Oxygen isotope in archaeological bioapatites from India: Implications to climate change and decline of Bronze Age Harappan civilization

• Anindya Sarkar
• , Arati Deshpande Mukherjee
• , M. K. Bera
• , B. Das
• , Navin Juyal
• , P. Morthekai
• , R. D. Deshpande
• , V. S. Shinde
•  & L. S. Rao

• Abstract

  The antiquity and decline of the Bronze Age Harappan civilization in the Indus-Ghaggar-Hakra river valleys is an enigma in archaeology. Weakening of the monsoon after ~5 ka BP (and droughts throughout the Asia) is a strong contender for the Harappan collapse, although controversy exists about the synchroneity of climate change and collapse of civilization. One reason for this controversy is lack of a continuous record of cultural levels and palaeomonsoon change in close proximity. We report a high resolution oxygen isotope (δ18O) record of animal teeth-bone phosphates from an archaeological trench itself at Bhirrana, NW India, preserving all cultural levels of this civilization. Bhirrana was part of a high concentration of settlements along the dried up mythical Vedic river valley ‘Saraswati’, an extension of Ghaggar river in the Thar desert. Isotope and archaeological data suggest that the pre-Harappans started inhabiting this area along the mighty Ghaggar-Hakra rivers fed by intensified monsoon from 9 to 7 ka BP. The monsoon monotonically declined after 7 ka yet the settlements continued to survive from early to mature Harappan time. Our study suggests that other cause like change in subsistence strategy by shifting crop patterns rather than climate change was responsible for Harappan collapse.

  Introduction

  The rise of the post-Neolithic Bronze Age Harappan civilization 5.7–3.3 ka BP (ca. 2500 to 1900 year BC; all ages henceforth mentioned are in cal year BP) spread along the Indus Valley of Pakistan through the plains of NW India, including into the state of Gujarat and up to the Arabian Sea and its decline has remained an enigma in archaeological investigation1,2,3,4,5,6. In the Indian subcontinent the major centers of this civilization include Harappa and Mohenjo-Daro in Pakistan and Lothal, Dholavira and Kalibangan in India (Fig. 1A). In recent years excavation at Rakhigarhi and few other places indicate that the civilization probably was more expansive than thought before7,8,9. Whatever may be the extent most Harappan settlements grew in the floodplains of river systems including those of the Indus or now defunct Ghaggar-Hakra (mythical river Saraswati?). Climatically although these regions fall under the influence of the Indian summer monsoon, they are currently semi-arid receiving much lesser rainfall than the mainland India. Because the monsoon showed significant variation over, both on short and long term time scale, throughout the Holocene period, attempts have been made to relate the evolution of the Harappan civilization to the changes in monsoon. Accordingly, the flourishing Harappan civilization and its decline have been linked to the intensification of monsoon during the Mid-Holocene climate optimum and its subsequent weakening, respectively. The evidence comes from a variety of sources like distant lake sediments in the Thar desert10,11, foraminiferal oxygen isotopes in Arabian sea cores12, fluvial morphodynamics3, and climate models13. Although the collapse of the Harappan as well as several contemporary civilisations like Akkadian (Mesopotamia), Minoan (Crete), Yangtze (China) has been attributed to either weakening of monsoon or pan-Asian aridification (drought events) at ~4.1 ka6,10,11, the evidence is both contradictory and incomplete. Either the climatic events and cultural levels are asynchronous11,14,15 or the climate change events themselves are regionally diachronous16 and references therein).

  (A) Map of Northwest India and Pakistan (created by Coreldraw x7;http://www.coreldraw.com) showing the locations of main Harappan settlements including phosphate sampling site of Bhirrana, Haryana, IWIN precipitation sampling station at Hisar and two paleo-lakes Riwasa and Kotla Dahar studied earlier (see Fig. 3 and text for details). Black dotted lines represent 100 mm rainfall isohyets. Approximate trace of dried paleo-channel of ‘Saraswati’ (dashed white lines in Fig. 1A) is also shown. Black arrow indicates the direction of monsoon moisture transport from Bay of Bengal. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article). Figure created by CorelDRAW Graphics Suite X7 (http://www.coreldraw.com) (B) Panoramic view of the excavation of mature Harappan stage at Bhirrana view from North-east (photograph reproduced with the permission of Archeological Survey of India).

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  Potential reasons for these conflicting interpretations is that the climate reconstructions were made from locations (e.g., Thar Desert or Arabian Sea) distant from the main Harappan settlement areas or that the climate proxies (e.g., sedimentology and geochemistry in lakes) could have been influenced by multiple local parameters apart from mere rainfall or temperature. To date no continuous climate record has existed close to or from the Harappan settlements. Here we report a high resolution bulk oxygen isotope (δ18O) record of animal teeth and bone phosphates (bioapatites) from an excavated archaeological trench at Bhirrana, state of Haryana, NW India, to reconstruct a paleomonsoonal history of the settlement site itself. Based on radiocarbon ages from different trenches and levels the settlement at Bhirrana has been inferred to be the oldest (>9 ka BP) in the Indian sub-continent8,17,18. To check its validity we dated archaeological pottery from two cultural levels using optically stimulated luminescence (OSL) method and thus investigated the interrelationship between the cultural levels and climate change that occurred right at the settlement, a critical gap in information that exists in our present understanding of the Harappan civilization.

  Harappan civilization and archaeology of Bhirrana

  Archaeological chronologies of Harappan (Indus) civilization in South Asia2,16,19 are given in SI. Conventionally the Harappan cultural levels have been classified into 1) an Early Ravi Phase (~5.7–4.8 ka BP), 2) Transitional Kot Diji phase (~4.8–4.6 ka BP), 3) Mature phase (~4.6–3.9 ka BP) and 4) Late declining (painted Grey Ware) phase (3.9–3.3 ka BP13,19,20). This chronology is based on more than 100 14C dates from the site of Harappa and nearby localities. These periodization is temporally correlatable with the Indus valley civilisations from Baluchistan and Helmand province proposed by Shaffer21. While the first two phases were represented by pastoral and early village farming communities, the mature Harappan settlements were highly urbanized with several organized cities, developed material and craft culture having trans-Asiatic trading to regions as distant as Arabia and Mesopotamia. The late Harappan phase witnessed large scale deurbanization, population decrease, abandonment of many established settlements, lack of basic amenities, interpersonal violence and disappearance of Harappan script22,23,24. Although referred to as a ‘collapse’ of Harappan civilization, evidences rather suggest that smaller settlements continued albeit dispersed from original river valleys of Indus and Ghaggar-Hakra (Fig. 1A) to more distant areas of the Himalayan foothills and Ganga-Yamuna interfluves or Gujarat and Rajasthan25,26,27.

