elephantids of African origin arrived in the Indian subcontinent during the Pliocene ~3.5 Ma in the form of E. planifrons which, in turn, was joined by E. hysudricus independently derived from the African E. ekorensis-recki complex during the latest Pliocene ~2.7 Ma

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(Maglio, 1973). The latest immigrant was the giant Palaeoloxodon arriving in the subcontinent sometime around Middle Pleistocene (Van Der Made, 2010 and references therein). Elephants being mega-herbivores, influence the surrounding ecology and associated mammalian species significantly (OwenSmith, 1987). Conversely, climate-induced variability in the regional ecology often forces them to move long distances in search of their preferred forage plants (Sukumar, 1989, 2003). The Asian elephant Elephas maximus is basically a mixed feeder with a higher contribution of organic carbon from browse (C3 plants) as reflected in the carbon isotope compositions of bone collagen (Sukumar, 1989; 2003; Sukumar and Ramesh, 1992; Pushkina et al., 2010; Rivals et al., 2012). Today, this solitary extant species of Elephas occupies about 0.5 million km2 of South and Southeast Asian forests (Sukumar, 2003). In the past, however, the Indian subcontinent was home to several proboscidean species that had a varied feeding ecology (Cerling et al., 1999; Patnaik et al., 2014a,b). The evidence of dietary and ecological preferences comes from proboscidean dental morphology such as hypsodonty indices, lamellar number counts (Maglio, 1973; Lister, 2013) and stable carbon (d13C) and oxygen (d18O) isotope composition of dental enamel (Quade et al., 1992; MacFadden and Cerling, 1996; Koch et al., 1998). Hypsodonty, the development of high-crowned molars in herbivore mammals, has long been interpreted as an adaptation to grazing. Conversely, low-crowned teeth are generally considered to be meant for browsing. However, it has been observed that this is not always the case, particularly analysing the African Neogene proboscidean hypsodonty versus isotope-based diet record (Lister, 2013), where some brachydont proboscideans such as the

gomphotheres shifted from browsing to grazing and others such as the deinotheres did not when a forest dominated landscape changed to a grassland dominated one. Such anomalies have also been recorded in the Neogene and Quaternary record of East and Southeast Asia (Wu et al., 2018; Suraprasit et al., 2018). Although, the Indian subcontinent Neogene-Quaternary wealth of mammalian fauna is well known, there has hardly been any study on proboscideans to compare their hypsodonty vis a vis dietary changes using stable isotope compositions as described earlier. Another important morphological adaptation from browsing to grazing among the African proboscideans has been the fusion of cusps into lophs or lamellae followed by their significant increase in numbers (Lister, 2013). Therefore, in order to understand the diet and habitat of proboscideans of the Indian subcontinent in space and time, we analysed hypsodonty index (HI), multiplication of lamallae numbers, and d13C and d18O of dental enamel recovered from modern as well as extinct elephant species. We also performed stable isotope analyses of tooth enamel from some associated mammals to get a better perspective of the ecological milieu of these proboscideans. 2. Fossil localities and their ages The freshwater Siwalik deposits, almost 6 km in thickness, are exposed all along the Himalayan foothills from the Brahmaputra River in the east to Potwar Plateau of Pakistan in the west (Fig. 1). Famous for their mammalian fossils including proboscideans, these sediments range in age from ~18 Ma (Johnson et al., 1985) to ~0.22 Ma (Ranga Rao et al., 1988). The Siwaliks have been classified

Fig. 1. Type localities and proboscidean yielding localities of Siwaliks and Karewas.

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as Lower, Middle and Upper Siwaliks, by Medlicott (1879) followed by Pilgrim (1910, 1913) who further divided them as Kamlial, Chinji, Nagri, Dhok Pathan, Tatrot, Pinjor and Boulder Conglomerate Formations, based mainly on their faunal content. The type sections of Lower and Middle Siwaliks and Tatrot Formation of Upper Siwaliks lie in Potwar Plateau, Pakistan. The type sections of Pinjor and Boulder Conglomerate Formations of the Upper Siwalik are situated in the Indian part. These two type sections are exposed along the banks of Ghaggar River in Panchkula (Harayana) near Chandigarh. The Plio-Pleistocene Himalayan inter-montane Karewa sediments of Kashmir Valley have also yielded elephantids (Kotlia, 1990). In the peninsular part of India identifiable fossil proboscideans occur in Miocene deposits of Kutch, Perim Island, Gujarat and Bokabil, Tripura, and Narmada, Son and other river valleys of Pleistocene age (see Chauhan, 2008; Patnaik, 2016 and references therein). Our

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samples were recovered mainly from Ramnagar, Haritalyangar, Kangra, Chandigarh, Karewas, Kutch, and Narmada Valley (Figs. 1 and 2). The Ramnagar locality is situated 70 km north east of Jammu town (Fig. 1). The red beds exposed around Ramnagar belong to Chinji Formation, which are of Middle Miocene age and range from 14.2 to 11.2 Ma in the Potwar Plateau of Pakistan (Barry et al., 2002). The mammalian fauna including primates and proboscideans (gomphotheres and deinotheres) represented at Ramnagar are very similar to those of Chinji in the Potwar, and therefore, have been placed between ~ 14 and 12.7 Ma (Sehgal and Patnaik, 2012; Gilbert et al., 2014). The magnetostratigraphically dated Haritalyangar locality (10.1e8.5 Ma) is famous for its mammalian diversity that includes the primates. Among the proboscideans, Deinotherium, Anancus,

Fig. 2. Proboscidean yielding sites tied to palaeomagnetically dated sections (after Ranga Rao et al., 1995; Tandon et al., 1984; Pillans et al., 2005; Sangode et al., 2003; Kumaravel et al., 2005). The Ramnagar and Kutch localities are tentatively placed based on biochronology (Gilbert et al., 2014; Bhandari et al., 2015).

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Tetralophodon, Choerolophodon, and Stegolophodon have been reported from this locality (Patnaik, 2013 and references therein). The sediments here belong to Late Miocene Nagri and Dhok Pathan Formations similar to those in the Potwar of Pakistan (Barry et al., 2002; Colbert, 1935; Raza, 1997). Younger sediments, most probably belonging to the Upper Alterations of Dhok Pathan Formation exposed near Haritalyangar, have recently yielded Stegodon, Choerolophodon, and Stegolophodon (Sankhyan and Chavasseau, 2018). These deposits could be as young as 6.5 Ma based on the early occurrence of Stegodon and the last appearance datum of Choerolophodon (Sankhyan and Chavasseau, 2018). The Chandigarh region has been extensively studied for mammalian remains since 1836 (Baker and Durand, 1836). Sahni and Khan (1964) were the first to report these pre-Pinjor ‘Tatrot beds’ from this region. The presence of Hipparion and Proamphibos, and complete absence of Equus and Bubalus are considered to be characteristic of the Tatrot Fauna. Nanda (2002) recognized two biostratigraphic interval zones for the Upper Siwalik Elephas planifrons IntervaleZone (3.6e2.6 Ma) and Equus sivalensis Interval e Zone (2.6e0.6 Ma). E. hysudricus is most common taxon of the latter interval-zone. Palaeomagnetic dating of continuous sections here have provided a better time frame to the rich assemblage (Ranga Rao et al., 1995; Tandon et al., 1984). The Tatrot Formation here has yielded Anancus, whereas the Pinjors of the region are known for Stegolophodon stegodontoides, Stegodon pinjorensis, E. hysudricus and E. platycephalus (Nanda, 2013). In Kutch (Gujarat, western India), Neogene terrestrial mammals including proboscideans such as Deinotherium and Gomphotherium are known to occur with marine fossils that have been biochronologically dated to 16.5 ¼ ± 0.5 Ma to ~11-10 Ma (Bhandari et al., 2010; Patnaik et al., 2014; Bhandari et al., 2015). The Karewa inter-montane basin, comprises of ~ 1 km thick PlioPleistocene glaciofluvial and lacustrine sediments ranging in age from ~4 Ma to 200 Ka (Kotlia, 1990 and references therein) and are commonly divided into the Lower and Upper Karewa Formations. This basin has yielded Elephas hysudricus from Romushi and Sombur sections that are <730 Ka (Kotlia, 1990). The Narmada Valley is one of the richest sites in the Peninsula and has yielded the only partial cranium of archaic Homo sapiens along with a diverse set of fauna (see Chauhan, 2008 for a review). Patnaik et al. (2009) constrained a time frame of ~50 Ka to ~160 Ka for the elephantid-bearing (Palaeoloxodon namadicus) lower unit belonging to the Surajkund Formation. 3. Stable isotopes and dietary and habitat reconstruction 3.1. Carbon isotopes It is now well established that the stable carbon isotope composition (d13C value) of body tissue of extant herbivores reflect the type of flora/vegetation (C3 vs. C4) they consume. The tooth enamel, the hardest biological tissue of all, is dense and is less susceptible to diagenetic alteration compared to bones, which therefore is ideal for reconstructing ancient diet, habitat and climatic changes (Cerling et al., 1997a, b; Lee-Thorp et al., 1989). Therefore, the d13C value of dental enamel of extinct herbivores that are millions of years old can yield accurate information about their diet and habitat (Deniro and Epstein, 1978; Van Der Merwe and Vogel, 1978; Van Der Merwe, 1982; Lee-Thorp and Van Der Merwe, 1987; Lee-Thorp et al., 1989; Quade et al., 1995; Cerling et al., 2003a, b; Nelson, 2003). The two stable isotopes of carbon, 13 C and 12C, are differentially assimilated by various plants, which in turn gets transferred into the body tissues, including bones and teeth of animals feeding onto them (Deniro and Epstein, 1978). Terrestrial plants follow three types of metabolic pathways to fix

