The extinction of the dinosaurswp.ufpel.edu.br/cdrehmer/files/2017/08/A-extinção-dos... · 2017-08-03 · ing dominance in extinction debates is problematic for two reasons. First,

Biol. Rev. (2014), pp. 000–000. 1doi: 10.1111/brv.12128

The extinction of the dinosaurs

Stephen L. Brusatte1,∗,†, Richard J. Butler2,†, Paul M. Barrett3,Matthew T. Carrano4, David C. Evans5, Graeme T. Lloyd6, Philip D. Mannion7,Mark A. Norell8, Daniel J. Peppe9, Paul Upchurch10 and Thomas E. Williamson11

1School of GeoSciences, University of Edinburgh, Edinburgh EH9 3JW, U.K.2School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, BirminghamB15 2TT, U.K.3Department of Earth Sciences, Natural History Museum, London SW7 5BD, U.K.4Department of Paleobiology, Smithsonian Institution, Washington, DC 20013, U.S.A.5Department of Natural History, Royal Ontario Museum, Toronto, Ontario M5S 2C6, Canada6Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, U.K.7Department of Earth Science and Engineering, Imperial College London, London SW7 2AZ, U.K.8Division of Paleontology, American Museum of Natural History, New York, NY 10024, U.S.A.9Department of Geology, Baylor University, Waco, TX 76706, U.S.A.10Department of Earth Sciences, University College London, London WC1E 6BT, U.K.11New Mexico Museum of Natural History and Science, Albuquerque, NM 87104, U.S.A.

ABSTRACT

Non-avian dinosaurs went extinct 66million years ago, geologically coincident with the impact of a large bolide(comet or asteroid) during an interval of massive volcanic eruptions and changes in temperature and sea level.There has long been fervent debate about how these events affected dinosaurs. We review a wealth of new dataaccumulated over the past two decades, provide updated and novel analyses of long-term dinosaur diversitytrends during the latest Cretaceous, and discuss an emerging consensus on the extinction’s tempo and causes.Little support exists for a global, long-term decline across non-avian dinosaur diversity prior to their extinctionat the end of the Cretaceous. However, restructuring of latest Cretaceous dinosaur faunas in North America ledto reduced diversity of large-bodied herbivores, perhaps making communities more susceptible to cascadingextinctions. The abruptness of the dinosaur extinction suggests a key role for the bolide impact, although thecoarseness of the fossil record makes testing the effects of Deccan volcanism difficult.

Key words: dinosaurs, end-Cretaceous, mass extinction, Cretaceous–Paleogene, extinctions, macroevolution,Chicxulub impact, Deccan Traps, global change, palaeontology.

CONTENTS

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2II. Timing of the dinosaur extinction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2III. Major hypotheses for the dinosaur extinction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3IV. Realities of the fossil record . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4V. The latest Cretaceous world . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5VI. How were dinosaurs changing during the latest Cretaceous? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7

(1) Long-term trends . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7(2) Short-term trends . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

VII. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10(1) The tempo and causes of the dinosaur extinction: an emerging view . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

* Address for correspondence (Tel: +44 01316506039; E-mail: [email protected]).† Authors contributed equally to this work and are listed alphabetically.All other authors are listed alphabetically.

Biological Reviews (2014) 000–000 © 2014 The Authors. Biological Reviews © 2014 Cambridge Philosophical Society

2 S. L. Brusatte and others

(2) What happened after the dinosaur extinction? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11(3) Future directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

VIII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12IX. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12X. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12XI. Supporting information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15

I. INTRODUCTION

What happened to the dinosaurs? This question hasfascinated the general public, and intrigued and chal-lenged scientists, for well over a century. Dinosaurs wereremarkably successful for over 160million years (Myr),evolving colossal size and diversifying into over 1000species distributed worldwide (Weishampel, Dodson& Osmólska, 2004). Birds—one of the most speciosegroups of living terrestrial vertebrates—are directevolutionary descendants of non-avian dinosaurs, andtherefore living dinosaurs (Padian & Chiappe, 1998).But in the popular lexicon dinosaurs are symbols offailure, because the last non-avian species disappearedfrom the fossil record approximately 66million yearsago (Ma) (Fig. 1).Dinosaurs are a cautionary tale that once-dominant

groups of organisms can, and often do, die out. Theyvanished with many other species in one of the largestmass extinctions in Earth history (MacLeod et al., 1997;Alroy et al., 2008), which occurred at the end of the Cre-taceous Period amidst a backdrop of massive volcaniceruptions (Courtillot & Renne, 2003; Chenet et al.,2009), major changes in temperature and sea level (Li& Keller, 1998; Barrera & Savin, 1999; Huber, Norris &MacLeod, 2002; Wilf, Johnson & Huber, 2003; Milleret al., 2005; Grossman, 2012; Tobin et al., 2012), and theimpact of a ∼10-km-wide bolide (asteroid or comet)(Alvarez et al., 1980; Alvarez, 1997; Schulte et al., 2010).Scientists have long debated how these events affecteddinosaurs, and to what extent may have been responsi-ble for their extinction (Archibald, 1996; Archibald &Fastovsky, 2004; Fastovsky & Sheehan, 2005; Archibaldet al., 2010).Over the past 20 years, an influx of new data has greatly

refined our understanding of dinosaur evolution andextinction. Driving this dynamic period of research is anexponential increase in the rate of dinosaur discovery,with a newMesozoic dinosaur species being named onceevery∼1.5 weeks at present (Benton, 2008). Increasinglyprecise radioisotopic dates have helped place latest Cre-taceous dinosaur fossils within the temporal context ofthe impact, volcanism, and climate change, allowingcausal relationships to be better constrained (Chenetet al., 2009; Renne et al., 2013). More robust analyticalmethods, which account for biases in the fossil record,have quantified trends in dinosaur diversity throughtime, which is essential for determining whether theirextinction was geologically gradual or abrupt (Pearson

et al., 2002; Fastovsky et al., 2004; Wang & Dodson, 2006;Lloyd et al., 2008; Barrett, McGowan & Page, 2009, Cam-pione & Evans, 2011; Upchurch et al., 2011; Brusatteet al., 2012; Lloyd, 2012; Mitchell, Roopnarine & Ang-ielczyk, 2012). Together, these advances are leading toan emerging consensus on when and why non-aviandinosaurs died out.Here we review current knowledge about the extinc-

