PALAEODIETARY AND PALAEOCLIMATIC INTERPRETATIONS FOR HERBIVORE FAUNA FROM LATE PLIOCENE TO EARLY PLEISTOCENE SIWALIKS OF PAKISTAN

A. M. Khan1,*, A. Iqbal1, M. T. Waseem1, R. M. Ahmad2 and Z. Ali1

1Department of Zoology, University of the Punjab, Lahore Pakistan (54590)
2Department of Zoology, University of Okara, Punjab, Pakistan.
Corresponding Author: majid.zool@pu.edu.pk

ABSTRACT

Stable isotopes analysis of carbon and oxygen have the potential to explore the diet and climate of past communities. The end of Miocene in the Siwaliks of Pakistan marks faunal turnover due to climatic change with higher rates of aridity and an expansion of C4 grasslands. But after the Miocene, the studies regarding diet and climate of herbivore communities are still highly un-explored. We present here the analysis of δ13C and δ18O to estimate the diet and climate endeavored by herbivore communities from the Plio-Pleistocene Siwaliks of Pakistan. Our results indicate that the proportion of C3 diet in the Pliocene fauna was diminished but not absent while Pleistocene fauna do not report any evidences of C3 vegetation. The Pliocene and Pleistocene time span reports the flood plain environment with increased aridity which favored more C4 grasses from 3.6 to 0.6 Ma. We found that Pliocene and Pleistocene Siwalik faunas have close affinities with African faunal communities with respect to their dietary and ecological niche.

https://doi.org/10.36899/JAPS.2020.2.0057                                                                   Published online March 02, 2020