CO2 from the atmosphere: the C4 photosynthesis pathway (HatcheSlack cycle); the C3 photosynthesis pathway (the Calvin Cycle); and the CAM (Crassulacean Acid Metabolism) pathway (Ehleringer et al., 1991; Bender, 1971; Farquhar et al., 1989; O’Leary, 1988). Due to their differential physiology, the C3 and C4 photosynthetic pathways exhibit different d13C values with most C4 plants (tropical grasses and sedges) falling between 10‰ and 15‰ and most C3 plants (most trees, shrubs, and highaltitude or high-latitude grasses) between 22‰ and 35‰ (Bender, 1971; Vogel, 1980). CAM plants (desert succulents) yield d13C values between 10‰ and 20‰, partially overlapping the range of C4 plants (O’Leary, 1988; Skrzypek et al., 2013). The distinct isotopic composition of C3 and C4 plants translates to a distinct isotopic signature in tooth enamel carbonate that can be used as a proxy for browsing (mostly C3) versus grazing (mostly C4) diet of animals, environmental conditions such as warm tropical low lying areas where high altitude and cool season C3 grasses do not exist. However, presence of minor (1e3%) C3 grasses including bamboo (similar isotopic composition as C3 plants) in the Siwaliks cannot be ruled out (Lakhanpal et al., 1987; Nelson, 2007). CAM plants are not expected to be a significant part of the diet of most ancient and modern proboscidean populations. Metabolic pathways in an animal increases the d13C values in the dental enamel apatite relative to plant tissue they consume. Different digestive systems of herbivores (ruminant vs. nonruminant) fractionates C-isotopes resulting in a 12e14‰ increase in the d13C of enamel apatite relative to that of the ingested plants (LeeThorp and Van Der Merwe, 1987; Lee-Thorp et al., 1989; Cerling and Harris, 1999; Passey et al., 2005). In the present study, we adopt an enrichment factor of 14‰ as per Cerling and Harris (1999) who undertook a comprehensive analysis of ungulates. However, a recent study on a variety of mammals suggests that this factor can vary significantly depending upon body mass (Tejada-Lara et al., 2018). For proboscideans and other large-bodied herbivores, d13C of enamel ranging from 21‰ to 8‰ reflect a pure C3 diet, between 2‰ and 3‰ a pure C4 diet, and between 8‰ and 2‰ a mixed C3eC4 diet (Cerling and Harris, 1999; Cerling et al., 2003a, b). Further, the herbivores that feed in closed canopy forests are expected to have lower d13C values compared to those feeding in more open environments due to the recycling of respired CO2 (13C depleted) on the forest floor and low light intensities at ground level that results in more negative d13C values in plants (Cerling et al., 2004; Van Der Merwe and Medina, 1991). In the present study, d13C values more negative than 14‰ in tooth enamel have been considered to represent sub-canopy browsing in multi-tiered, closed forests, 14‰ to 12‰ for browsing in forest, 12‰ to 8‰ for browsing in woodlands, and 8‰ to 3‰ for the mixed feeding and/or grazing in more open habitats (Cerling et al., 1997a, b, 2004; Kohn et al., 2005). Modern d13C values are generally depleted by ~1.5‰ relative to Late Miocene values due to a shift in atmospheric d13C since the Industrial Revolution and burning of fossil fuels. Therefore, a value of 8‰ today, is comparable to a Late Miocene value of 6.2‰ or a pre-industrial average of 6.5‰ (Cerling et al., 1997a, b; Passey and Cerling, 2002; Tipple et al., 2010). 3.2. Oxygen isotopes Palaeoecological and palaeoenvironmental interpretation based on d18O of dental enamel is not straight forward because of the complexity of oxygen flux in mammals. However, it is very useful in reconstructing the diet and habitat preferences as well as seasonality conditions (Fricke and O’Neil, 1996; Longinelli, 1984). The d18O of tooth enamel depends upon the body water which, in turn, is controlled by the d18O of ingested water. The d18O of ingested water is influenced by precipitation, latitude, altitude, aridity and

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evaporative processes, and physiological and behavioural water conservation factors as well as metabolic processes of the mammals (Kohn, 1996; Kohn et al., 1996; Luz and Kolodony, 1985; Luz et al., 1984). The d18O of mammals that frequently drink water depend on d18O of rainfall; drought-tolerant animals usually have relatively higher d18O values because of 18O enrichement of environmental water due to evaporation (Ayliffe and Chivas, 1990; Kohn et al., 1996; Levin et al., 2006). The variation in d18O of water has been attributed to environmental temperature changes, leading to the enrichment of 18O in warmer conditions and relative depletion in cooler conditions (Bryant et al., 1996). Thus, summer is characterized with higher d18O of water whereas winter has lower d18O in temperate regions. However, in the tropical regions, where the environmental temperatures remain above 20  C, the “amount effect” dominates, whereby lower d18O of water indicate periods of increased rainfall compared to higher values during drier periods (Dansgaard, 1964; Feranec and MacFadden, 2000; Higgins and MacFadden, 2004). However, under a monsoonal system, the effect of temperature is masked or dominated by the effect of precipitation amount. Due to kinetic fractionation, the more it rains, the less 18O is present in the atmospheric water, which in turn gets more depleted with further precipitation (Dansgaard, 1964). Monsoon experiences both monthly differences in temperature as well as rainfall. The rainfall is typically 18O-depleted during monsoonal months, in spite of high summer temperatures (Rozanski et al., 1993; Araguas-Araguas and Froehlich, 1998). This effect can be seen in the d 18O vs precipitation for Hong Kong and New Delhi (affected by monsoons) shown in SI Fig. 1. Amphibious mammals such as hippopotamus generally have lower d18O values compared to their terrestrial counterparts (Bocherens et al., 1996; Cerling et al., 2003b; Clementz et al., 2008). Warm season C4 grasses growing in open areas would generally have higher d18O values due to loss of d16O by transpiration compared to C3 plants growing in wetter and closed areas. Therefore grazers adapted to feeding on water stressed grasses that grow in drier conditions may generally yield higher d18O values than forest dwelling browsers (Bocherens et al., 1996; Sternberg et al., 1989). 3.3. Serial sampling of teeth and stable carbon and oxygen isotope analysis Teeth of herbivorous mammals, particularly those of high crowned ones such as horses, bisons and rhinocerotids, offer excellent opportunity to study dietary and environmental signals at a very high resolution (inter and intra annual) since they preserve isotopic record of 2e5 years span, the time required by the tooth to mineralize (Feranec and MacFadden, 2000; Kohn et al., 1998; Sharp and Cerling, 1998). Therefore, serial d18O values along the growth axis of unworn teeth of a mammal reflect the seasonal variation during the development of the tooth (Green et al., 2018). Serial sampling technique has been widely applied to extinct mammoths and mastodons in order to track their individual life history with signatures related to climate change, seasonal dietary shifts, and tooth enamel growth rates (Koch et al., 1998; Feranec and MacFadden, 2000; Metcalfe and Longstaffe, 2012, 2014; Ma et al., 2019). A low d18O of enamel would indicate a period with significantly high precipitation or humidity, for example during the rainy season, whereas higher d18O values would indicate a dry period with lower precipitation or aridity (Dansgaard, 1964; Feranec and MacFadden, 2000; Higgins and MacFadden, 2004). However, seasonal signals of enamel d18O vary from place to place depending upon latitude or if the temperature reaches close to or exceeds the amount effect threshold (Higgins and MacFadden, 2004). Similarly, the serial d13C values along the growth line of a tooth are

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informative of seasonal variation in foraging, availability of C3/C4 plants and temporal partitioning of food resources (Feranec and MacFadden, 2000; Sharp and Cerling, 1998). The molars of ungulate grazers wear down rapidly due to the presence of fibre, silica, dust, and grit in the grasses consumed. Therefore, hypsodonty in ungulates, i.e. increased height of molar crown has long been considered as an adaptation to eating abrasive forage such as grasses. Janis (1988) divided ungulates into dietary types based on their measured hypsodonty index (HI), which compares maximum unworn molar crown height to molar width. The low crowned (brachydont) ungulates were usually thought to be browsers, whereas the high crowned (hypsodont) ones were likely grazers (Janis, 1988). In the African Neogene-Quaternary elephant dietary record, Lister (2013) observed an interesting trend in hypsodonty vs diet. He found that some Miocene brachydont browsers such as gomphotheres turned to grazing on the grassland-dominated Plio-Pleistocene landscape. On the other hand, the elephantid Loxodonta with hypsodont teeth turned to mixed feeding and browsing. 4. Materials and methods In order to understand the changing diets and environment of ancestral proboscideans in relation to a changing climate, we analysed fossil proboscidean dental remains and those of associated mammals collected by us and previous workers from fairly well-dated Middle Miocene to Late Pleistocene localities in India (Figs. 1 and 2). Our analysis also includes data reported in earlier publications (e.g. Cerling et al., 1999; Patnaik et al., 2014) to cover a wider spectrum of these changes at the subcontinent level. We also carried out d13C and d18O analysis of present-day Elephas maximus teeth and those of some associated larger mammals such as Cervus unicolor (sambar deer), Axis axis (axis deer or chital), Bos gaurus (gaur), Sus scrofa (wild pig) and Semnopithecus priam (tufted gray langur) from southern India. The main reasons for choosing modern taxa were to compare their diet and habitat variability in a monsoonal climate to those of the extinct forms, and to infer whether any diagenetic alteration could have occurred in the selected fossil samples analysed in this study. We performed d13C and d18O analyses of 157 bulk and 141 serial samples belonging to various mammals collected from localities ranging in age from Middle Miocene to Latest Pleistocene (Tables 1e4; Supplementary Tables 1e8). Several of our samples are from the Plio-Pleistocene mammalian collection of Sahni and Khan (1964) and Nanda (1973), now housed at the Geology Museum of Panjab University, India. Since these specimens were not collected by us, we have assigned approximate dates to these samples based on a tentative placement of sites into the palaeomagnetically dated nearby sections. We also analysed recent mammalian teeth from Mudumalai National Park (Tamil Nadu) collected during an earlier study of mammalian ecology, including the isotopic ecology of E. maximus (Sukumar et al., 1987; Sukumar and Ramesh, 1992) done during the 1980s and early 1990s. This was undertaken to detect any seasonal variation in elephant diet and to understand niche partitioning of plant forage resources by large mammal species constituting most of large animal biomass of this tropical forest type. The seasonally dry tropical forests of Mudumalai receive rains during both summer and winter monsoons with seasonal variation in vegetation phenology and dietary quality (Sukumar et al., 2004; Sukumar and Ramesh, 1992). The enamel (~10 mg) was removed from the tooth using a diamond tipped rotary drill. The bulk samples were taken from each tooth perpendicular to the growth axis. The serial samples were collected from the teeth by cutting parallel grooves on the plate surface reaching the inner enamel surface (IES) at intervals of

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Table 1 Bulk and serial d13C and d18O values of selected Mudumalai mammals.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47

Specimen no.

