Oxygen isotopes of East Asian dinosaurs reveal exceptionally cold Early Cretaceous climates

Romain Amiot, Xu Wang, Zhonghe Zhou, Xiaolin Wang, Eric Buffetaut, Christophe Lécuyer, Zhongli Ding, Frédéric Fluteau, Tsuyoshi Hibino, Nao Kusuhashi, Jinyou Mo, Varavudh Suteethorn, Yuanqing Wang, Xing Xu, and Fusong Zhang
PNAS March 29, 2011 108 (13) 5179-5183; https://doi.org/10.1073/pnas.1011369108

  1. Edited by Paul E. Olsen, Columbia University, Palisades, NY, and approved November 4, 2010 (received for review August 3, 2010)

Abstract

Early Cretaceous vertebrate assemblages from East Asia and particularly the Jehol Biota of northeastern China flourished during a period of highly debated climatic history. While the unique characters of these continental faunas have been the subject of various speculations about their biogeographic history, little attention has been paid to their possible climatic causes. Here we address this question using the oxygen isotope composition of apatite phosphate (δEmbedded Image) from various reptile remains recovered from China, Thailand, and Japan. δEmbedded Image values indicate that cold terrestrial climates prevailed at least in this part of Asia during the Barremian—early Albian interval. Estimated mean air temperatures of about 10 ± 4 °C at midlatitudes (∼42 °N) correspond to present day cool temperate climatic conditions. Such low temperatures are in agreement with previous reports of cold marine temperatures during this part of the Early Cretaceous, as well as with the widespread occurrence of the temperate fossil wood genus Xenoxylon and the absence of thermophilic reptiles such as crocodilians in northeastern China. The unique character of the Jehol Biota is thus not only the result of its evolutionary and biogeographical history but is also due to rather cold local climatic conditions linked to the paleolatitudinal position of northeastern China and global icehouse climates that prevailed during this part of the Early Cretaceous.

Since the last decade, continuous discoveries of Early Cretaceous invertebrates, plants and vertebrates in East Asia, and more particularly exceptionally preserved specimens in northeastern China belonging to the Jehol Biota, have fed numerous current evolutionary debates (1, 2). This latter assemblage is preserved in the lacustrine and volcanic sediments that mainly constitute the Yixian and Jiufotang formations of Liaoning Province. The peculiar character of the Jehol Biota, with “unusual” forms such as feathered dinosaurs, is clearly in part a result of the exceptional preservation of many fossils which show well preserved integumentary structures seldom preserved in other localities. However, it has been suggested that the Jehol Biota show peculiar floral and faunal compositions, which may, for instance, be indicative of a “relict” character (3) although this interpretation has been disputed (1). To date, possible relations between global climatic conditions and the taxonomic composition of the Jehol Biota have not been investigated, and no quantitative local climate reconstruction has been proposed so far. In the marine record, cold climatic intervals have been recognized during the Early Cretaceous period, with two major events occurring (i) during the early Valanginian, and (ii) from the late Barremian to the early Albian (4, 5). The most recent 40Ar/39Ar dating of sanidine crystals from tuff beds within the Yixian Formation and the base of the overlying Jiufotang Formation gave an age bracket of 129.7 ± 0.5 Ma to 122.1 ± 0.3 Ma for the deposition of the Yixian Formation (6). These ages correspond to a Barremian to early Aptian age interval which is encompassed by the second cold interval. We have estimated water δ18O values and related mean air paleotemperatures at eight contemporaneous localities covering a large range of paleolatitudes in order to define a latitudinal climatic gradient and its influence upon the geographic distribution of East Asian fauna and flora.

Results and Discussion

We have used 99 new and 17 published [(7–9); Table S1] oxygen isotope compositions of apatite phosphate (δEmbedded Image) measured on dinosaurs, tritylodont synapsids, and freshwater crocodilian teeth, as well as turtles shell bones. These apatitic remains were recovered from deposits of the Yixian Formation and seven other Early Cretaceous formations in China, Japan, and Thailand. All these deposits are dated from the Barremian to the Aptian-Albian intervals and cover palaeolatitudes ranging from 21.0 ± 7.2 °N to 43.2 ± 8.0 °N (Table 1 and Fig. 1). Oxygen isotope compositions of apatite phosphates were measured using the procedure described in the Analytical method section, and are reported on in Table S1.

