Chinese Science Bulletin

© 2008 SCIENCE IN PRESS Springer

Geochemical environmental changes and extinction during the - (K/T) transition in the Nanxiong Basin, South China: Evidence from dinosaur eggshells

ZHAO ZiKui1†, MAO XueYing2, CHAI ZhiFang2, YANG GaoChuang2, ZHANG FuCheng1 & YAN Zheng3

1 Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 100044, China; 2 Institute of High Energy Physics and Laboratory of Nuclear Analytical Techniques, Chinese Academy of Sciences, Beijing 100080, China; 3 Institute of Geology, State Seismological Bureau, Beijing 100029, China The complex patterns of trace elements including Ir and isotope distributions in the three K/T sections of the Nanxiong Basin prove the existence of two environmental events in the latest Cretaceous and earliest . The first geochemical environmental event occurred at about 2 Ma prior to the K/T boundary interval, where the dinosaur diversity was hardly reduced, except that a number of patho- logical eggshells appeared. The second one was larger and occurred just at and near the Creta- ceous-Paleogene (K/T) boundary. The extinction of the spread out within 250 ka with major extinction beginning at the boundary interval. This is even later than their extinction in Montana, North America and in India. The cause of the dinosaur extinction may be the result of a complex multiple events brought about by the coincidence of global environment change marked by multiple Ir and δ 18O anomalies, and environmental poisoning characterized by other trace elements derived from the local source. Successive short- and long-term conditions of geochemically induced environmental stress negatively affected the reproductive process and thus contributed to the extinction of the dinosaurs.

Nanxiong Basin of Province, Cretaceous-Paleogene (K/T) boundary, Ir anomaly, trace element, stable isotope, dinosaur eggshell, dinosaur extinction

One of the most striking events in the era was Province are a relatively continuous sequence containing the almost complete extinction of the dinosaurs at the end a record of fauna spanning the K/T bound- of the Cretaceous. The observation of a widespread Ir ary and Paleocene , and seem to provide some anomaly at the K/T boundary led by Alvarez et al.[1―3] to direct evidence for interpreting the dinosaur extinction. propose that the extinction event at the boundary results Previously published data[10―16] from the CGY-CGD and from the impact of an extraterrestrial body on earth. CGT-CGF sections (Figure 1) showed that the geo- However, it is difficult to find strong support for this hy- chemical environmental changes and the dinosaur ex- pothesis, because of the paucity of suitable stratigraphic tinction in South China may have been a rather long- sections and the comparative scarcity of fossil material. Virtually all the evidence or debates that have been drawn Received February 20, 2008; accepted October 30, 2008; published online December 14, 2008 about the final dinosaur extinction derive from a few sec- doi: 10.1007/s11434-008-0565-1 tions in the North American Western Interior[4―9]. †Corresponding author (email: [email protected]) Supported by National Natural Science Foundation of China (Grant No. 40472018) The “red beds” in the Nanxiong Basin of Guangdong and the Chinese Academy of Sciences (Grant No. 21039751) www.scichina.com | csb.scichina.com | www.springerlink.com Chinese Science Bulletin | March 2009 | vol. 54 | no. 5 | 806-815

duration process rather than an instantaneous event that Formation, from which about 10 clutches of eggs have