Taxa

Tooth position

Locality

d13C VPDB

d18O VPDB

Wt. % CaCO3

%C4

E1/P1 E1/P2 E1/P3 E1/P4 E1/P5 E1/P6 E1/P7 E1/P8 E1/P9 E1/P10 E1/P11 E1/P12 E1/P13 E1/P14 E2/P1 E2/P2 E2/P3 E2/P4 E2/P5 E2/P6 E2/P7 E2/P8 E2/P9 E2/P10 E2/P11 E2/P12 E2/P13 E2/P14 E2/P15 E2/P16 E2/P17 G 1/P1 G 1/P2 G 1/P3 G 1/P4 G2 S 1/P1 S 1/P2 S 1/P3 C 150/P1 C 150/P2 C 50/P1 C 50/P2 SM 1 CES (N) SS 1 SS 2

Elephas maximus , , , , , , , , , , , , , Elephas maximus , , , , , , , , , , , , , , , , Bos gaurus , , , , Cervus unicolor , , Axis axis , Axis axis , Cervus unicolor Semnopithecus Sus scrofa Sus scrofa

Upper 2nd molar

Madumalai , , , , , , , , , , , , , Madumalai , , , , , , , , , , , , , , , , Madumalai , , , Madumalai Madumalai , , Madumalai , Madumalai , Madumalai Madumalai Madumalai Madumalai

10.57 10.37 11.03 11.35 11.39 10.88 11.42 11.34 11.27 11.49 11.86 10.94 10.99 11.46 9.82 9.29 8.74 8.97 8.02 8.35 7.2 7.85 7.66 8.38 8.35 9.44 9.37 8.61 10.24 10.08 10.25 3.01 6.45 1.74 3.74 5.18 6.02 7.06 6.77 2.52 4.77 5.11 3.76 11.10 12.94 11.41 16.79

2.86 3.11 2.80 3.69 4.09 3.91 5.34 2.50 3.62 3.99 4.70 3.74 4.94 4.19 4.72 4.59 6.27 5.26 4.61 15.91 4.32 2.93 5.02 7.17 4.59 4.40 5.33 4.71 8.17 5.64 6.84 4.07 4.79 2.42 4.94 3.43 6.20 5.07 5.36 1.54 2.12 3.21 3.06 1.45 10.17 5.77 6.32

4.15 4.27 5.19 6.10 6.67 9.51 2.13 8.02 7.07 9.26 8.40 6.24 6.04 10.30 9.98 3.79 3.69 8.05 2.94 1.51 1.31 6.12 7.41 3.02 2.53 3.54 2.87 3.53 5.62 6.19 4.87 7.04 4.96 8.04 9.19 5.38 10.21 6.77 8.31 3.43 6.33 5.19 6.75 3.84 6.18 4.85 4.79

21 23 19 17 16 20 16 17 17 16 13 19 19 16 26 29 33 31 37 35 42 38 40 35 35 28 29 34 24 25 23 69 47 77 64 55 50 43 45 72 58 56 64 18 7 16 17

Upper 2nd molar , , , , , , , , , , , , , , , , Upper M2 , , , Lower , , Lower , Lower , Lower Upper Lower Lower

M2

M2 M2 M2 M2 M2 M2

3e5 mm, perpendicular to the growth axis of the tooth (see Metcalfe et al., 2011) (Fig. 3A). However, enamel of modern Elephas maximus was very thin and there was technical difficulty in obtaining enamel from close to IES. The plate formation times or enamel secretion and extension rates in Elephas maximus are not known. Dirks et al. (2011) studied enamel secretion and extension rates, and plate formation time in Palaeoloxodon and Mammuthus and found that the enamel extension rates vary from crown to base. Mammuthus have been considered phylogenetically closest to Elephas maximus (Shoshani and Eisenberg, 1982; Shoshani and Tassy, 1996; Sanders, 2018). Therefore, we follow the enamel extension rates among mammoth Mammuthus spp., i.e. 13e14 mm per year (Metcalfe and Longstaffe, 2012). We took several samples and combined samples from close by grooves into a single sample for the analysis of modern mammalian specimens (Fig. 3A). This combining of samples was intended to overcome the attenuation of a primary time-series of body water isotopic composition as reflected in tooth enamel (Passey and Cerling, 2002). Serial sampling from deinotheres, gomphothere, and some of the fossil Elephas teeth were attempted close to the IES by drilling pits and discarding

the top 1e2 mm enamel layer to reduce damping effect in isotope signals (Metcalfe et al., 2011). Three fossil samples were also subjected to analysis of outer enamel surface (OES) beside IES to compare the stable isotope results from these two portions of the enamel. The enamel powder was pre-treated with 2.5% sodium hypochlorite (NaOCl) for 12 h, followed by 1 M acetic acid (pH: 3.8) for 6 h to remove organics and secondary carbonates (method of Koch, 1997; Lee-Thorp et al., 1989; Lee-Thorp and Van Der Merwe, 1991a,b). Additional OES samples from three fossil specimens were pre-treated with 0.1 M acetic acid. Samples were centrifuged at high speed and rinsed in distilled water to neutral pH before proceeding with the next solution. Samples were then freeze-dried for a maximum of 48 h. About 1e2 mg pretreated samples were reacted with 100% H3PO4 for 90 min at 70  C using a ThermoFinnigan Gasbench II peripheral device. The d13C and d18O of CO2 released from the carbonate in the apatite was determined in continuous flow mode using a Thermo Scientific Delta V Plus Mass Spectrometer at the Indian Institute of Technology, Kanpur (Paul and Skrzypek, 2007). The d13C and d18O of sixteen samples

R. Patnaik et al. / Quaternary Science Reviews 224 (2019) 105968

7

Table 2 Bulk stable d13C and d18O values of fossil proboscideans.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35

Specimen No.

Taxa

Locality

Age

Formation

d13C VPDB

d18O VPDB

Wt. % CaCO3

%C4

RS 66 RK 10 RK 97 TG 2 TE 12 TD 1 H 782 QD CHP 1 B 92 B413 B 478 B 166 KPP 2 B 613 KPST4 B 600 KPST B 276 CASG F 316 KP 1 H 302 I 192 A 155 A 167 A 219 B 93 DG 3 DG 6 A 191 CASG F 336 SKF-E-1 GRF-2 G367 VPL/B 2060

Gomphotheridae indet. Gomphotheridae indet. Gomphotheridae indet. Gomphotherium sp. Deinotherium sp. Deinotherium sp. Gomphotherium sp. Deinotherium sp. Proboscidean Elephas planifrons Elephas planifrons Elephas planifrons Elephas planifrons Elephas sp. Stegodon insignis Stegodon sp. Stegodon sp. Stegodon sp. Stegodon sp. Pentalophodon khetpuraliensis Anancus sp. Elephas hysudricus Elephas hysudricus Elephas planifrons Elephas planifrons Elephas planifrons Elephas hysudricus Elephas sp. Elephas sp. Stegodon sp. Elephas hysudricus Palaeoloxodon namadicus Palaeoloxodon namadicus Palaeoloxodon namadicus Elephas hysudricus

Ramnagar Ramnagar Ramnagar Tappar Tappar Tappar Haritalyangar Haritalyangar Chakrana Masol Quranwala Nathuwala Masol Khetpurali Nathuwala Khetpurali Masol Khetpurali Masol Khetpurali Khetpurali Masol Masol Nathuwala Quranwala Nathuwala Beddi Dudh-Garh Dudh-Garh Nathuwala Led, Khetpurali Hathnora Hathnora Hoshangabad Sombur

14e12.7 Ma 14e12.7 Ma 14e12.7 Ma 11-10 Ma 11-10 Ma 11-10 Ma 10-9 Ma 10-9 Ma 7-6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma 2.5e1.5 Ma 2.5e1.5 Ma 2.5e1.5 Ma 2.5e1.5 Ma 2.5e1.5 Ma 2.5e1.5 Ma 2.5e1.5 Ma ~1.5 Ma 50-150 Ka 50-150 Ka 10 Ka 500Ka

Chinji Chinji Chinji Khari Nadi Khari Nadi Khari Nadi Nagri Nagri Dhok Pathan Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot/Pinjor Tatrot/Pinjor Pinjor Pinjor Pinjor Pinjor Pinjor Pinjor Pinjor Pinjor Surajkund Gurla Beach Baneta Upper Karewas

11.55 10.49 10.43 10.99 12.95 13.33 11.38 10.81 12.14 0.16 0.21 0.03 0.07 0.79 0.84 0.18 0.46 0.36 1.00 2.97 0.13 0.16 3.33 1.64 0.82 1.96 0.28 0.72 0.63 0.58 1.88 0.10 2.8 0.00 9.17

9.49 10.36 9.63 2.67 4.39 4.71 8.89 9.55 7.25 4.42 6.37 6.81 5.20 5.55 6.67 0.02 5.94 1.47 3.02 4.17 4.29 3.12 0.61 6.85 5.16 4.89 4.29 7.02 5.87 5.78 7.57 2.7 0.10 0.4 6.13

12.06 11.61 12.22 7.85 5.59 4.10 5.61 17.72 4.90 12.00 10.21 9.51 8.78 10.35 5.36 9.20 5.48 7.68 4.23 5.67 5.89 8.51 4.26 7.74 6.94 13.32 7.43 5.57 9.18 7.70 5.12 e e e e

15 22 22 19 7 4 16 20 12 89 86 88 87 83 93 86 90 85 94 69 87 89 100 77 82 75 89 92 84 91 76 90 70 92 30

Table 3 Serial d13C and d18O isotopic values of fossil proboscideans, including calcium carbonate content and an approximate percentage of C4 plants in the diet. Specimen No. 1 2 3 4 5 6 7

DD 1/1 DD 1/2 DD 1/3 DD 1/4 DD 1/5 DD 1/6 B 608/1

8 9 10 11 12 13 14 15 16

B 608/2 B 608/3 B 608/4 B 608/5 B 608/6 B 608/7 B 608/8 B 608/9 VPL/B 2063/1

17 18 19 20 21 22

VPL/B VPL/B VPL/B VPL/B VPL/B VPL/B

2063/2 2063/3 2063/4 2063/5 2063/6 2063/7

Taxa Deinotherium sp. , , , , , Elephas planifrons , , , , , , , , Elephas hysudricus

Tooth Lower M3 , , , , , Molar fragment , , , , , , , , Molar fragment , , , , , ,