INTRODUCTION

                The Stable isotope analysis of carbon and oxygen is a pivotal tool to explore the palaeodiet and palaeoecology of the past communities (Quade et al., 1992; Levin et al., 2008; Levin, 2015; Cerling et al., 2011, 2015; Wynn et al., 2013). The reconstruction of palaeovegetation on floodplains in sub-tropical regions can be done precisely by using stable isotopes of carbon (Quade et al., 1989, 1995; Barry et al., 2002). The SI analysis of carbon is a reliable tool to differentiate C3 and C4 cycles utilized by any regional flora for photosynthesis (Ehlinger and Cooper, 1988; Vogel, 1978). The particular carbon isotopes markers can subsequently be recorded in the body tissues of primary consumers as C3 pathway mostly utilized by trees and most of the plants while C4 pathway is utilized by some shrubs and most of the grasses (DeNiro and Epstein, 1978). Thus carbon isotopes can be used to infer the dietary preferences of animals living in a specific landscape and carbon & oxygen isotopes can be utilized to reconstruct palaeoclimatic picture endeavored by these animals (Bibi, 2007; Cerling et al., 2011, 2015; Sponheimer et al., 2013; Du et al., 2019).  Thus, palaeo vegetation can be estimated from dietary signals being recorded in teeth of an animal, based on the fact that species dietary preferences are linked to physical as well as ecological attributes of its habitat (Cerling et al., 1997, 2015; Kingsten and Harris, 2007; Levin et al., 2015; Sponheimer et al., 2003, 2013; White et al., 2009). Such community based studies of carbon isotopes from enamel of herbivores are mostly used to infer the link between diet, vegetation and environment (Bibi, 2007; Levin, 2015).
                Oxygen isotopes depict the water intake preferences of herbivores. δ18O values of leaf are recorded to be higher than that of meteoric sources mainly due to evaporative enrichment factor (Yakir, 1997). Thus those mammals which take their water from plants tend to show a little higher δ18O values than that are obligate drinkers (Spoonheimer and Lee Thorp, 1999, 2001). Thus, we think browser should represent a more negative values than that of grazers. But the interpretation of oxygen isotopes is not straightforward, the oxygen isotope values are also linked to canopy effect, open land, open water holes, flowing water as well as the drinking preferences of animal (Estes, 1991). In this paper we have utilized oxygen isotopes to infer water intake preferences of Plio-Pleistocene fauna of the Upper Siwaliks of Pakistan.
                The Upper Siwaliks in Pakistan extends from 3.3-0.6 Ma, more conventionally, from late Pliocene to middle Pleistocene and allows us to investigate one of longest fluvial sequences (Dennell et al., 2006). Upper Siwaliks has been divided in three faunal stages viz. Tatrot, Pinjor and Boulder conglomerates (Pilgrim 1910, 1913). Tatrot/Pinjor boundary has been set at 2.58 Ma and latest Pinjor at <0.78 Ma. The Upper Siwaliks fauna has been explored scantily with reference to stable isotope analysis. Thus here we use stable isotopes of carbon and oxygen to explore the palaeodiet, palaeoclimate and palaeovegetation of mammalian communities of the Upper Siwaliks of Pakistan.
Geological Settings: Rendell, (2004) assigned two biostratigraphic intervals in the Upper Siwaliks on the basis of mammalian fauna and magnetostratigraphic controls. First is the Elephas planifrons interval spanning 3.6-2.6 Ma and second is Equus sivalensis interval spanning 2.6 to 0.6 Ma. These faunal intervals are based upon mammalian fauna and magnetostratigraphy. The taxa that are reported from Elephas planifron interval include Equids, Elephantids, Cervids, Bovids, Suids and Giraffes (Barry et al., 1982, 2002; Nanda, 2002). While Equus sivalensis interval also documents Equids, Cervids, Hippos, Giraffids, Suids, Bovids and Rhinos (Ghaffar et al., 2017).
                The village of Tatrot (Fig. 1a) is situated in Upper Siwaliks, 70 km west of Jhelum city (32°22`N, 72°47`E). The composition of Tatrot Formation includes clays, siltstone and shales while the color varies from reddish orange to brown. The medium to fine sized sandstones along with interbedded dark gray conglomerates are part of Tatrot Fm. The average thickness is accounted to be 300 m (Shah, 1980).
                The Pinjor Fm. is exposed at Sar Dhok and Pabbi Hills area (included in this study). The Sar Dhok (Fig. 1b) is characterized by greyish brown medium to fine grained sandstones with intermingling pebbles and large scaled cross stratification. Brown mudstones are also visible with pedogenic horizons while conglomerates are well imbricated in between. The type locality of Pinjor in India has been dated magneto-stratigraphically and has been assigned an age of 2.48-0.63 Ma. While Pabbi Hills also represent a large fluvial sequence with many fossiliferous sites (Fig. 1c) and the average thickness has been calculated as 1000 m. A comprehensive work of Dennell (2008) and Dennell et al., (2006) on Pabbi Hills reports the age of these foothills as upper Pliocene to middle Pleistocene (2.2-0.9 Ma). Our study includes the samples from Choawala Kas which contain the Sandstone 12 (Dennell et al., 2006) hence can be assigned an age of 1.2-1.4 Ma. So on the basis of above mentioned stratigraphic controls, we assign Tatrot as late Pliocene having an age of 3.4-2.6 Ma.  While the samples which are recovered from Sar Dhok has been assigned an age of 2.5-0.6 Ma and samples collected from Pabbi Hills Sandstone, an age of 1.4-1.2 Ma (Hussain et al., 1992; Barry et al., 2002, Nanda, 2008; Dennell et al., 2006).
                The collection for this study has been carried out from Tatrot, district Jhelum; Sar Dhok, district Gujrat and Pabbi Hills, northern Punjab, Pakistan (Fig. 1a,b,c).
                The stable isotope analysis of carbon and oxygen from Tatrot and Pinjor stage along with above mentioned stratigraphic controls, allow us to investigate the palaeodiet, palaeovegetation and palaeoclimate of late Pliocene to early Pleistocene mammalian fauna of the Upper Siwaliks, Pakistan.