  Based on the spatio-temporal distribution of the archaeological remains spread throughout the subcontinent a much older chronology has, however, been advocated by Possehl22,16. Accordingly the time spans of the above four phases have been suggested as ~9–6.3 ka BP, 6.3–5.2 ka BP, 5.2–3 ka BP and 3–2.5 ka BP respectively. Clearly the later time scale pushes back the Harappan chronology to at least 1–2 ka older. Evidences of a post-Neolithic-Pre Harappan (often referred to as the Hakra ware) phase were first reported by Mughal28,29 in the Cholistan region east of the Indus valley along the Indo-Pakistan border, but have now been found from several localities in India. The Hakra settlements, spread along the Ghaggar-Hakra river valleys have been found at Kalibangan, Farmana, Girawad, Rakhigarhi and Bhirrana, the present site of investigation (Fig. 1A 30,31,32,33). A large number (~70) of conventional and AMS radiocarbon dates indeed support the antiquity of this phase in different parts of the Indus-Ghaggar Hakra river belts viz. Girawad (Pit-23, 6.2 ka BP), Mithathal (Trench A-1, 8.2 ka BP), Kalibangan (sample TF-439, 7.6 ka BP). The recent excavations at Rakhigarhi suggest hitherto unknown largest Harappan settlement in India preserving all the cultural levels including the Hakra phase (sample S-4173, 6.4 ka BP8,9,34,35).

  A compilation of calibrated radiocarbon dates of the charcoal samples and OSL dates of pottery (see later discussion) from various cultural levels of Bhirrana (Lat. 29°33′N; Long. 75°33′E), retrieved during the excavation of 2005, is given in SI8,18. At Bhirrana the earliest level has provided mean 14C age of 8.35 ± 0.14 ka BP (8597 to 8171 years BP8). The successive cultural levels at Bhirrana, as deciphered from archeological artefacts along with these 14C ages, are Pre-Harappan Hakra phase (~9.5–8 ka BP), Early Harappan (~8–6.5 ka BP), Early mature Harappan (~6.5–5 ka BP) and mature Harappan (~5–2.8 ka BP8,17,18,20,34). Cultural stratigraphy of Bhirrana settlement depicting the periods, cultural levels, ages based on calibrated radiocarbon ages in different trenches and characteristic archeological artefacts and attributes are given in SI8,17,20. A panoramic view of the excavation of the mature Harappan level at Bhirrana view from north-east is shown in Fig. 1B. Figure 2Ashows the settlement pattern of pre-Harappan Hakra phase (period 1A 8) along with locations of three major trenches at Bhirrana mound YF-2, A-1, and ZE-10. A schematic E-W cross section of the trench YF-2 depicting the cultural levels at Bhirrana is shown in SI. Fig. 2B (inset) shows the tentative lateral time correlation based on radiocarbon and OSL dates generated during present investigation (see later discussion). The Bhirrana settlement, close to the presently dried up Ghaggar-Hakra (Saraswati) river bed preserves all the major laterally traceable and time correlatable cultural levels. As expected in trench A-1, the central part of the archaeological mound, the Hakra or other phases are much thicker (>3 m) compared to the flanking trenches of YF-2 and ZE-10. At Bhirrana the Hakra ware culture period is the earliest and occurs as an independent stratigraphic horizon17,34. The Hakra phase was primarily identified by ceramics such as mud appliqué ware, incised ware, and bi-chrome ware, much similar to the Pre-Harappan phase in Cholistan (Figs 1A and 3C 36) and was characterized by its subterranean dwelling, sacrificial and industrial pits8,17,34. The Early Harappan phase shows settlement expansion, mud brick houses with advanced material culture including arrow heads, rings and bangles of copper; beads of carnelian, jasper, and shell; bull figurines; chert blades; terracotta bangles, etc. (Fig. 3C) 17,32,34). The early mature to mature Harappan phases yielded ceramics with geometric, floral and faunal motifs; steatite bull seals; beads of semi-precious stone, shell and terracotta; animal figurines; bangles of faience and shell; copper bangles, chisels, rings, rods, etc.17,34. The excavations also yielded large quantities of faunal remains comprising bones, teeth, horn cores, etc. from all the four periods at Bhirrana and were identified at species levels37. Detail methods of faunal analysis for materials from the Bhirrana trench YF2 are given in the SI. Preliminary faunal investigations suggest presence of domestic cattle e.g., cow/ox (Bos indicus), buffalo (Bubalus bubalis), goat (Capra hircus) and sheep (Ovis aries) from the earliest levels. Besides the dietary use of cattle and goats, wild fauna such as nilgai (Boselaphas tragocamelus), Indian spotted deer (Axis axis) and antelope (Antilope cervicapra) were also a part of the diet37,38,39,40. Representative photographs of the artefacts and animal remains from various cultural levels of Bhirrana are shown in SI.

  (A) Settlement pattern of period 1A (pre-Harappan Hakra) along with locations of trenches at Bhirrana mound. Figure created by CorelDRAW Graphics Suite X7 (http://www.coreldraw.com) (B) Tentative lateral time correlation of different cultural levels between the trenches based on radiocarbon and OSL dates. Contours are in cm. above msl. Only the trench YF-2 yielded continuous bioapatite samples (see text).

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  (A) Arabian Sea upwelling intensity as monsoon index57. (B) Carbonate δ18O and lake level records from paleo-lakes Riwasa and Kotla Dahar, Haryana (refs 5 and 6). (C) Bioapatite based paleo-meteoric water δ18O (monsoon proxy) record at Bhirrana along with characteristic archaeological and faunal elements from different cultural levels. Note monsoon intensification from ~9 ka to 7 ka BP (blue shaded region and arrows) and monotonous decline from ~7 ka to 2.8 ka BP (brown shaded region, red arrows); dotted pink lines denote approximate time correlation of these two phases across the sites. (D) Bhirrana chronology based on archaeological evidences17,18,32, 14C and new OSL dates. OSL dates are from trench YF-2; the oldest 14C date is from correlatable level of trench ZE-10 (E) Conventional chronology19,20; note new dates, archaeological evidences and climate pattern are all suggestive of a much older age for the beginning of Harappan civilization at Bhirrana.