Locality Kangra , , , , , Nathuwala , , , , , , , , Romushi

Age 11.3 Ma , , , , .. ~2.6 Ma

, , , , , .730 Ka , , , , , ,

d13C VPDB IES

d13C VPDB

d18O VPDB IES

d18O VPDB OES

Wt.% CaCO3

%C4

OES

Chinji , , , , , Tatrot

12.71 12.55 12.44 12.32 12.40 12.78 0.99

12.69 12.87 12.58 12.79 12.96 12.78 1.30

8.60 8.25 7.95 8.15 7.76 8.65 4.72

6.93 6.83 6.77 6.12 6.80 7.47 4.12

3.68 7.74 9.26 8.18 8.47 4.88 13.74

8 9 10 10 10 8 94

, , , , , , , , Upper Karewas , , , , , ,

0.98 0.75 0.82 0.87 1.04 1.00 1.22 1.31 8.95

1.36 1.21 1.29 1.23 1.18 1.33 1.42 1.15 8.91

4.90 4.62 4.78 5.59 2.71 3.78 4.42 4.87 6.71

3.17 3.72 3.85 4.61 4.41 4.76 5.18 3.73 6.01

10.65 10.35 11.37 14.52 13.29 9.26 8.70 10.69 11.07

94 92 93 93 94 94 95 96 32

9.14 9.03 8.88 8.95 8.77 9.20

8.86 9.37 8.84 9.03 8.79 8.48

5.86 6.42 6.99 6.55 6.87 6.89

6.96 7.42 6.18 5.81 6.76 6.48

11.11 12.40 10.63 9.54 21.14 11.81

30 31 32 32 33 30

Formation

analysed twice were reproducible within 0.15‰. Analytical precision, based on repetitive analyses (n ¼ 5) of the Carrara Marble standard was 0.05‰ for d13C and 0.11‰ for d18O. Stable isotope data are reported in the conventional delta (d)

notation for carbon (d13C) and oxygen (d18O) relative to V-PDB (Vienna-Pee Dee Belemnite): d ¼ [(R sample/R standard) 1]  1000‰, where R denotes 13C/12C or 18O/16O. The raw d-values were normalized to V-PDB reference scale using a linear multi-

8 R. Patnaik et al. / Quaternary Science Reviews 224 (2019) 105968 Table 4 13 18 Serial d C and d O isotopic values of fossil proboscideans, including calcium carbonate content and an approximate percentage of C4 plants in the diet. Specimen No.

Taxa

Tooth

Locality

Age

Formation

d13C VPDB

d18O VPDB

Wt.% CaCO3

%C4

1

B 72/1

Molar fragment

Quranwala

~2.6 Ma

Tatrot

0.75

1.85

12.64

92

2 3 4 5 6 7 8

B 72/2 B 72/3 B 72/4 B 72/5 B 72/6 B 72/7 VPL/B 2062/1

Elephas platycephalus , , , , , , Elephas hysudricus

, , , , , , Molar fragment

, , , , , , Sombur

0.80 0.83 0.73 0.69 0.76 0.50 9.40

3.62 3.87 4.03 4.32 1.37 4.72 6.89

10.31 10.74 9.08 8.82 10.51 10.75 9.23

93 93 92 92 92 91 29

9 10 11 12

VPL/B VPL/B VPL/B VPL/B

, , , , , , Upper Karewas , , , ,

9.92 9.93 9.89 10.15

6.41 6.93 6.24 6.96

8.76 6.60 8.81 7.64

26 25 26 24

2062/2 2062/3 2062/4 2062/5

, , , ,

point normalization utilizing NBS19, L-SVEC, and CO-8 reference standards from the International Atomic Energy Agency (IAEA), which were also analysed with the unknown samples (Paul et al., 2007). In addition, the carbonate content (CaCO3%) was determined using the linear relationship between amount of CO2 released by the reaction as reflected by the area of all peaks (m/z ¼ 44, 45, and 46) and the (variable) weight of the NBS19 standard, with an analytical error of 0.3%, based on multiple analysis of reference enamel samples. An approximate percentage of C4 plants in the diet was calculated for all analysed taxa (ex. Table 1), following the isotope mass balance: C4% ¼ d13Cenamel obtained -d13Cenamel C3 feeder)/ (d13Cenamel C4 feeder - d13Cenamel C3 feeder) 100, where the mean d13Cenamel C4 feeder is þ2‰ and d13Cenamel C3 feeder is 14‰ (see also Koch et al., 1998; Pushkina et al., 2010). Basu et al. (2015) found the average d13C of C4 grasses of the Gangetic plain to be similar to those of global standards for mid-latitude, tropical regions. However, they noted a lowered (29.6 ± 1.9‰) average d13C of C3 plants compared to the global standard of 28.5‰ (Diefendorf et al., 2010; Kohn, 2010). Note that, because average isotopic composition of C3 or C4 pure feeder are used instead of the associated range of values, the calculated C4 dietary percentage obtained using the mass balance equation could produce negative values for some pure C3 feeders or over 100% for some pure C4 grazers. This calculation might therefore represent an underestimated amount of C4 plants in ecosystems because it is reliant only on the dietary preferences of mammals (see Pushkina et al., 2010). Nevertheless, the calculation of C4% in diet provides general information regarding the relative presence of C4 vegetation in local ecosystems. One of the specimens (SKE-1) from Narmada Valley was earlier identified as Elephas hysudricus (Patnaik et al., 2009). Here we designate it to Palaeoloxodon namadicus based on a revised comparison. Isotope data on Choerolophodon, Stegolophodon, Stegodon and Elephas from Late Miocene and early Pliocene of Pakistan (Cerling et al., 1999 and reference therein) have been included in the overall analysis of the diet of proboscideans. For the analysis of hypsodonty index and lamellar numbers, 59 samples of only proboscideans were selected from Miocene to Recent (14 - 0 Ma). Hypsodonty index were taken from Janis (1988), i.e. crown height divided by the occlusal width (buccolingual breadth) of the same tooth and values calculated by using the rule H/W X 100 (Lister, 2013). For cusp pairs/lophs/lamellar numbers we followed the procedure of Lister (2013). Crown height was taken as the distance from the base to the tip of the crown and width was measured at the maximum from buccal to lingual. Because of fully erupted M3, we used only the hypsodonty index and lamellar counts of M3 for the present analyses. The data of HI and lamellar were collected from the Museum of Department of Geology, Panjab

, , , .500 Ka , , , ,

University, Chandigarh, but additional data were obtained from the existing literature (Table 6). 5. Results and discussion 5.1. Extant mammals from Mudumalai National Park A comprehensive bulk, bone collagen sample-based isotope study on Elephas maximus (n ¼ 56) indicate variable feeding strategies of these mega-herbivores from mixed (grass-browse) feeding to browsing (Sukumar and Ramesh, 1992). We therefore applied serial sampling on just two upper M3s of adult Elephas maximus from Mudumalai (ex. Fig. 3 A). The intra-tooth d13C values of 10.25 to 7.2‰ (mean-m: 8.86; standard deviation-s: 0.900) in one tooth sample (E2) is likely due to seasonal variation in browsing and mixed feeding, with ~23e42% of grass intake (Table 1). Elephas maximus being an obligate drinker, the intratooth variation in E2 d18O values mostly ranging from 7.17 to 2.93‰ (m: 5.91, s: 2.77) (Table 1, Fig. 3B), could be attributed to variation in meteoric water values due to seasonal changes in O isotopic composition of summer and winter (more depleted in 18O) monsoons (Srivastava et al., 2014); the sole outlier (15.91‰) may be due to a measurement error and therefore has been shown by a dotted line in Fig. 3 B. Another tooth (E1) with d13C values ranging from 11.86‰ to 10.37‰ (m: 11.16, s: 0.38) (Fig. 3B) indicate that the individual mostly browsed on shrubs and trees, with only 13e23% grass in its diet. Seasonal variation in water intake is indicated by a fluctuation in d18O ranging from 5.34 to 2.5‰ (m: 3.82, s: 0.79). The d13C (7.06 to 6.02‰, m: 6.61; s: 0.43) and d18O (6.2 to 5.07‰, m: 5.54, s: 0.47) values from serial sampling of molars from a cervid Sambar (Cervus unicolor) indicate that they were mixed feeders consuming 43e50% grass in the diet and likely drank water from a localized source. However, isotopic composition (d13C of 11.79‰ and d18O of 1.45‰, Table 1) of one bulk sample from a Sambar specimen indicates browsing behaviour under water stressed condition. The d13C (5.11 to 2.52‰) and d18O (3.21 to 1.54‰) of Cheetal (Axis axis) suggest mixed feeding on more monocot and less dicot plants with 56e72% grass in its diet in an open habitat and water intake from drier streams or water-stressed plants such as grass. The d13C (6.45 to 1.74‰, m: 3.73, s: 1.72) and d18O (4.94 to 2.42‰, m: 4.05, s: 0.99) of bovid Bos gaurus indicate seasonal variation in mixed feeding and pure grazing with 47e77% grass in the diet (Fig. 4). The wild boar Sus scrofa is an omnivore, feeding on a variety of plant parts and small animals (d13C: 16.79 to 11.61‰) and likely derived its water from wetter areas of the forest (d18O: 6.32 to 5.77‰). The langur Semnopithecus priam (d13C ¼ 12.94‰ and d18O ¼ 10.17‰) is mainly an arboreal species feeding on C3 leaves/fruits that are depleted in 18O.

R. Patnaik et al. / Quaternary Science Reviews 224 (2019) 105968

9

Table 5 A summary of proboscidean and associated mammals d13C and d18O values (range, mean m and SD s) diet and environment. Serial nos.

Sample nos.

Middle Miocene 1 RS 66, RK 10, RK 97 2

DD1

3

RTP 6, RK 65, RK 16

4

RB 41, RB 62, RH 1, RK 15, RS 124 RK 56, RS 4

5 6

Taxa

d13C VPDB (range, mean m and SD s)

d18O VPDB (range, mean m and SD s)

Diet Browser/Grazer/ Mixed feeder

Environment Wet/Dry/Intermediate

Gomphothere (n ¼ 3)

11.55‰ to 10.43‰, m 10.82, s 0.63 12.78‰ to 12.40‰, m 12.53, s 0.18 13.09‰ to 12.44‰, m 12.86, s 0.36 13.98‰ to 11.74‰, m 12.80, s 1.08 13.19‰ to 13.08‰, m 13.14, s 0.08 13.02‰ to 10.96‰, m 12.05, s 0.79

10.36‰ to 9.49‰, m 9.83, s 0.46 8.65‰ to 7.76‰, m 8.23, s 0.35 9.04‰ to 5.78‰, m 7.79, s 1.76 12.75‰ to 9.41‰, m 10.15, s 2.35 9.76‰ to 7.5‰, m 8.63, s 1.60 12.50‰ to 3.02‰, m 7.22, s 3.39

Browser

Wet

Browser

Wet

Browser

Wet

Browser

Wet

Browser

Wet

Browser

Wet

13.33‰ to 12.95‰, m 13.14, s 0.27 10.99‰ 10.81‰ 15.85‰ to-12.31‰, m 13.61, s 1.16 13.72‰ to 11.62‰, m 13.04, s 0.98 13‰ to 11.11‰, m 12.25, s 0.88 10.50‰