MATERIALS AND METHODS

                A sum of 40 fossil specimens were selected on the basis of their morphologic and morphometric characteristics and their stratigraphic provenance. The specimens were cleaned by using detergents and water while dust was separated by using low speed drills. Specimens were then identified up to the species level. Twenty specimens from the Tatrot Fm. and twenty specimens from the Pinjor Fm. (5 from each studied family from Tatrot and Pinjor, respectively) were sampled for stable isotope analysis to check our hypothesis that there are significant differences in palaeodiet and palaeoclimate among the Pliocene and Pleistocene mammalian communities. The studied families included Rhinocerotidae, Bovidae, Suidae, Elephantidae and Equidae.   
                For the extraction of enamel, Foredom Rotary Dental Drill with carbide burrs was used. 15-20 mg of enamel was extracted from each tooth (only molars and pre-molars were included). Enamel was extracted along one single transect from root to crown (longitudinal) from buccal surface of upper and lingual surface of lower molars. Enamel was selected for the analysis due to its high resistance against diagenesis and large crystal size which make it the best tissue for isotope analysis (Koch et al., 1997).
                The powdered enamel was further pre-treated with 10 ml of 2% NaOCl for one hour and the solution was decanted and rinsed with distilled water for 3 times. The samples were than treated with 10 ml of 0.1% Acetic Acid for 1 hour and then samples were oven dried for further isotope analysis (Basics from Koch et al., 1997).
                For the Isotopic Ratio Mass Spectrometry, samples were shipped to PINSTECH, Islamabad, where further analysis was done. Carbon and oxygen isotope values were reported to isotope standards such that:
δ13C or δ18O = (R sample/R standard – 1)/1000
                The values were reported in V-PDB for both carbon and oxygen isotopes. As isotopic values were calculated from enamel samples of large herbivore species, thus a fractionation factor of 14 ‰ for elephants, bovids, equids, rhinos and 13‰ for suids was selected according to the Cerling and Harris (1999) and Sponheimer et al., (2003). For the Statistical analysis between Pinjor and Tatrot fauna, student t-test along with Wilcoxon test was used assuming un-equal variances. For the analysis of families within each stage, one-way ANOVA was applied along with post-hoc test. All the analysis and graphs were made using SPSS, version 16.

RESULTS

Carbon Isotopes Values: In carbon isotopes ratios, a range of values across Tatrot and Pinjor Fm. was found to be in between -9.38 ‰ to 3.29 ‰ and the difference of 12.67 ‰ was calculated for all the forty samples and across all the five families. The mean of all the analyzed samples is -3.55 ‰. The t-test along with the Wilcoxon test revealed significant differences (p<0.05; p=0.023) among late Pliocene (average δ13C = -5.7‰) and Pleistocene (average δ13C = 1.17‰) samples. When one-way ANOVA was applied, to check out the differences among Tatrot families (Pliocene), a significant difference was recorded (p=0.004). While Pleistocene families did not show any significant differences (p=0.138) among each other. The Pinjor (Pleistocene) fauna represented more enriched values of carbon stable isotopes as compared to the Tatrot fauna (late Pliocene) (Table 1).   
Oxygen Isotope Values: The δ18O ratios between all samples range from -11.2 ‰ to +2.46 ‰ and the average is -6.52 ‰. The t-test along with Wilcoxon test among Pinjor and Tatrot samples revealed non-significant differences (p=0.397). When the inter family comparison was carried out by applying one-way ANOVA with post hoc test, non-significant differences were found for oxygen isotopic ratios (p=0.072 and 0.342 for Tatrot and Pinjor families respectively).