Fig. 1.
Fig. 1.

Palaeogeographic map of eastern Asia in the Early Cretaceous modified from ref. 42. Number refers to the following horizons and localities: 1: Napai Fm., Guangxi, China, Aptian?; 2: Sao Khua Fm., Thailand, Barremian? (43); 3: Khok Kruat Fm., Thailand, Aptian (43); 4: Xinmingbao Fm., Gansu, China, Aptian-Albian (44); 5: Yixian Fm., Liaoning, China, Barremian-early Aptian (6); 6: Shahai and 7:Fuxin formations, Liaoning, China, Aptian-Albian (45); and 8: Kuwajima Fm., Japan, Barremian-early Aptian (46). Palaeolatitude of each locality was calculated using the Apparent Polar Wander Path (APWP) of refs. 47, 48. Abbreviations refer to major tectonic divisions: EUR, Europe; INC, Indo-China; IND, India; J, Japan; JUN, Junggar; K, Korea; KAZ, Kazakhstan; LH, Lhassa; MON, Mongolian; NCB, north China; QI, Qiangtang; SCB, south China; SH, Shan Thai; SIB, Siberian; and TAR, Tarim.

View this table:
Table 1.

Formation, age, sample number (N), and computed palaeolatitudes are given along with mean vertebrate δEmbedded Image values, environmental water δEmbedded Image values obtained by subtracting 21.9 to mean δEmbedded Image values (15) and estimated mean air temperatures using the following equation: δEmbedded Image (15)

Preservation of the Original Oxygen Isotope Compositions.

Secondary precipitation of apatite and isotopic exchange during microbially mediated reactions may alter the primary isotopic signal (10, 11). However, apatite crystals that make up tooth enamel are large and densely packed, and in the absence of high temperature conditions which Kolodny and others argue that they enable microbial mediated reactions to reset the bone phosphate oxygen isotopic signal, isotopic exchange might not affect the oxygen isotope composition of phosphates even at geological time scales (12, 13). Turtle shell and dinosaur bones should be more susceptible to diagenetic alteration because hydroxylapatite crystals of bones are smaller and less densely intergrown than those of enamel (14), even though several case studies have shown that the original oxygen isotope composition can be preserved in Mesozoic reptile remains (7–9, 15–17). Although no method is available to demonstrate definitely whether or not the oxygen isotope composition of fossil vertebrate phosphate was modified by diagenetic processes, several ways to assess the preservation state of the primary isotopic record have been proposed [e.g., (14, 18–21)]. Here the main argument supporting the preservation of the original oxygen isotope composition is the latitudinal variation of the offset observed between the δEmbedded Image values of probable endotherms (dinosaurs and trytilodont synapsids) and ectotherms (turtles and crocodilians) that mimics present day variations of the offset observed between the δEmbedded Image values of endotherms and ectotherms (Fig. 2). If early diagenetic processes had occurred, they would have erased the expected offsets in δEmbedded Image values of vertebrate remains having different ecologies or physiologies (20).

Fig. 2.
Fig. 2.

Latitudinal variations in δEmbedded Image values of dinosaurs, crocodilians, and turtles compared to expected latitudinal variations in δEmbedded Image values of present day endotherms and ectotherms drawn using δEmbedded Image and mean air temperature values of IAEA (International Atomic Energy Agency)/WMO (World Meteorological Organization) (27), and the following equations : δEmbedded Image-26.44 [endotherms; (15)] and T = 113.3 - 4.38∗ (δEmbedded Image) [ectotherms; (12)].

Climatic and Ecologic Implications.