tion of non-avian dinosaurs. We discuss the evolutionof dinosaurs immediately prior to their extinction,describe how Earth systems were changing in the latestCretaceous, and assess limitations of the available fos-sil record. We use this information to address two gen-eral issues. (i) Tempo: did the extinction result fromevents that had been underway for millions of years,or was it caused by geologically brief or instantaneousevents? (ii) Causes: what are the most likely explana-tions for the extinction, and which can be ruled out?The focus here is on non-avian dinosaurs only. Althoughtheir disappearance cannot be divorced from the largerend-Cretaceous mass extinction, the specific narrativeand tempo of dinosaur extinction may differ from thoseof other groups that vanished at this time (especiallythose inhabiting other ecosystems, such as the oceans),given the many global changes of the latest Cretaceous.

II. TIMING OF THE DINOSAUR EXTINCTION

Dinosaurs appeared in the Middle–early Late Triassic(approximately 245–230Ma), gradually rose to domi-nance over the next 50Myr, and subsequently diversi-fied into an extraordinary array of species in terrestrialenvironments worldwide throughout the remainder ofthe Mesozoic (Sereno, 1999; Weishampel et al., 2004;Brusatte et al., 2010). Non-avian dinosaurs fluctuatedin diversity over the course of their ∼160-million-yearhistory, with many individual species, and some largersubgroups, experiencing extinction as part of a nor-mal ‘background’ rate (Weishampel et al., 2004; Barrettet al., 2009; Upchurch et al., 2011). Dinosaurs survived amass extinction at the end of the Triassic that had lit-tle clear impact on their diversity, as well as a poorlyunderstood, but possibly important, extinction event atthe end of the Jurassic (Weishampel et al., 2004; Barrettet al., 2009; Upchurch et al., 2011).Non-avian dinosaurs disappear from the fossil record

at the end of the Cretaceous, at the boundary with


Dinosaur extinction 3

Fig. 1. Schematic illustration of representative members of major Campanian, Maastrichtian, and earliest Paleogene(Puercan, Paleocene) North American terrestrial vertebrate faunas, with coeval palaeogeographic reconstructions (Pale-ocene reconstruction at ∼60Ma; other reconstructions more closely match the dates of the faunas depicted). Thedinosaur-dominatedHell Creek fauna witnessed the bolide impact at the end of the Cretaceous and was replaced in the ear-liest Paleogene by a mammal-dominated fauna. Maps courtesy of Dr Ron Blakey (http://cpgeosystems.com/nam.html).

the ensuing Paleogene Period (K–Pg, formerly K–T,boundary), 66.043± 0.043Ma (mean± analytical uncer-tainty) based on high-precision 40Ar/39Ar radioisotopicdates (Renne et al., 2013), within chron 29r of thegeomagnetic polarity timescale (Gradstein et al., 2012)(Fig. 1). This disappearance is so dramatic that, priorto the advent of radioisotopic dating, the absence ofdinosaur fossils was often considered sufficient to assignstrata above dinosaur-bearing rocks a Cenozoic age.Supposed Paleocene non-avian dinosaur fossils fromNorth America (e.g. Sloan et al., 1986; Fassett, 2009; Fas-sett, Heaman & Simonetti, 2011) are either reworkedCretaceous specimens or incorrectly dated (e.g. Lof-gren, Hotton & Runkel, 1990; Lucas et al., 2009; Koeniget al., 2012; Renne & Goodwin, 2012). Although it isconceivable that some local populations of non-aviandinosaurs survived into the earliest Paleocene, theK–Pg boundary clearly marks the dramatic end of thedinosaur-dominated world.

III. MAJOR HYPOTHESES FOR THE DINOSAUREXTINCTION

Few issues in palaeontology have generated as muchspeculation as the dinosaur extinction. The numberand variety of hypotheses is astounding (Benton, 1990),but most scientific debate over the past century hasboiled down to whether the extinction was geologicallyabrupt or gradual, whether it was caused by somethingintrinsic to dinosaurs or an extrinsic physical driver,and, if the latter, whether this driver was terrestrial orextraterrestrial in origin (Archibald, 1996; Archibald &Fastovsky, 2004; Fastovsky & Sheehan, 2005). Linkedto these controversies is the question of whether theextinction had a single overriding cause or was theresult of a disastrous temporal coincidence of multiplebiological and/or physical factors.The most celebrated theory, and the most recogniz-

able, is that dinosaurs and other organisms went extinct



suddenly after a giant bolide impact set off a globalcataclysm of environmental upheaval (Alvarez et al.,1980; Alvarez, 1997). The impact hypothesis has gainedwide traction thanks to extensive study (Sheehan et al.,1991; Fastovsky & Sheehan, 2005) and is an elegantsingle explanation for why so many groups disappearedsimultaneously. Nonetheless, some scientists remainunconvinced that it was the sole cause of the dinosaurextinction specifically, and the end-Cretaceous massextinction more broadly (Archibald, 1996; Archibald &Fastovsky, 2004; Archibald et al., 2010; Keller, 2012).Although evidence for an end-Cretaceous impact

is unequivocal (Schulte et al., 2010), doubts remainbecause other severe changes occurred in Earth sys-tems at or near the end of the Cretaceous: intensive vol-canism (Courtillot & Renne, 2003; Chenet et al., 2009),temperature oscillations (Li & Keller, 1998; Barrera &Savin, 1999; Huber et al., 2002; Wilf et al., 2003; Gross-man, 2012; Tobin et al., 2012), and sea-level fluctua-tions (Miller et al., 2005). It has been argued that eachof these factors may be the primary cause of dinosaurextinction, that their sum resulted in the extinction, orthat a bolide impact finished off the dinosaurs after amulti-million-year period of stress triggered by one ormore of these changes (Archibald, 1996, 2011).Each of these hypotheses makes predictions that can

be tested with the fossil record. The impact hypothe-sis predicts a sudden extinction, whereas hypothesescentred on climate and sea-level changes, includingthose invoking the bolide as a coup de grâce, implythat dinosaurs experienced a prolonged decline.Recent increases in the volume of data bearing on theextinction, combined with ongoing methodologicaladvances, have allowed scientists to expand the scopeand complexity of testable scenarios, and assemble anincreasingly nuanced narrative of how dinosaur faunaschanged in concert with their environments in thelatest Cretaceous.

