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

R. Amiot, X. Wang, Z. Zhou, E. Buffetaut, C. Lécuyer, Z. Ding, F. Fluteau, T. Hibino, N. Kusuhashi

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R. Amiot, X. Wang, Z. Zhou, E. Buffetaut, C. Lécuyer, et al.. Oxygen isotopes of East Asian dinosaurs reveal exceptionally cold Early Cretaceous climates. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108 (13), pp.5179-5183. 10.1073/pnas.1011369108 . hal-02994739

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

Romain Amiot<sup>a,1,2</sup>, Xu Wang<sup>b</sup>, Zhonghe Zhou<sup>a</sup>, Xiaolin Wang<sup>a</sup>, Eric Buffetaut<sup>c</sup>, Christophe Lécuyer<sup>d,2</sup>, Zhongli Ding<sup>b</sup>, Frédéric Fruteau<sup>e</sup>, Tsuyoshi Hibino<sup>f</sup>, Nao Kusuhashi<sup>g</sup>, Jinyou Mo<sup>h</sup>, Varavudh Suteethorn<sup>i</sup>, Yuanqing Wang<sup>a</sup>, Xing Xu<sup>a</sup>, and Fusong Zhang<sup>b</sup>

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

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 (δ¹⁸O~P~) from various reptile remains recovered from China, Thailand, and Japan. δ¹⁸O~P~ 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.

vertebrate phosphate | oxygen isotopes | paleoclimate

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 (δ¹⁸O~P~) 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.

**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

<footnote><sup>a</sup>Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences (CAS), 142 Xi Zhi Men Wai DaJie, Beijing 100044, China; <sup>b</sup>Key Laboratory of Cenozoic Geology and Environment, Institute of Geology and Geophysics, Chinese Academy of Sciences, 19 Beitucheng Xilu, Beijing 100029, China; <sup>c</sup>CNRS (Centre National de la Recherche Scientifique) UMR (Unité Mixte de Recherche) 8538, Laboratoire de Géologie de l'Ecole Normale Supérieure, 24, Rue Lhomond, 75231 Paris Cedex 05, France; <sup>d</sup>CNRS (Centre National de la Recherche Scientifique) UMR (Unité Mixte de Recherche) 5125, Université Claude Bernard Lyon 1, 2, Rue Raphaël Dubois, 69622 Villeurbanne Cedex, France; <sup>e</sup>Institut de Physique du Globe de Paris, 1 Rue Jussieu, 75238 Paris Cedex 05, France; <sup>f</sup>Shiramine Institute of Paleontology, Kuwajima, Hakusan, Ishikawa 920-2502, Japan; <sup>g</sup>Department of Earth's Evolution and Environment, Graduate School of Science and Engineering, Ehime University, 2-5 Bunkyo-cho, Matsuyama, Ehime 790-8577, Japan; <sup>h</sup>Faculty of Earth Sciences, China University of Geosciences, 388 Lumo Road, Wuhan 430074, China; and <sup>i</sup>Department of Mineral Resources, Rama VI Road, Bangkok 10400, Thailand</footnote>

<footnote>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.</footnote>

<footnote>The authors declare no conflict of interest.</footnote>

<footnote>This article is a PNAS Direct Submission.</footnote>

<footnote n="1">¹To whom correspondence should be addressed. E-mail: Romain.amiot@univ-lyon1.fr.</footnote>

<footnote n="2">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.</footnote>

<footnote>This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1011369108/-/DCSupplemental.</footnote>
<table><caption>Table 1. Formation, age, sample number (N), and computed palaeolatitudes are given along with mean vertebrate δ¹⁸Oₚ values, environmental water δ¹⁸Oₗ values obtained by subtracting 21.9 to mean δ¹⁸Oₚ values (15) and estimated mean air temperatures using the following equation: δ¹⁸Oₗ = 0.49(±0.03)T °C – 14.18(±0.52) (15)</caption><thead><tr><th rowspan="2">Formation</th><th rowspan="2">Age</th><th rowspan="2">N</th><th rowspan="2">Paleolatitude (°)</th><th colspan="2">δ¹⁸Oₚ (%o V-SMOW)</th><th>δ¹⁸Oₗ</th><th colspan="2">M.A.T. (°C)</th></tr><tr><th>Mean</th><th>Std. Dev.</th><th>(‰ V-SMOW)</th><th>mean</th><th>Std. Dev.</th></tr></thead><tbody><tr><td>Kuwajima (1)</td><td>Barremian-Early Aptian</td><td>16</td><td>43.2(+8.2/-7.8)</td><td>12.7</td><td>1.8</td><td>-9.2</td><td>10</td><td>4</td></tr><tr><td>Fuxin (2)</td><td>Aptian-Albian</td><td>10</td><td>42.1(+6.6/-6.5)</td><td>11.7</td><td>1.6</td><td>-10.3</td><td>8</td><td>3</td></tr><tr><td>Shahai (3)</td><td>Aptian-Albian</td><td>9</td><td>42.1(+6.6/-6.5)</td><td>11.9</td><td>0.7</td><td>-10.0</td><td>9</td><td>1</td></tr><tr><td>Yixian (4)</td><td>Barremian-Early Aptian</td><td>16</td><td>41.9(+6.6/-6.6)</td><td>12.7</td><td>1.8</td><td>-9.2</td><td>10</td><td>4</td></tr><tr><td>Xinminbao (5)</td><td>Aptian-Albian</td><td>29</td><td>35.2(+6.4/-6.6)</td><td>14.9</td><td>2.9</td><td>-7.0</td><td>15</td><td>6</td></tr><tr><td>Khok Kruat (6)</td><td>Aptian</td><td>18</td><td>24.3(+1.9/-1.8)</td><td>15.2</td><td>2.8</td><td>-6.7</td><td>15</td><td>6</td></tr><tr><td>Sao Khua (7)</td><td>Barremian?</td><td>11</td><td>24.3(+1.9/-1.8)</td><td>17.0</td><td>0.5</td><td>-4.9</td><td>19</td><td>1</td></tr><tr><td>Napai (8)</td><td>Aptian?</td><td>9</td><td>21.0(+7.2/-7.2)</td><td>17.1</td><td>2.5</td><td>-4.9</td><td>19</td><td>5</td></tr></tbody></table>