Considering at least partial preservation of the primary isotopic compositions of analyzed apatites, mean δEmbedded Image values of meteoric waters can be estimated at each site using present day relationships established between vertebrate phosphate and water (δEmbedded Image). Due to ecological differences between herbivorous (sauropods, ornithopods, ceratopsians, and ankylosaurs) and carnivorous (theropods) dinosaurs, systematic offsets in δEmbedded Image values between these dinosaur groups that would reflect differences in diet, water strategies, and foraging micro habitats were expected (7, 22, 23). However, the δEmbedded Image value differences observed between coexisting theropods, sauropods, ornithopods, ceratopsians, and ankylosaurs appear to be randomly distributed from one site to another (Fig. 2) instead of being ordered the same way at all sites. This observation suggests that these differences are more related to spatial or seasonal variability in ingested water δ18O values than to taxon-specific ecological differences. Moreover, as dinosaur teeth took from a few months up to more than a year to grow depending on their size (24), significant differences in δEmbedded Image values between teeth coming from the same deposit are expected. The same pattern can be observed on crocodilian and turtles δEmbedded Image values but with less scattering due to their semiaquatic lifestyle and their living environment consisting of large water bodies (rivers, lakes) that buffer seasonal variations in local meteoric water δEmbedded Image values (Fig. 2). From present day data, it has been shown that a first order estimation of δEmbedded Image value can be calculated by substracting 21.9‰ to the average δEmbedded Image value of both endotherms and ectotherms (15). Based on these considerations, δEmbedded Image values were estimated for the eight Early Cretaceous sites (Table 1 and Fig. 3). At the global scale, these values are slightly lower than those found today at similar latitudes, suggesting lower Mean Annual Air Temperatures (MAAT) than present day ones.

Fig. 3.
Fig. 3.

Calculated mean meteoric water δEmbedded Image gradient during the Early Cretaceous of eastern Asia vs. absolute latitudes. The Early Cretaceous thermal gradient was calculated using fossil vertebrate δEmbedded Image values and published equations (15). The present day continental temperature gradient for low altitude localities and the calculated Late Campanian—Middle Maastrichtian gradient are given for comparison.

Despite the possibility that, at the global scale, Mesozoic hygrometry differed from present day condition, thus affecting the latitudinal distribution of δEmbedded Image values, there is no compelling evidence to indicate that the systematics of ancient meteoric waters were radically different from today (25). On the contrary, it was argued that the “δEmbedded Image-MAAT” relationship may be conservative through time, at least throughout the Quaternary (26). Mean air palaeotemperatures were thus proposed (Table 1 and Fig. 4) using the same present day relationship established between meteoric water and MAAT (δEmbedded Image—MAAT) that was previously used to establish a terrestrial temperature gradient for the terminal Cretaceous (15; Fig. 4).

Fig. 4.
Fig. 4.

Estimated mean annual temperatures during the Early Cretaceous of eastern Asia vs. absolute latitudes. The Early Cretaceous thermal gradient was calculated using fossil vertebrate δEmbedded Image values and published equations (15). The present day continental temperature gradient for low altitude localities and the calculated Late Campanian—Middle Maastrichtian gradient (15) are given for comparison.