4.71‰ to 4.39‰, m 4.55, s 0.23 2.67‰ 9.55‰ 11.77‰e0.6‰, m 6.52, s 3.98 11.77‰ to 6.12‰, m 8.39, s 2.49 11.94‰ to 4.99‰, m 7.77, s 3.06 7.96‰

Browser

Intermediate

Browser Browser Browser

Intermediate Wet Intermediate seasonal

Browser

Wet

Browser

Intermediate Wet

7.91‰ to 7.25‰, m 7.58, s 0.47 7.27‰

Browser/ Omnivores Browser

Wet

Browser

Wet

Mixed feeder Browser/ Omnivore Grazer

Intermediate Wet

Grazer Mixed feeder

Intermediate Intermediate

Deinotherium indicum (serial sampling) Bovids (n ¼ 3) Rhinocerotids (n ¼ 5) Giraffids (n ¼ 2) Dorcatherium sp. (n ¼ 6)

RK 100, DH 17, RS 70, RB 9, RS 72, RS 27 Late Miocene 7 TE 12, TD 1

Deinotheres (n ¼ 2)

8 9 10

Gomphothere (n ¼ 1) Gomphothere (n ¼ 1) Bovids (n ¼ 7)

11 12

TG 2 H 782 H 55e68, H 252, H 475, H 41, H 194, H 664, H 34 HR 45, HRH, QAR, H 280

Rhinocerotids (n ¼ 4) Dorcatherium sp. (n ¼ 4)

13

RN 89-76 A, 194/76 B, RN 114-76 B, H 185 S1 B

Suid (n ¼ 1)

14

CHP 1, CHR 1

Rhinocerotids (n ¼ 2)

15 Pliocene 16 17

CHH 1

Hipparion sp. (n ¼ 1)

14.26‰ to 12.41‰, m 13.2, s 1.50 10.81‰

KA-DP 1 KA-DP 2

Hipparion sp. (n ¼ 1) Suid (n ¼ 1)

2.37‰ 11.63‰

4.49‰ 12.06‰

18

B 613, B 600, KPST, B 276

Stegodon (n ¼ 4)

19 20

KP 1 CASG F 316

6.67‰ to 1.47‰, m 4.28, s 2.45 4.29‰ 4.17‰

21

B 92, B 413, B478, B166

Anuncus sp. (n ¼ 1) Pentalophodon khetpuraliensis (n ¼ 1) Elephas planifrons (n ¼ 4)

0.36‰e1‰, m 0.49, s 0.607152 0.13‰ 2.97‰

Intermediate

B 608

Grazer

Intermediate seasonal

23

H 302, I 192

Grazer

Dry seasonal

24

B 72

Grazer

Intermediate seasonal

25 26

B 14 B 15

Elephas platycephalus (serial sampling) Leptobos falconeri (n ¼ 1) Hemibos sp. (n ¼ 1)

Grazer Grazer

Intermediate Intermediate

27

DKB 3, B 385, B 278

Bovines (n ¼ 3)

BH 2 DK 1

Dry Dry seasonal

30 31 32

KB 2 PR 1 CASG F 354, BH 1

Hipparion sp. (n ¼ 1) Hipparion sp. (serial sampling) Cervid (n ¼ 1) Merycopotamus sp. (n ¼ 1) Hexaprotodon sp. (n ¼ 2)

Grazer to mixed feeder Grazer Grazer

Intermediate

28 29

Browser Grazer grazer

Intermediate Intermediate Intermediate

33 34 35

A 546 A 811 B 276 S, B 276, A796

Camelus sp. (n ¼ 1) Hydaspitherium sp. (n ¼ 1) Sivatherium sp. (n ¼ 3)

Grazer Grazer Grazer

Dry Dry Dry

36

C 355, S 1

Suid (n ¼ 2)

6.81‰ to 4.42‰, m 5.7, s 1.09 5.59‰ to 2.71‰, m 4.49, s 0.82 3.12‰ to 0.61‰, m 3.73, s 4.41 4.72‰ to 1.37‰, m 3.40, s 1.28 4.05‰ 7.74‰ to 6.2‰, m 6.97, s 1.09 7.74‰ to 6.20‰, m 1.49, s 3.48 1.94‰ 1.55‰ to 3.78‰, m 0.15, s 1.88 4.20‰ 4.09‰ 9.22‰ to 7.28‰, m 8.25, s 1.37 0.72‰ 0.02‰ 2.04‰ to 0.82‰, m 1.45, s 0.61 10.58‰ to 5.69‰, m 8.14, s 3.46

Grazer

22

0.21‰e0.16‰, m 0.02, s 0.16 0.75‰e1.31‰, m 0.10, s 0.18 3.33‰e0.16‰, m 1.75, s 2.24 0.83‰e0.5‰, m 0.72, s 0.11 2.11‰ 1.99‰e0.99‰, m 1.45, s 0.65 0.2‰e1.83‰, m 1.24, s 0.90 0.62‰ 0.14‰ to 0.25‰, m 0.08, s 0.15 9.03‰ 0.82‰ 2.97‰ to 2.73‰, m 2.85, s 0.17 0.12‰ 1.41‰ 0.28‰e3.09‰, m 2.09, s 1.57 10.84‰ to 7.59‰, m 9.22, s 2.30

Mixed feeder to browser

Wet

0.58‰ 1.96‰ to 0.82‰, m 1.47, s 0.59 0.28‰ 0.63‰e0.72‰, m 0.05, s 0.95

5.78‰ 6.85‰ to 4.89‰, m 5.63, s 1.06 4.29‰ 7.02‰ to 5.87‰, m 6.45, s 0.81

Grazer Grazer

Intermediate Intermediate

Grazer Grazer

Intermediate Intermediate

Elephas planifrons serial sampling) Elephas hysudricus (n ¼ 2)

Pleistocene 37 A 191 38 A 155, A 167, A 219

Stegodon sp. (n ¼ 1) Elephas planifrons (n ¼ 3)

39 40

Elephas hysudricus (n ¼ 1) Elephas sp. (n ¼ 2)

B 93 G 3, DG 6

Intermediate seasonal

(continued on next page)

10

R. Patnaik et al. / Quaternary Science Reviews 224 (2019) 105968

Table 5 (continued ) Serial nos.

Sample nos.

Taxa

d13C VPDB (range, mean m and SD s)

d18O VPDB (range, mean m and SD s)

Diet Browser/Grazer/ Mixed feeder

Environment Wet/Dry/Intermediate

41

B 9, B 11

Bubalus platyceros (n ¼ 2)

Intermediate

Damalops sp. (n ¼ 1) Hemibos sp. (n ¼ 1) Bovini (n ¼ 12)

Grazer Grazer Mixed feeder to Grazer

Intermediate Dry Intermediate seasonal

45

M2 M5 A 253, A 274, B 346, CASG 330, A 402, DG 4, TT 1, DG 1, DG 2, GB 2, DG 5, GB 1 B 287

4.37‰ to 3.18‰, m 3.78, s 0.84 4.5‰ 2.75‰ 9.38 to 0.31‰, m 4.4, s 2.84

Grazer

42 43 44

0.28‰e1.81‰, m 0.77, s 1.48 0.57‰ 1.31‰ 3.05 to 3.4‰, m 0.17, s 2

Bovid (serial sampling)

Intermediate

A 296 A 569 A 587, B 43 T, B 40

Bovini (n ¼ 1) Hipparion sp. (n ¼ 1) Equus sp. (n ¼ 3)

Browser Grazer Grazer

Intermediate Intermediate Dry seasonal

49

A 566

Grazer

Dry seasonal

50

A 571

Grazer

Intermediate seasonal

51

B 46

Grazer

Intermediate

52

B 36, CASG F 356

Grazer

Intermediate

53

B 33, B 30

Grazer

Intermediate seasonal

54 55

G 397 A 794, A798, A542, A 800, I 189, JDS 1 CASG F 1140, A 242, A 228 MB G 129, F 14 A

Hipparion sp. (serial sampling) Hipparion sp. (serial sampling) Equus sp. (serial sampling) Rhinoceros palaeindicus (n ¼ 2) Rhinoceros sivalensis (n ¼ 2) Rhinoceros sp. (n ¼ 1) Sivatherium gigantum (n ¼ 6) Hexaprotodon sp. (n ¼ 3) Camelus sp. (n ¼ 1) Cervids (n ¼ 2)

6.18‰ to 5.49‰, m 5.79, s 0.30 0.21‰ 3.38‰ 6.51 to 0.76‰, m 2.90, s 3.14 1.16‰ to 2.15‰, m 0.56, s 1.33 8.33‰e1.58‰, m 0.75, s 4.25 6.81‰ to 5.42‰, m 6, s 0.61 3.14‰ to 2.01‰, m 2.58, s 0.80 6.20‰ to 1.25‰, m 3.73, s 3.50 6.43‰ 4.89‰ to 0.77‰, m 2.69, s 1.60 9.44 to 4.04‰, m 7.18, s 2.81 0.55‰ 5.18‰ to 4.22‰, m 4.7, s 0.68 4.15 to 0.36‰, m 2.47, s 1.67

Grazer

46 47 48

1.05‰e1.37‰, m 1.22, s 0.13 11.24‰ 1.32‰ 2 to 1.49‰, m 0.11, s 1.86 1.44‰ to 0.24‰, m 1.17, s 0.52 0.73‰e0.39‰, m 0.23, s 0.41 0.47‰e0.66‰, m 0.06, s 0.47 0.83‰e0.90‰, m 0.87, s 0.05 0.79‰e0.30‰, m 0.25, s 0.77 2.97‰ 1.96‰e3.24‰, m 1.44, s 2.09 0e1.72‰, m 1.03, s 0.91 1.23‰ 0.51‰e2.27‰, m 1.39, s 1.24 0.08e2.77‰, m 1.14, s 0.95

Mixed feeder Grazer

Intermediate Intermediate seasonal

Grazer

Intermediate seasonal

Grazer Grazer

Dry Intermediate

Grazer

Seasonal condition

2.83 to 0.49‰, m 0,20, s 1.24 0.18‰

6.73 to 1.38‰, m 3.29, s 1.71 1.70‰

Mixed feeder to Grazer Grazer

Seasonal condition

4.68‰

3.60‰

9.20‰ to 8.77‰, m 8.99, s 0.15 10.15‰ to 9.40‰, m 9.86, s 0.28 2.8‰e0.00‰, m 0.9, s 1.65

6.99‰ to 5.86‰, m 6.61, s 0.39 6.96‰ to 6.24‰, m 6.69, s 0.34 2.7‰e0.10‰, m 1, s 1.49