DISCUSSION

Palaeodiet: Generally, the carbon isotope ratios follow the inferences based upon the functional morphology of tooth structure (Bibi, 2007), but sometimes it leads to confusions. For example, while predicting the diet for elephants, there was a confusion raised when some of the researchers reported that the recent elephants graze while other reported a browsing behavior (Tangley, 1997; Laws et al., 1974; Dublin, 1995; Norten and Griffiths, 1979). Such confusions while estimating the dietary niche of species require a more accurate proxy such as stable isotopes of carbon (Cerling and Harris, 1999).
                Here we try to reconstruct dietary and habitat preferences among 5 families across the Plio-Pleistocene Siwaliks of Pakistan. We present a comparative approach between 3 families from Pliocene and Pleistocene respectively, while elephantidae and suidae are reported only from Pliocene and Pleistocene respectively.
Family Equidae: Family Equidae has been considered as one of the early families who shifted their diets towards C4 grasses (Uno et al., 2011). The samples analyzed in this study show an average value for δ13C of -4.31‰ from Pliocene and -0.62‰ from Pleistocene indicating a clear shift towards C4 grasses (Fig. 3,4). Our results for equid diet are in-line with Uno et al., (2011) who explored the African fauna and reported an average of -1.0 ‰ from Apak Formation dated early Pliocene (4.2 Ma).
                The reported isotopic data complements the hypothesis based on morphological as well as mesowear analysis. The high HI index, sharp or blunt buccal apices of cusp and the increased complexity has indicated a grazing diet for Equid (Wolf et al., 2013; Fortelius and Solunieus, 2000). Such type of characters are also evident in recent horses which are grazers.
                The higher values for δ18O (-3.62 ‰ and -4.04 ‰ for Pliocene and Pleistocene Equids respectively) as compared to late Miocene horses (Nelson, 2005) indicate that open evaporating water holes were available for drinking to the horses in Pliocene and Pleistocene time spans while the riverine system was shrank as compared to late Miocene (Barry et al., 2002; Dennell, 2008).
Family Rhinocerotidae: The family Rhinocerotidae represents an interesting case across the Plio-Pleistocene Siwaliks of Pakistan. The Pliocene Rhinos (R. sivalensis and R. platirhinus) represent δ13C average of -7.96‰ which is indicative of mixed C3 and C4 feeding with closer affinities towards C3 type feeding. R. sivalensis show dental affinities towards C3 type vegetation as its dental size is smaller and less complex but R. platirhinus has complex dental pattern with high crown (Khan et al., 2014) indicative of C4 feeding. While the Rhinos from Pleistocene (R. sondicus and R. unicornis) reveals highly enriched values with δ13C averaging as 0.3 ‰ which is indicative of feeding purely on C4 grasses. The picture in African faunal community is synchronous to Pleistocene of Siwaliks but not with Pliocene values. Uno et al., (2011) report a δ13C average of -2.4‰ and 0.3‰ from Apak (4.2Ma) and Kaymun Formation (3.2Ma) which represents that Rhinos shifted on C4 type feeding at the end of late Miocene time span in Africa. We suggest that some species of Rhinos were still C3 feeders in Pliocene while other shifted to C4 feeding. This hypothesis needs further attestation with larger sample size across all the Plio-Pleistocene Rhinoceros species of the Siwaliks of Pakistan.
                Oxygen isotope analysis of family Rhinocerotidae shows δ18O average of -9.54‰ and -5.79‰ for Pliocene and Pleistocene Rhinos respectively. These values indicate that the water intake behavior of Pliocene Rhinos was different from Pleistocene Rhinos with former drinking under shaded ecosystem while later drinking on open water bodies with higher rates of evaporation. Alternatively, there was a shift in rainfall seasons or amount rainfall from Pliocene to Pleistocene due to further uplift of Himalaya which caused more pronounced seasonality (Nelson, 2007).
Family Bovidae: Family Bovidae has been reported to be adapted towards more C4 feeding at the end of late Miocene (Barry et al., 2002; Uno et al., 2011) and shifted completely on C4 feeding in Plio-Pleistocene as our results show δ13C average value of 0.87‰ and -2.37‰ (Figure 2,3) from Pliocene and Pleistocene respectively. Contemporary African bovids shows a range of -6.6‰ to -2.2‰ at 3.2 Ma (Uno et al., 2011) indicating a slow shift towards C4 vegetation. However, our results show no significant difference between Pliocene to Pleistocene bovids (p>0.05) thus, we assume that bovids were consistently grazers throughout the Upper Siwaliks. Our results agree with the findings of Wynn et al., (2013); Cerling et al., (2015) and White et al., (2009) who reported that bovids fed on C4 grasses at the start of Pliocene.
                The δ18O values of -7.65‰ and -6.40 ‰ across Plio-Pleistocene respectively indicate that former utilized plant water (based on the bovids physiology) from shaded areas while later utilized foliage from more open environment with higher rates of evapotranspiration (Bibi, 2007, 2009). We suppose that the environment of Pleistocene has more pronounced seasonality which effected the pattern of rainfall, plant cover and overall environment.
Family Elephantidae and Suidae: Stable isotope values of carbon and oxygen for Elephants and Suids are reported from Pliocene and Pleistocene respectively. Our analysis of Elephants (E. planifrons and E. hysudricus) indicate a pure C4 grazing behavior for Pliocene elephants with δ13C average of -1.3 ‰. In the late Miocene, the elephants were more browsers but they shifted their dietary niche towards grazing in Pliocene having enriched carbon isotope value (Cerling and Harris, 1999; Sukumar and Ramesh, 1995 and Uno et al., 2011).
                The average δ13C value for suids in Pleistocene is -2.0‰ which supports that suids fed on grasses in Pleistocene. The results are in-line with African picture with suids feeding on C4 vegetation in Pleistocene. Extant suids also feed on C4 grasses (Cerling et al., 2015).
                The δ18O values for Elephants from Pliocene and Suids from Pleistocene are -5.28‰ and -6.84‰ (Figure 2,3) respectively indicating that these animals preferred a mosaic of shady and open environment. The role of seasonality should be evaluated in order to understand amount of annual rainfall. We suppose that the rainfall was seasonal where few months of summers have more rainfall as compared to other months of dry winters (Unpublished data).