The fitted temperature gradient has a curvature similar to that of the present day gradient but shifted towards lower mean temperatures (Fig. 4). For consistency, the same (δEmbedded Image—MAAT) relationship was used for all sites (Table 1), but this leads to underestimation of mean air temperatures in tropical sites of the Khok Kruat and Sao Khua formations of Thailand, as well as the Napai Formation of Guangxi (China), which were closer to a typical 20–25 °C range because of the possible occurrence in these areas of monsoon-like precipitations having 18O-depleted meteoric waters (7). Calculated mean air palaeotemperatures for the Liaoning region range from 8 ± 3 °C (Fuxin Formation) to 10 ± 4 °C (Yixian Formation), matching modern cool temperate midlatitude climatic conditions (27). These temperature estimates are supported by previous studies (4, 5, 28) that have documented global cold intervals during the Early Cretaceous with subfreezing to freezing conditions in polar regions. Throughout the early Aptian, low latitude surface seawaters of the western Tethys were about 20 °C with high seasonality (4, 28) while polar ice was present at high latitudes (5). The fossil wood genus Xenoxylon, recognized as an indicator of temperate to cool temperate climates (29), was widely distributed in northeastern Asia during the Early Cretaceous, where it reached a level of anatomical diversity unmatched elsewhere in the world (30). Most strikingly, no crocodilian remains have been found so far either in northeastern China or Japan in deposits corresponding to the Jehol Biota, whereas they were abundant at lower latitudes, the northernmost occurrence being in the Dongmyeong Formation (Barremian) in the southern part of South Korea (31). During the late Early Cretaceous, crocodilians occurred again in Japan in the Albian Kitadani Formation (32) and colonized higher latitudes during the Late Cretaceous, as shown by their occurrence in the Late Turonian to Early Santonian Nenjiang Formation of Jilin Province (latitude about 44 °N). It is noteworthy that during the Late Campanian-Middle Maastrichtians interval, for which a terrestrial temperature gradient with higher mid- to high-latitudes temperatures was previously established [(Fig. 4; 15)], crocodilians occurred at latitudes up to 60 °N. Because of modern crocodilians restricted temperature requirements, they can live only under climates where mean air temperatures exceed 13–14 °C (33). According to the calculated Early Cretaceous gradient, these minimum mean temperatures tolerated by crocodilians occurred at latitudes of 35 °N, as illustrated by their presence in the Xinminbao Formation of Gansu Province (Fig. 1, Locality 4) and in the Dongmyeong Formation of the southern part of South Korea. Under the cool climatic conditions of the Jehol Biota, ectothermic vertebrates such as turtles, lizards, or amphibians may have hibernated, whereas endothermic animals such as mammals, non avian dinosaurs, birds, and possibly pterosaurs may have benefited from their integumentary structures (hair, feathers, or feather-like structures) as insulation devices, allowing them to keep sustained activity all year round. The occurrence of choristoderes (crocodile–like archosauromorph reptiles) in the Jehol Biota raises the question of whether they can be used as an ecological analogue to crocodilians in terms of temperature tolerance, as has been proposed (34). Choristoderes were semiaquatic active predators and some of them, such as Ikechosaurus from the Jehol Biota, resembled modern gharials. Although choristoderes commonly occur along with crocodilians, their presence in assemblages from which crocodilians are absent has led to the hypothesis that they were ecological competitors of crocodilians (35, 36) and had similar environmental temperature requirements (34). On the basis of present data, we argue that choristoderes could tolerate low temperatures, and thus probably occupied the ecological niches of crocodilians in colder environments where the latter could not live, although they definitely occurred together in warmer environments. This interpretation suggests that the distribution of choristoderes cannot be used as an indicator of warm climates simply on the basis of a supposed ecological analogy with crocodilians.

The relatively cold climatic conditions under which the formations containing the Jehol Biota were deposited may partly explain their singularity, notably by comparison with assemblages from other parts of Asia, which during the Early Cretaceous were located farther South. Such comparison applies, in particular, to the Barremian (?) Sao Khua and Aptian Khok Kruat formations of northeastern Thailand, which have yielded abundant vertebrate remains, and for which isotopic data are available (7). Although there are a few faunal elements shared by the Jehol Biota and the Khok Kruat Formation, such as the ceratopsian dinosaur Psittacosaurus (37), faunal similarities between the two formations seem to be very limited. Such differences may partly be owing to different depositional environments between the fluvial Thai formations and the largely lacustrine formations of northeastern China, with consequences in both composition and preservation. However, the different climatic conditions, themselves linked to geography, may have played a major role by preventing forms restricted to warm environments from entering northeastern Asia during part of the Early Cretaceous. More globally, the palaeotemperatures estimated from the oxygen isotope compositions of Jehol Biota fossils support previous claims that “icehouse” events took place during the Early Cretaceous, resulting in climatic conditions that might have been close to present day global climate but with a lesser extent of polar ice caps (5). The peculiar composition of the Jehol Biota may therefore largely reflect relatively cold climatic conditions in northeastern Asia during part of the Early Cretaceous, which contrasts with the usual “greenhouse” conditions under which many Mesozoic ecosystems flourished. A climatic gradient similar in some respects to the present one may at least partly explain the differences between the Jehol Biota and floral and faunal assemblages from regions located farther South.

Analytical method.

