The Extinction of The Dinosaurs

Biol. Rev. (2014), pp. 000–000.
1
doi: 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
1 School of GeoSciences, University of Edinburgh, Edinburgh EH9 3JW, U.K.
2 School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham
B15 2TT, U.K.
3 Department of Earth Sciences, Natural History Museum, London SW7 5BD, U.K.
4 Department of Paleobiology, Smithsonian Institution, Washington, DC 20013, U.S.A.
5 Department of Natural History, Royal Ontario Museum, Toronto, Ontario M5S 2C6, Canada
6 Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, U.K.
7 Department of Earth Science and Engineering, Imperial College London, London SW7 2AZ, U.K.
8 Division of Paleontology, American Museum of Natural History, New York, NY 10024, U.S.A.
9 Department of Geology, Baylor University, Waco, TX 76706, U.S.A.
10 Department of Earth Sciences, University College London, London WC1E 6BT, U.K.
11 New Mexico Museum of Natural History and Science, Albuquerque, NM 87104, U.S.A.
ABSTRACT
Non-avian dinosaurs went extinct 66 million 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 data
accumulated over the past two decades, provide updated and novel analyses of long-term dinosaur diversity
trends 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 extinction
at the end of the Cretaceous. However, restructuring of latest Cretaceous dinosaur faunas in North America led
to reduced diversity of large-bodied herbivores, perhaps making communities more susceptible to cascading
extinctions. The abruptness of the dinosaur extinction suggests a key role for the bolide impact, although the
coarseness 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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
II.Timing of the dinosaur extinction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
III.Major hypotheses for the dinosaur extinction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
IV. Realities of the fossil record . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
V. The latest Cretaceous world . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
VI. 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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
IX. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
X. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
XI. Supporting information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
I. INTRODUCTION et al., 2002; Fastovsky et al., 2004; Wang & Dodson, 2006;
Lloyd et al., 2008; Barrett, McGowan & Page, 2009, Cam-
What happened to the dinosaurs? This question has pione & Evans, 2011; Upchurch et al., 2011; Brusatte
fascinated the general public, and intrigued and chal- et al., 2012; Lloyd, 2012; Mitchell, Roopnarine & Ang-
lenged scientists, for well over a century. Dinosaurs were ielczyk, 2012). Together, these advances are leading to
remarkably successful for over 160 million years (Myr), an emerging consensus on when and why non-avian
evolving colossal size and diversifying into over 1000 dinosaurs died out.
species distributed worldwide (Weishampel, Dodson Here we review current knowledge about the extinc-
& Osmólska, 2004). Birds—one of the most speciose tion of non-avian dinosaurs. We discuss the evolution
groups of living terrestrial vertebrates—are direct of dinosaurs immediately prior to their extinction,
evolutionary descendants of non-avian dinosaurs, and describe how Earth systems were changing in the latest
therefore living dinosaurs (Padian & Chiappe, 1998). Cretaceous, and assess limitations of the available fos-
But in the popular lexicon dinosaurs are symbols of sil record. We use this information to address two gen-
failure, because the last non-avian species disappeared eral issues. (i) Tempo: did the extinction result from
from the fossil record approximately 66 million years events that had been underway for millions of years,
ago (Ma) (Fig. 1). or was it caused by geologically brief or instantaneous
Dinosaurs are a cautionary tale that once-dominant events? (ii) Causes: what are the most likely explana-
groups of organisms can, and often do, die out. They tions for the extinction, and which can be ruled out?
vanished with many other species in one of the largest The focus here is on non-avian dinosaurs only. Although
mass extinctions in Earth history (MacLeod et al., 1997; their disappearance cannot be divorced from the larger
Alroy et al., 2008), which occurred at the end of the Cre- end-Cretaceous mass extinction, the specific narrative
taceous Period amidst a backdrop of massive volcanic and tempo of dinosaur extinction may differ from those
eruptions (Courtillot & Renne, 2003; Chenet et al., of other groups that vanished at this time (especially
2009), major changes in temperature and sea level (Li those inhabiting other ecosystems, such as the oceans),
& Keller, 1998; Barrera & Savin, 1999; Huber, Norris & given the many global changes of the latest Cretaceous.