only lasted a few years or centuries as is often portrayed been collected by the local museums (the Nanxiong ARTICLES in the asteroid hypothesis. Museum and the Museum) and the Museum of Natural History from 1972 to 1994. The complete clutches preserved in situ show no evidence of transport. Excellent preservation of the clutch geometry indicates that the egg laying and sediment formation were nearly synchronous. Many eggshell fragments were found in heaps in this section, and may represent clutches destroyed in situ or nearby. It suggests that the sediments with abundant eggshell fragments were clearly not reworked. Because palynomorphs were scarcer than expected, the exact location of the K/T boundary interval has not yet been determined in this section[15], but it should be present at CGN 220―240 m, Figure 1 Locations of the studied K/T boundary sections in the as discussed later. Nanxiong Basin. Fifteen eggshell samples, belonging to Macroolithus To obtain a better idea on how the cause and timing of yaotunensis, collected at 15 levels from this section by [10,15] the dinosaur extinction took place, we have investigated the Sino-German team in 1984 have been analyzed trace elements including Ir, stable isotope composition, by radiochemical neutron activation analysis (RNAA) and eggshell structures in a series of dinosaur eggshells for their iridium concentration, and by instrumental neu- from the third K/T section (the CGN section) in this ba- tron activation analysis (INAA) for other trace elements; sin. besides, another 15 eggshell samples collected at the The purpose of the present paper is to establish the same levels of this section were used for stable-isotope environmental change pattern across the K/T boundary analysis. The eggshell samples for the chemical analysis and the geochemical environmental stress played a role have been examined using a light microscope and/or in dinosaur extinction, based on the geochemical signals SEM, and display a well-preserved microstructure with GEOLOGY (e.g. trace elements including Ir, stable carbon- and primary calcite growth and little or no recrystallization. oxygen-isotope composition), histo-structures of dino- The eggshell samples were then abraded on the outer saur eggshells with other data regarding stratigraphy and inner surfaces in order to remove any contamination taken from the above-mentioned three sections (CGY- by the surrounding sediments. CGD, CGT-CGF and CGN sections). Theoretically, Ir is nonexistent in eggshell and/or bone because this element is not vital to life. Eggshell 1 Element and isotope distribution in samples of living ostrich (Struthio camelus) from Bei- jing Zoo, wild Chinese alligator (Alligator sinensis) dinosaur eggshells from the CGN Section from Anhui Province, and (Gallus gallus) [12,17] The CGN Section is situated south of the Nanxiong showed no detectable Ir with limits of <6―<10 ppt . county town (Figure 1). Lithologically, the section is The results of Ir abundances and the stable carbon- essentially similar to both the CGY-CGD Section and and oxygen-isotope composition in the eggshell samples the CGT-CGF Section. However, the Pingling Formation from the CGN Section are given in Table 1. Four here attains a thickness of about 270 m, and its upper- Ir-bearing levels have been identified. The highest Ir most part and the overlying strata, the Shanghu Forma- abundance occurs in eggshell sample CGN 912 from tion, are not exposed because of the town buildings in 215.5 m in the CGN Section, and reaches 236.8 ppt this area. (normalized to Ca) over a background level of <10 ppt. According to the field observation, complete eggs in The three other Ir peaks (of 42.7 ppt, 53.3 ppt and 179.7 nest and eggshell fragments are more frequent and ppt) were detected in the eggshell samples CGN 909, widespread in the sedimentary sequence of the Pingling CGN 903 and CGN 901 from 202―203 m, 85.5 m and

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Table 1 Iridium concentration and stable-isotope composition in the dinosaur eggshell samples of Macroolithus yaotunensis from the CGN Section of the Pingling Formation Ir concentration Ir concentration normalized to Sample number Depth (m) Ca (%) δ 13C (‰, PDB) δ 18O (‰, PDB) (ppt, 10−12g/g) Ca (ppt, 10−12g/g) CGN 915 235―235.5 29.7 39.5 28.0 −10.93 +5.50 CGN 914 231.5―232 29.4 39.6 27.6 −10.27 −3.29 CGN 913 223.5―225 <16.3 9.25 −10.18 −3.85 CGN 912 215.5 268 42.1 236.8 −10.85 +0.36 CGN 911 213.5 <18.5 41.4 −10.09 −1.63 CGN 910 208 8.91 41.4 8.1 −9.62 +1.45 CGN 909 202―203 48.4 42.2 42.7 −9.90 −2.19 CGN 908 198―199.5 23 42.8 20.0 −12.01 −6.75 CGN 907 186 25.1 40.5 23.1 −11.13 −2.31 CGN 906 176.5 26.5 40 24.6 −10.55 −3.26 CGN 905 110―112 29.3 42.5 25.6 −10.77 −2.20 CGN 904 104.5―106 <11.6 41.9 −10.46 −3.36 CGN 903 85.5 60.6 42.3 53.3 −9.54 −4.54 CGN 902 76.5 <20.9 41.8 −9.09 +1.11 CGN 901 44 185 38.3 179.7 −9.23 −0.97