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  For retrieving information on past climatic changes we isotopically analysed bulk (see SI text) teeth and bone phosphates, wherever available, from the trench YF-2 which has both stratigraphic and sampling continuity (SI Table 2). To check the validity of the radiocarbon dates and the antiquity of the Bhirrana settlement we dated two pottery fragments (SI Fig. 1) in the same trench by OSL technique from both early mature and mature Harappan intervals. Detail methodology is given in SI text. The pottery at 42 cm, identified as mature Harappan level yielded mean 4.8 ± 0.3 (1σ) ka BP age (range 5120 to 4520 year BP) while the pottery from deeper level corresponding to early mature Harappan at 143 cm yielded 5.9 ± 0.25 (1σ) ka BP age (range 6185 to 5695 year BP). Within the experimental errors both the stratigraphically controlled new ages agree with the time scale based on archaeological evidences (as well as 14C ages) proposed by earlier workers8,17,18,34; Fig. 3C,D) and suggest that the Bhirrana settlements are the oldest of known sites in the Ghaggar-Hakra tract.Figure 3D,E show the comparison between the conventional chronology of the Harappan civilization with the proposed chronology at Bhirrana. Clearly the Bhirrana levels are few thousand years older. The 5.9 ka age at 143 cm along with the 8.38 ka age of the Hakra level below suggest that the base of the Bhirrana section, representing initiation of Harappan settlements (Hakra phase), is older than 8 ka BP. Below we show that isotope based paleoclimatic information also lends supports to the antiquity of Harappan settlements at Bhirrana.

  Oxygen isotope (δ18O) in bioapatites and past monsoon record at Bhirrana excavation site

  δ18O [defined as δ (%) = {(Rsample − Rreference)/Rreference} × 1000; R = 18O/16O ratio] composition of fossil bone or tooth enamel bioapatite [carbonated hydroxyapatite41] is a robust tool for estimating the past meteoric water composition (drinking water for land animals41,42,43,44,45,46) compared to carbonates which are prone to diagenetic alteration. Near-continuous teeth and bone samples were available only in trench YF-2 and have been analysed. SI Fig. 4 shows the representative teeth and bone samples analysed from all the four cultural levels of Bhirrana. The samples comprise a large variety of bioapatites from mandibular and maxillary molar teeth of cattle, goat, deer and antelope to rib and vertebra bones. Since diagenetic alteration can alter isotopic signals we investigated the animal bones under electron microprobe that suggests preservation of original bioapatites suitable for isotopic analysis (see diagenetic investigation of bioapatites in SI). Detail methods of δ18O analysis of bioapatites are given in SI text. Under a constant body temperature of ~37 °C, the δ18O in mammalian phosphate (δ18Op) essentially depends on the δ18O value of water (δ18Ow) ingested by the organism. Between the water and phosphate, oxygen isotope is fractionated in two steps, i.e., between environmental and body water and between body water and phosphate in teeth and bones47,48. Large numbers of studies have been made on modern mammalian phosphates to constrain the interrelationship between δ18Op and δ18Ow41,49,50,51. Although in general most large mammals have been found to preserve equilibrium isotopic signature, species specific fractionation equations have also been proposed by several workers (ibid). For the Bhirrana mammals we used the taxon specific herbivorous mammal equations of Bryant and Froelich47. Because these equations are dependent on body mass it is desirable to infer paleoclimate from large body sized mammals. All Bhirrana mammals satisfy this criterion representing only cattle, deer or goats. δ18Op data of bioapatites and calculated δ18OW are given in Table 1 of SI.

  Figure 3C shows δ18OW variation as a function of depth and against Harappan chronology at Bhirrana proposed by Rao et al.17 and Mani18. In general the bulk bioapatite δ18O in large mammals reflects the integrated mean annual δ18O of local meteoric water ingested by the animal during its life time. At several cultural levels we analysed multiple samples of either teeth or both teeth and bones. The spread in estimated δ18OW ranges from <1‰ to maximum ~4‰ and are probably due to the seasonal variation in δ18OW52,53,54,55,56. Because our purpose was to retrieve the mean meteoric water δ18OW value from successive layers, we sampled bulk enamel or phosphate along the entire length of a single tooth or a bone (see SI text), yet the inter-sample seasonal signature might have been preserved in some cases. In spite of the inter-sample spread, the mean δ18OW values (dotted line in Fig. 3C) through the levels show a clear trend. At the base of the trench section (355 cm), equivalent to ~9 ka Pre-Harappan Hakra level, the δ18OWvalues are enriched (+3.75‰). The δ18OW values rapidly decreases towards the early Harappan phase reaching δ18O minimum of −9.01‰ at ~8 ka (trench depth ~308 cm). Thereafter the δ18OW monotonically gets enriched from early Harappan through early mature Harappan to mature Harappan, a time span from ~8 ka BP to 2.8 ka BP. We interpret this δ18OW variation through all the cultural levels at Bhirrana as major change in monsoonal precipitation during the last 9.5 ka. We compare the Bhirrana record with available monsoon records from Arabian Sea (G. bulloides upwelling index; Fig. 3A 57) and composite gastropod-carbonate δ18O records from two inland lakes Riwasa and Kotla Dahar, proximal to Bhirrana (Fig. 3B; re-plotted from supplementary information in refs 5 and 6). A weak monsoon phase is identified before 9 ka BP (lower part of Hakra phase). The well constrained monsoon intensification phase from 9 ka BP to 7 ka BP (late Hakra to middle part of early Harappan) is clearly discernible in all three records (blue shaded bars in Fig. 3A–C). Monsoon monotonically declined from 7 ka BP to 2 ka BP, i.e., during later part of the early Harappan to mature Harappan phase (brown shaded bar) with concomitant lowering of lake levels (Fig. 3B). The early Holocene monsoon intensification and its subsequent decline, as recorded in Bhirrana archaeological bioapatites, have been widely documented in Asia and were principally driven by boreal summer insolation5,54,56. Presence of aeolian sands in lake Riwasa, higher salinity in Bay of Bengal, lower G. bulloides upwelling intensity and enriched δ18O in Arabian speleothems suggest a weak monsoon phase before 10 ka BP throughout the Asia5,55,56,57,58,59,60. Correspondingly the 9–7 ka monsoon intensification phase is recorded in high lake levels (negative δ18O), lower oceanic salinity, increased upwelling, reduction in δ18O in speleothems from Arabia to Tibet, higher erosion rate in the Himalayas, and increased sedimentation in the Ganges deltaic plains (ibid61,62,63,64,65,66). The late Holocene (7 ka onwards) gradual reduction in monsoon is also amply evident throughout the Asia.