MacLeod, 2002; Wilf, Johnson & Huber, 2003; Miller
et al., 2005; Grossman, 2012; Tobin et al., 2012), and the
impact of a ∼10-km-wide bolide (asteroid or comet)
(Alvarez et al., 1980; Alvarez, 1997; Schulte et al., 2010). II. TIMING OF THE DINOSAUR EXTINCTION
Scientists have long debated how these events affected
dinosaurs, and to what extent may have been responsi- Dinosaurs appeared in the Middle–early Late Triassic
ble for their extinction (Archibald, 1996; Archibald & (approximately 245–230 Ma), gradually rose to domi-
Fastovsky, 2004; Fastovsky & Sheehan, 2005; Archibald nance over the next 50 Myr, and subsequently diversi-
et al., 2010). fied into an extraordinary array of species in terrestrial
Over the past 20 years, an influx of new data has greatly environments worldwide throughout the remainder of
refined our understanding of dinosaur evolution and the Mesozoic (Sereno, 1999; Weishampel et al., 2004;
extinction. Driving this dynamic period of research is an Brusatte et al., 2010). Non-avian dinosaurs fluctuated
exponential increase in the rate of dinosaur discovery, in diversity over the course of their ∼160-million-year
with a new Mesozoic dinosaur species being named once history, with many individual species, and some larger
every ∼1.5 weeks at present (Benton, 2008). Increasingly subgroups, experiencing extinction as part of a nor-
precise radioisotopic dates have helped place latest Cre- mal ‘background’ rate (Weishampel et al., 2004; Barrett
taceous dinosaur fossils within the temporal context of et al., 2009; Upchurch et al., 2011). Dinosaurs survived a
the impact, volcanism, and climate change, allowing mass extinction at the end of the Triassic that had lit-
causal relationships to be better constrained (Chenet tle clear impact on their diversity, as well as a poorly
et al., 2009; Renne et al., 2013). More robust analytical understood, but possibly important, extinction event at
methods, which account for biases in the fossil record, the end of the Jurassic (Weishampel et al., 2004; Barrett
have quantified trends in dinosaur diversity through et al., 2009; Upchurch et al., 2011).
time, which is essential for determining whether their Non-avian dinosaurs disappear from the fossil record
extinction was geologically gradual or abrupt (Pearson 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 ∼60 Ma; other reconstructions more closely match the dates of the faunas depicted). The
dinosaur-dominated Hell 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, III. MAJOR HYPOTHESES FOR THE DINOSAUR
boundary), 66.043 ± 0.043 Ma (mean ± analytical uncer- EXTINCTION
tainty) based on high-precision 40 Ar/39 Ar radioisotopic
dates (Renne et al., 2013), within chron 29r of the Few issues in palaeontology have generated as much
geomagnetic polarity timescale (Gradstein et al., 2012) speculation as the dinosaur extinction. The number
(Fig. 1). This disappearance is so dramatic that, prior and variety of hypotheses is astounding (Benton, 1990),
to the advent of radioisotopic dating, the absence of but most scientific debate over the past century has
dinosaur fossils was often considered sufficient to assign boiled down to whether the extinction was geologically
strata above dinosaur-bearing rocks a Cenozoic age. abrupt or gradual, whether it was caused by something
Supposed Paleocene non-avian dinosaur fossils from intrinsic to dinosaurs or an extrinsic physical driver,
North America (e.g. Sloan et al., 1986; Fassett, 2009; Fas- and, if the latter, whether this driver was terrestrial or
sett, Heaman & Simonetti, 2011) are either reworked extraterrestrial in origin (Archibald, 1996; Archibald &
Cretaceous specimens or incorrectly dated (e.g. Lof- Fastovsky, 2004; Fastovsky & Sheehan, 2005). Linked
gren, Hotton & Runkel, 1990; Lucas et al., 2009; Koenig to these controversies is the question of whether the
et al., 2012; Renne & Goodwin, 2012). Although it is extinction had a single overriding cause or was the
conceivable that some local populations of non-avian result of a disastrous temporal coincidence of multiple
dinosaurs survived into the earliest Paleocene, the biological and/or physical factors.