44 m of the section, respectively. The distribution of oospecies: Macroolithus yaotunensis, Macroolithus ru- some other trace elements (As, Br, K, La, Na, Au, U, Yb, gustus, andrewsi, Elongatoolithus elon- Fe, Co, Sc and Sr) shows (Figure 2(c)) that most of them gatus, Elongatoolithus oosp., Apheloolithus shuinanen- are distinctly the most abundant in eggshell sample sis, Nanshiungoolithus chuetienensis and Shixingoolithus CGN 913 from 223.5―225 m of the same section, ex- erbeni. cepting Au, U and Fe whose maximum levels occur in Normal eggshells of different oospecies have each the eggshell sample CGN 901 from 44 m. structural pattern and a normal range of shell thickness. [14] The stable-isotope values (Table 1) of the eggshell According to Zhao et al. , in the CGH Section of the samples belonging to Macroolithus yaotunensis from the Yuanpu Formation the eggshell thickness of CGN Section range for δ 13C from −12.01‰ to −9.09‰ Macroolithus yaotunensis range between 1.70 and 2.52 (PDB), and for δ 18O from −6.75‰ to +5.50‰ (PDB), mm, those of Macroolithus rugustus between 1.66 and 13 2.38 mm, those of Elongatoolithus andrewsi between respectively. The values of δ C oscillate within a nar- 1.36 and 1.58 mm, and Elongatoolithus elongatus be- row range of about 3‰. The values of δ 18O, by contrast, tween 0.9 and 1.26 mm. Obviously, each oospecies has a have a range of about 12‰, and is characterized by mul- small variation in eggshell thickness. The average values tiple positive δ 18O perturbations within the CGN Sec- of eggshell thickness in each oospecies at various levels ― 18 tion interval of 208 235.5 m, except for the δ O value show almost no change, and represent the normal range of +1.11‰ for sample CGN 902 from 76.5 m. The three of predominating variation (see Figure 6(a) published in eggshell samples (CGN 910, CGN 912 and CGN 915) Zhao et al.[14]). 18 from 208 m, 215.5 m and 235―235.5 m have δ O Measurements of the eggshell thicknesses involve values of +1.45‰, +0.36‰ and +5.50‰, respectively. 1758 eggshell fragments of the above-mentioned four This shows that the oxygen-isotope record in the CGN oospecies from the CGN Section. The eggshell thickness Section is comparable to that of the two other sections of Macroolithus yaotunensis ranges from 0.9 to 2.36 mm, (CGY-CGD and CGT-CGF)[13]. that of Macroolithus rugustus from 0.92 to1.96 mm, that of Elongatoolithus andrewsi from 0.6 to 1.52 mm, and 2 Pathologic dinosaur eggshells from that of Elongatoolithus elongatus from 0.6 to 1.16 mm, the CGN Section indicating an abnormal variation in eggshell thickness. The mean values of eggshell thickness of each oospecies Dinosaur eggs and eggshell fragments collected at the from successive horizons of this section vary distinctly CGN Section are represented by eight distinct eggshell (Figure 3), and are similar to those from the CGY-CGD

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ARTICLES GEOLOGY

Figure 2 Variations in the trace-element concentration in the dinosaur eggshells from the studied K/T sections in the Nanxiong Basin. (a) CGY-CGD Section; (b) CGT-CGF Section; (c) CGN Section. and CGT-CGF sections (see Figure 6(b), (c) published in defined cone layer and a columnar layer in Macroolithus Zhao et al.[14]). yaotunensis. Figure 4(a) shows the healthy eggshell with a well- An examination of the eggshells with the polarizing

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spaces in the columnar layer of the eggshell (Figure 4(b), (c), (d)). By random analysis of Macroolithus yaotunen- sis from this section, the frequency of histopathological eggshells of this oospecies was found to be a confidence interval of 17% to 53% in the levels of 44 to 106 m, and 12% to 46% in those from 110 to 199 m. In the levels of 202 to 235 m (i.e. at the K/T boundary interval, as dis- cussed later), the frequency increases to 50% to 85% (Table 2). This is one more proof that anomalous con- centrations of trace elements including Ir are associated with the formation of pathological eggshells[10,11,14,18]. The enrichment of Ir and other trace elements in the eggshells may have been caused by the assimilation of these elements into the dinosaur body through food (mechanisms discussed in Zhao[18]; Zhao et al.[10,14]; Yang et al.[17]). Figure 3 Variations in the average values of eggshell thickness of the four oospecies from the successive horizons in the CGN Section. Table 2 Frequency of pathological eggshells in Macroolithus yao- ○ Elongatoolithus elongatus; ● Elongatoolithus andrewsi; □ tunensis from successive horizons in the CGN Section Number of Number of Frequency: con- Macroolithus rugustus; ■ Macroolithus yaotunensis. Sampling eggshell pathologic fidence interval interval (m) samples eggshells (%) light microscope and the scanning electron microscope CGN 235― − − − shows that many of them have various histopathological CGN 202―235 30 21 50―85 ― ― patterns such as a bi- or multi-layered cone and disor- CGN 110 199 30 8 12 46 CGN 44―106 30 10 17―53 derly arranged crystallines, and irregular or dendritic

Figure 4 Radial section of healthy and pathologic eggshells from the CGN Section. (a) Healthy eggshell of the Macroolithus yaotunensis (CGN 908). Note a well-defined cone layer and a columnar layer, an undulating demarcation between both the layers, thin outer secondary deposit (arrow). (b) Pathologic eggshell of the Macroolithus yaotunensis, (CGN 912). Note multi-layered cone (MC) and disorderly arranged crystallines (DC) in the lower part of the columnar layer, outer secondary deposit (arrow). (c) Pathologic eggshell of the Macroolithus yaotunensis, (CGN 903). A secondary cone layer or a multi-layered cone is formed between the original cone layer and the columnar layer (arrows). (d) Pathologic eggshell of the Elongatoolithus andrewsi, (CGN 913). Note irregular or dendritic spaces in the upper part of the columnar layer (arrows).