  Although compared to marine or lake archives the time resolution of the archaeological bioapatite based monsoon record is poor, preservation of the major phases of Holocene monsoon change combined with the OSL dates of potteries lend strong support to the antiquity of the Bhirrana settlement. To further constrain the change in paleo-meteoric water composition we generated time series δ18O of modern precipitation for successive three years at Hisar, a place 50 km SE of Bhirrana (Fig. 4) under the national program of ‘Isotopic Fingerprinting of Water in India (IWIN)’. As in other places of north-western India, rainfall is highest during the summer months from June to September (Fig. 4A). The monsoon moisture originates in Bay of Bengal and successively rains inland towards north-western India (Fig. 1A). The continental effect thus causes depletion in precipitation δ18O from −5.4‰ near the coast to −6.5‰ in north western India67. The modern mean annual rainfall isohyets for this part of semi-arid NW India (Fig. 1A) show that all the Harappan settlement areas (including Bhirrana) receive 400 to 600 mm precipitation compared to >1000 mm in eastern and southern India67. At Hisar the modern precipitation δ18O ranges from ~+5‰ in non-monsoon (extreme evaporation) to −15‰ in peak monsoon periods (depletion) with weighted mean annual δ18O value of −7‰. The large monsoon depletion in δ18O results from well-known amount effect where excess rainfall is known to produce extreme depletion (an increase in 100 mm of rainfall associated with a decrease in δ18O by 1.5‰ 67,68). The most depleted paleo-meteoric water value at Bhirrana is −9.01‰ (SI Table 2; Fig. 3C). Considering the δ18OWvalue at each level represents mean annual precipitation and using a simple moisture flux model67, we estimate that the early Holocene (9–7 ka) monsoon precipitation at Bhirrana was ~100–150 mm higher than today. The subsequent enrichment from 7 ka onwards (by more than 6‰) reaching maximum towards the mature Harappan time indicates very low rainfall generating mean annual δ18OW similar to present day non-monsoon months. Such a climate scenario is indeed catastrophic and if persisted for several thousand years could easily convert large monsoon-fed perennial rivers to ephemeral or even dry ones.

  (A) Seasonal variation in temperature and rainfall and (B) Time series of precipitation δ18O at IWIN station Hisar, close to Bhirrana archaeological site.

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  Climate-culture relationship at Harappan Bhirrana

  The climate reconstruction at Bhirrana demonstrates that some of the Harappan settlements in the Ghaggar-Hakra valley are the oldest in India and probably developed at least by the ninth millennium BP over a vast tract of arid/semi-arid regions of NW India and Pakistan. The Ghaggar (in India)-Hakra (in Pakistan) river, referred to as mythical Vedic river ‘Saraswati’ (Fig. 1A) originates in the Siwalik hills, ephemeral in the upper part with dry river bed running downstream through the Thar desert to Rann of Kachchh in Gujarat3. More than 500 sites of Harappan settlements have been discovered in this belt during the last hundred years. Of these several sites both in India viz. Kalibangan, Kunal, Bhirrana, Farmana, Girawad7,9,31,33,69 and Pakistan viz. Jalilpur, Mehrgarh in Baluchistan, Rehman Dheri in Gomal plains29,69,70 have revealed early Hakra levels of occupation preceding the main Harappan period. We infer that monsoon intensification from 9 ka onwards transformed the now dried up Ghaggar-Hakra into mighty rivers along which the early Harappan settlements flourished. That the river Ghaggar had sufficient water during the Hakra period is also attested by the faunal analysis. Frequency of occurrence of aquatic fauna like freshwater fish bones, turtle shells and domestic buffalo in these early levels of trench YF-2 is higher (compared to early or mature Harappan periods; SI) indicating a relatively wetter environment.

  Study of fluvial morphodynamics coupled with detrital zircon analysis of river channel sands indicated presence of a more energetic fluvial regime before 5 ka across the entire Harappan landscape, stabilized alluvial systems during early Harappan (5.2–4.6 ka BP) and drying up of many river channels during post-Harappan period3. Consequently floodplain agriculture helped in the expansion of the Harappan civilization which diminished as the monsoon waned during the late Holocene. Interestingly, the large scale droughts at ~8.2 and ~4.1 ka BP, recorded in the two lake records of Riwasa and Kotla Dahar of Haryana5,6 correspond to the base of early Harappan and middle part of mature Harappan period at Bhirrana. These events were not local, extended from the Mediterranean through Mesopotamia to China and also are recorded as dust spike in Tibetan ice cores71,72,73. Yet the settlements survived and evolved at several sites of Ghaggar-Hakra belt including at Bhirrana. The climate data and chronology of Bhirrana suggest that not only the Harappan civilization originated during the 8–9th millennium BP, it continued and flourished in the face of overall declining rainfall throughout the middle to late Holocene period11,74. It is difficult to point to one single cause that drove the Harappan decline although diverse suggestions from Aryan invasion, to catastrophic flood or droughts, change in monsoon and river dynamics, sea-levels, trade decline2,3,73,74,75,76,77,78,79 to increased societal violence and spread of infectious diseases26 have been proposed. The continued survival of Harappans at Bhirrana suggests adaptation to at least one detrimental factor that is monsoon change. Although direct paleobotanical data from Bhirrana does not exist, archeobotanical study from nearby Farmana excavation, located ~100 km SW of Bhirrana clearly indicated change in crop pattern through cultural levels. At Farmana, compared to early levels a dramatic decrease in both ubiquity (from 61% to 20%) and seed density (1.5% to 0.7%) in wheat and barley in the later Harappan period has been documented. The study also indicates increasing dependence on summer crops like millet and has been inferred as a direct consequence of lesser rainfall80. Such pattern have also been found elsewhere in Indus valley where the Harappans shifted their crop patterns from the large-grained cereals like wheat and barley during the early part of intensified monsoon to drought-resistant species of small millets and rice in the later part of declining monsoon and thereby changed their subsistence strategy16,81. Because these later crops generally have much lower yield, the organized large storage system of mature Harappan period was abandoned giving rise to smaller more individual household based crop processing and storage system and could act as catalyst for the de-urbanisation of the Harappan civilization rather than an abrupt collapse as suggested by many workers82,83,84,85. Our study suggests possibility of a direct connect between climate, agriculture and subsistence pattern during the Harappan civilization.