Measurements of oxygen isotope compositions of apatite phosphate consist in isolating phosphate ions using acid dissolution and anion-exchange resin, according to a protocol derived from the original method published by Crowson et al. (38) and slightly modified by Lécuyer et al. (39). Silver phosphate was quantitatively precipitated in a thermostatic bath set at a temperature of 70 °C. After filtration, washing with double deionised water, and drying at 50 °C, 15 mg of Ag3PO4 were mixed with 0.8 mg of pure powder graphite. Oxygen isotope ratios were measured by reducing silver phosphate to CO2 using graphite reagent (40, 41). Samples were weighed into tin reaction capsules and loaded into quartz tubes and degassed for 30 min at 80 °C under vacuum. Each sample was heated at 1,100 °C for 1 min to promote the redox reaction. The CO2 produced was directly trapped in liquid nitrogen to avoid any kind of isotopic reaction with quartz at high temperature. CO2 was then analyzed with a Thermo-Finnigan MAT253 mass spectrometer at the Institute of Geology and Geophysics, Chinese Academy of Sciences. Isotopic compositions are quoted in the standard δ notation relative to V-SMOW (Vienna Standard Mean Ocean Water). Silver phosphate precipitated from standard NBS120c (natural Miocene phosphorite from Florida) was repeatedly analyzed (δ18O = 21.7 ± 0.2‰; n = 37) along with the silver phosphate samples derived from the fossil vertebrate remains.

Acknowledgments

This work was supported by the Chinese Academy of Sciences, the National Natural Science Foundation of China (Grants 40730208, 40502019, and 40862001), the Major Basic Research Projects (2006CB806400) of MST (Ministry of Science and Technology) of China, the French CNRS ECLIPSE II programme, and a Thai-French joint project (PHC n° 16610UJ).

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: Romain.amiot{at}univ-lyon1.fr.

  • ↵2Present address: CNRS (Centre National de la Recherche Scientifique) UMR (Unité Mixte de Recherche) 5276, Université Claude Bernard Lyon 1, and Ecole Normale Supérieure de Lyon, 2, Rue Raphaël Dubois, 69622 Villeurbanne Cedex, France.

  • Author contributions: R.A. and Z.Z. designed research; R.A., Xu Wang, Z.Z., Xiaolin Wang, E.B., T.H., N.K., J.M., V.S., Y.W., X.X., and F.Z. performed research; R.A., Xu Wang, E.B., C.L., F.F., and F.Z. analyzed data; and R.A., Z.Z., E.B., C.L., Z.D., F.F., T.H., N.K., J.M., V.S., Y.W., X.X., Xu Wang, Xiaolin Wang, and F.Z. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1011369108/-/DCSupplemental.