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3 Discussion and conclusion the underlying level (CGD 109) in the CGD Section

(Figure 2(a)); these levels correspond also with levels ARTICLES 3.1 Position of the Cretaceous-Paleogene (K/T) bound- CGF 402 and CGF 401, respectively, in the CGT-CGF ary interval at the CGN Section Section (Figure 2(b)). In addition, the δ 18O record (Ta- The distribution of Ir and some other trace elements in ble 1) is characterized by three positive perturbations the three studied K/T sections (e. g. CGY-CGD, CGT- within the CGN Section interval of 208―235.5 m, and CGF and CGN sections) is shown in Figure 2. It is clear seems to have coincided with that of the CGY-CGD and [13] that the distribution pattern of the various trace elements CGT-CGF sections . Based on all the geochemical including Ir is, in general, similar in each succession. data mentioned above, the placement K/T boundary in- The CGY-CGD Section has relatively continuous se- terval of this section consequently probably lies within quence from the to early Paleocene and the 220―240 m interval. has been exposed very well. The section has been stud- The eight oospecies were found up to 215.5―235.5 ied in detail by biostratigraphy, magnetostratigraphy, m of CGN (Table 1) in 1984, and no eggshell specimens sedimentology and geochemistry, and presently serves were collected in the levels above 235.5 m. However, a [10,15] as a reference section for the K/T boundary . Based clutch with 16 eggs, belonging to Elongatoolithus oosp., [15,16] on a palynofloral study , the K/T chronostratigraphic collected by the Shanghai Museum of Natural History in boundary is placed in the upper part of the Pingling 1972, may come from about 240―250 m of CGN. Four Formation, which occurs in a stratigraphic interval of clutches containing a few dozen eggs belonging to approximately 20 m (CGD 57―78 m). This corresponds Macroolithus yaotunensis, and a large number of elon- to a time span of about 50 ka, assuming a sedimentation gatoolithid eggshells as well as a badly preserved ovi- rate of 40 cm/ka. raptorid skull with lower jaws[19], have been discovered It is very interesting that six levels of Ir enhancement within a range of about 0.6 km2 by workers at about [14] have been identified in the CGY-CGD Section (Fig- 250―280 m of CGN during the construction of build- ure 2(a)); the two highest peaks (118 ppt in CGD 111 ings in the 1980―1990s. The material has been depos- and 117.6 ppt in CGD 109) occur exactly within the ited in the local museum (the Nanxiong Museum). This palynological K/T boundary interval (CGD 111) and at case indicates that the Paleocene beds with dinosaur ― 2 5 m (CGD 109) below the boundary interval, respec- eggs and eggshell fragments were clearly not reworked. GEOLOGY tively. It is worth noting that most other trace elements, Thus, the dinosaur population represented by the elon- such as Ni, Co, Pb, Cu and Mn, all reach a maximum gatoolithids did overstep the boundary interval and sur- level (CGD 110) at the base of the palynological bound- vived into the early Paleocene, as those observed in the ary interval, which is just sandwiched between both Ir CGY-CGD and CGT-CGF sections[14]. peaks (CGD 111 and CGD 109) mentioned above (Fig- 3.2 Geochemical environment during the Creta- ure 2(a)). The distinct geochemical anomalies found in ceous-Paleogene (K/T) transition the palynological K/T boundary interval are seen as con- formable to the international K/T boundary standards. Eggshell formation is a relatively fast process (19―21 h Therefore, this section can be used as a reference for the for most )[20,21]. Generally, the eggshell chemistry interpretation and comparison of data from other K/T reflects the animal’s diet (and hence the characteristics boundary sections in the Nanxiong Basin. of their living environment) over the few days of the A comparison of the concentrations of trace elements laying period. In feeding experiments of ostrich and including Ir measured in the CGN Section (Figure 2(c)) chickens, the changes in the drinking water supply were with the other two sections (the CGY-CGD Section and fully recorded in the eggshell δ 18O after 10 days[22,23]. the CGT-CGF Section) shows that the level (CGN 913) Experiments with a flock of domestic hens show that from 223.5―225 m with the anomalous abundances of changes in the supply of a forage containing (NH4)2IrCl6 some other trace elements and the underlying level with are fully recorded in the eggshell Ir concentration after an Ir anomaly (236.8 ppt in CGN 912) at 215.5 m in the 4―6 days, and the accumulation rate of Ir from the feed CGN Section correspond with the level (CGD 110) at in the eggshell is about 0.08%[17], similar to that of REE the base of the palynological boundary interval and with (rare earth elements) in mammals[24]. It seems logical,