  Additional Information

  How to cite this article: Sarkar, A. et al. Oxygen isotope in archaeological bioapatites from India: Implications to climate change and decline of Bronze Age Harappan civilization. Sci. Rep. 6, 26555; doi: 10.1038/srep26555 (2016).

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  Download references
  Supplementary Information

  ‘Oxygen isotope in archaeological bioapatites from India: Implications to climate change and decline of Bronze Age Harappan civilization’ byAnindya Sarkar, Arati Deshpande Mukherjee, M. K. Bera, B. Das, Navin Juyal, P. Morthekai, R.D. Deshpande, V. Shinde and L. S. Rao

  
  

  A. Archeological information of Bhirrana site

  1) Chronology of Indus valley civilization

  Two major archaeological chronologies of Harappan (Indus) civilization in South Asia (compiled based on data from previously published papers of Kenoyer, 1998; Possehl 2002; Madella and Fuller, 2006)

  
  

  	Kenoyer (2011)#	Possehl (2002)@
  Phase/Period	Cal Years BP	Cal Years BP	Stage
  EarlyHarappan/Ravi Phase: 1A/B	5700–2800	9000–6300	Early village farming communities and pastoral societies
  EarlyHarappan/KotDiji Phase:2	4800–4600	6300–5200	Advancedvillagefarmingcommunitiesand pastoralsocieties
  HarappanPhase:3A	4600–4450	5200-4600	Early Harappan
  HarappanPhase:3B	4450-4200	4600–4500	EarlyHarappan/MatureHarappanTransition
  HarappanPhase:3C	4200–3900	4500–3900	MatureHarappan
  Harappan/Late HarappanTransitional	3900–3700	3900–3000	Post-urbanHarappan
  LateHarappan (CemeteryH)	3700–3300	3000–2500	EarlyIron Age of India and Painted GreyWare

  # Proposed based on the stratigraphy of Harappa (Punjab), Pakistan

  @ Proposed based on larger regional compilation in south Asia

  
  

  
  

  
  

  
  

  
  

  
  

  
  

  
  

  
  

  2) Radiocarbon and OSL chronology in Bhirrana trenches

  Uncalibrated and calibrated radiocarbon dates of the charcoal samples analysed from the Bhirrana after the excavation of 2005 (compiled based on data from previously published papers of Mani, 2008^#); OSL dates are from present work^@ (see below).

  
  

  Site/ Sample no.	Trench	Lab.  No.	Depth (m)	14C age±1s year  BC	Calibrated  age±1s year  BC		Calibrated  age±1s year  BP		OSL Date Cal year BP
  					Max.	Min.	Max.	Min.	Max.	Min.
  BRN-1#	A-1	BS-2308	0.45-.50	1350±200	1876	1324	3826	3274
  BRN-Pot-1@	YF-2	PRL-43	0.42-0.46						5120	4520
  BRN-3#	ZE-10	BS-2310	1.25	1240±160	1679	1264	3629	3214
  BRN-Pot-2@	YF-2	PRL-143	1.43-1.45						6185	5695
  BRN-5#	ZE-10	BS-2318	1.42	4170±250	5336	4721	7286	6671
  BRN-6#	A-1	BS-2333	2.95	5640±240	6647	6221	8597	8171

  
  

  ¹⁴C ages were determined by conventional method [¹⁴C/¹²C ratios normalized assuming organic matter d¹³C = –25.0 ‰ (Stuiver and Polach 1977)] and were then calibrated to get calendar ages. Calibration was carried out by the probability method of OxCal v 4.1 (Bronk Ramsey, 2009) and the IntCal09 data set (Reimer et al., 2009). All ¹⁴C ages are based on a half life of 5.730± 40 year (for detail methods see Sukumar et al., Nature, 1993; Goyal et al., 2013). OSL methods described below.

  
  

  3) Schematic E-W cross section of the trench YF-2 depicting the cultural levels at Bhirrana (Rao et al., 2005; Dikshit, 2013; with permission from Archaeological Survey of India)

  
  

  
  

  
  

  4) Cultural stratigraphy of Bhirrana settlement (compiled based on data from previously published papers of Rao et al., 2004-05; Dikshit and Mani, 2012)

  Period	Cultural levels	Year BP (based on radiocarbon ages in different trenches)	Attributes
  II B	Mature Harappan culture	3000-1800 BCE	Fully developed house complexes contain painted  ceramics which included geometric, floral and faunal motifs. Incised figure of a dancing girl closely resembling the famous bronze dancing girl from Mohenjo-daro. Antiquities typical of the Mature Harappan period were recovered such as steatite seals, beads of semi-precious stone, shell and terracotta, animal figurines, bangles of faience, shell, copper bangles, chisels, rings, rods, stylised terracotta horns with symbolic head painted in black.
  II A	Early Mature Harappan culture	4500-3000 BCE	Beginning of fortification wall, house-complexes, streets and lanes
  IB	Early Harappan culture	6000-4500 BCE	Settlement expanded and the entire site came under occupation. The houses were built of mud bricks in the ratio of 3:2:1 and measured 45x30x15cm; 42x28x 14cm and 39x36x 13cm. Yielded terracotta figurines, arrow heads, rings and bangles of copper, beads of carnelian, jasper, shell, bull figurines, chert blades, terracotta bangle.
  I A	Hakra ware culture	7500-6000 BCE	Earliest cultural phase at Bhirrana, primarily identified from the ceramics quite similar to those identified from sites in Cholistan. The ceramics comprise mud appliqué ware, incised ware, Bi-chrome ware, tan slipped ware, blackburnished ware, brown on buff ware, simple red ware of medium fabric with common shapes like vase, bowl and cup. Also characterized by its subterranean dwelling pits Antiquities from the dwelling pits included beads of semiprecious stones like carnelian, agate, terracotta bangles, unbaked triangular clay cakes, querns, crucible, chert blade, crucible fragments with molten copper.