IV. REALITIES OF THE FOSSIL RECORD

Understanding how dinosaurs evolved prior to theK–Pg boundary and how they may have responded toglobal catastrophes is constrained by the available, andimperfect, fossil record. Only a fraction of all dinosaursthat ever lived are preserved, fossil record quality variesthrough time and space, different regions and time peri-ods have been unevenly sampled, and precise radioiso-topic dates for specimens or faunas are often unavail-able. A pragmatic evaluation of these limitations helpsconstrain what we do know, and identify what we do notor cannot know, about the extinction.The greatest challenge in studying the dinosaur

extinction is a set of biases that affects their lat-est Cretaceous record (Campanian–Maastrichtianstages, approximately 83.6 to 66Ma). Although

Campanian–Maastrichtian dinosaurs are known fromacross the globe, only North America boasts a detailedrecord of correlative, stratigraphically stacked faunas,in many cases accurately dated (Weishampel et al.,2004; Roberts, Deino & Chan, 2005; Eberth et al., 2013)(Fig. 1). Only these faunas, therefore, present a clearpicture of how dinosaurs changed in a single regionover the ∼15Myr before the K–Pg boundary. How-ever, even here some periods of time are much betterrepresented and sampled than others (e.g. late Campa-nian and late Maastrichtian versus early Maastrichtian).Campanian–Maastrichtian units in Asia, Europe, India,Madagascar, and South America also provide data rele-vant to a global-scale understanding of latest Cretaceousdinosaur diversity (Weishampel et al., 2004), and theypromise also to contribute important regional-scaleinformation as they become better sampled and dated.Currently, only theHell Creek Formation (and tempo-

ral equivalents) of the North AmericanWestern Interiorprovides a well-sampled, relatively continuous record ofdinosaur fossils during the final million years of the Cre-taceous, up to a precisely located K–Pg boundary (Shee-han et al., 1991; Pearson et al., 2002; Fastovsky & Shee-han, 2005). This one formation, therefore, providesthe only well-constrained evidence for how dinosaurschanged immediately before the bolide impact, andthe fine-scale relationships between dinosaur diver-sity, climate and sea-level changes, and Deccan vol-canism during the waning days of the Cretaceous.Because the Hell Creek is continuous with overlyingPaleocene sediments, it also provides clear evidence thatdinosaurs did not survive locally past the end of theCretaceous. Recently identified stratigraphic sections inSpain (Riera et al., 2009; Vila et al., 2013) and China(Jiang et al., 2011) with dinosaur fossils in close prox-imity to the K–Pg boundary hold great potential forfuture work.Although intense study of the North American

record has provided critical insights, its overwhelm-ing dominance in extinction debates is problematicfor two reasons. First, its local patterns of dinosaurdiversity, evolution, and extinction may not accuratelydocument the generalized global extinction event(Godefroit et al., 2009). For example, the almost com-plete absence of long-necked sauropod dinosaurs inthe Campanian–Maastrichtian of North America, com-pared with their high diversity elsewhere, is strongevidence that these faunas are not representativeof a global reality (Mannion et al., 2011). Second,although the North American record of Campanian–Maastrichtian dinosaurs is the most extensive, it is stillimperfect. As elsewhere, there is a substantial preserva-tional bias against dinosaurs of human-size or smaller(Horner, Goodwin & Myhrvold, 2011; Brown et al.,2013; Evans et al., 2013), and intense debate surroundswhether some species are really juveniles or sexualmorphs of other taxa (e.g. Scannella & Horner, 2010).



These issues complicate accurate estimates of latestCretaceous species diversity.One final caveat about the fossil record concerns

scale. A growing global database of Campanian–Maastrichtian dinosaurs is enabling more completeestimates of broad-scale trends in dinosaur diversityover the final ∼10–15Myr of the Cretaceous. At itsfinest resolution, however, even the Hell Creek recordis not well-enough sampled or dated to examine trendson a 1000–10000-year timescale (Pearson et al., 2002).We do not, and probably cannot, know how individualdinosaurs or populations responded to environmen-tal change. This makes it exceedingly difficult to testspecific possible kill mechanisms—e.g. acid rain orwildfires caused by an impact, extreme temperaturechanges caused by an impact or volcanism, or fluctuat-ing home ranges caused by sea-level change. For thisreason, our focus here is on using the dinosaur recordto address broad-scale questions about the tempo andoverarching causes of the extinction.

V. THE LATEST CRETACEOUS WORLD

The end-Cretaceous extinction is closely associated witha clay layer containing anomalously high abundancesof iridium and other platinum-group elements (Alvarezet al., 1980; Smit & Hertogen, 1980) with impactejecta, such as spherules and shocked minerals (Smit,1999), derived from a ∼10 km wide bolide that hit theYucatan Peninsula of modern-day Mexico, creating the∼180–200-km-wide Chicxulub crater (Hildebrand et al.,1991).The effects of the impact were broad and devas-

tating. It triggered tsunamis that may have reached>300 km inland around the Gulf of Mexico (Matsuiet al., 2002), potentially caused >11 magnitude earth-quakes (Ivanov, 2005), and created a global heat pulse(Goldin & Melosh, 2009) that perhaps ignited largewildfires near the impact site (Wolbach, Lewis & Anders,1985; Kring, 2007). The impact occurred in a carbon-ate and sulphate-rich region, thereby releasing massivequantities of sulphur and other aerosols into the atmo-sphere, which would have caused sulphuric acid rain(Pope et al., 1997) and at least temporarily destroyed theozone layer (Kring, 2007). These aerosols would havealso briefly cooled the Earth by several to tens of degreesCelsius following the initial heat pulse (Pope et al.,1997). Dust thrown up by the impact would have formeda thick cloud that darkened the Earth and depressedphotosynthesis (Alvarez et al., 1980; Pope et al., 1997).Over a slightly longer term, the injection of carbon diox-ide, methane, and water vapour into the atmospheremay have caused greenhouse warming of a few degrees(Beerling et al., 2002).The end-Cretaceous impact did not occur in a vac-