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therefore, that the Ir concentration in the geological en- CGT-CGF Section, and 236.8 ppt at about 6 m below the vironment during the K/T transition time in the Nan- boundary interval in the CGN Section. xiong Basin would be of the order of 10−7―10−9 g/g, In addition, the oxygen-18 records from the CGY- which is roughly consistent with the Ir value at various CGD and CGT-CGF sections are also characterized by K/T boundaries on earth. multiple positive δ18O perturbations occurring just in the Figures 2 and 5 show that, when the relative abun- interval of around 50 m at and near the boundary inter- dances of Ir and other trace elements from the three val, indicating the existence of unusually fluctuating studied sections are plotted, there are two events marked climatic changes (Figure 5). The various above-men- by these elemental abundances from the latest Creta- tioned lines of evidence further demonstrate that the ceous into the earliest Paleocene. The earlier geochemi- geochemical environmental changes that occurred lo- cal environmental event occurs at 67 Ma in magnetic cally during the K/T transition did not occur instantane- chron 31N below the K/T boundary interval, where three ously, but stretched out over a considerable time inter- distinct Ir anomalies are identified in the CGY-CGD Sec- val. [14] [14] tion , four Ir anomalies in the CGT-CGF Section , and It is noteworthy, however, that the maximum concen- two Ir anomalies in the CGN Section. trations of Ir and most other trace elements were not The second one occurs just at and near the K/T produced during the same time span, as they invariably boundary interval. The iridium concentrations in the occur at different levels at and near the boundary inter- three sections show maxima with varying strength: 118 val in each section (Figure 2). The distribution pattern of ppt in the boundary interval and 117.6 ppt at 2―5 m these elements shows that Ir and other trace elements below the boundary interval in the CGY-CGD Section, apparently had a different genesis. Possibly, the anoma- 168 ppt at 2―3 m below the boundary interval in the lous concentrations of the other trace elements contained

Figure 5 Ir and oxygen isotope anomalies, magnetochron, and stratigraphic occurrence of oospecies of dinosaur eggshells from the studied K/T sections in the Nanxiong Basin (Ir abundance data of the CGY-CGD and CGT-CGF sections from Zhao et al.[14]; δ18O from Zhao and Yan [13]. (a) Magnetic chrons[10]; (b) stratigraphic occurrence of different oospecies (solid bars).

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in the eggshells could be introduced from an unknown boundary, coevally with the major eruptive period of the [10]

source of the locality , or other volcanic centers Deccan volcanism (also see below). The results gained in ARTICLES nearby. the Nanxiong Basin, therefore, again indicate that the 3.3 Extinction and survivorship of dinosaurs across disappearance of the dinosaurs in different parts of the the K/T boundary world appears not to be synchronous but to vary in time from one part to another. The Nanxiong dinosaur eggs occur as nests, eggs and eggshell fragments. Parataxonomically, the eggs have 3.4 Cause of the dinosaur extinction been classified into 12 oospecies belonging to eight The current data indicate that the mass extinctions at the oogenera and four oofamilies (, Pris- K/T boundary are generally attributed to impact or major matoolithidae, Ovaloolithidae and ). flood basalt volcanism (e.g. ) and associated Though the available data do not permit to relate a par- environmental extremes. With the discovery of the Chic- ticular type of egg with a particular dinosaur species, xulub crater on the Yucatan Peninsula of Mexico[35―37], correlation at higher taxonomic levels is possible. The many scientists believe that the impact of a massive as- Elongatoolithidae and are related to teroid or comet immediately caused the global extinction theropods. Based on embryonic remains within eggs of the dinosaurs and many other organisms at the end of from southern Central [25,26] and western Mon- the Cretaceous. tana (North America)[27,28], the similarity of the eggshell However, no other direct evidence for an asteroid or structure, and the pattern of the egg arrangement in the comet impact at the K/T boundary has been found thus nest, the eggs of these two oofamilies can be safely re- far within the Nanxiong Basin sediments[15], except for lated to the families of the [29] and Troo- the multiple Ir anomalies. Neither shocked quartz grains dontidae[30], respectively. nor microtektites have been reported. It is possible, The combined record of oospecies from the three therefore, that it had no decisive or direct sudden influ- studied sections (right side of Figure 5) shows that the ence on the paleoenvironment and the dinosaur groups dinosaur diversity, represented by these oospecies in the in the Nanxiong Basin in southeastern China. interval corresponding to magnetic chron 31N (67 Ma) The Deccan volcanism in India is the largest volcanic where about three Ir anomalies occurred, was hardly event in the past 245 Ma. The 40Ar/39Ar ages and Re-Os