  
  

  
  

  
  

  
  

  
  

  
  

  5) Archeological artefacts from different cultural levels at Bhirrana (Rao et al., 2004-05; Mani, 2008; permission taken from Archeological Survey of India)

  
  

  
  

  B. Experimental methods

  
  

  Supplementary Method 1:

  Optically stimulated luminescence (OSL) dating of potteries

  The pottery samples were collected from the corresponding sections (Fig. 1). The outer 1-2 mm layers were physically scraped under the subdued red light. The unexposed inner part of the pottery was gently crushed using acetone in an agate mortar. The powdered samples were treated with 1 N HCl and 40 % H₂O₂to remove carbonates and organic materials respectively. Following this the samples were deflocculated by using 0.01 N sodium oxalate and the clay minerals were removed from the solution. The samples were then suspended in an alcohol column and the ~ 4-11 mm grain fractions were separated using Stokes’ times of 1.5 and 15 minutes. The separated fraction was re-suspended in alcohol and ~1 ml volumes were pipetted on to 9.65 mm aluminum discs and dried at ~45°C (Singhvi et al., 2001).

   The Infrared Stimulated Luminescence (IRSL) measurements were carried out in automated Risoe TL/OSL Reader DA-20 (Boetter-Jensen et al., 2003). It is equipped with a calibrated b-particles dose rate 0.09 Gy.s^-1 to the fine grains of feldspar mounted on Al discs. The samples were stimulated by IR LEDs (870 ± 40 nm) and the luminescence photons were detected in the range of 395 ± 50 nm using PMT (EMI9235QB) and the combination of optical filters of Corning 7-59 (4 mm) and BG-39 (2 mm). A preheat value of 260°C held of 10 s was used.  The dose response curve of BRN 5 - 6 (42-46) is shown in Fig. 1 and a typical shine down curve is shown in figure1Sa (inset). Recycling ratios were unity within 5 % error and the recuperation was less than 1 %. Equivalent doses (D_e’s) were evaluated using single aliquot regenerative dose (SAR) of Murray and Wintle (2003). Around 20 aliquots were measured from each sample which shows insignificant over-dispersion (< 3 %) in the dose distribution (Fig. 2).

  In order to estimate the α- efficiency (a-value), six fresh aliquots were bleached in the solar simulator for 6 hours and were irradiated with calibrated ²⁴¹Am for 30 minutes. The α irradiated aliquots are treated as natural signal and the dose is recovered using the appropriate b-dose using SAR protocol. The a-value (a-efficiency) in IRSL production was calculated by comparing equivalent b-dose and the irradiated a-dose. For radioactivity assay, concentrations of U, Th and K in the sediment matrix has been measured using high pure Ge (HPGe) detector by comparing the photo-peak of the sample against that of corresponding standards (Shukla, 2011). Considering the small size and the thickness of the pottery, it is reasonable to assume that the dose contribution would be predominantly from the sediment and hence only the dose rate from the sediment has been considered for the age estimation. In absence of sediment sample for Early Harappan pottery, we used the average dose rate of the BRN-5 (143-145) and BRN 5-6 (42-46). Details of the dose rate equivalent dose and the ages obtained are given in Table 1.

              In order to correct for the fading of feldspar luminescence signal (anomalous fading), the percentage fading rate (g-values; %/decade) were measured (Auclair et al., 2003) and corrected using the method suggested by Huntley-Lamothe (2001).

  
  

  
  

  Fig. 1: Pottery fragments (photographs taken by us) from YF-2 trench (left: 42 cm.), right (143 cm)

  
  

  
  

                                       Fig. 2                                                                         Fig. 3

  Fig. 2: The dose response function of BRN 5 (42-46 cm) fitted to single saturating exponential (green line). Sensitivity change corrected IRSL (corr. L/T) has been plotted versus the laboratory administered radiation dose. IRSL shine down curve (natural) of the same sample is shown in the inset.

  Fig. 3: Probability and probability density function (PDF) were plotted for the same sample. 15 aliquots were measured for this sample and they were clustered around the mean value of 15.5 Gy.

  
  

  
  

  Table 1                                        

  Concentrations of U, Th and K, calculated dose rates and the OSL ages of potteries

  Sample Type/Code/Depth	U (ppm)	Th (ppm)	K (%)	a- value	Dose rate (Gy/ka)	Palaeodose (Gy)	g2days-value(%/decade)	Corr. Age (years)
  Pottery,  YF-2 trench, BRN 5 (143-145 cm)	5.1 ± 0.6	6.9 ± 1.2	1.3 ± 0.2	0.036 ± 0.002	3.9 ± 0.1	17.6 ± 0.8	4.3 ± 0.8	5940 ± 245
  Pottery,  YF-2 trench, BRN 5 (42-46 cm)	7.3 ± 0.9	7.1 ± 1.5	1.8 ± 0.1	0.029 ± 0.003	4.9 ± 0.2	15.5 ± 0.7	6.0 ± 2.0	4820 ± 300

  1)      Water content was assumed to 5 ± 2 %

  2)      Cosmic ray dose rate was assumed to be 150 ± 20 mGy/ka. 