uum, however, and changes to Earth’s climate and

landscape were already underway. Among the mostprominent was a tremendous episode of volcanic activ-ity that formed the Deccan flood basalts of India. Theseeruptions proceeded in three main phases during theLate Cretaceous–early Paleocene: the first during C30n,the second in C29r, and the third during C29n (Cour-tillot & Renne, 2003; Chenet et al., 2009; Jay et al., 2009).The second phase, which probably began∼400000 yearsbefore the K–Pg boundary (Robinson et al., 2009), wasthe largest and formed up to 80% of the volume ofthe Deccan Traps (Chenet et al., 2009). This phasewas similar in size to other large-scale flood basalt vol-canism in the geological record, such as the CentralAtlantic Magmatic Province (CAMP), which has beenimplicated in the end-Triassic extinction (Courtillot &Renne, 2003). All phases of the Deccan Traps werelikely emplaced rapidly and are composed of a series ofsmaller, single eruptions that occurred on the order ofevery ∼2000 years (Jay et al., 2009).Determining the precise age of the Deccan Traps has

proven difficult because of the low potassium content ofthe basalts and chemical alteration due to weathering,rendering whole-rock ages unreliable (Hofmann, Fer-aud & Courtillot, 2000). Consequently, dates for Deccaneruptions have large error margins, and there are dis-crepancies between dates for the same flows, making itimpossible to determine their ages more precisely thanwithin polarity chrons (Courtillot & Renne, 2003). Fur-thermore, the position of the K–Pg boundary within theeruptive sequence is uncertain. An iridium anomaly hasbeen found in sediment between flows (Bhandari et al.,1995), but may be volcanic in origin and discordant withthe impact-clay layer (Hansen, Mohabey & Toft, 2001;Sant et al., 2003).Regardless of their precise timing, the Deccan erup-

tions would have caused major environmental pertur-bations in the Late Cretaceous–early Paleocene. Eacheruption would have injected substantial amounts of sul-phur dioxide into the atmosphere, causing sulphuricacid rain (Wignall, 2001; Self et al., 2006) and short-termcooling, depending on their frequency and whetherthe sulphur dioxide reached the stratosphere (Wignall,2001). Large amounts of carbon dioxide added to theatmosphere may have caused warming (Li & Keller,1998; Wilf et al., 2003), although the pace of this maynot have been fast enough to create significant, rapidclimate change (Self et al., 2006). Unfortunately, it isstill unclear whether these eruptions caused significantbiotic changes even locally.Sea levels also changed dramatically during the latest

Cretaceous, although changes of similar magnitudeoccurred at other points in dinosaur evolutionaryhistory (Figs 2 and 3). Peak Late Cretaceous lev-els of 50–70m above present sea levels at ∼80Mawere followed by a long-term fall through most ofthe Campanian–Maastrichtian (Miller et al., 2005).Globally, the Campanian is dominated by highstands



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Fig. 2. Long-term trends in global temperature (Grossman, 2012), sea level (Miller et al., 2005), dinosaur diversity(Upchurch et al., 2011), and dinosaur fossil sampling (Upchurch et al., 2011) over the entire Cretaceous (145 to 66Ma).Isotopic temperatures based on 𝛿

18O data (Grossman, 2012). DBC refers to ‘dinosaur bearing collections’ (a measure ofsampling intensity: Upchurch et al., 2011), and gaps represent missing data. Dinosaur diversity is shown both globally andlocally for North America (NA), and the residual diversity curves are corrected estimates based on sampling intensity(Upchurch et al., 2011). Note that there are no long-term dinosaur diversity declines based on the observed or thesampling-corrected data.

with a few relatively short lowstands in the earlyand middle Campanian (Miller et al., 2005). TheCampanian–Maastrichtian boundary is marked by asubstantial global regression and subsequent low standthat persisted for up to a few million years (Milleret al., 2005). This was followed by a high stand duringthe middle Maastrichtian, a low stand during the lateMaastrichtian, and a rise to a global high stand thatpeaked at the end of the Maastrichtian and then fellacross the K–Pg boundary (Miller et al., 2005).In general, global sea levels were more varied, and

fluctuated more intensely on shorter time scales, duringthe Maastrichtian than the Campanian (Miller et al.,2005). This also applied to the Western Interior Seaway(WIS), the shallow epicontinental sea that coveredmuch of North America during this time. The WIS wasexpansive during much of the Campanian and Maas-trichtian, at times connecting the Arctic Ocean andGulf of Mexico (Lillegraven & Ostresh, 1990). During

the late Maastrichtian the WIS drastically constricted,probably due to the global sea-level low stand combinedwith local tectonism (Weimer, 1984; Lillegraven &Ostresh, 1990).Temperature changes also characterize the latest Cre-

taceous (Figs 2–4). Carbon dioxide levels declinedthrough the Late Cretaceous (Royer, 2006, 2014; Hong& Lee, 2012), coincident with a long-term cooling trend(Barrera & Savin, 1999; Huber et al., 2002). Campa-nian andMaastrichtian climates were generally equable,with relatively low latitudinal temperature gradients andpolar regions kept above freezing (Wolfe & Upchurch,1987). Globally, the Campanian was warmer, but theMaastrichtian climate was more variable (Huber et al.,2002). During the middle Maastrichtian there may havebeen a short-lived warming event related to an increasein atmospheric carbon dioxide from the first Deccaneruption phase (Nordt, Atchley & Dworkin, 2003; Tobinet al., 2012). Thismid-Maastrichtian warming is followed



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Fig. 3. Short-term trends in global temperature (Grossman, 2012), sea level (Miller et al., 2005), subsampled dinosaurdiversity (see text for details), and dinosaur morphological disparity (Brusatte et al., 2012) over the latest Cretaceous(Campanian–Maastrichtian, 83.6–66Ma). Subsampled dinosaur diversity is an estimate based on Shareholder QuorumSubsampling that takes into account differences in sampling intensity over time (see text). Diversity is shown both globallyand locally for North America (NA). Note that there are no progressive decreases in global dinosaur diversity, all NorthAmerican dinosaur diversity, or North American theropod dinosaur diversity and disparity, but a progressive decline inNorth American ornithischian diversity and significant declines in and ceratopsid and hadrosauroid disparity.

by another warming event in the oceans and on landduring the last few hundred thousand years of the Cre-taceous, likely linked to carbon dioxide outgassing fromthe second Deccan eruption phase (Li & Keller, 1998;Barrera & Savin, 1999; Nordt et al., 2003; Wilf et al.,2003; Tobin et al., 2012). Subsequently, global climatecooled during the latest Maastrichtian and across theK–Pg boundary (Li & Keller, 1998; Wilf et al., 2003) per-haps due to enhanced silicate weathering of the Deccanbasalts (Dessert et al., 2001).