K–Pg boundary clearly marks the dramatic end of the The most celebrated theory, and the most recogniz-
dinosaur-dominated world. able, is that dinosaurs and other organisms went extinct
suddenly after a giant bolide impact set off a global Campanian–Maastrichtian dinosaurs are known from
cataclysm of environmental upheaval (Alvarez et al., across the globe, only North America boasts a detailed
1980; Alvarez, 1997). The impact hypothesis has gained record of correlative, stratigraphically stacked faunas,
wide traction thanks to extensive study (Sheehan et al., in many cases accurately dated (Weishampel et al.,
1991; Fastovsky & Sheehan, 2005) and is an elegant 2004; Roberts, Deino & Chan, 2005; Eberth et al., 2013)
single explanation for why so many groups disappeared (Fig. 1). Only these faunas, therefore, present a clear
simultaneously. Nonetheless, some scientists remain picture of how dinosaurs changed in a single region
unconvinced that it was the sole cause of the dinosaur over the ∼15 Myr before the K–Pg boundary. How-
extinction specifically, and the end-Cretaceous mass ever, even here some periods of time are much better
extinction more broadly (Archibald, 1996; Archibald & represented and sampled than others (e.g. late Campa-
Fastovsky, 2004; Archibald et al., 2010; Keller, 2012). nian and late Maastrichtian versus early Maastrichtian).
Although evidence for an end-Cretaceous impact Campanian–Maastrichtian units in Asia, Europe, India,
is unequivocal (Schulte et al., 2010), doubts remain Madagascar, and South America also provide data rele-
because other severe changes occurred in Earth sys- vant to a global-scale understanding of latest Cretaceous
tems at or near the end of the Cretaceous: intensive vol- dinosaur diversity (Weishampel et al., 2004), and they
canism (Courtillot & Renne, 2003; Chenet et al., 2009), promise also to contribute important regional-scale
temperature oscillations (Li & Keller, 1998; Barrera & information as they become better sampled and dated.
Savin, 1999; Huber et al., 2002; Wilf et al., 2003; Gross- Currently, only the Hell Creek Formation (and tempo-
man, 2012; Tobin et al., 2012), and sea-level fluctua- ral equivalents) of the North American Western Interior
tions (Miller et al., 2005). It has been argued that each provides a well-sampled, relatively continuous record of
of these factors may be the primary cause of dinosaur dinosaur fossils during the final million years of the Cre-
extinction, that their sum resulted in the extinction, or taceous, up to a precisely located K–Pg boundary (Shee-
that a bolide impact finished off the dinosaurs after a han et al., 1991; Pearson et al., 2002; Fastovsky & Shee-
multi-million-year period of stress triggered by one or han, 2005). This one formation, therefore, provides
more of these changes (Archibald, 1996, 2011). the only well-constrained evidence for how dinosaurs
Each of these hypotheses makes predictions that can changed immediately before the bolide impact, and
be tested with the fossil record. The impact hypothe- the fine-scale relationships between dinosaur diver-
sis predicts a sudden extinction, whereas hypotheses sity, climate and sea-level changes, and Deccan vol-
centred on climate and sea-level changes, including canism during the waning days of the Cretaceous.
those invoking the bolide as a coup de grâce, imply Because the Hell Creek is continuous with overlying
that dinosaurs experienced a prolonged decline. Paleocene sediments, it also provides clear evidence that
Recent increases in the volume of data bearing on the dinosaurs did not survive locally past the end of the
extinction, combined with ongoing methodological Cretaceous. Recently identified stratigraphic sections in
advances, have allowed scientists to expand the scope Spain (Riera et al., 2009; Vila et al., 2013) and China
and complexity of testable scenarios, and assemble an (Jiang et al., 2011) with dinosaur fossils in close prox-
increasingly nuanced narrative of how dinosaur faunas imity to the K–Pg boundary hold great potential for
changed in concert with their environments in the future work.