Numbers in brackets associated with Formation names are the same as those displayed in Fig. 1.

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 δ¹⁸Oₚ values of probable endotherms (dinosaurs and trytilodont synapsids) and ectotherms (turtles and crocodilians) that mimics present day variations of the offset observed between the δ¹⁸Oₚ values of endotherms and ectotherms (Fig. 2). If early diagenetic processes had occurred, they would have erased the expected offsets in δ¹⁸Oₚ values of vertebrate remains having different ecologies or physiologies (20).

<figure><img src="image_2.png" /><figcaption>**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.</figcaption></figure>

**Climatic and Ecologic Implications.** Considering at least partial preservation of the primary isotopic compositions of analyzed apatites, mean δ¹⁸Omw values of meteoric waters can be estimated at each site using present day relationships established between vertebrate phosphate and water (δ¹⁸Oₚ – δ¹⁸Oₗ). Due to ecological differences between herbivorous (sauropods, ornithopods, ceratopsians, and ankylosaurs) and carnivorous (theropods) dinosaurs, systematic offsets in δ¹⁸Oₚ values between these dinosaur groups that would reflect differences in diet, water strategies, and foraging micro habitats were expected (7, 22, 23). However, the δ¹⁸Oₚ 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 δ¹⁸Oₚ values between teeth coming from the same deposit are expected. The same pattern can be observed on crocodilian and turtles δ¹⁸Oₚ 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 δ¹⁸Omw values (Fig. 2). From present day data, it has

<figure><img src="image_3.png" /><figcaption>**Fig. 2.** Latitudinal variations in δ¹⁸Oₚ values of dinosaurs, crocodilians, and turtles compared to expected latitudinal variations in δ¹⁸Oₚ values of present day endotherms and ectotherms drawn using δ¹⁸Omw and mean air temperature values of IAEA (International Atomic Energy Agency)/WMO (World Meteorological Organization) (27), and the following equations: δ¹⁸Omw = 1.11 * δ¹⁸Oₚ - 26.44 [endotherms; (15)] and T = 113.3 - 4.38 * (δ¹⁸Oₚ - δ¹⁸Omw) [ectotherms; (12)].</figcaption></figure>
been shown that a first order estimation of δ¹⁸Omw value can be
calculated by substracting 21.9‰ to the average δ¹⁸Oₚ value of
both endotherms and ectotherms (15). Based on these considera-
tions, δ¹⁸Omw values were estimated for the eight Early Cretac-
eous 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.

Despite the possibility that, at the global scale, Mesozoic
hygrometry differed from present day condition, thus affecting
the latitudinal distribution of δ¹⁸Omw values, there is no compel-
ling evidence to indicate that the systematics of ancient meteoric
waters were radically different from today (25). On the contrary,
it was argued that the “δ¹⁸Omw-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 (δ¹⁸Omw-MAAT) that was
previously used to establish a terrestrial temperature gradient for
the terminal Cretaceous (15; Fig. 4).

The fitted temperature gradient has a curvature similar to that
of the present day gradient but shifted towards lower mean tem-
peratures (Fig. 4). For consistency, the same (δ¹⁸Omw-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 tempe-
rate 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. Through-
out 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 tem-
perate climates (29), was widely distributed in northeastern Asia
during the Early Cretaceous, where it reached a level of anato-
mical 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 occur-
rence in the Late Turonian to Early Santonian Nenjiang Forma-
tion 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 cro-
codilians 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 pter-
osaurs 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). Choristo-
deres 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 tempera-
ture 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 defi-
nitely occurred together in warmer environments. This interpre-

<figure><img src="image_4.png" /><figcaption>**Fig. 3.** Calculated mean meteoric water $\delta^{18}$O$_{mw}$ gradient during the Early Cretaceous of eastern Asia vs. absolute latitudes. The Early Cretaceous thermal gradient was calculated using fossil vertebrate $\delta^{18}$O$_{p}$ 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.</figcaption></figure>

<figure><img src="image_5.png" /><figcaption>**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 δ¹⁸Oₚ 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.</figcaption></figure>
tation 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

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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).

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