VI. HOW WERE DINOSAURS CHANGING DURINGTHE LATEST CRETACEOUS?

The Campanian–Maastrichtian was an interval of majorglobal changes, and a better understanding of howdinosaurs were evolving during this time can illuminatehow they were affected by Earth system changes, andtherefore the tempo and causes of their extinction. Thisrequires examination of trends in dinosaur biodiversityover time. Two very different types of trends give insightinto dinosaur extinction: long-term patterns over thefinal ∼10–15Myr of the Cretaceous (Figs 2 and 3) andshort-term patterns during the ∼1Myr before the K–Pgboundary (Fig. 4).

(1) Long-term trends

Historically, the standard view of dinosaur evolutionprior to the extinction based on the North Americanrecord was of a decline in total species numbers (rich-ness) through the Campanian–Maastrichtian (Marsh,1882; Colbert, 1961; Archibald & Clemens, 1982;Archibald, 1996; Dodson, 1996; Sullivan, 2006). Thiswas based primarily upon the higher species richness ofseveral Campanian formations from southern Canada,

including what is now recognized as the DinosaurPark Formation (42 valid species), than that of thelate Maastrichtian Hell Creek Formation (25–33 validspecies). Simple comparisons of species richness donot, however, take into account possible variations insampling intensity or preservation potential of rocksof different geological ages (Russell, 1984; Fastovskyet al., 2004), the fact that not all Campanian taxa weredirectly contemporaneous, or that the faunas beingcompared might represent different environments(Fastovsky et al., 2005).Various approaches have been taken to address this

suite of possible biases, including subsampling (Rus-sell, 1984; Fastovsky et al., 2004; Lloyd et al., 2008),models based on estimates of variation in rock volumeor collecting effort through time (Barrett et al., 2009;Upchurch et al., 2011; Lloyd, 2012), and statistical esti-mates of the true number of species represented by abiased record (Wang & Dodson, 2006). These methodshave been applied at differing geographic (e.g. conti-nental versus global) and taxonomic (e.g. all dinosaursversus separate comparisons of major dinosaur clades)scales. None of these studies has supported a globaldecline in diversity occurring across all dinosaurgroups (Fig. 2). However, some evidence has supportedCampanian–Maastrichtian declines in the richness ofornithischians (Barrett et al., 2009; Upchurch et al.,2011) and theropods (Barrett et al., 2009; but notUpchurch et al., 2011), but not sauropodomorphs.Here, we present new results (Fig. 3; see online

File S1, Fig. S1) based on sampling-standardized anal-yses of current data within the Paleobiology Database.This dataset is an up-to-date record of global dinosaurdiversity and incorporates hundreds of new latest Cre-taceous fossils discovered over the past decade thatare relevant to understanding the K–Pg extinction. Inorder to produce the subsampled dinosaur richness



66.5

67.5

66.0

67.0

Deccan P

hase 2

C2

9r

C3

0nCR

ET

AC

EO

US

Pale

ogene

Age(Ma)

Period ChronDinosaur species

occurences

MAT(oC)

Global sea level (mapl)

12

34

56

78

910

1112

1314

Deccan

volcanism

50

25 08 12 16

Fig. 4. Dinosaur species occurrences in the Hell Creek Formation in the Williston Basin, North Dakota, USA, duringthe latest Cretaceous (latest Maastrichtian), along with curves of local mean annual temperature (MAT) derived fromfossil leaves (Wilf et al., 2003), global sea level (mapl, metres above present level) (Miller et al., 2005), and an indicationof the timing of the voluminous second Deccan volcanic pulse (Chenet et al., 2009; Robinson et al., 2009). The MATcurve is based on range-through fossil leaf data and the minimum uncertainty for estimates is ±2∘C. The thicker linein the sea-level curve indicates a global transgressive phase (Miller et al., 2005). Dinosaur occurrence data from Pearsonet al. (2002) are plotted by occurrences of each taxon collected through the Hell Creek Formation. Plotted taxa: (1)Ceratopsidae indet.; (2) Richardoestesia isosceles; (3) Hadrosaurinae indet.; (4) Caenagnathidae indet.; (5) Coelurosauriaindet.; (6) Ornithomimidae indet.; (7) Tyrannosaurus rex; (8) Paronychodon lacustris; (9) Saurornitholestes; (10) Thescelosaurusneglectus; (11) Torosaurus latus; (12) Triceratops horridus; (13) cf. Avisaurus archibaldi (some of this material may be avian);(14) Troodon sp. Age estimates for dinosaur occurrences are based on a sedimentation rate model for the Hell CreekFormation fromHicks et al. (2002) and Peppe, Evans & Smirnov (2009). Note that there is high dinosaur diversity throughthe Deccan phase, up to the K–Pg boundary.