latest Cretaceous. Although intense study of the North American
record has provided critical insights, its overwhelm-
ing dominance in extinction debates is problematic
IV. REALITIES OF THE FOSSIL RECORD for two reasons. First, its local patterns of dinosaur
diversity, evolution, and extinction may not accurately
Understanding how dinosaurs evolved prior to the document the generalized global extinction event
K–Pg boundary and how they may have responded to (Godefroit et al., 2009). For example, the almost com-
global catastrophes is constrained by the available, and plete absence of long-necked sauropod dinosaurs in
imperfect, fossil record. Only a fraction of all dinosaurs the Campanian–Maastrichtian of North America, com-
that ever lived are preserved, fossil record quality varies pared with their high diversity elsewhere, is strong
through time and space, different regions and time peri- evidence that these faunas are not representative
ods have been unevenly sampled, and precise radioiso- of a global reality (Mannion et al., 2011). Second,
topic dates for specimens or faunas are often unavail- although the North American record of Campanian–
able. A pragmatic evaluation of these limitations helps Maastrichtian dinosaurs is the most extensive, it is still
constrain what we do know, and identify what we do not imperfect. As elsewhere, there is a substantial preserva-
or cannot know, about the extinction. tional bias against dinosaurs of human-size or smaller
The greatest challenge in studying the dinosaur (Horner, Goodwin & Myhrvold, 2011; Brown et al.,
extinction is a set of biases that affects their lat- 2013; Evans et al., 2013), and intense debate surrounds
est Cretaceous record (Campanian–Maastrichtian whether some species are really juveniles or sexual
stages, approximately 83.6 to 66 Ma). Although morphs of other taxa (e.g. Scannella & Horner, 2010).
These issues complicate accurate estimates of latest landscape were already underway. Among the most
Cretaceous species diversity. prominent was a tremendous episode of volcanic activ-
One final caveat about the fossil record concerns ity that formed the Deccan flood basalts of India. These
scale. A growing global database of Campanian– eruptions proceeded in three main phases during the
Maastrichtian dinosaurs is enabling more complete Late Cretaceous–early Paleocene: the first during C30n,
estimates of broad-scale trends in dinosaur diversity the second in C29r, and the third during C29n (Cour-
over the final ∼10–15 Myr of the Cretaceous. At its tillot & Renne, 2003; Chenet et al., 2009; Jay et al., 2009).
finest resolution, however, even the Hell Creek record The second phase, which probably began ∼400000 years
is not well-enough sampled or dated to examine trends before the K–Pg boundary (Robinson et al., 2009), was
on a 1000–10000-year timescale (Pearson et al., 2002). the largest and formed up to 80% of the volume of
We do not, and probably cannot, know how individual the Deccan Traps (Chenet et al., 2009). This phase
dinosaurs or populations responded to environmen- was similar in size to other large-scale flood basalt vol-
tal change. This makes it exceedingly difficult to test canism in the geological record, such as the Central
specific possible kill mechanisms—e.g. acid rain or Atlantic Magmatic Province (CAMP), which has been
wildfires caused by an impact, extreme temperature implicated in the end-Triassic extinction (Courtillot &
changes caused by an impact or volcanism, or fluctuat- Renne, 2003). All phases of the Deccan Traps were
ing home ranges caused by sea-level change. For this likely emplaced rapidly and are composed of a series of
reason, our focus here is on using the dinosaur record smaller, single eruptions that occurred on the order of
to address broad-scale questions about the tempo and every ∼2000 years (Jay et al., 2009).
overarching causes of the extinction. Determining the precise age of the Deccan Traps has
proven difficult because of the low potassium content of
the basalts and chemical alteration due to weathering,
V. THE LATEST CRETACEOUS WORLD rendering whole-rock ages unreliable (Hofmann, Fer-
aud & Courtillot, 2000). Consequently, dates for Deccan
The end-Cretaceous extinction is closely associated with eruptions have large error margins, and there are dis-
a clay layer containing anomalously high abundances crepancies between dates for the same flows, making it
of iridium and other platinum-group elements (Alvarez impossible to determine their ages more precisely than
et al., 1980; Smit & Hertogen, 1980) with impact within polarity chrons (Courtillot & Renne, 2003). Fur-
ejecta, such as spherules and shocked minerals (Smit, thermore, the position of the K–Pg boundary within the
1999), derived from a ∼10 km wide bolide that hit the eruptive sequence is uncertain. An iridium anomaly has
Yucatan Peninsula of modern-day Mexico, creating the been found in sediment between flows (Bhandari et al.,
∼180–200-km-wide Chicxulub crater (Hildebrand et al., 1995), but may be volcanic in origin and discordant with
1991). the impact-clay layer (Hansen, Mohabey & Toft, 2001;
The effects of the impact were broad and devas- Sant et al., 2003).