References

  1. ↵
    1. Zhou Z,
    2. Barrett PM,
    3. Hilton J
    (2003) An exceptionally preserved Lower Cretaceous ecosystem. Nature 421:807–814.
    OpenUrlCrossRefPubMed
  2. ↵
    1. Barrett PM,
    2. Hilton JM
    (2006) The Jehol Biota (Lower Cretaceous, China): new discoveries and future prospects. Integrative Zoology 1:15–17.
    OpenUrlCrossRefPubMed
  3. ↵
    1. Luo Z
    (1999) A refugium for relicts. Nature 400:23–25.
    OpenUrlCrossRef
  4. ↵
    1. Pucéat E,
    2. et al.
    (2003) Thermal evolution of Cretaceous Tethyan marine waters inferred from oxygen isotope composition of fish tooth enamels. Paleoceanography 18:1029, doi: 10.1029/2002PA000823.
    OpenUrlCrossRef
  5. ↵
    1. Price GD
    (1999) The evidence and implications of polar ice during the Mesozoic. Earth Science Reviews 48:183–210.
    OpenUrlCrossRef
  6. ↵
    1. Chang S,
    2. Zhang H,
    3. Renne PR,
    4. Fang Y
    (2009) High-precision 40Ar/39Ar age for the Jehol Biota. Palaeogeogr Palaeocl 280:94–104.
    OpenUrlCrossRef
  7. ↵
    1. Buffetaut E,
    2. Cuny G,
    3. Le Loeuff J,
    4. Suteethorn V
    1. Amiot R,
    2. et al.
    (2009) Late Paleozoic and Mesozoic continental ecosystems in SE Asia. in Geological Society London Special Publications, eds Buffetaut E, Cuny G, Le Loeuff J, Suteethorn V (The Geological Society, London), 271–283.
  8. ↵
    1. Amiot R,
    2. et al.
    (2010) Oxygen isotope evidence for semi-aquatic habits among spinosaurid theropods. Geology 38:139–142.
    OpenUrlAbstract/FREE Full Text
  9. ↵
    1. Amiot R,
    2. et al.
    (2006) Oxygen isotopes from biogenic apatites suggest widespread endothermy in Cretaceous dinosaurs. Earth Planet Sc Lett 246:41–54.
    OpenUrlCrossRef
  10. ↵
    1. Blake RE,
    2. O'Neil JR,
    3. Garcia GA
    (1997) Oxygen isotope systematics of biologically mediated reactions of phosphate: I. Microbial degradation of organophosphorus compounds. Geochim Cosmochim Ac 61:4411–4422.
    OpenUrlCrossRef
  11. ↵
    1. Zazzo A,
    2. Lécuyer C,
    3. Mariotti A
    (2004) Experimentally-controlled carbon and oxygen isotope exchange between bioapatites and water under inorganic and microbially-mediated conditions. Geochim Cosmochim Ac 68:1–12.
    OpenUrl
  12. ↵
    1. Kolodny Y,
    2. Luz B,
    3. Navon O
    (1983) Oxygen isotope variations in phosphate of biogenic apatites, I. Fish bone apatite—rechecking the rules of the game. Earth Planet Sc Lett 64:398–404.
    OpenUrlCrossRef
  13. ↵
    1. Lécuyer C,
    2. Grandjean P,
    3. Sheppard SMF
    (1999) Oxygen isotope exchange between dissolved phosphate and water at temperatures ≤ 135 °C: Inorganic versus biological fractionations. Geochim Cosmochim Ac 63:855–862.
    OpenUrlCrossRef
  14. ↵
    1. Kolodny Y,
    2. Luz B,
    3. Sander M,
    4. Clemens WA
    (1996) Dinosaur bones: fossils or pseudomorphs? The pitfalls of physiology reconstruction from apatitic fossils. Palaeogeogr Palaeocl 126:161–171.
    OpenUrlCrossRef
  15. ↵
    1. Amiot R,
    2. et al.
    (2004) Latitudinal temperature gradient during the Cretaceous Upper Campanian-Middle Maastrichtian: δ18O record of continental vertebrates. Earth Planet Sc Lett 226:255–272.
    OpenUrlCrossRef
  16. ↵
    1. Barrick RE,
    2. Fischer AG,
    3. Showers WJ
    (1999) Oxygen isotopes from turtle bone; applications for terrestrial paleoclimates? Palaios 14:186–191.
    OpenUrlAbstract/FREE Full Text
  17. ↵
    1. Tütken T,
    2. Pfretzschner H,
    3. Vennemann TW,
    4. Sun G,
    5. Wang YD
    (2004) Paleobiology and skeletochronology of Jurassic dinosaurs: implications from the histology and oxygen isotope compositions of bones. Palaeogeogr Palaeocl 206:217–238.
    OpenUrlCrossRef
  18. ↵
    1. Zazzo A,
    2. Lécuyer C,
    3. Sheppard SMF,
    4. Grandjean P,
    5. Mariotti A
