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Oxygen Isotopes of East Asian Dinosaurs Reveal Exceptionally Cold Early Cretaceous Climates

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Oxygen Isotopes of East Asian Dinosaurs Reveal Exceptionally Cold Early Cretaceous Climates Oxygen isotopes of East Asian dinosaurs reveal exceptionally cold Early Cretaceous climates Romain Amiota,1,2, Xu Wangb, Zhonghe Zhoua, Xiaolin Wanga, Eric Buffetautc, Christophe Lécuyerd,2, Zhongli Dingb, Frédéric Fluteaue, Tsuyoshi Hibinof, Nao Kusuhashig, Jinyou Moh, Varavudh Suteethorni, Yuanqing Wanga, Xing Xua, and Fusong Zhangb aKey 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; bKey Laboratory of Cenozoic Geology and Environment, Institute of Geology and Geophysics, Chinese Academy of Sciences, 19 Beitucheng Xilu, Beijing 100029, China; cCNRS (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; dCNRS (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; eInstitut de Physique du Globe de Paris, 1 Rue Jussieu, 75238 Paris Cedex 05, France; fShiramine Institute of Paleontology, Kuwajima, Hakusan, Ishikawa 920-2502, Japan; gDepartment of Earth's Evolution and Environment, Graduate School of Science and Engineering, Ehime University, 2-5 Bunkyo-cho, Matsuyama, Ehime 790-8577, Japan; hFaculty of Earth Sciences, China University of Geosciences, 388 Lumo Road, Wuhan 430074, China; andiDepartment of Mineral Resources, Rama VI Road, Bangkok 10400, Thailand 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 parti- sanidine crystals from tuff beds within the Yixian Formation cularly the Jehol Biota of northeastern China flourished during a and the base of the overlying Jiufotang Formation gave an age period of highly debated climatic history. While the unique charac- bracket of 129.7 Æ 0.5 Ma to 122.1 Æ 0.3 Ma for the deposition ters of these continental faunas have been the subject of various of the Yixian Formation (6). These ages correspond to a Barre- speculations about their biogeographic history, little attention has mian to early Aptian age interval which is encompassed by the 18 been paid to their possible climatic causes. Here we address this second cold interval. We have estimated water δ O values and question using the oxygen isotope composition of apatite phos- related mean air paleotemperatures at eight contemporaneous δ18 phate ( Op) from various reptile remains recovered from China, localities covering a large range of paleolatitudes in order to δ18 Thailand, and Japan. Op values indicate that cold terrestrial cli- define a latitudinal climatic gradient and its influence upon the mates prevailed at least in this part of Asia during the Barremian— geographic distribution of East Asian fauna and flora. early Albian interval. Estimated mean air temperatures of about 10 Æ 4 °C at midlatitudes (∼42 °N) correspond to present day cool Results and Discussion – temperate climatic conditions. Such low temperatures are in agree- We have used 99 new and 17 published [(7 9); Table S1] oxygen δ18 ment with previous reports of cold marine temperatures during isotope compositions of apatite phosphate ( Op) measured on this part of the Early Cretaceous, as well as with the widespread dinosaurs, tritylodont synapsids, and freshwater crocodilian occurrence of the temperate fossil wood genus Xenoxylon and teeth, as well as turtles shell bones. These apatitic remains were the absence of thermophilic reptiles such as crocodilians in north- recovered from deposits of the Yixian Formation and seven other eastern China. The unique character of the Jehol Biota is thus Early Cretaceous formations in China, Japan, and Thailand. not only the result of its evolutionary and biogeographical history All these deposits are dated from the Barremian to the Aptian- Albian intervals and cover palaeolatitudes ranging from 21.0Æ but is also due to rather cold local climatic conditions linked to 7 2 43 2 Æ 8 0 the paleolatitudinal position of northeastern China and global . °N to . °N (Table 1 and Fig. 1). Oxygen isotope com- icehouse climates that prevailed during this part of the Early positions of apatite phosphates were measured using the proce- dure described in the Analytical method section, and are reported Cretaceous. GEOLOGY on in Table S1. vertebrate phosphate ∣ oxygen isotopes ∣ paleoclimate Preservation of the Original Oxygen Isotope Compositions. Secondary precipitation of apatite and isotopic exchange during microbially ince the last decade, continuous discoveries of Early Cretac- mediated reactions may alter the primary isotopic signal (10, 11). Seous invertebrates, plants and vertebrates in East Asia, and However, apatite crystals