in Fig. 3 and File S1, Fig. S1 we extracted all globaldinosaurian body fossil occurrences from the Paleobi-ology Database (Carrano, 2008, and updates thereafter)(downloaded 12/07/2013) that could be definitivelyassigned to latest Cretaceous substage time bins (lateCampanian, early Maastrichtian, late Maastrichtian)and valid genera (920 occurrences). This dataset wasthen reduced to just occurrences from North Americaand then divided into two further subsets, Ornithischiaand Theropoda. Sauropodomorpha was not examinedseparately because only one genus (Alamosaurus) isknown from the latest Cretaceous of North America.The dataset is included as online Supporting Informa-tion (see online File S1).We note that this binning scheme groups together

non-contemporaneous taxa; this is necessary due to thecoarseness of the fossil record and the need for reason-able sample sizes in each bin to enable the subsamplinganalyses. As the North American record in particularbecomes better sampled over time, it should be possibleto conduct diversity analyses with shorter time bins thattake into account detailed intra-formational samplingsuch as that recently presented for the Dinosaur ParkFormation and Edmonton Group of Canada by Mallonet al. (2012) and Eberth et al. (2013).We implemented two forms of subsampling to recon-

struct past diversity. Sample-based rarefaction (using thenumber of localities at which each genus is found ineach substage) was performed using PAST (Hammer,Harper & Ryan, 2001), and Shareholder Quorum Sub-sampling (SQS: Alroy, 2010a–c) was run in R, usingthe R implementation posted on J. Alroy’s website(version 2.0; posted online 14 February 2011). Weused an arbitrary ‘quorum’ (i.e. sampling) level (q)of 0.5 that will return results for all comparisons,although similar relative numbers can be obtainedwith other q values. The data and code used areincluded as online Supporting Information (see onlineFile S2).The primary difference between SQS and rarefac-

tion is that the former samples fairly whereas the lat-ter samples equally. SQS achieves this by sampling a setarea (q) underneath a species frequency curve. Thisapproach offers a number of key advantages over rar-efaction (Alroy, 2010a–c). Of particular note is themuch more consistent relative subsampled richnessvalues recovered between bins as q varies. Rarefac-tion curves, on the other hand, often cross, meaningthat sampling level can determine which bin(s) arerelatively more diverse. However, we implement bothmethods so that the results can be directly comparedwith earlier attempts that used only rarefaction. SQSresults are shown in Fig. 3 and rarefaction results inFile S1, Fig. S1.The new subsampling analyses provide no evidence

for a progressive Campanian–Maastrichtian decline intotal dinosaur species richness at either the global or

North American scales (Fig. 3). However, finer-grainedanalyses support a decline in the species richness ofNorth American ornithischians, but not theropods. Thisornithischian decline occurs from the late Campanianto the early Maastrichtian, and ornithischian diversityremains low during the late Maastrichtian.These results are congruent with recent studies that

examined trends in morphological disparity, a measurethat quantifies the diversity of anatomical form in agroup of organisms (Wills, Briggs & Fortey, 1994).Because anatomy is often closely tied to function andecology, disparity is an important addition to speciesrichness for documenting the spectrum of body plans,behaviours, and niches exploited by a group. Studies ofdinosaur disparity during the latest Cretaceous suggestthat Campanian–Maastrichtian declines are evidentin large-bodied, bulk-feeding ornithischian herbivores(ceratopsians, hadrosaurs) within North America, butnot in other groups or regions (Campione & Evans,2011; Brusatte et al., 2012) (Fig. 3).Current evidence for a long-term diversity decline

prior to the non-avian dinosaur extinction is thereforelimited to ornithischian dinosaurs, with the signalalmost certainly being driven by declines among twolarge-bodied subclades (Ceratopsidae, Hadrosauri-dae) within North America. For other groups ofdinosaurs, and at a global scale, there is little evidencefor a long-term diminution in diversity. All majorgroups of Campanian dinosaurs survived into the lateMaastrichtian, so there was no gradual loss of majorcomponents of dinosaur diversity through the latest Cre-taceous. Moreover, it is worth stressing that even if somegroups declined in diversity through this time interval,similar (and often more extreme) waxing and waningin the diversity of particular clades occurred repeat-edly across dinosaur evolutionary history (Fastovskyet al., 2004, 2005; Barrett et al., 2009; Upchurchet al., 2011), and does not indicate that dinosaurs,or particular groups of them, were doomed toextinction.When interpreting diversity trends, it is important

to remember that they summarize patterns. It is moredifficult to evaluate what consequences these pat-terns, such as an ornithischian diversity decline, wouldhave had on the processes of dinosaur evolution. Aprovocative recent study has attempted to bridge thepattern–process divide (Mitchell et al., 2012). Thisstudy showed that the ornithischian decline resultedin a Campanian–Maastrichtian decrease of dinosaurbeta diversity (i.e. decreases in provincialism) withinNorth America (see also Vavrek & Larsson, 2010).When hypothetical food webs of Campanian and Maas-trichtian communities were subjected to simulatedprimary productivity disruptions (like those causedby a bolide impact), the Maastrichtian communitiessuffered greater extinctions. These results imply thatthe decreased diversity of large-bodied Maastrichtian



herbivores made their communities more vulnerable tocascading extinctions.

(2) Short-term trends

Detailed intra-formational (sub-million-year timescale)assessments of dinosaur biodiversity immediately pre-ceding the K–Pg boundary are limited to the WesternInterior of the United States, and most focus ondocumenting changes within the Hell Creek For-mation (Sheehan et al., 1991, 2000; Pearson et al.,2001, 2002) (Fig. 4). The first systematic study ofHell Creek dinosaur diversity used a 3-year field sur-vey of in situ dinosaur macrofossils (Sheehan et al.,1991), and was later expanded to include microfos-sils and non-dinosaurian vertebrates (Pearson et al.,2001, 2002), to address some criticisms of the originalmethods (Williams, 1994; Hurlbert & Archibald, 1995;Archibald, 1996). These studies found little supportfor a decline in dinosaur species richness or ecologicaldiversity through the Hell Creek Formation, particu-larly when variations in sample size were accountedfor (Fig. 4). A more recent, decade-long census ofdinosaur macrofossils also found no change in thediversity of large dinosaur taxa (primarily genera)from the lower to the upper Hell Creek (Horner et al.,2011).The rarity of dinosaur fossils in the uppermost 3m