tating. It triggered tsunamis that may have reached Regardless of their precise timing, the Deccan erup-
>300 km inland around the Gulf of Mexico (Matsui tions would have caused major environmental pertur-
et al., 2002), potentially caused >11 magnitude earth- bations in the Late Cretaceous–early Paleocene. Each
quakes (Ivanov, 2005), and created a global heat pulse eruption would have injected substantial amounts of sul-
(Goldin & Melosh, 2009) that perhaps ignited large phur dioxide into the atmosphere, causing sulphuric
wildfires near the impact site (Wolbach, Lewis & Anders, acid rain (Wignall, 2001; Self et al., 2006) and short-term
1985; Kring, 2007). The impact occurred in a carbon- cooling, depending on their frequency and whether
ate and sulphate-rich region, thereby releasing massive the sulphur dioxide reached the stratosphere (Wignall,
quantities of sulphur and other aerosols into the atmo- 2001). Large amounts of carbon dioxide added to the
sphere, which would have caused sulphuric acid rain atmosphere may have caused warming (Li & Keller,
(Pope et al., 1997) and at least temporarily destroyed the 1998; Wilf et al., 2003), although the pace of this may
ozone layer (Kring, 2007). These aerosols would have not have been fast enough to create significant, rapid
also briefly cooled the Earth by several to tens of degrees climate change (Self et al., 2006). Unfortunately, it is
Celsius following the initial heat pulse (Pope et al., still unclear whether these eruptions caused significant
1997). Dust thrown up by the impact would have formed biotic changes even locally.
a thick cloud that darkened the Earth and depressed Sea levels also changed dramatically during the latest
photosynthesis (Alvarez et al., 1980; Pope et al., 1997). Cretaceous, although changes of similar magnitude
Over a slightly longer term, the injection of carbon diox- occurred at other points in dinosaur evolutionary
ide, methane, and water vapour into the atmosphere history (Figs 2 and 3). Peak Late Cretaceous lev-
may have caused greenhouse warming of a few degrees els of 50–70 m above present sea levels at ∼80 Ma
(Beerling et al., 2002). were followed by a long-term fall through most of
The end-Cretaceous impact did not occur in a vac- the Campanian–Maastrichtian (Miller et al., 2005).
uum, however, and changes to Earth’s climate and Globally, the Campanian is dominated by highstands
Epoch Age Ma Chron

Observed Observed Residual Residual
Dan. Sel.
Paleocene
60 C26
Isotopic temperature Sea level global NA Global DBCs global NA
C27
C28
diversity diversity diversity diversity
C29
Maas.
C30
70 C31
C32
Late Cretaceous
Campanian
C33
80
Tur. Con. San.
90
Cen.
100
C34
Albian
110
Early Cretaceous
Aptian
120
Hau. Barr.
130
Val.
140
Berr.
10 15 20 25 -50 0 50 100 0 200 400 0 100 200 0 1000 2000 -0.5 0 0.5 -0.5 0 0.5
o
C m
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 66 Ma).
Isotopic temperatures based on 𝛿 18 O data (Grossman, 2012). DBC refers to ‘dinosaur bearing collections’ (a measure of
sampling intensity: Upchurch et al., 2011), and gaps represent missing data. Dinosaur diversity is shown both globally and
locally 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 the
sampling-corrected data.
with a few relatively short lowstands in the early the late Maastrichtian the WIS drastically constricted,
and middle Campanian (Miller et al., 2005). The probably due to the global sea-level low stand combined
Campanian–Maastrichtian boundary is marked by a with local tectonism (Weimer, 1984; Lillegraven &
substantial global regression and subsequent low stand Ostresh, 1990).