Conclusion: The analysis of carbon and oxygen stable isotopes revealed that Plio-Pleistocene environment supported C4 grasslands at the expense of C3 vegetation and most of the mammalian species fed on grasses which is also evident from morphological and mesowear analysis. The environment was arid and the aridity increased towards Pleistocene times while most of the animals relied on evaporative water holes or on the foliage cover of open areas for their water intake. The higher oxygen isotope values in Pleistocene indicate that the riverine system was shrunk as compared to late Miocene and Pliocene.
                We suggest a detailed study of seasonality with large samples size across the Upper Siwaliks which can answer our question more precisely and will allow us to reconstruct the role of seasonal extremes in the Upper Siwalik mammalian communities.
Acknowledgments: The financial support for this study was provided by University of the Punjab, Lahore, Pakistan. We thank Dr. Sherry V. Nelson and Dr. Larry Flynn for their comments on the manuscript which helped us to improve the quality of the initial version of this manuscript. We also want to thank Abid Seth for his assistance during the field work.  

REFERENCES

1. Barry, J. C., E. H. Lindsay and L. L. Jacobs (1982). A biostratigraphic zonation of the middle and upper Siwaliks of the Potwar Plateau of northern Pakistan. Palaeogeograp. Palaeoclimatol. Palaeoecol. 37: 95–130.