Mixed feeder/ Omnivore Browser

Wet

Browser

Wet

Mixed feeder to Grazer

Intermediate to Dry

56 57 58 59

61

A A A A A A

62

A 642

63

VPL/B 2063

64

VPL/B 2062

65

SKF-E1, GER 2, G367

60

521, 288, 426, 590, 578, 559

A A A A A

520, A 534, A512, 505, A 368, 286 or 216 592, B 585, 601, A 602, A 639

Bovines (n ¼ 9)

Equus sp. (n ¼ 7) Rhinoceros platyrhinus (n ¼ 1) Suid (n ¼ 1) Elephas hysudricus (serial sampling) Elephas hysudricus (serial sampling) Palaeoloxodon namadicus (n ¼ 3)

Overall, results of limited bulk and serial samples comprising both large and medium sized obligate drinkers Elephas maximus, Bos gaurus, Cervus unicolor and Axis axis do exhibit seasonal dietary variability and niche partitioning of the wooded forest (Fig. 4) in accordance with their known dietary habits (Ahrestani et al., 2012). 5.2. Fossil proboscideans and associated mammals 5.2.1. d13C and d18O analyses results Both bulk and serial sampling of fossil proboscideans and associated mammals are summarised in Table 5. Growth lines in elephantids emerge from the EDJ (enamel dentine junction) at a very low angle (~60) and run almost parallel to the enamel surface. In order to avoid damping in seasonal isotopic signature, it has been recommended to sample the inner enamel surface (cf. Metcalfe et al., 2011). We have followed this method in this study. However, three fossil specimens were subjected to sampling of both inner and outer enamel surfaces in order to compare the results. We found that d13C of IES were not significantly different from those of

Intermediate Intermediate

OES. The d13C of OES in DD1 (Deinotherium), a C3 browser, was lower by 0.02e0.56‰ from those of IES. Most of the OES d13C values in B608 (Elephas planifrons), a C4 grazer, were higher by 0.14e0.47‰ from those of IES, whereas in VPL/B2603 (Elephas hysudricus) this difference was 0.02e0.72‰ (Table 3; Fig. 5). In contrast, the d18O of OES and IES differ significantly. DD1 d18O values of OES were higher by 0.96e2.03‰ than those of IES (Table 3; Fig. 5), whereas those of B608 varied between 0.60 and 1.7‰ (Table 3; Fig. 5). In VPL/B2603 the difference in OES and IES d18O values ranged between 0.11 and 1.1‰. We did not observe any particular trend in the OES and IES d13C and d18O results. The isotope data (Table 5) indicate Middle Miocene (~14e12.7 Ma) gomphotheres from Ramnagar were mainly C3 browsers, but might also have consumed ~15e22% of C4 plants such as grass. They likely lived in somewhat open parts of the forest and drank from streams under moist conditions. Deinotherium indicum from the Kangra Valley (~11.3 Ma) also consumed dominantly C3 plants (and ~8e10% C4 plants) and acquired its water under wet conditions. Overall, the forest habitat of the gomphotheres might

R. Patnaik et al. / Quaternary Science Reviews 224 (2019) 105968

11

Table 6 Hypsodonty index and cusps pairs or lamellae values for proboscidean. Note: Hypsodonty index (HI) ¼ Crown height/crown width x 100 (after Janis, 1988). Specimen No.

Taxa

Locality

Formations

Age

Tooth position

Cusps pairs or Lamellae

HI

Data Collection

NPR 2

Deinotherium indicum

Nurpur

Chinji

14e12.7 Ma

LM3

2

35

13 Ma 13 Ma 13 Ma 13 Ma 13 Ma 13 Ma 13 Ma 13 Ma 13 Ma 13 Ma 13 Ma 13 Ma 13 Ma 13 Ma

3

RM LM3 LM3 LM3 LM3 LM3 LM3 RM3 LM3 LM3 RM2 RM3 LM3 LM3

4 4 4 5 4 6 6 6 6 6 6 6 6 5

49.2 53.2 51.4 44.6 59.5 52.9 51.7 51.7 51.2 65.1 50.8 58 59.7 47.1

Sankhyan and (2014) Chavasseau et Chavasseau et Chavasseau et Chavasseau et Chavasseau et Chavasseau et Chavasseau et Chavasseau et Chavasseau et Chavasseau et Chavasseau et Chavasseau et Chavasseau et Chavasseau et

TF 6266 a TF 6266 b TF 6267 a TF 6268 TF 6269 TF 6271 f TF 6271 a TF 6271 c TF 6274 TF 6275 TF 6276 a TF 2648 TF 2650 Cmu 2-1

Mae Mae Mae Mae Mae Mae Mae Mae Mae Mae Mae Mae Mae Mae

DD-1 (enamel)

Gomphotherium cf. browni Gomphotherium cf. browni Gomphotherium cf. browni Gomphotherium cf. browni Gomphotherium cf. browni Stegolophodon praelatidens Stegolophodon praelatidens Stegolophodon praelatidens Stegolophodon praelatidens Stegolophodon praelatidens Stegolophodon praelatidens Stegolophodon nasaiensis Stegolophodon nasaiensis Tetralophodon cf. xiaolongtanensis Deinotherium indicum

Kangra

Chinji

11.3 Ma

LM3

3

50

YUDG-Mge 047

Stegolophodon stegodontoides

Kyauksaungsan, Myanmar Kyauksaungsan, Myanmar Kyauksaungsan, Myanmar Kyauksaungsan, Myanmar Padri, Jhelum Pakistan Padri, Jhelum Pakistan Haritalyangar

Irrawaddy

8-7 Ma

LM3

6

39

(Sahni and Gupta (1982)) VPL. Geology,PU Sein and Thein (2008)

8-7 Ma

3

5

46

Sein and Thein (2008)

3

YUDG-Sbw 035

Stegolophodon stegodontoides

YUDG-Sbw 003

Stegolophodon stegodontoides

YUDG-Mge 007

Stegolophodon cf. stegodontoides Stegolophodon cautleyi Stegolophodon cautleyi aff. Stegolophodon

Moh, Moh, Moh, Moh, Moh, Moh, Moh, Moh, Moh, Moh, Moh, Moh, Moh, Moh,

Thailand Thailand Thailand Thailand Thailand Thailand Thailand Thailand Thailand Thailand Thailand Thailand Thailand Thailand

Mae Mae Mae Mae Mae Mae Mae Mae Mae Mae Mae Mae Mae Mae

Moh Moh Moh Moh Moh Moh Moh Moh Moh Moh Moh Moh Moh Moh

Sharma

Irrawaddy

LM

al. al. al. al. al. al. al. al. al. al. al. al. al. al.

(2009) (2009) (2009) (2009) (2009) (2009) (2009) (2009) (2009) (2009) (2009) (2009) (2009) (2009)

Irrawaddy

8-7 Ma

RM

6

33

Sein and Thein (2008)

Irrawaddy

8-7 Ma

LM3

4þ

43

Sein and Thein (2008)

Dhok Pathan Dhok Pathan Dhok Pathan

7-6 Ma 7-6 Ma 7-6 Ma

?M3 ?M2/3 RM3

5 5 5

43 48 74

Haritalyangar

Dhok Pathan

7-6 Ma

RM3

6

33

HTA 92

Stegolophodon cf. stegodontoides Stegodon sp.

Haritalyangar

Dhok Pathan

7-6 Ma

RM2/3

4þ

39

HTA 33

Gomphotheriidae indet.

Haritalyangar

Dhok Pathan

7-6 Ma

LM3

3þ

45

KPST B 613 B 88 B 71 H 310 KP-1 B 608

Stegodon sp. Stegodon insignis Stegodon insignis Stegodon insignis Stegodon insignis Anuncus sp. Elephas planifrons

Khetpurali Nathuwala Masol Masol Masol Khetpurali Nathuwala

Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot

~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma

?M3 LM2/3 RM2 RM2/3 RM3 RM3 ?M2/3

8 6þ 7 5þ 6 4 4þ

36 83 65 50 66 58 106

B 194 H 301 B 84 F 317 G 395 B 478 B 72 B 166 A 191 B 244

Elephas planifrons Stegodon sp. Stegodon sp. Stegodon sp. Elephas planifrons Elephas planifrons Elephas sp. Elephas sp. Stegodon sp. Stegodon ganesa

Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot Tatrot Pinjor Pinjor

~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma ~2.6 Ma 2.5e1.5 Ma 2.5e1.5 M a

RM3 ?M3 RM3 RM3 LM3 ?M3 LM3 ?M3 ?M3 ?M3

10 10 6 7 15 4þ 13 11 7 5

153 55 52 62 143 112 150 150 54 66

A 253 A 215 B 91 F 458 A 164 JU/DG/VPL/9001

Stegodon sp. Stegodon sp. Stegodon insignis Elephas sp. Elephas sp. Elephas cf. planifrons

Pinjor Pinjor Pinjor Pinjor Pinjor Pinjor

2.5e1.5 Ma 2.5e1.5 Ma 2.5e1.5 Ma 2.5e1.5 Ma 2.5e1.5 Ma 2.5e1.5 Ma

?M3 RM3 RM3 ?M3 ?M3 LM3

6 8 8 6þ 10 6þ

63 63 78 200 100 87

Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, PU Geology Kundal et al. (2017)

B 93 A 216 A 145 VPL/B 2060

Elephas Elephas Elephas Elephas

Masol NE of Masol Masol Quranwala Masol Nathuwala Quranwala Masol Nathuwala 4 ½ mile NE of Panjab University Quranwala Quranwala Masol Mirzapur Quranwala Nangal Village, Jammu and Kashmir Beddi Quranwala Surajpur railway Sombur

Samiullah et al. (2015) Samiullah et al. (2015) Sankhyan and Chavasseau (2018) Sankhyan and Chavasseau (2018) Sankhyan and Chavasseau (2018) Sankhyan and Chavasseau (2018) Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, Panjab University, Chandigarh Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, PU Geology Museum, PU Geology

pinjor Pinjor Pinjor Upper Karewa

2.5e1.5 Ma 2.5e1.5 Ma 2.5e1.5 Ma 500 Ka

LM3 LM2/3 LM3 ?M3

16 10 15 11

184 100 166 200

VPL/B 2065

Elephas hysudricus

Sombur

Upper Karewa

500 Ka

?M3

6þ

157

50 Ka 200 Ka 169 Ka 169 Ka 0

3

15 11 4þ 5þ 18

162 214 58 164 185

Museum, PU Geology Museum, PU Geology Museum, PU Geology (Kotlia, 1990) Museum, PU Geology (Kotlia, 1990) Museum, PU Geology Museum, PU Geology Museum, PU Geology Suraprasit et al. (2016) Suraprasit et al. (2016) VPL, PU, Chandigarh