    (2004) Diagenesis and the reconstruction of paleoenvironments: a method to restore original δ18O values of carbonate and phosphate from fossil tooth enamel. Geochim Cosmochim Ac 68:2245–2258.
    OpenUrlCrossRef
  19. ↵
    1. Fricke HC,
    2. Clyde WC,
    3. O'Neil JR,
    4. Gingerich PD
    (1998) Evidence for rapid climate change in North America during the latest Paleocene thermal maximum: oxygen isotope compositions of biogenic phosphate from the Bighorn Basin (Wyoming) Earth Planet Sc Lett 160:193–208.
    OpenUrlCrossRef
  20. ↵
    1. Lécuyer C,
    2. et al.
    (2003) Stable isotope composition and rare earth element content of vertebrate remains from the Late Cretaceous of northern Spain (Lano): did the environmental record survive? Palaeogeogr Palaeocl 193:457–471.
    OpenUrlCrossRef
  21. ↵
    1. Pucéat E,
    2. Reynard B,
    3. Lécuyer C
    (2004) Can crystallinity be used to determine the degree of chemical alteration of biogenic apatites? Chem Geol 205:83–97.
    OpenUrlCrossRef
  22. ↵
    1. Fricke HC,
    2. Pearson DA
    (2008) Stable isotope evidence for changes in dietary niche partitioning among hadrosaurian and ceratopsian dinosaurs of the Hell Creek Formation, North Dakota. Paleobiology 34:534–552.
    OpenUrlAbstract/FREE Full Text
  23. ↵
    1. Fricke HC,
    2. Rogers RR,
    3. Backlund R,
    4. Dwyer CN,
    5. Echt S
    (2008) Preservation of primary stable isotope signals in dinosaur remains, and environmental gradients of the Late Cretaceous of Montana and Alberta. Palaeogeogr Palaeocl 266:13–27.
    OpenUrlCrossRef
  24. ↵
    1. Erickson G
    (1996) Incremental lines of von Ebner in dinosaurs and the assessment of tooth replacement rates using growth line counts. Proc Natl Acad Sci USA 93:14623–14627.
    OpenUrlAbstract/FREE Full Text
  25. ↵
    1. Sheppard SMF
    (1986) Characterization and isotopic variations in natural waters. Rev Mineral Geochem 16:165–183.
    OpenUrlAbstract
  26. ↵
    1. Rozanski K
    (1985) Deuterium and oxygen-18 in European groundwaters-Links to atmospheric circulation in the past. Chemical Geology: Isotope Geoscience section 52:349–363.
    OpenUrlCrossRef
  27. ↵
    1. IAEA/WMO
    (2006) Global Network of Isotopes in Precipitation. The GNIP Database. Accessible at: http://isohis.iaea.org.
  28. ↵
    1. Steuber T,
    2. Rauch M,
    3. Masse JP,
    4. Graaf J,
    5. Malkoč M
    (2005) Low-latitude seasonality of Cretaceous temperatures in warm and cold episodes. Nature 437:1341–1344.
    OpenUrlCrossRefPubMed
  29. ↵
    1. Philippe M,
    2. Thevenard F
    (1996) Distribution and palaeoecology of the Mesozoic wood genus Xenoxylon: palaeoclimatological implications for the Jurassic of Western Europe. Rev Palaeobot Palyno 91:353–370.
    OpenUrlCrossRef
  30. ↵
    1. Philippe M,
    2. et al.
    (2009) Structure and diversity of the Mesozoic wood genus. Xenoxylon in Far East Asia: implications for terrestrial palaeoclimates. Lethaia 42:393–406.
    OpenUrlCrossRef
  31. ↵
    1. Yun CS,
    2. Lim JD,
    3. Yang SY
    (2004) The first crocodyliform (Archosauria: Crocodylomorpha) from the Early Cretaceous of Korea. Curr Sci India 86:1200–1201.
    OpenUrl
  32. ↵
    1. Azuma Y
    (2002) Early Cretaceous vertebrate remains from Katsuyama City, Fukui Prefecture, Japan. Memoir of the Fukui Prefectural Dinosaur Museum 2:17–21.
    OpenUrl
  33. ↵
    1. Markwick PJ
    (1998) Fossil crocodilians as indicators of Late Cretaceous and Cenozoic climates: implications for using palaeontological data in reconstructing palaeoclimate. Palaeogeogr Palaeocl 137:205–271.
    OpenUrlCrossRef
  34. ↵
    1. Tarduno JA,
    2. et al.
    (1998) Evidence for extreme climatic warmth from Late Cretaceous Arctic vertebrates. Science 282:2241–2244.
    OpenUrlAbstract/FREE Full Text
  35. ↵