that persisted for up to a few million years (Miller Temperature changes also characterize the latest Cre-
et al., 2005). This was followed by a high stand during taceous (Figs 2–4). Carbon dioxide levels declined
the middle Maastrichtian, a low stand during the late through the Late Cretaceous (Royer, 2006, 2014; Hong
Maastrichtian, and a rise to a global high stand that & Lee, 2012), coincident with a long-term cooling trend
peaked at the end of the Maastrichtian and then fell (Barrera & Savin, 1999; Huber et al., 2002). Campa-
across the K–Pg boundary (Miller et al., 2005). nian and Maastrichtian climates were generally equable,
In general, global sea levels were more varied, and with relatively low latitudinal temperature gradients and
fluctuated more intensely on shorter time scales, during polar regions kept above freezing (Wolfe & Upchurch,
the Maastrichtian than the Campanian (Miller et al., 1987). Globally, the Campanian was warmer, but the
2005). This also applied to the Western Interior Seaway Maastrichtian climate was more variable (Huber et al.,
(WIS), the shallow epicontinental sea that covered 2002). During the middle Maastrichtian there may have
much of North America during this time. The WIS was been a short-lived warming event related to an increase
expansive during much of the Campanian and Maas- in atmospheric carbon dioxide from the first Deccan
trichtian, at times connecting the Arctic Ocean and eruption phase (Nordt, Atchley & Dworkin, 2003; Tobin
Gulf of Mexico (Lillegraven & Ostresh, 1990). During et al., 2012). This mid-Maastrichtian warming is followed
Chron
Late Cretaceous Period
All-dinosaur All-dinosaur Ornithischian Theropod Ceratopsid Hadrosauroid Theropod
Age
Isotopic Sea level
Ma m global NA NA NA NA NA NA
temperature -25 0 25 50 75 diversity diversity diversity diversity disparity disparity disparity
Campanian Maas
C30
70 C31
C32
C33
80
10 15 20 30 34 38 42 46 19 23 27 7 11 15 7 11 15 5 45 85 0 3000 600 900 1200

o
C
Fig. 3. Short-term trends in global temperature (Grossman, 2012), sea level (Miller et al., 2005), subsampled dinosaur
diversity (see text for details), and dinosaur morphological disparity (Brusatte et al., 2012) over the latest Cretaceous
(Campanian–Maastrichtian, 83.6–66 Ma). Subsampled dinosaur diversity is an estimate based on Shareholder Quorum
Subsampling that takes into account differences in sampling intensity over time (see text). Diversity is shown both globally
and locally for North America (NA). Note that there are no progressive decreases in global dinosaur diversity, all North
American dinosaur diversity, or North American theropod dinosaur diversity and disparity, but a progressive decline in
North American ornithischian diversity and significant declines in and ceratopsid and hadrosauroid disparity.
by another warming event in the oceans and on land including what is now recognized as the Dinosaur
during the last few hundred thousand years of the Cre- Park Formation (42 valid species), than that of the
taceous, likely linked to carbon dioxide outgassing from late Maastrichtian Hell Creek Formation (25–33 valid
the second Deccan eruption phase (Li & Keller, 1998; species). Simple comparisons of species richness do
Barrera & Savin, 1999; Nordt et al., 2003; Wilf et al., not, however, take into account possible variations in
2003; Tobin et al., 2012). Subsequently, global climate sampling intensity or preservation potential of rocks
cooled during the latest Maastrichtian and across the of different geological ages (Russell, 1984; Fastovsky
K–Pg boundary (Li & Keller, 1998; Wilf et al., 2003) per- et al., 2004), the fact that not all Campanian taxa were
haps due to enhanced silicate weathering of the Deccan directly contemporaneous, or that the faunas being
basalts (Dessert et al., 2001). compared might represent different environments
(Fastovsky et al., 2005).