PUPC 09/13 PUPC 09/120 HTA 115 HTA 175

G 367 GRF 3 DMR-KS-05-03-22-19 DMR-KS-05-03-17-12 Recent

hysudricus planifrons sp. hysudricus

Palaeoloxodon namadicus Elephas sp. Stegodon cf. orientalis Elephas sp. Elephas maximus

Hoshangabad Hoshangabad Khok Sung, Thailand Khok Sung, Thailand Simlipal

Narmada Narmada Khok Sung Khok Sung Recent

RM ?M3 RM3 LM3 ?M3

12

R. Patnaik et al. / Quaternary Science Reviews 224 (2019) 105968

Fig. 3. A, Serial sample sites on E2- Elephas maximus M3 from Mudumalai National Park. B, Serial d13C and d18O values of E2 and E1. The d18O value of 15.91‰ at E2-P6 is connected by dotted lines as it is likely a measurement error.

have been less dense compared to those of deinotheres during this part of the Middle Miocene. Isotopic composition of associated mammals such as bovids, rhinoceratids, giraffids (ex. Bramatherium), tragulids (Dorcatherium) and a suid suggest that these mammals thrived under wet conditions and predominantly on a C3 plant diet (see Table 5), which also indicates presence of forests. The Late Miocene (11-10 Ma) deinotheres from Kutch were almost exclusively C3 browsers, whereas contemporary gomphotheres might have consumed ~19% C4 grass in their diet. The presence of C3 grasses such as bamboo cannot be totally ruled out as microwear studies on Late Miocene equids and primates indicate presence of some C3 grass on the landscape (Nelson, 2007; Patnaik et al., 2014a,b). Gomphothere from Haritalyangar (10-9 Ma) was also a browser with ~20% C4 grass in its diet and so were the

associated bovids, rhinocerotids, tragulids, and suids thriving under wet to intermediate seasonal environment (Tables 2 and 5). The Latest Pliocene (~3e2.6 Ma) brachydont Stegodon from Tatrot Formation had variable mode of dietary habit from grazing, mixed feeding to browsing and deriving their water under intermediate seasonal conditions (also see Patnaik et al., 2014a,b). It probably utilised gallery forests within the grasslands to browse. The diet of the other brachydont genus Anancus sp. varied from mixed feeding to grazing in open and partly wooded areas of the grassland (Table 3). The hypsodont Elephas planifrons show grazing (92e96% grass) under rather seasonal condition. Elephas hysudricus was a pure grazer too but lived in open water stressed areas. Elephas platycephalus likely fed on grasses also growing under seasonal condition (SI Fig. 2A). A high seasonality around this time similar to

R. Patnaik et al. / Quaternary Science Reviews 224 (2019) 105968

Fig. 4. d13C versus d18O values of bulk and serial samples of selected Mudumalai mammals indicate niche partitioning.

monsoons, as evident from the large variability in d18O values (6.81 to 0.02‰, Table 2), would have led to opportunistic feeding among the various proboscidean taxa living together on the grassland. Presence of a landscape dominated by grasslands is further supported by C4 grazers such as bovid Leptobos falconeri, buffalo Hemibos sp. horse Hipparion and rhinocerotids. Isotopic composition of one ~3 Ma old cervid (Table 5: SI Fig. 3), however, showed C3 browsing habit. The amphibious anthracothere Merycopotamus sp. was a grazer and obtained its water from 18O depleted (Table 5) sources. The hippo Hexaprotodon shows mixed feeding behaviour and as expected a depleted water source (Table 5) being amphibious. Previous study (Patnaik et al., 2014a,b) on Hexaprotodon from this time period showed that it was a pure grazer and lived in wetter areas. The semi-aquatic behaviour of anthracotheres and hippos is likely responsible for such depleted d18O values because of reduced evaporative loss of 16O-enriched water from the body (Bocherens et al., 1996). Other factors could be nocturnal foraging leading to a reduction in evaporative water loss through the skin and also consumption of 18O-depleted water, or the unique physiology of the hippos (Bocherens et al., 1996). Extant hippos from several localities in Africa show consistently lower d18O values than those of associated fauna (Bocherens et al., 1996; Kohn et al., 1996; Levin et al., 2006). As expected, suids around this time were mixed feeder to browser/omnivore and also were water dependent. Other reason for these suids to have low d13C values could be that they belong to a different ecological condition than the rest of the mammals. Camelus sp. from these deposits was a pure C4 grazer (~88% grass) under a water stressed condition. Similar results were obtained earlier (Patnaik et al., 2014a,b) from Camelus sp. of this time as they are drought resistant taxa that intake water mostly from the plants they consume, such as waterstressed grass in this case (Table 5). The giraffids around this time such as Hydaspitherium and Sivatherium were both pure grazers and consumed water from drier areas (Table 5). The African sivatheres have been found to be associated with habitats ranging from forest to open woodland (Churcher, 1978; Geraads, 1985). It has also been suggested that having a relatively short neck point to grazing or mixed low browsing/grazing (Meladze, 1964; Hamilton, 1973; Churcher, 1978; Geraads, 1985). Solounias et al. (1988) found that Samotherium boissieri, a Miocene sivathere and a potential ancestor of

13

Sivatherium, was likely a committed grazer. A predominantly C4 diet is also inferred for the Late Miocene ?Bramatherium sp. of Baynunah succession, Abu Dhabi, another potential ancestor of Sivatherium (Kingston, 1999). However, Sivatherium hendeyi from early Pliocene of South Africa had a mixed feeding strategy (Franz-Odendall and Solounias, 2004), whereas S. maurusium from the Upper Laetoli and Upper Ndolanya Beds reveal dominantly browsing behaviour (Kingston and Harrison, 2007). Early Pleistocene (~2.5e2 Ma) Stegodon from the younger levels of Pinjor Formation was a C4 grazer with over 90% grass in its diet but likely obtained its water and food from wet to intermediate areas. Elephas planifrons (n ¼ 4) from these deposits were all grazers (with 75e82% grass) and so were Elephas hysudricus and Elephas sp. (Table 5). It appears that all the proboscideans around this time were pure grazers and obligate drinkers (SI Fig. 4). Associated bovines such as Bubalus platyceros, Damalops sp. and Hemibos sp. were all C4 grazers and obtained water from water bodies and grasses under wet conditions. Bovids graze on foliage from open and irradiated portion of the vegetation, which is usually enriched in 18O due to transpiration (Sternberg et al., 1989), thus they usually have relatively high d18O values. Associated Hipparion and Equus sp. were C4 grazers (SI Fig. 5). Rhinoceros palaeindicus and Rhinoceros sivalensis were C4 grazers having their water intake from drier areas. The so-called woolly rhinoceros Coelodonta platyrhinus/Punjabitherium identified by Khan (1971) and Nanda (1973) and later attributed to Rhinoceros platyrhinus (Pandolfi and Maiorino, 2016) was a pure C4 grazer living and getting water from intermediate conditions (Table 5). Pandolfi and Maiorino (2016) also predicted a C4 diet based on its dental morphology. The Indian rhinoceros Rhinoceros unicornis feeds mainly on grasses and secondarily on leaves, branches of shrubs and trees, and fruits (Hoogerwerf, 1970; Laurie et al., 1983; Pradhan et al., 2008). The short necked giraffid Sivatherium gigantium shows seasonal variation in C4 grazing and water intake (SI Fig. 6). In contrast the modern giraffe Giraffa camelopardalis is not an obligate drinker and derives its water from the C3 vegetation, resulting in 18O-enriched enamel (Cerling et al., 1997a). Associated Hexaprotodon was a grazer. The drought resistant taxa Camelus sp. from these deposits show water stressed pure C4 grazing habit. Cervids from these sediments show pure grazing and obligate drinking (Table 5). Early to Middle Pleistocene Elephas hysudricus and associated mammals from the Siwaliks were all grazers and exhibit seasonal variation in water intake. But Middle Pleistocene (<750 Ka) Elephas hysudricus from the Karewas of Kashmir (Kotlia, 1990) shows a variable C3 browsing signature without much seasonal variation in the drinking water intake (SI Fig. 2B). The various mammalian taxa known from the Karewas include Bos, Sus, Felis, Elephas, Equus, Rhinoceros and Sivatherium (Kotlia, 1990 and references therein). The fauna as such indicates presence of grasslands, although the presence of gallery forests during the Middle Pleistocene cannot be ruled out. Isotopic composition of Late Pleistocene Narmada Valley Palaeoloxodon namadicus indicate mixed feeding to pure grazing behaviour under water stressed conditions (Table 5). 5.2.2. Hypsodonty indices and lamellar counts The results from hypsodonty index analyses carried out on South and Southeast asian proboscidean upper third molars (M3’s) housed at the Geology Museum along with fossil specimens from published literature indicate that Middle to Late Miocene forms were all brachydonts, that is low crowned (Table 6, Fig. 6). The main genera included Gomphotherium (HI, 44e59), Deinotherium (HI, 35e50), Stegolophodon (HI, 33e65), Tetralophodon (HI, 47) and Stegodon (HI, 39). In the Pliocene, the indigenous Stegodon (HI, 36e83) and Anancus (HI, 58) were brachydont forms, whereas the immigrant Elephas planifrons was moderately hypsodont (HI,

14

R. Patnaik et al. / Quaternary Science Reviews 224 (2019) 105968

Fig. 5. Serial sample sites on Deinotherium indicum M3 from Middle Miocene (~11.3 Ma) sediments of Kangra Valley, India.A, IES and B, OES d13C and d18O values. C and D E. planifrons; E and F, E. hysudricus d13C and d18O values.

R. Patnaik et al. / Quaternary Science Reviews 224 (2019) 105968

15

Fig. 6. A, d13C value based scatter plot of the proboscideans representing the last 14 Ma. Data from India and Pakistan is based on published literature (Quade et al., 1992; Morgan et al., 1994; Stern et al., 1994; Cerling et al., 1999; Patnaik et al., 2014a,b). B and C, Hypsodonty index and lamellar counts in M3 of proboscidean from specimens housed at CAS in Geology, PU and from published literature.