    1. Liu J
    (2004) A nearly complete skeleton of I kechosaurus pijiagouensis sp. nov.(Reptilia: Choristodera) from the Jiufotang Formation (Lower Cretaceous) of Liaoning, China. Vertebrat Palasiatic 42:120–129.
    OpenUrl
  36. ↵
    1. Zhou Z
    (2006) Evolutionary radiation of the Jehol Biota: chronological and ecological perspectives. Geol J 41:377–393.
    OpenUrlCrossRef
  37. ↵
    1. Tantiwanit W
    1. Buffetaut E,
    2. Suteethorn V,
    3. Khansubha S
    (2007) in Proceedings of the International Conference on Geology of Thailand: towards sustainable development and sufficiency economy, ed Tantiwanit W (Department of Mineral Resources, Bangkok), pp 338–343.
  38. ↵
    1. Crowson RA,
    2. Showers WJ,
    3. Wright EK,
    4. Hoering TC
    (1991) A method for preparation of phosphate samples for oxygen isotope analysis. Anal Chem 63:2397–2400.
    OpenUrl
  39. ↵
    1. Lécuyer C,
    2. Grandjean P,
    3. O'Neil JR,
    4. Cappetta H,
    5. Martineau F
    (1993) Thermal excursions in the ocean at the Cretaceous-Tertiary boundary (northern Morocco): δ18O record of phosphatic fish debris. Palaeogeogr Palaeocl 105:235–243.
    OpenUrlCrossRef
  40. ↵
    1. Lécuyer C,
    2. et al.
    (1998) δ18O and REE contents of phosphatic brachiopods: a comparison between modern and lower Paleozoic populations. Geochim Cosmochim Ac 62:2429–2436.
    OpenUrlCrossRef
  41. ↵
    1. O’Neil JR,
    2. Roe LJ,
    3. Reinhard E,
    4. Blake RE
    (1994) A rapid and precise method of oxygen isotope analysis of biogenic phosphate. Israel J Earth Sci 43:203–212.
    OpenUrl
  42. ↵
    1. Enkin RJ,
    2. Yang Z,
    3. Chen Y,
    4. Courtillot V
    (1992) Paleomagnetic constraints on the geodynamic history of the major blocks of China from the Permian to the present. J Geophys Res 97:13953–13989.
    OpenUrlCrossRef
  43. ↵
    1. Buffetaut E,
    2. Cuny G,
    3. Le Loeuff J,
    4. Suteethorn V
    1. Racey A,
    2. Goodall JGS
    (2009) Late Paleozoic and Mesozoic continental ecosystems in SE Asia. in Geological Society of London Special Publications, eds Buffetaut E, Cuny G, Le Loeuff J, Suteethorn V (The Geological Society, London), 69–83.
  44. ↵
    1. Tang F,
    2. et al.
    (2001) Biostratigraphy and palaeoenvironment of the dinosaur-bearing sediments in Lower Cretaceous of Mazongshan area, Gansu Province, China. Cretaceous Res 22:115–129.
    OpenUrlCrossRef
  45. ↵
    1. Li C,
    2. Setoguchi T,
    3. Wang Y,
    4. Hu Y,
    5. Chang Z
    (2005) The first record of “eupantotherian” (Theria, Mammalia) from the late Early Cretaceous of western Liaoning, China. Vertebrat Palasiatic 43:245–255.
    OpenUrl
  46. ↵
    1. Kusuhashi N
    (2008) Early Cretaceous multituberculate mammals from the Kuwajima Formation (Tetori Group), central Japan. Acta Palaeontol Pol 53:379–390.
    OpenUrl
  47. ↵
    1. Lin W,
    2. Chen Y,
    3. Faure M,
    4. Wang Q
    (2003) Tectonic implications of new Late Cretaceous paleomagnetic constraints from eastern LiaoningPeninsula NE China. J Geophys Res 108:2313, doi: 10.1029/2002JB002169.
    OpenUrlCrossRef
  48. ↵
    1. Shen Z,
    2. et al.
    (2005) Paleomagnetic results of the Cretaceous marine sediments in Tongyouluke, southwest Tarim. Sci China Ser D 48:406–416.
    OpenUrlCrossRef
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Oxygen isotopes of East Asian dinosaurs reveal exceptionally cold Early Cretaceous climates
Romain Amiot, Xu Wang, Zhonghe Zhou, Xiaolin Wang, Eric Buffetaut, Christophe Lécuyer, Zhongli Ding, Frédéric Fluteau, Tsuyoshi Hibino, Nao Kusuhashi, Jinyou Mo, Varavudh Suteethorn, Yuanqing Wang, Xing Xu, Fusong Zhang
Proceedings of the National Academy of Sciences Mar 2011, 108 (13) 5179-5183; DOI: 10.1073/pnas.1011369108
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