that make up tooth enamel are large more particularly exceptionally preserved specimens in north- and densely packed, and in the absence of high temperature eastern China belonging to the Jehol Biota, have fed numerous conditions which Kolodny and others argue that they enable current evolutionary debates (1, 2). This latter assemblage is microbial mediated reactions to reset the bone phosphate oxygen preserved in the lacustrine and volcanic sediments that mainly isotopic signal, isotopic exchange might not affect the oxygen constitute the Yixian and Jiufotang formations of Liaoning Pro- “ ” isotope composition of phosphates even at geological time scales vince. The peculiar character of the Jehol Biota, with unusual (12, 13). Turtle shell and dinosaur bones should be more suscep- forms such as feathered dinosaurs, is clearly in part a result of the tible to diagenetic alteration because hydroxylapatite crystals exceptional preservation of many fossils which show well pre- served integumentary structures seldom preserved in other local- ities. However, it has been suggested that the Jehol Biota show Author contributions: R.A. and Z.Z. designed research; R.A., Xu Wang, Z.Z., Xiaolin Wang, peculiar floral and faunal compositions, which may, for instance, 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., be indicative of a relict character (3) although this interpreta- Xu Wang, Xiaolin Wang, and F.Z. wrote the paper. tion has been disputed (1). To date, possible relations between The authors declare no conflict of interest. global climatic conditions and the taxonomic composition of This article is a PNAS Direct Submission. the Jehol Biota have not been investigated, and no quantitative 1To whom correspondence should be addressed. E-mail: [email protected]. local climate reconstruction has been proposed so far. In the mar- 2Present address: CNRS (Centre National de la Recherche Scientifique) UMR (Unité Mixte ine record, cold climatic intervals have been recognized during de Recherche) 5276, Université Claude Bernard Lyon 1, and Ecole Normale Supérieure de the Early Cretaceous period, with two major events occurring Lyon, 2, Rue Raphaël Dubois, 69622 Villeurbanne Cedex, France. i ii ( ) during the early Valanginian, and ( ) from the late Barremian This article contains supporting information online at www.pnas.org/lookup/suppl/ 40 39 to the early Albian (4, 5). The most recent Ar∕ Ar dating of doi:10.1073/pnas.1011369108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1011369108 PNAS ∣ March 29, 2011 ∣ vol. 108 ∣ no. 13 ∣ 5179–5183 Downloaded by guest on September 24, 2021 δ18 Table 1. Formation, age, sample number (N), and computed palaeolatitudes are given along with mean vertebrate Op values, δ18 δ18 environmental water Ow values obtained by subtracting 21.9 to mean Op values (15) and estimated mean air temperatures using δ18 ¼ 0 49ð0 03ÞT − 14 18ð0 52Þ the following equation: Ow . °C . (15) δ18 ‰ δ18 Op ( V-SMOW) Ow M.A.T. (°C) Formation Age N Paleolatitude (°) Mean Std. Dev. (‰ V-SMOW) mean Std. Dev. Kuwajima (1) Barremian-Early Aptian 16 43.2ðþ8.2∕−7.8Þ 12.7 1.8 −9.2 10 4 Fuxin (2) Aptian-Albian 10 42.1ðþ6.6∕−6.5Þ 11.7 1.6 −10.3 8 3 Shahai (3) Aptian-Albian 9 42.1ðþ6.6∕−6.5Þ 11.9 0.7 −10.0 9 1 Yixian (4) Barremian-Early Aptian 16 41.9ðþ6.6∕−6.6Þ 12.7 1.8 −9.2 10 4 Xinminbao (5) Aptian-Albian 29 35.2ðþ6.4∕−6.6Þ 14.9 2.9 −7.0 15 6 Khok Kruat (6) Aptian 18 24.3ðþ1.9∕−1.8Þ 15.2 2.8 −6.7 15 6 Sao Khua (7) Barremian? 11 24.3ðþ1.9∕−1.8Þ 17.0 0.5 −4.9 19 1 Napai (8) Aptian? 9 21.0ðþ7.2∕−7.2Þ 17.1 2.5 −4.9 19 5 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 Climatic and Ecologic Implications. Considering at least partial enamel (14), even though several case studies have shown that preservation of the primary isotopic compositions of analyzed δ18 the original oxygen isotope composition can be preserved in apatites, mean Omw values of meteoric waters can be esti- Mesozoic reptile remains (7–9, 15–17). Although no method is mated at each site using present day relationships established δ18 − δ18 available to demonstrate definitely whether or not the oxygen between vertebrate phosphate and water ( Op Ow). Due isotope composition of fossil vertebrate phosphate was modified to ecological differences between herbivorous (sauropods, by diagenetic processes, several ways to assess the preservation ornithopods, ceratopsians, and ankylosaurs) and carnivorous (theropods) dinosaurs, systematic offsets in δ18O values between state of the primary isotopic record have been proposed [e.g., p – these dinosaur groups that would reflect differences in diet, water (14, 18 21)].
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