of the Hell Creek Formation has historically beentaken as evidence that dinosaurs declined in abun-dance, or even went extinct, before the bolide impact(Clemens, Archibald & Hickey, 1981; Williams, 1994;Archibald, 1996). Some workers, however, suggestedthat this ‘three metre gap’ was an artefact causedby sampling (Sheehan et al., 2000) or preservationalfactors, including acidic leaching associated with theimpact (Retallack, Leahy & Spoon, 1987). Although therecent discovery of a ceratopsian fossil in a mudstoneunit within the ‘gap’, about 15 cm below the K–Pgboundary, provides strong evidence that dinosaursprobably witnessed the impact at the end of theCretaceous (Lyson et al., 2011), this does not shedlight on changes in community composition, relativeabundances, or other aspects of dinosaur biodiver-sity over this presumably short terminal Cretaceousinterval.South of the Hell Creek area, dinosaurs maintained

diversity and abundance, without any sign of decline,throughout the latest Cretaceous in the Ferris Forma-tion of Wyoming (Lillegraven & Eberle, 1999). Furtherafield, in the Tremp Basin of Spain, dinosaurs remainedcommon and diverse throughout the Maastrichtian,with no noticeable decline or local extinctions beforethe K–Pg boundary (Riera et al., 2009; Vila et al., 2013).However, precise dating of these deposits is problematicand diversity trends have not been analysed with thesame statistical rigour and stratigraphic precision as theHell Creek studies (Pearson et al., 2002). Future work

will undoubtedly focus not only on the Spanish sections,but on other units straddling the K–Pg boundary inNorth America that are becoming better sampled, suchas the Edmonton Group of Alberta, Canada (Eberthet al., 2013).

VII. DISCUSSION

(1) The tempo and causes of the dinosaur extinction:an emerging view

The wealth of data accumulated over the past twodecades is leading to an emerging picture of howthe Earth changed during the latest Cretaceous andhow these changes affected dinosaurs. The tempo ofthe non-avian dinosaur extinction appears to havebeen sudden, at least in geological terms. Our currentknowledge of the dinosaur fossil record provides noindication of obvious long-term declines in global biodi-versity over the final 15Myr of the Cretaceous (althoughsome North American herbivores did diminish in diver-sity), no major dinosaur groups went extinct during thistime, and a diverse assemblage of abundant dinosaurspecies persisted until the very end of the Cretaceous inlocal faunas in North America and Europe. Whateverkilled the dinosaurs seems to have been focused at thevery end of the Maastrichtian, within a few hundredthousand years of the K–Pg boundary.The causes of the dinosaur extinction are more neb-

ulous, although new data help to better constrainand test possible scenarios. Long-term environmentalchanges through the Campanian and Maastrichtian,such as sea-level fluctuations, likely affected the ecologi-cal structure of dinosaur communities, at least in NorthAmerica. Loss of beta diversity, combined with reduc-tion in species richness and morphological diversityof large-bodied herbivores, perhaps due to the regres-sion of the WIS in the Maastrichtian and a resultantchange in habitat distribution (Archibald, 1996; Gates,Prieto-Márquez & Zanno, 2012), may have made Maas-trichtian dinosaur communities more susceptible to cas-cading extinctions (Mitchell et al., 2012) caused by acatastrophic extrinsic forcing factor, such as an impactor large-scale volcanism. These long-term environmen-tal changes may have restructured dinosaur communi-ties at the regional level in North America, but currentevidence does not support a major influence on globalbiodiversity through the latest Cretaceous, suggestingthey are not the driving force behind the dinosaurextinction.Instead, current evidence indicates that the dinosaur

extinction was abrupt, which evokes the bolide impactas the potential major driver. What is less clear atthis stage is how Deccan volcanism affected dinosaursduring the immediate run-up to the impact. Existingdata on dinosaur diversity, richness, and community



structure in the last few hundred thousand years ofthe Cretaceous—when the voluminous second Deccanpulse occurred—are not robust enough to tease apartthe differential effects of Deccan-induced environmen-tal change versus the direct effects of the impact ondinosaurs. It is clear that the major dinosaur species per-sisted in theHell Creek (and probably Spain) during thesecond Deccan phase, up until the K–Pg boundary andthe impact, suggesting that at least in North AmericaDeccan volcanism did not cause any substantial changein dinosaur species richness. However, volcanic-inducedenvironmental changes may have affected dinosaurcommunities in other ways during this time, such aschanges in population structure or community ecology,or at regional scales that are currently undetectable inthe fossil record.Given the weight of current evidence, we hold here

that the bolide impact was probably the fundamentalcause of the dinosaur extinction, though it does notautomatically follow that this event was also primarilyresponsible for the extinction of other taxa at theK–Pg boundary. Longer term phenomena such assea-level-mediated faunal restructuring and shorterterm Deccan-induced climate changes may have madelatest Maastrichtian communities less resilient tothe impact, as ‘press’ events before the sudden andcatastrophic ‘pulse’ of the impact (Arens & West,2008). But we hypothesize that without the impact,non-avian dinosaurs probably would not have com-pletely died out. This hypothesis, however, must betested as more data come to light, especially concern-ing the effects of Deccan volcanism on dinosaurianecosystems.

(2) What happened after the dinosaur extinction?

The dinosaur extinction was part of a mass extinc-tion that devastated terrestrial and marine ecosystems(MacLeod et al., 1997). On land, many organisms liv-ing alongside dinosaurs also went extinct, includingnon-neornithine birds (Longrich, Tokaryk & Field,2011), many lizards and snakes (Longrich, Bhullar &Gauthier, 2012), pterosaurs, and numerous crocodyli-forms (MacLeod et al., 1997). Conversely, aquaticfreshwater tetrapods such as amphibians, turtles, andchoristodires experienced lower losses across the K–Pgboundary (Archibald & Bryant, 1990; MacLeod et al.,1997). There is general agreement that organisms infreshwater ecosystems were less affected by the extinc-tion than those in terrestrial (non-aquatic) or marineenvironments (Archibald & Fastovsky, 2004), possiblybecause freshwater food chains were more relianton detritus feeding than photosynthesis (Sheehan &Hansen, 1986).With the extinction of dinosaurs, which had been

incumbent in many terrestrial niches for over 160Myr,mammals had the opportunity to diversify and radiate

(Archibald, 2011; Slater, 2013). Mammals evolved rea-sonable ecological diversity during the Jurassic and Cre-taceous (Luo, 2007), but compared to extant specieswere generally small. All mammal groups were severelyaffected by the end-Cretaceous extinction, particularlymetatherians (marsupials and their fossil relatives)(Williamson et al., 2012; Wilson, 2013), larger-bodiedspecies, and those with specialized diets (Wilson, 2013).Nonetheless, at least some representatives of manymajor groups, including metatherians and eutherians(placentals and fossil relatives), were able to endure.These survivors proliferated rapidly after the dinosaurextinction, forming diverse mammalian faunas in NorthAmerica no later than 400000 years into the Paleocene(Renne et al., 2013; Wilson, 2013), which set the stagefor the ensuing 66Myr of mammalian dominance in ter-restrial ecosystems.