  3)      Grain size used: 4-11 mm

  
  

  Supplementary Method 2:

  Oxygen isotope analysis of bioapatites

  Individual tooth or bone was cleaned by distilled water, surface coatings removed, ultrasonicated, dried and only the surficial enamel part (~0.2-0.4 mm layer) was sampled perpendicular to the entire growth axis by a micro-dental drill to obtain bulk phosphate sample. Extraction of pure phosphate from bioapatite in the form of Ag₃PO₄ is a necessary pre-requisite for isotopic measurements. The Ag₃PO₄ was extracted by following the method described in Stephen (2000). Typically 2 mg of bioapatite yields ~1 mg of Ag₃PO₄. About 300mg of Ag₃PO₄ was packed into pure silver capsules and loaded onto the automated carousel atop a temperature conversion elemental analyzer (TC-EA). The sample was combusted at ~1450^oC and the generated CO was analysed in a Delta Plus^XP mass spectrometer via a ConFlo interface. For routine analysis of bioapatites, an inter-laboratory calibration exercise was performed by two standards, namely international NIST 120C Phosphate Rock standard (d¹⁸O_SMOW = +22.65 ‰) and Acros Silver Phosphate (ASP) standard (d¹⁸O_SMOW = +14.2 ‰) obtained from the KPESIL Isotope Laboratory, University of Kansas. The NIST phosphate rock was chemically treated to precipitate the Ag₃PO₄ crystals following the method described above. The obtained d¹⁸O_ASP-SMOW value (via NIST) at IIT, Kharagpur is +14.4 ‰ and is in excellent agreement with the value of +14.2 ‰ recommended by KEPSIL. Overall analytical reproducibility was ± 0.2 ‰ similar to obtained elsewhere by both dual inlet and on-line CFIRMS technique. For retrieving paleo-meteoric water value from the Bhirrana teeth and bones we used the general mammal equation, d¹⁸O_W= 1.0247*d¹⁸Op - 25.02 (Amiot et al. (2004). The relationship is based on global compilation of teeth and bone phosphates of variety of continental mammalian apatites with large range of d¹⁸O_W­ varying from +5‰ to -25‰, independent of species or genera, exhibiting high degree of correlation between d¹⁸O_p and d¹⁸O_W­ and therefore robust.

  
  

  
  

  
  

  
  

  
  

  Table 2: d¹⁸O ingested water calculated from Tooth and Bone phosphate in Bhirrana trench YF-2

  Sl. No.	Depth (cm)	Sample type (Teeth)	d18Op ‰* (VSMOW)	d18Ow‰ @ (VSMOW)	Sl. No.	Depth (cm)	Sample type (Bone)	d18Op‰* (VSMOW)	d18Ow‰@ (VSMOW)
  1	42	Goat Tooth	23.86	-2.19	1	42	Cattle Bone	22.56	-2.08
  2	42	Goat Tooth	22.11	-3.39	2	42	Cattle Bone	19.57	-5.16
  3	60	Cattle Molar	25.91	1.37	3	42	Cattle Bone	19.91	-4.81
  4	60	Cattle Molar	24.81	0.24	4	133	Cattle rib	19.61	-5.12
  5	60	Goat Molar	20.76	-4.32	5	175	Cattle Long Bone	20.83	-3.87
  6	60	Cattle Molar	25.91	1.37	6	175	Cattle Femur shaft	21.65	-3.02
  7	148	Deer pre-Molar	22.73	-2.53	7	175	Cattle Femur shaft	21.17	-3.52
  8	148	Deer pre-Molar	21.27	-3.81	8	183	Cattle Long Bone	20.60	-4.10
  9	185	Cattle Tooth fragment	20.51	-4.20	9	195	Cattle long Bone shaft	21.10	-3.59
  10	185	Ruminant tooth fragment	20.90	-3.79	10	230	Cattle Bone	19.67	-5.06
  11	185	Unidentified Tooth fragment	17.88	-6.90	11	240	Cattle Bone	19.99	-4.73
  12	195	Cattle pre-Molar	20.42	-4.29	12	240	Cattle Bone	21.73	-2.94
  13	205	Cattle Molar	21.05	-3.64	13	278	Cattle rib	16.41	-8.42
  14	212	Cattle Molar	22.54	-2.10	14	278	Cattle rib	19.24	-5.51
  15	212	Cattle Molar	21.78	-2.89	15	302	Cattle long Bone shaft	19.77	-4.96
  16	212	Cattle Molar	21.81	-2.86	16	308	Cattle Long Bone shaft	15.84	-9.01
  17	300	Cattle maxillary molar fragment	21.86	-2.80	17	308	Cattle Long Bone shaft	18.64	-6.12
  18	300	Cattle tooth fragment	18.43	-6.34	18	325	Cattle Vertebral  spine	18.42	-6.35
  19	302	Cattle Molar	19.25	-4.20	19	330	Cattle Long Bone splinter	19.99	-7.51
  20	314	Antelope Molar	24.99	0.38
  21	314	Cattle Molar	24.83	0.26
  22	320	Cattle Molar	19.94	-4.78
  23	339	Goat Molar	24.04	-2.07
  24	340	Cattle pre-Molar	21.94	-2.72
  25	340	Goat mandibular	22.94	-2.82
  26	355	Ruminant tooth fragment	27.4	2.91
  27	355	Ruminant tooth fragment	28.22	3.75

  *d¹⁸O_p =  d¹⁸O of tooth enamel /bone phosphate;

  @ d¹⁸O_w =  d¹⁸O of ingested water (proxy meteoric water), calculated using the taxon specific mammal equations of Bryant and Froelich (1995).

  
  

  
  

  
  

  
  

  
  

  
  

  
  

  
  

  
  

  Supplementary Method 3:

  Faunal analysis in trench YF2

  Faunal material recovered from Trench YF2 at Bhirrana through use of systematic recovery techniques such as dry and wet sieving was analysed at the Archaeozoology Laboratory DCPRI, Pune following standard procedures in Archaeozoological  analysis. Identification  to the species level was carried out by  comparison  with the  reference collection of  modern animal skeletons  housed within the Archaeozoology lab and by referring to Schimd’s  (1972),  Hillson (1992) and Prater (1971).  For more   specific identification between cattle and Nilgai (Joglekar et.al. 1994), sheep and goat  (Boessneck, 1969; Prummel and Fisch 1986; Zeder and Lapham 2010),  blackbuck (Antelope cervicapra), goat (Capra hircus ) and sheep (Ovisaires)  (Pawankar and Thomas 2001) both MNI and NISP estimation were done.  The age estimation of individual animal was calculated by studying teeth eruption patterns following Grant (1982) and epiphysal fusion in long bones (Silver, 1963). Bone measurements were taken wherever possible (Driesh 1976).  Each bone fragment was carefully scrutinized for traces of human activity such as charring, cut and chop marks, abrasion, polishing, breakage patterns and state of preservation. The faunal remains showed fairly good preservation and in spite of the fragmentation   identification to species level was possible for many of the bones. A total of 1039 animal skeletal elements were analysed  from all the 4 cultural periods  of which  total identifiable specimens accounted for n=561.