1. Barry, J. C., M. Morgan, L. J. Flynn, D. Pilbeam, A. K. Behrensmeyer, S. M. Raza, I. Khan, C. Badgely,  J. Hicks and J. Kelley (2002). Faunal and Environmental change in the Late Miocene Siwaliks of Northern Pakistan. Palaeobiology, 28:1–72. doi:10.1666/0094-837328
2. Badgley, C., J. C. Barry, M. E. Morgan, S. V. Nelson, A. K. Behrensmeyer, T. E, Cerling and D. Pilbeam (2008). Ecological changes in Miocene mammalian record show impact of prolonged climatic forcing. Proc. Nat. Acad. Scien. 105: 12145–12149.
3. Bibi, F. (2007). Origin, paleoecology, and paleobiogeography of early Bovini. Palaeogeograp. Palaeoclimatol. Palaeoecol. 248(1–2): 60–72. https://doi.org/10.1016 /j.palaeo.2006.11.009.
4. Bibi, F. (2009). Evolution, Systematics, and Paleoecology of Bovinae (Mammalia: Artiodactyla) from the Late Miocene to the Recent.Ph.D. Thesis, Yale University, New Haven.
5. Cerling, T. E., S. A. Andanje, S. A. Blumenthal, F. H. Brown, K. L. Chritz, J. M. Harris, J. Hart,  F. Kirera, P. Kaleme, L. Leakey, L. Meave, N. E. Levin, F. Manthi, B. H. Passey and K. T. Uno, (2015). Dietary changes of large herbivores in the Turkana Basin, Kenya from 4 to 1 Ma. Proc. Natl. Acad. Sci. U. S. A. 112: 11467–11472.
6. Cerling, T. E. and J. M. Harris (1999). Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120: 347–363.
7. Cerling, T.E., J. M. Harris, S. H.  Ambrose, M. G.  Leakey and N. Solounias (1997). Dietary and environmental reconstruction with stable isotope analyses of herbivore tooth enamel from the Miocene locality of Fort Ternan, Kenya. J. Hum. Evol. 33: 635–650.
8. Cerling, T. E., J. G. Wynn, S. A. Andanje, M. I. Bird, D. K. Korir, N. E. Levin, W. Mace, A. N. Macharia, J. Quade and C. H. Remien (2011). Woody cover and hominin environments in the past 6 million years. Nature 476: 51–56.
9. DeNiro, M.J. and S. Epstein (1978). Influence of diet on the distribution of carbon isotopes in animals. Geo. Cosm. Acta 42: 495–506.
10. Dennell, R. W. (2008). The taphonomic record of Upper Siwalik (Pinjor stage) landscapes in the Pabbi Hills, northern Pakistan, with consideration regarding the preservation of hominin remains. Quarter. Int. 192(1): 62–77. https://doi.org/ 10.1016/j.quaint.2007.06.024
11. Dennell, R., R. Coard. and A. Turner (2006). The bio - stratigraphy and magnetic polarity zonation of the Pabbi Hills, northern Pakistan: An Upper Siwalik (Pinjor Stage) Upper Pliocene-Lower Pleistocene fluvial sequence. Palaeogeog. Palaeoclimatol. Palaeoecol. 234: 168-185.
12. Du, A., I. A. Lazagabaster, J. R. Robinson, A. K. Behrensmeyer and J. Rowan (2018). Stable carbon isotopes from paleosol carbonate and herbivore enamel document differing paleovegetation signals in the eastern African Plio-Pleistocene. Rev. Palaeobot. Palynol. 261: 41–52. https://doi.org/10.1016/ j.revpalbo. 2018.11.003
13. Dublin, H.T. (1995). Vegetation dynamics in the Serengeti-Mara ecosystem: the role of elephants, fire, and other factors. In: Sinlair ARE, Arcese P (eds) Serengeti II: dynamics, manage- ment, and conservation of an ecosystem. University of Chicago Press, Chicago, pp 71-90
14. Ehleringer, J. R., and T. A. Cooper (1988). Correlations between carbon isotope ratio and microhabitat in desert plants. Oecologia 76: 562–566.
15. Estes, R. D. (1991). The Behavior Guide to African Mammals. University of California Press, Berkeley and Los Angeles.
16. Fortelius, M. and N. Solounias (2000). Functional characterization of ungulate molars using the abrasion-attrition wear gradient: A new method for reconstructing paleodiets. Am. Mus. Novit. 3301: 1–36.