reduced, except that a number of pathological eggshells isotopic data for Deccan basalts indicate that the erup- GEOLOGY appeared. tive phase occurred around 67―64 Ma[38―45], and the The major extinction occurred at the K/T boundary major pulse is dated between 65.2 and 65.4 Ma[46]. Ac- interval. However, only seven rare oospecies became cording to Cox[47], the Deccan traps consists of 100― extinct exactly at this interval. The remaining five oo- 500 volcanic events separated by relatively short repose species belonging to elongatoolithids overstepped the periods in between. boundary interval and survived into the early Paleocene, Recently, Sant et al.[48] have found the concordant subsequently disappearing one after another over an in- distribution of cristobalite (a silica polymorph of vol- terval of about 100 m. Only one oospecies, Macroolithus canic origin) and Ir peaks during the K/T transition (65 yaotunensis, is found up to the contact between the Ma) in the intertrappean beds at Anjar, western India, Pingling Formation and the Shanghu Formation. This and suggested that the Ir anomalies there may be of vol- corresponds to a time span of 250 ka, assuming a sedi- canic source. It has been established that the hotspot [15] mentation rate of 40 cm/ka . volcano on Reunion Island that produced the Deccan In the light of presently available data, this group might traps is yet liberating iridium[49]. well have disappeared in Montana, North American at the The geochemical data and the stepwise extinction [8,9] [5] K/T boundary , about 3 m below it , or even have ex- pattern gained in the Nanxiong Basin nearly coincide [6,7] tended 1.3 m above the K/T boundary . Most recently, with the duration of the Deccan volcanism. The occur- [31] Mohabey further investigated dinosaur eggs and egg- rence of multiple volcanic events could explain the shells in west India based on an interdisciplinary research complex patterns of element and isotope distributions [32―34] by Hansen et al. , and demonstrated that the last di- found across the K/T boundary interval in the Nanxiong nosaurs in India disappeared 300 ka before the K/T Basin. However, the Ir and other trace elements in the

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eggshells at and near the K/T boundary apparently had a thus contributed to the extinction of the dinosaurs. different genesis, as mentioned above. The anomalous This geochemical study of dinosaur eggshells reveals concentrations of the other trace elements contained in a strong influence of the environment on the elemental the eggshells could be introduced from an unknown and isotope composition of eggshell and on the forma- source of the locality, or other volcanic centers nearly. tion of pathologic eggshells, and also shows the impor- Reviewing all the data collected by our group, it is tance of working within a detailed stratigraphic frame- possible that the cause of the dinosaur extinction may be work. Fortunately, rather continuous outcrops of the K/T the result of a complex multiple events brought about by boundary interval are available for study in several ba- the coincidence of global environment change marked sins of China, and work in progress should help to test by multiple Ir and δ 18O anomalies, and environmental the above scenario. poisoning characterized by other trace elements derived from the local source. Successive short- and long-term The authors thank Dr. Gerta Keller (Princeton University), Dr. Desui Miao (Kansas University), Dr. Monique Vianey-Liaud (Universite de conditions of geochemically induced environmental Montpellier), and Dr. A. J. van Loon (University of Silesiua) for helpful stress negatively affected the reproductive process and comments and suggestions on the manuscript.