Various approaches have been taken to address this
VI. HOW WERE DINOSAURS CHANGING DURING suite of possible biases, including subsampling (Rus-
THE LATEST CRETACEOUS? sell, 1984; Fastovsky et al., 2004; Lloyd et al., 2008),
models based on estimates of variation in rock volume
or collecting effort through time (Barrett et al., 2009;
The Campanian–Maastrichtian was an interval of major
global changes, and a better understanding of how Upchurch et al., 2011; Lloyd, 2012), and statistical esti-
dinosaurs were evolving during this time can illuminate mates of the true number of species represented by a
how they were affected by Earth system changes, and biased record (Wang & Dodson, 2006). These methods
therefore the tempo and causes of their extinction. This have been applied at differing geographic (e.g. conti-
requires examination of trends in dinosaur biodiversity nental versus global) and taxonomic (e.g. all dinosaurs
over time. Two very different types of trends give insight versus separate comparisons of major dinosaur clades)
into dinosaur extinction: long-term patterns over the scales. None of these studies has supported a global
final ∼10–15 Myr of the Cretaceous (Figs 2 and 3) and decline in diversity occurring across all dinosaur
short-term patterns during the ∼1 Myr before the K–Pg groups (Fig. 2). However, some evidence has supported
boundary (Fig. 4). Campanian–Maastrichtian declines in the richness of
ornithischians (Barrett et al., 2009; Upchurch et al.,
2011) and theropods (Barrett et al., 2009; but not
(1) Long-term trends Upchurch et al., 2011), but not sauropodomorphs.
Historically, the standard view of dinosaur evolution Here, we present new results (Fig. 3; see online
prior to the extinction based on the North American File S1, Fig. S1) based on sampling-standardized anal-
record was of a decline in total species numbers (rich- yses of current data within the Paleobiology Database.
ness) through the Campanian–Maastrichtian (Marsh, This dataset is an up-to-date record of global dinosaur
1882; Colbert, 1961; Archibald & Clemens, 1982; diversity and incorporates hundreds of new latest Cre-
Archibald, 1996; Dodson, 1996; Sullivan, 2006). This taceous fossils discovered over the past decade that
was based primarily upon the higher species richness of are relevant to understanding the K–Pg extinction. In
several Campanian formations from southern Canada, order to produce the subsampled dinosaur richness
Age Dinosaur species MAT Deccan Global sea

Period Chron volcanism
(Ma) occurences (oC) level (mapl)
Paleogene
1 3 5 7 9 11 13
2 4 6 8 10 12 14
66.0
Deccan Phase 2
C29r
66.5
CRETACEOUS
C30n
67.0
67.5
8 12 16
50
25
Fig. 4. Dinosaur species occurrences in the Hell Creek Formation in the Williston Basin, North Dakota, USA, during
the latest Cretaceous (latest Maastrichtian), along with curves of local mean annual temperature (MAT) derived from
fossil leaves (Wilf et al., 2003), global sea level (mapl, metres above present level) (Miller et al., 2005), and an indication
of the timing of the voluminous second Deccan volcanic pulse (Chenet et al., 2009; Robinson et al., 2009). The MAT
curve is based on range-through fossil leaf data and the minimum uncertainty for estimates is ±2∘ C. The thicker line
in the sea-level curve indicates a global transgressive phase (Miller et al., 2005). Dinosaur occurrence data from Pearson
et 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) Coelurosauria
indet.; (6) Ornithomimidae indet.; (7) Tyrannosaurus rex; (8) Paronychodon lacustris; (9) Saurornitholestes; (10) Thescelosaurus
neglectus; (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 Creek
Formation from Hicks et al. (2002) and Peppe, Evans & Smirnov (2009). Note that there is high dinosaur diversity through
the Deccan phase, up to the K–Pg boundary.
in Fig. 3 and File S1, Fig. S1 we extracted all global North American scales (Fig. 3). However, finer-grained
dinosaurian body fossil occurrences from the Paleobi- analyses support a decline in the species richness of
ology Database (Carrano, 2008, and updates thereafter) North American ornithischians, but not theropods. This
(downloaded 12/07/2013) that could be definitively ornithischian decline occurs from the late Campanian
assigned to latest Cretaceous substage time bins (late to the early Maastrichtian, and ornithischian diversity
Campanian, early Maastrichtian, late Maastrichtian) remains low during the late Maastrichtian.
and valid genera (920 occurrences). This dataset was These results are congruent with recent studies that
then reduced to just occurrences from North America examined trends in morphological disparity, a measure
and then divided into two further subsets, Ornithischia that quantifies the diversity of anatomical form in a
and Theropoda. Sauropodomorpha was not examined group of organisms (Wills, Briggs & Fortey, 1994).