17. Ghaffar, A., M. A. Khan, A. M. Khan, M. K. Siddiq, M. Akhtar and M. I. Azeem (2017). Antler remains (Cervidae, Artiodactyla, Mammalia) from a new locality in the Pinjor Formation (1.6–0.8 Ma), Pakistan. Revist. Brasileira de Paleontologia. 20(1): 23–30. https://doi.org/10.4072/rbp. 2017.1.02.
18. Hussain, S., G. Van Der Bergh, K. Steensma, J. De Vissier, J. De Vos, M. Arif, J. Van Dam, P. Sondaar and S. Malik (1992). Biostratigraphy of the Plio–Pleistocene continental sediments (Upper Siwaliks) of the Mangla–Samwal anticline, Azad Kashmir, Pakistan. Proc. K. Ned. Akad. Wet., Ser. B. 95: 65–80.
19. Kingston, J. D. and T. Harrison (2007). Isotopic dietary reconstructions of Pliocene herbivores at Laetoli: Implications for early hominin evolution. Palaeogeogr. Palaeoclimatol. Palaeoecol. 243: 272–306.
20. Koch, P. L., N. Tuross, and M. L. Fogel (1997). The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite. J. Archaeol. Sci. 24: 417–429.
21. Kohn, M. J., J. Rakovan and J. M. Hughes (2002). Phosphates. Geochemical, Geobiological, and Materials Importance. Reviews in Mineralogy and Geochemistry. Mineralogical Society of America, Washington, D. C. 48: 455-488
22. Laws, R. M., I. S. C. Parker and R. C. B. Johnstone, (1974). Elephants and their habitats: the ecology of elephants in North Bunyoro, Uganda. Clarendon, Oxford.
23. Levin, N. E. (2015). Environment and climate of early human evolution. Annu. Rev. Earth Planet. Sci. 43: 405–429.
24. Levin, N. E., Y. Haile-Selassie, S. R. Frost and B. Z. Saylor (2015). Dietary change among hominins and cercopithecids in Ethiopia during the early Pliocene. Proc. Natl. Acad. Sci. U. S. A. 112: 12304–12309.
25. Levin, N. E., S. W. Simpson, J. Quade, T. E. Cerling and S. R. Frost (2008). Herbivore enamel carbon isotopic composition and the environmental context of Ardipithecus at Gona, Ethiopia. Geol. Soc. Am. Spec. Pap. 446, 215–234.
26. Nanda, A. C. (2002). Upper Siwalik mammalian faunas of India and associated events. Jour. Asian Earth Sci. 21: 47–58.
27. Nanda, A. C. (2008). Comments on the Pinjor Mammalian Fauna of the Siwalik Group in relation to the post-Siwalik faunas of Peninsular India and Indo-Gangetic Plain, Quaternary Internat. 192: 6-13.
28. Nelson, S. V. (2005). Paleoseasonality inferred from equid teeth and intra-tooth isotopic variability. Palaeogeograp. Palaeoclimatol. Palaeoecol. 222: 122–144.
29. Nelson, S. V. (2007). Isotopic reconstructions of habitat change surrounding the extinction of. Sivapithecus, a Miocene hominoid, in the Siwalik Group of Pakistan. Paleogeogr. Paleoclimatol. Paleoecol. 243: 204–222.
30. Norton and M. Griffiths (1979). The influence of grazing, browsing, and fire on the vegetation dynamics of the Serengeti. In: Sinclair ARE, Norton-Griffiths M (eds) Serengeti: dynamics of an ecosystem. University Chicago Press, Chicago, pp 310-352
31. Pilgrim, G. E. (1910). Notices of new Mammalian genera and species from the Tertieries of India-Calcutta. Rec. Geol. Surv. Ind. 40: 63–71.
32. Pilgrim, G. E. (1913). Correlation of the Siwaliks with mammal horizons of Europe. Rec. Geol. Surv. Ind. 43:264–326.
33. Quade J., T. E. Cerling, M. M. Morgan, D. R. Pilbeam, J. Barry, A. R. Chivas, J. A. Lee–Thorp and N. J. van der Merwe (1992). A 16 million year record of paleodiet using carbon and oxygen isotopes in fossil teeth from Pakistan. Chem. Geol. 94: 183–192.
34. Quade, J., T. E. Cerling, P. Andrews and B. Alpagut (1995). Paleodietary reconstruction of Miocene faunas from Paşalar, Turkey using stable carbon and oxygen isotopes of fossil tooth enamel. J. Hum. Evol. 28: 373.
35. Quade, J., T. E. Cerling and J. R. Bowman (1989). Development of Asian monsoon revealed by marked ecological shift during the latest Miocene in northern Pakistan. Nature 342: 163–166.