1 Alvarez L W, Alvarez W, Asaro F, et al. Extraterrestrial cause for the 1998, 28: 425―430 Cretaceous-Tertiary extinction. Science, 1980, 208: 1095―1108 13 Zhao Z K, Yan Z. Stable isotopic studies of dinosaur eggshells from 2 Alvarez W, Alvarez L W, Asaro F, et al. The end of the Cretaceous the Nanxiong Basin, South China. Sci China Ser D-Earth Sci, 2000, sharp boundary or gradual transition? Science, 1984, 223: 1183― 43(1): 84―92 1186 14 Zhao Z K, Mao X Y, Chai Z F, et al. A possible causal relationship 3 Alvarez W, Kauffman E G, Surelyk F, et al. Impact theory of mass between extinction of dinosaurs and K/T iridium enrichment in the extinctions and the invertebrate fossil record. Science, 1984, 223: Nanxiong Basin, South China: Evidence from dinosaur eggshells. 1135―1141 Palaeogeogr Palaeoclimatol Palaeoecol, 2002, 178: 1―17 4 Archibald J D. Dinosaur Extinction and the End of an Era: What the 15 Erben H K, Ashraf A R, Bohm H, et al. Die Kreide/Tertiar-Grenze im Fossils Say. New York: Columbia University Press, 1996. 1―237 Nanxiong-Becken (Kontinentalfazies, Sudostchina). Mainz: Franz 5 Archibald J D, Clemens W A. Late Cretaceous extinctions. Am Sci, Steiner Verlag, Erdwiss Forsch, 1995, 32: 1―245 1982, 70: 377―385 16 Stets J, Ashraf A R, Erben H K, et al. The Cretaceous-Tertiary 6 Sloan R E, Rigby J K Jr, Van Valen L M, et al. Gradual dinosaur ex- boundary in the Nanxiong Basin (Continental facies, Southeast China). tinction and simultaneous ungulate radiation in the Hell Creek For- In: MacLeod N, Keller G, eds. The Cretaceous-Tertiary Mass Extinc- mation. Science, 1986, 232: 629―633 tion: Biotic and Environmental Effect. New York: Norton W W, 1996. 7 Rigby J K Jr, Newman K R, Smit J, et al. Dinosaurs from the Paleo- 349―371 cene part of the Hell Creek Formation, McCone County, Montana. 17 Yang G C, Mao X Y, Wang J C, et al. A study on the relationship Palaios, 1987, 2: 296―302 between iridium concentration in hen eggshell and iridium-enriched 8 Smit J, Alexander W, Van Der Kaars, et al. Stratigraphic aspects of the feed by NAA. J Radioanal Nucl Chem, 2001, 247: 567―570 Cretaceous-Tertiary boundary in the Bug Creek area of eastern Mon- 18 Zhao Z K. The dinosaur eggs in China: On the structure and evolution tana, USA. Men Soc Geol France, 1987, 150: 53―73 of eggshells. In: Carpenter K, Hirsch K F, Horner J R, eds. Dinosaur 9 Sheehan P M, Fastovsky D E, Hoffman R G, et al. Sudden extinction Eggs and Babies. Cambridge: Cambridge University Press, 1994. of the dinosaurs: Latest Cretaceous, Upper Great Plains, USA. Sci- 184―203 ence, 1991, 254: 835―839 19 Lü J C. Oviraptorid Dinosaurs From Southern China (in Chinese). 10 Zhao Z K, Ye J, Li H M, et al. Extinction of the dinosaurs across the Beijing: Geological Publishing House, 2005. 1―200 Cretaceous-Tertiary in Nanxiong Basin, Guangdong Province (in 20 Taylor T G. How an eggshell is made. In: Vertebrate Structures and Chinese). Vert PalAsia, 1991, 29: 1―20 Functions, San Francisco, Freeman, 1974. 371―377 11 Zhao Z K, Wang J K, Chen S X, et al. Amino acid composition of 21 Thibault C, Beaumont A, Levasseur M C. La reproduction des verte- dinosaur eggshells nearby the K/T boundary in Nanxiong Basin, bras. Paris: Masson, 1998. 1―307 Guangdong Province, China. Palaeogeogr Palaeoclimatol Palaeoecol, 22 Folinsbee R E, Fritz P, Krouze H R, et al. Carbon-13 and oxygen-18 in 1993, 104: 213―218 dinosaur, crocodile, and eggshells indicate environmental condi- 12 Zhao Z K, Mao X Y, Chai Z F, et al. Iridium anomalies in dinosaur tions. Science, 1970, 168: 1353―1356 eggshells at the Cretaceous-Paleogene (K/T) boundary in the Nanx- 23 Von Schirnding Y, Merwe N J, Van Der Vogel J C. Influence of diet iong Basin, South China (in Chinese). Sci China. Ser D-Earth Sci, and age on carbon isotope ratios in ostrich eggshells. Archaeometry,

814 ZHAO ZiKui et al. Chinese Science Bulletin | March 2009 | vol. 54 | no. 5 | 806-815

1982, 24: 3―20 crystals from the Cretaceous-Tertiary boundary layer, Saskatchewan: ―