  The analysis revealed the presence of a diverse range of domestic and wild mammals with few birds and fish from trench YF-2 and ZE-10 (Table 3).  Faunal evidence strongly suggests the heavy reliance on animal foods by the Bhirrana inhabitants throughout its occupation. Of these the cattle (Bos/Bubalus) show maximum exploitation specifically of the domestic cow/ox (Bos indicus) in all the four cultural periods followed by that of domestic goat. In the Hakra period i.e. the earliest occupation phase at Bhirrana, Zebu the famed humped variety of Bos indicus has been recorded. In this period, the varied wild fauna identified unlike cattle diminishes in the succeeding Early Harappan and Early Mature Harappan periods only to occur once again in the Mature Harappan period. Identification of the domestic buffalo (Bubalus bubalis) in the early levels in YF2 further indicates a wet environment. However, there is no definitive trend in the animal abundances that can be related to monsoon vagaries. The only inference that can be made is  the  river Ghaggar  had  sufficient water to support  aquatic  fauna  during the Hakra  period  as attested by the occurrence  of freshwater fish bones and  turtle shells and is discussed in the text.

  
  

  Table 3: Depth wise NISP distribution of identified fauna in trench YF2 at Bhirrana

  Depth (cm)	B/B	BI	BB	C/O	Ch	Oa	SR	Ac	Bt	Aa	Gz	Mm	Cu	P	FH	BRD	Total
  42-46	9	13		4	1			4									31
  58-70	28	12				3											43
  60-88	53	17					3				1			1			75
  83-94	28	34					5		2	1							70
  90-115	18	31						3	2								54
  125-133		2															2
  143-162	23	9	1			2	2										37
  162-175		1	1	2			1										5
  175-187	5	2					1										8
  185-195		1							1						1		3
  195-200	1	1			5												7
  205-208	13						1			1							15
  212-230	1	2			1		1										5
  225-250	31	8	5		2				1								47
  240-260	2	5	1	2				1	3								14
  260-278	2	5			1												8
  278-290	4	2				2					1						9
  300-326	17	4	1	1	2		3	2				1	1		3		35
  325-330	4	2					4										10
  330-335	2		1			1	2										6
  335-340	14	4		2	1		3	1		1							25
  340-355	30	4			1		4	1		1		1				1	43
  351-362	2			1			1										4
  362-364		3					1										4
  Total	287	162	10	12	14	8	32	12	9	4	2	2	1	1	4	1	561

  Abbreviations used B/B: Cattle (Bos/bubalus); BI: Cow/ox (Bos indicus),  BB: Buffalo  (Bubalus bubalis), C/O: Goat/sheep (Capra/Ovis), Ch: Goat ( Capra hircus ), Oa: Sheep (Ovis aries),SR: Small ruminant;  Ac:Black buck (Antilope cervicapra), Bt: Nilgai (Boselaphas tragocamelus), Aa: Spotted deer (Axis axis), Cu: Sambar (Cervus unicolor ), Gz: (Gazella bennetti), Mm:(Muntiacus muntjack), P: (Panthera pardus), BRD: Bird, FH: fish.

  
  

  
  

  Fig. 4: Representative teeth and bone samples analysed from all

  the four cultural levels of Bhirrana (photographs taken by us)

  Supplementary Method 4:

  Diagenetic investigation of bioapatites

  
  

  Carbon-coated polished halves of thin sections up to 300 mm thick were used for the Electron microprobe analysis (EPMA). The sample were analysed for major and minor elements using the Cameca SX 100 microprobe. The spot analysis were done with an accelerating voltage of 15 kV with a beam diameter of 20 micrometer in order to account for the limited stability of bioapatite under  the electron beam. Counting times were 20-60s on the peak and 10-40s on the background. Fig. 5 gives the Back Scatter Electron (BSE) images of Ca and P.

  
  

  
  

  Fig. 5: BSE image of  bioapatite of mammal bones. Left: Ca; Right: P

  (photographs taken by us)

  
  

  
  

  The Ca/P ratio is approximately 1.4 and the CaO/P₂O₅ ratios are very constant suggesting near-pristine values (Newseley, 1998). The Back Scatter Electron (BSE) images of the samples show uniformity in Ca and P distribution and are indicative of original bioapatite preservation suitable for isotopic analysis. 

  
  

  
  

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   Acknowledgements

  This work was supported by a Diamond Jubilee Grant from IIT Kharagpur. Isotope data were generated in the National Stable Isotope facilities, IIT, Kharagpur and Physical Research Laboratory funded by the DST, New Delhi. We thank Archaeological Survey of India for the permission to use the photographs of excavation and archaeological elements of Bhirrana and Dr. Anil Pokharia of BSIP for discussion. We thank three anonymous reviewers for their critical comments. We dedicate this paper to the late Dr. L.S. Rao who excavated the Bhirrana site and established the Harappan cultural levels.

  Author information

  Author notes

  1. • L. S. Rao
     Deceased.

  Affiliations

  1. Department of Geology and Geophysics, Indian Institute of Technology, Kharagpur 721302, India

     • Anindya Sarkar
     • , M. K. Bera
     •  & B. Das

  2. Deccan College Post Graduate and Research Instiute, Pune 411006, India

     • Arati Deshpande Mukherjee
     •  & V. S. Shinde

  3. Physical Research Laboratory Navrangpura, Ahmedabad 380009, India

     • Navin Juyal
     •  & R. D. Deshpande

  4. Birbal Sahni Institute of Palaeosciences, Lucknow, India

     • P. Morthekai

  5. Archaeological Survey of India, Nagpur, 440006, India

     • L. S. Rao

  Contributions

  A.S. conceived the problem, prepared the figures, helped in analysis and wrote the paper. A.D.M. did the field work, collected samples and did the faunal analysis of teeth and bone samples, M.K.B. and B.D. carried out the chemical extraction of phosphates from bioapatites and did the stable isotope anlaysis, N.J. and P.M. did the OSL dating of potteries, R.D.D. coordinated the Hissar IWIN precipitation station and carried out the stable isotope analysis of rain water, V.S. provided input about Harappan archeology. Late L.S.R. excavated the Bhirrana archeological site.

  Competing interests

  The authors declare no competing financial interests.

  Corresponding author

  Correspondence to Anindya Sarkar.