(3) Future directions

We identify the following as critical research objec-tives for the next decade: (i) better sampling ofCampanian–Maastrichtian dinosaurs from outsideNorth America, especially those within chron 29r.(ii) Detailed intra-formational sampling, like thatachieved for the Hell Creek, of dinosaur-bearing K–Pgsections elsewhere in North America (EdmontonGroup, San Juan Basin, Big Bend), Europe (south-ern France, Spain, Romania), Asia (Nanxiong Basin,Amur Region), India, and South America (Patago-nia). (iii) Late Cretaceous dinosaur diversity analyseswith shorter time bins based on a finer-scale levelof intra-formational sampling, like those conductedby Mallon et al. (2012) and Eberth et al. (2013). (iv)Improved radioisotopic dating of the Deccan eruptionsand increasingly constrained dates for North Ameri-can sections (Renne et al., 2013), to enable fine-scalecorrelations between diversity changes and volcanism.(v) Additional metre-scale studies of whole-communityecological dynamics within the Hell Creek Formation,such as have been carried out for contemporary mam-mals (Wilson, 2005). (vi) More long-term studies ofhow dinosaur ecology, not only diversity, changed overthe Campanian–Maastrichtian, and other periods ofcomparable length in dinosaur evolution. (vii) Workfocused on aspects of dinosaur biology that may explainwhy they went extinct, and particularly why certain birdssurvived whereas many bird-like feathered dinosaursdied off. (viii) More robust theoretical models of howglobal, geological-scale changes might have impactedpopulations and local environments, and be detectedwithin a single formation. (ix) Comparisons betweendinosaur alpha- and beta-diversity patterns and those ofother latest Cretaceous plants and animals, to identifycomplementary or contradictory patterns that mighthelp to identify the specific kill mechanisms for theend-Cretaceous extinction.



VIII. CONCLUSIONS

(1) Over the past two decades, a wealth of new data andadvances in analytical techniques have given new insightsinto one of the great riddles of palaeontology: why thedinosaurs went extinct. These advances are leading toan emerging consensus on when and why the non-aviandinosaurs died out at the end of the Cretaceous.(2) Precise new 40Ar/39Ar radioisotopic dates place theextinction of the dinosaurs at 66.043± 0.043Ma, at thesame time as the Chicxulub impact and shortly after theinitiation of the most voluminous phase of the Deccaneruptions in India.(3) A major challenge in studying the dinosaur extinc-tion is a biased fossil record. Only North Americapreserves a series of well-dated, temporally stackeddinosaur-bearing rock units that cover the final ∼15Myrof the Cretaceous, and only a single formation (theHell Creek Formation) includes a well-studied andwell-dated record of dinosaurs over the final ∼1Myrof the Cretaceous. This makes it difficult to test cer-tain hypotheses about the timing and tempo of theextinction.(4) The latest Cretaceous world was volatile. Beforethe Chicxulub impact occurred, there were dramaticchanges in sea level and temperature, as well as twophases of Deccan volcanism.(5) There is no evidence for a global, long-termdeclinein the diversity of non-avian dinosaurs prior to theirextinction, although some groups (the bulk-feeding her-bivorous ceratopsids and hadrosaurids in North Amer-ica) did experience a loss of diversity and morpholog-ical disparity over the final ∼15Myr of the Cretaceous.Ecological food-web modelling suggests that these losseswould have made terminal Cretaceous (Maastrichtian)ecosystems more susceptible to cascading extinctions byan external forcingmechanism (such as a bolide impact)relative to ecosystems from earlier in the late Cretaceous(Campanian).(6) There is little evidence of any decline in dinosaurspecies richness or ecological diversity during the final∼1Myr of the Cretaceous in the Hell Creek Formation.The major dinosaur taxa persisted until very close tothe K–Pg boundary, including during ∼400000 years ofDeccan eruptions.(7) Current evidence indicates that the dinosaurextinction was abrupt in geological terms, suggestingthat long-term temperature and sea-level trends werenot a major factor in the extinction. The abruptnessevokes the Chicxulub impact as the most likely funda-mental cause of the extinction, although the coarsenessof the fossil record makes it difficult to test how Deccanvolcanism may have affected dinosaurs during the final∼400000 years of the Cretaceous. Furthermore, longerterm changes in sea level in North America may have ledto the ecological restructuring that made Maastrichtiandinosaurs particularly susceptible to extinction.

(8) There is much still to learn about the dinosaurextinction, and advances in radioisotopic dating, thediscovery of more latest Cretaceous dinosaur fos-sils outside of North America, and additional workon dinosaur biology and ecology will be particularlyimportant in testing the ‘emerging consensus’ that weidentify here.

IX. ACKNOWLEDGEMENTS

This work was funded by NSF EAR-1325544 (S.L.B.,T.E.W.) and EAR-1325552 (D.J.P.), a Marie Curie CareerIntegration Grant EC 630652 (S.L.B.), and an ImperialCollege Junior and Alexander von Humboldt ResearchFellowships (P.D.M.). We thank two anonymous refereesfor their helpful comments and A. Cooper andW. Fosterfor their editorial assistance.

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XI. SUPPORTING INFORMATION

Additional supporting information may be found in theonline version of this article.File S1. Dataset and Fig. S1 showing Campanian andMaastrichtian dinosaur occurrence records and rar-efied and Shareholder Quorum Subsampling diversitystatistics.

File S2. R file with data and code for ShareholderQuorum Subsampling analysis.

(Received 5 December 2013; revised 7 June 2014; accepted 16 June 2014 )


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