24 Guo B S, Zhu W M, Xiong B K, et al. Rare earth elements in agri- Evidence from new U-Pb data. Geology, 1995, 23: 281 284 ARTICLES culture (in Chinese). Beijing: China Argicultural Science and Tech- 38 Courtillot V. Deccan volcanism at the Cretaceous-Tertiary boundary: nology Press, 1988. 1―220 Past climatic crisis as a key to future? Palaeogeogr Palaeoclimatol 25 Norell M A, Clark J M, Demberelyin D, et al. A theropod dinosaur Palaeoecol, 1990, 89: 291―299 and the affinities of the Flaming Cliffs dinosaur eggs. Science, 39 Duncan R A, Pyle D G. Rapid eruption of the Deccan flood basalts at 1994, 266: 779―782 the Cretaceous/Tertiary boundary. Nature, 1988, 333: 841―843 26 Norell M A, Clark J M, Chiappe L M, et al. A nesting dinosaur. Nature, 40 Venkatesan T R, Pande K, Gopalan K. Did Deccan volcanism pre-date 1995, 378: 774―776 the Cretaceous/Tertiary transition? Earth Planet Sci Lett, 1993, 119: 27 Horner J R, Weishampel D B. A comparative embryological study of 181―189 two ornithischian dinosaurs: Correction. Nature, 1996, 383: 103 41 Baksi A K. Geochronological studies on whole-rock basalts, Deccan 28 Varricchio D J, Horner J R, Jackson F D. and eggs for the Traps, India: Evaluation of the timing of volcanism relative to the K-T Cretaceous theropod dinosaur Troodon formosus. J Vertebr Paleontol, boundary. Earth Planet Sci Lett, 1994, 121: 43―56 2002, 22: 564―576 42 Bhattacharji S, Chatterjee N, Wampler J M, et al. Indian intraplate and 29 Zhao Z K. Nesting behavior of dinosaurs as interpreted from the continental margin rifting, lithospheric extension, and mantle up- Chinese Cretaceous dinosaur eggs. Paleont Soc Korea, Spec Publ, welling in Deccan flood basalt volcanism near the K/T boundary: 2000, 4: 115―126 Evidence from mafic dike swarms. J Geol, 1996, 104: 379―398 30 Zhao Z K. The nesting behavior of troodontid dinosaurs (in Chinese). 43 Sheth H C, Duncan R A, Chandrasekharam D, et al. Deccan Trap Vert PalAsia, 2003, 41: 157―168 dioritic gabbros from the western Satpura-Tapi region. Current Sci, 31 Mohabey D M. Understanding community structure, nesting and ex- 1997, 72: 755―757 tinction of Upper Cretaceous (Maestrichtian) Indian Dinosaurs: Evi- 44 Allegre C J, Birck J L, Capmas F, et al. Age of the Deccan Traps using dences from eggs and nests. Gond Geol Mag, 2000, 15: 1―23 187Re-187Os systematics. Earth Planet Sci Lett, 1999, 170: 197―204 32 Hansen H J, Toft P, Mohabey D M, et al. Lameta age: Dating the main 45 Mahoney J J, Sheth H C, Chandrasekharam D, et al. Geochemistry of pulse of Deccan Trap volcanism. Gond Geol Mag, 1996, 2: 365―374 flood basalts of the Toranmal section, northern Deccan traps, India: 33 Hansen H J, Mohabey D M, Toft P. New data on Indian K-T bounda- Implications for region Deccan stratigraphy. J Petrol, 2000, 41: ries. In: International Seminar on Recent Advances in the Study of 1099―1120 Cretaceous Sections. (ONGC) Chennal, India, 1998. 25―26 46 Hoffmann C, Feraud G, Courtillot V. 40Ar/39Ar dating of mineral 34 Hansen H J, Toft P, Mohabey D M. No K-T boundary at Anjar, Gujarat, separates and whole rocks from the Western Ghats lava pile: Further India. In: Seminar on Deccan Trap Basalts and K-T Boundary. PRL, constraints on duration and age of Deccan Traps. Earth Planet Sci Lett, GEOLOGY Ahmedabad, 1999. 9―10 2000, 180: 13―27 35 Hildebrand A R, Penfield G T, Kring D A, et al. Chicxulub crater: A 47 Cox K G. Gradual volcanic catastrophes? Nature, 1988, 333: 802 possible Cretaceous-Tertiary boundary impact crater on the Yucatan 48 Sant D A, Mathew G, Khadkikar A S, et al. Co-existent cristobalite Peninsula, Mexico. Geology, 1991, 19: 867―871 and iridium at 65 Ma, Anjar Intertrappeans, Kachchh, western India. 36 Hildebrand A R, Pilkington M, Connors M, et al. Size and structure of Cretac Res, 2003, 24: 105―110 the Chicxulub crater revealed by horizontal gradients and cenotes. 49 Toutain J, Meyer G. Iridium-bearing sublimates at the hot-spot vol- Nature, 1995, 376: 415―417 cano (Piton de la Fournaise, Indian Ocean). Geophys Res Lett, 1989, 37 Kamo S L, Krogh T E. Chicxulub crater source for shocked zircon 16: 1391―1394

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