36. Rendell, H. (2004). Magnetic polarity stratigraphy of Upper Siwalik sediments in the Pabbi Hills. In: Dennell, R.W. (Ed.), Early Hominin Landscapes in the Pabbi Hills, Northern Pakistan, British Archaeological Reports International Series. 1265: 32– 36.
37. Sanyal, P., S. K. Bhattacharya and M. Prasad (2005). Chemical diagenesis of Siwalik sandstone : Isotopic and mineralogical proxies from Surai Khola section , Nepal, 180: 57–74. https://doi.org/10.1016/j.sedgeo.2005.06.005
38. Sanyal, P., S. K. Bhattacharya, R. Kumar, S. K. Ghosh and S. J. Sangode (2005). Palaeovegetational reconstruction in Late Miocene: A case study based on early diagenetic carbonate cement from the Indian Siwalik, 228: 245–259. https://doi.org/10.1016/j.palaeo.2005.06.007
39. Shah, S. M. I. (1980). Stratigraphy and economic geology of Central Salt Range. – Records of the Geological Survey of Pakistan, 52: 1-104.
40. Sponheimer, M., Z. Alemseged, T. E. Cerling, F. E. Grine, W. H. Kimbel, M. G. Leakey, J. A. Lee- Thorp, F. K. Manthi, K. E. Reed, B. A. Wood and J. G. Wynn (2013). Isotopic evidence of early hominin diets. Proc. Natl. Acad. Sci. U. S. A. 110: 10513–10518.
41. Sponheimer, M. and J. A. Lee-Thorp (1999). Oxygen isotopes in enamel carbonate and their ecological significance. J. Archaeol. Sci. 26: 723–728.
42. Sponheimer, M. and J. A. Lee-Thorp (2001). The oxygen isotope composition of mammalian enamel carbonate from Morea Estate, South Africa. Oecologia. 126: 153–157.
43. Sponheimer, M., J. A. Lee-Thorp, D. DeRuiter, J. Smith, N. van der Merwe, K. E. Reed, C. Grant, L. Ayliffe, T. Robinson, C. Heidelberger and W. Marcus (2003). Diets of southern African Bovidae: Stable isotope evidence. J. Mammal. 84: 471–479.
44. Sukumar, R. and R. Ramesh (1995). Elephant foraging: Is browse or grass more important? A Week with Elephants, eds Daniel JC, Datye H (Bombay Natural History Society, Bombay and Oxford University Press, New Delhi) Pp 368–374.
45. Tangley, L. (1997). In search of Africa's forgotten forest elephant. Science. 275:1417-1419
46. Uno, K. T., T. E. Cerling, J. M. Harris, Y.  Kunimatsu, M. G. Leakey and M. Nakatsukasa (2011). Late Miocene to Pliocene carbon isotope record of differential diet change among East African herbivores. Proc. Nat. Acad. Sci. USA. 18: 1–6. https://doi.org/10.1073/pnas.1018435108
47. van der Merwe, N.J. and E. Medina (1991). The canopy effect, carbon isotope ratios and foodwebs in Amazonia. J. Archaeol. Sci. 18: 249–259.
48. Vogel, J. C., (1978). Recycling of CO2 in a forest environment. Oecologia Plantarum 13: 89–94.
49. White, T. D., S. H. Ambrose, G. Suwa, D. F. Su, D. DeGusta, R. L. Bernor, J. R. Boisserie, M. Brunet, E. Delson, S. Frost, N. Garcia,  I. X. Giaourtsakis, Y. Haile-Selassie, F. C. Howell, T. Lehmann, A. Likius, C. Pehlevan, H. Saegusa,  G. Semprebon, M. Teaford and E. Vrba (2009). Macrovertebrate paleontology and the Pliocene habitat of Ardipithecus ramidus. Science. 19. 327: 1454.
50. Wolf, D., R. L Bernor and S. T. Hussain (2013). A systematic, biostratigraphic, and paleobiogeographic reevaluation of the Siwalik Hipparionine horse assemblage from the Potwar Plateau, Northern Pakistan. Palaeontographica Abt. A.300: 1–115.
51. Wynn, J. G., M. Sponheimer, W. H. Kimbel, Z. Alemseged, K. Reed, Z. K. Bedaso and J. N. Wilson (2013). Diet of Australopithecus afarensis from the Pliocene Hadar formation, Ethiopia. Proc. Natl. Acad. Sci. U. S. A. 110, 10495–10500.
52. Yakir, D. (1997). Oxygen-18 of leaf water: a crossroad for plant associated isotopic signals. In: Griffiths, H. (Ed.), Stable Isotopes: Integration of Biological, Ecological, and Geochemical Processes. BIOS, Oxford, pp. 147–168.