106e153). Early Pleistocene Elephas planifrons (HI, 87e100) ranged from being brachydont to moderately hypsodont, whereas E. hysudricus (HI, 184) and Elephas sp. (HI, 100e200) were moderate to highly hypsodont. Middle Pleistocene E. hysudricus from Karewas of Kashmir were also highly hypsodont (HI, 157e200). The late Pleistocene Palaeoloxodon namadicus was also moderately hypsodont (HI, 167). Late Pleistocene Elephas sp. from Narmada Valley was also highly hypsodont (HI, 214). The lamellar counts on the same specimens showed a similar tendency of increasing numbers through time (Table 6, Fig. 6). The Miocene forms such as Gomphotherium (LC, 2), Deinotherium (LC, 45), Stegolophodon (LC, 4-6), Tetralophodon (LC, 5), and Stegodon (LC, 4) had low cusp pairs/lamillae. The Pliocene indigenous Stegodon (LC, 6e8) and Anancus (LC, 4) had low to moderate numbers of cusp pairs, whereas the immigrant Elephas planifrons had high lamellar counts (LC, 10e15). Early Pleistocene Elephas planifrons (LC, 6-10) had moderate LC, whereas E. hysudricus (LC, 16) and Elephas sp. (LC, 6-15) had moderate to high lamellar counts. Middle Pleistocene E. hysudricus from Karewas of Kashmir also shows similar counts (LC, 6-11). The Late Pleistocene Palaeoloxodon namadicus and Elephas sp. from Narmada Valley were high in lameller counts (LC, 1516).

5.2.3. Comparision of Late Miocene dietary shift between the proboscideans from Africa and Indian subcontinent Lister (2013, Fig. 2), while analysing the environmental, behavioural, and morphological trends for East African proboscideans spanning the last 20 Myr, identified a Late Miocene ecological shift during which the brachydont gomphotheres with low lamellar counts shifted their diet from browsing to grazing. In constrast, the deinotheres continued browsing through out the Neogene. There was a significant increase in proboscidean lamellae numbers as the landscape changed from forest dominated to grassland dominated one. A clear trend in the increase in the hypsodonty of the grazing proboscideans also coincided with this major ecological shift. The Early Miocene vegetation in the Indian subcontinent was dominantly warm tropical rainforest (Patnaik, 2016 and reference therein). Palaeobotanical data suggest that the dominant

vegetation of the Siwaliks during the Middle Miocene comprised of evergreen forest with some moist deciduous elements (Srivastava et al., 2014). Therefore, the conditions were conducive for the African deinotheres and gomphotheres to disperse, even to higher latitudes to reach the Indian subcontinent. The isotope composition, hypsodonty, and lamellar count data shown in Fig. 6 indicate that the Middle Miocene deinotheres and gomphotheres were predominantly C3 browsers living in relatively closed forests and deriving water from 18O-depleted source(s) such as streams and ponds, and some likely from the leaves, branches and barks. This scenario is further supported by the isotope signature of associated mammals such as the tragulids, bovids, rhinocerotids and giraffids, which are C3 browsers (Table 5). By the Late Miocene, the Indian subcontinent landscape became drier and grasslands started replacing tropical forests (Hoorn et al., 2000). The Himalayan uplift during this time led to cooler and drier climate as indicated by the presence of high-altitude plant taxa such as Abies, Larix and Picea (Hoorn et al., 2000) in the Late Miocene Siwalik record. Palaeosols and mammalian data suggest a major ecological shift in the subcontinent between 8 and 5.5 Ma (Barry et al., 2002; Badgley et al., 2008 and references therein). Our results (Fig. 6) clearly indicate that the Late Miocene brachydont deinotheres and gomphotheres were still browsing in open wooded subtropical forests along with bovids, rhinocerotids, tragulids, and suids. Around this time (8-7 Ma), new brachydont proboscideans such as the indigenous Stegolophodon, Stegodon, and an immigrant Choerolophodon emerged on the Siwalik landscape. The early Stegolophodon, Stegodon, and a proboscidea indet. were all browsers whereas Choerolophodon and a gomphotherid were mixed feeder (Morgan et al., 1994; Stern et al., 1994; Cerling et al., 1999). Interestingly, the hypsodont equid Hipparion was also largely feeding on C3 plants around this time (cf. Nelson, 2007; Patnaik et al., 2014a,b). By Early Pliocene the landscape was dominated by grasslands with early immigrant Elephas sp. and proboscidea indet., which were all pure grazers (Quade et al., 1992; Morgan et al., 1994; Cerling et al., 1999). Interestingly, a mixed feeder (~84% grass in diet, SI Table 8) Hipparion emerged around this time, which was

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probably an immigrant. By Late Pliocene, the grassland dominated landscape favoured a variety of proboscideans Stegodon, Anancus, Elephas planifrons, Elephas platycephalus, and Elephas hysudricus. All these proboscideans were primarily grazers. However, Stegodon had a varied diet comprising of C3 browsing, mixed feeding to pure grazing. The Early Pleistocene Siwalik landscape was dominated by wet grasslands interspersed with gallery forests and water bodies such as ponds/swamps under monsoonal climatic conditions (Phadtare et al., 1994; Kotla et al., 2018). Highly hypsodont and pure grazers Elephas hysudricus and Elephas sp. were present on the landscape. Earlier workers (Ranga Rao et al., 1995) have recorded Elephas planifrons from this interval as well. We find Elephas planifrons to be almost purely a C4 grazer. It has been hypothesised that Palaeoloxodon arrived in Eurasia around 1 Ma ago (Van Der Made, 2010 and references therein). However, Palaeoloxodon namadicus fossils are recorded in only ~200 Ka deposits of central India. This study reveals mixed feeding to pure grazing signatures for these specimens. Besides, central India Palaeoloxodon has also been recorded from the Upper Karewas of Kashmir in the North-West Himalaya (Craig et al., 2014). From the Upper Karewas, Elephas hysudricus has also been recorded (Kotlia, 1990). The d13C (Table 5) of Karewa Elephas hysudricus clearly indicate that they were mainly browsers and occupied some sort of wooded or gallery forest. There appears to be a quantum shift in the diet of Elephas hysudricus from being a pure grazer in the early Pleistocene to a dominant browser in the Middle Pleistocene. We suggest this distinct dietary shift in Elephas hysudricus could be the result of its competition for the grassland with the colossal grazer immigrant Palaeoloxodon namadicus, which is considered by some as the largest terrestrial mammal to have ever lived on this planet (Larramendi, 2016). Maglio (1973) proposed that earlier species of Elephas including Elephas hysudricus were displaced by the invading Palaeoloxodon namadicus and Elephas hysudricus gave rise to Elephas maximus about 0.25 Ma ago. Our results indicate that browsing behaviour developed by Elephas hysudricus is most likely due to inter-species competition, pushing it into forested habitat, rather than due to any major climate change overall. Another factor that might have influenced this dietary shift among Elephas hysudricus could be the presence of early humans on the landscape. However, there is no evidence yet of hunting and butchery of elephants by early humans in India. Elephas maximus, descendant of E. hysudricus, would then have largely continued this dietary habit of substantial browsing within forest and woodland habitat in spite of their dentition being more indicative of adaptation to grazing. The spread of tropical moist forest during the Early Holocene under a warmer climate and intensified monsoon, as well as the spread of agricultural societies across river valleys and plains (thereby pushing elephants into hill forests) would have contributed to E. maximus sustaining a browsing diet. Modern observational studies on E. maximus indicate a predominantly browsing diet in tropical moist forest, and a mixed feeding strategy in tropical dry forest and savannawoodland (Sukumar, 2003). Carbon isotopic data from bone collagen of modern E. maximus also indicate a predominant browsing diet in tropical moist habitats (M. Roy and R. Sukumar, unpublished data) and mixed browse-grass diet in tropical dry forest (Sukumar and Ramesh, 1992). At the same time, modern E. maximus also feed on substantial quantities of grass both in their natural habitat as well as crop fields (both C3 and C4 cultivated grasses) when available or the opportunity arises (Sukumar, 1989, 2003). In other words, E. maximus is dentally adapted to grazing but its evolutionary history and its competition with modern humans has meant that browsing continues to be an important part of its diet.

6. Conclusions  Bulk and serial sampling d13C and d18O compositions of modern mammals from Mudumulai National Park clearly demonstrate niche partitioning.  The d13C values of IES are not significantly different from those of OES, but d18O of these surfaces show significant differences without displaying any particular trend.  A comparision of carbon and oxygen isotope compositions, hypsodonty, and lamellar count records in Neogene proboscideans from African and Indian subcontinent reveals an overall similar trend in the Late Miocene dietary shift (browsing to grazing) in both the continents. However, in Africa the Late Miocene ecological shift induced dietary shift among the indigenous proboscideans whereas, in the Indian subcontinent this shift led to immigration of proboscideans that were preadapted to the changing landscape.  Hypsodonty indices and lamellar counts of South Asian and some Southeast Asian proboscideans suggest that Middle and Late Miocene brachydonts with less lamellae were replaced by mostly hypsodont multilamellar taxa, while a few remained brachydont throughout. Except for Stegodon, all the Pleistocene taxa were hypsodont.  d13C values of dental enamel indicate that until the Latest Miocene all the brachydont proboscideans were predominantly browsers, supported by similar data from associated mammals such as giraffids (ex. Bramatherium), rhinoceratids, equids (ex. Hipparion), and bovids.  Pliocene brachydont Stegodon remained flexible with both browsing and grazing, whereas Anancus was a pure grazer. The hypsodont elephantine Elephas planifrons, E. platycephalus and E. hysudricus were all dominantly grazers.  Early Pleistocene Elephas planifrons and E. hysudricus as well as the associated mammals remained predominantly grazers.  With the arrival of the giant grazer Palaeoloxodon namadicus in the Middle Pleistocene, E. hysudricus shifted from grazing to predominantly browsing giving rise to E. maximus a mixed feeder with more C3 plants in its diet compared to C4 grasses. Acknowledgements This work was supported by a grant to RP by the Ministry of Earth Sciences, Government of India (MoES/P.O.(Geosci)/46/2015). RP thanks Chris Gilbert and Biren Patel for their help in fieldwork. RS was a JC Bose National Fellow, Department of Science and Technology, Government of India, during the tenure of this study. RS thanks the Tamil Nadu Forest Department for research permits since the 1980s on the ecology of Mudumalai which made it possible to analyse modern mammalian samples. We are very thankful to all the three reviewers and the handling editor for their critical and constructive comments. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.quascirev.2019.105968. References € nig, I.M.A., Prins, H.H.T., 2012. Diet and habitat-niche reAhrestani, F.S., Heitko lationships within an assemblage of large herbivores in a seasonal tropical forest. J. Trop. Ecol. 28 (4), 385e394. Araguas-Araguas, L., Froehlich, K., 1998. Stable isotope composition of precipitation over southeast Asia. J. Geophys. Res. 103 (D22), 28721e28742. Ayliffe, L., Chivas, A., 1990. Oxygen isotope composition of the bone phosphate of Australian kangaroos: potential as a paleoenvironmental recorder. Geochem.

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