separately because only one genus (Alamosaurus) is Because anatomy is often closely tied to function and
known from the latest Cretaceous of North America. ecology, disparity is an important addition to species
The dataset is included as online Supporting Informa- richness for documenting the spectrum of body plans,
tion (see online File S1). behaviours, and niches exploited by a group. Studies of
We note that this binning scheme groups together dinosaur disparity during the latest Cretaceous suggest
non-contemporaneous taxa; this is necessary due to the that Campanian–Maastrichtian declines are evident
coarseness of the fossil record and the need for reason- in large-bodied, bulk-feeding ornithischian herbivores
able sample sizes in each bin to enable the subsampling (ceratopsians, hadrosaurs) within North America, but
analyses. As the North American record in particular not in other groups or regions (Campione & Evans,
becomes better sampled over time, it should be possible 2011; Brusatte et al., 2012) (Fig. 3).
to conduct diversity analyses with shorter time bins that Current evidence for a long-term diversity decline
take into account detailed intra-formational sampling prior to the non-avian dinosaur extinction is therefore
such as that recently presented for the Dinosaur Park limited to ornithischian dinosaurs, with the signal
Formation and Edmonton Group of Canada by Mallon almost certainly being driven by declines among two
et al. (2012) and Eberth et al. (2013). large-bodied subclades (Ceratopsidae, Hadrosauri-
We implemented two forms of subsampling to recon- dae) within North America. For other groups of
struct past diversity. Sample-based rarefaction (using the dinosaurs, and at a global scale, there is little evidence
number of localities at which each genus is found in for a long-term diminution in diversity. All major
each substage) was performed using PAST (Hammer, groups of Campanian dinosaurs survived into the late
Harper & Ryan, 2001), and Shareholder Quorum Sub- Maastrichtian, so there was no gradual loss of major
sampling (SQS: Alroy, 2010a–c) was run in R, using components of dinosaur diversity through the latest Cre-
the R implementation posted on J. Alroy’s website taceous. Moreover, it is worth stressing that even if some
(version 2.0; posted online 14 February 2011). We groups declined in diversity through this time interval,
used an arbitrary ‘quorum’ (i.e. sampling) level (q) similar (and often more extreme) waxing and waning
of 0.5 that will return results for all comparisons, in the diversity of particular clades occurred repeat-
although similar relative numbers can be obtained edly across dinosaur evolutionary history (Fastovsky
with other q values. The data and code used are et al., 2004, 2005; Barrett et al., 2009; Upchurch
included as online Supporting Information (see online et al., 2011), and does not indicate that dinosaurs,
File S2). or particular groups of them, were doomed to
The primary difference between SQS and rarefac- extinction.
tion is that the former samples fairly whereas the lat- When interpreting diversity trends, it is important
ter samples equally. SQS achieves this by sampling a set to remember that they summarize patterns. It is more
area (q) underneath a species frequency curve. This difficult to evaluate what consequences these pat-
approach offers a number of key advantages over rar- terns, such as an ornithischian diversity decline, would
efaction (Alroy, 2010a–c). Of particular note is the have had on the processes of dinosaur evolution. A
much more consistent relative subsampled richness provocative recent study has attempted to bridge the
values recovered between bins as q varies. Rarefac- pattern–process divide (Mitchell et al., 2012). This
tion curves, on the other hand, often cross, meaning study showed that the ornithischian decline resulted
that sampling level can determine which bin(s) are in a Campanian–Maastrichtian decrease of dinosaur
relatively more diverse. However, we implement both beta diversity (i.e. decreases in provincialism) within
methods so that the results can be directly compared North America (see also Vavrek & Larsson, 2010).
with earlier attempts that used only rarefaction. SQS When hypothetical food webs of Campanian and Maas-
results are shown in Fig. 3 and rarefaction results in trichtian communities were subjected to simulated
File S1, Fig. S1. primary productivity disruptions (like those caused
The new subsampling analyses provide no evidence by a bolide impact), the Maastrichtian communities
for a progressive Campanian–Maastrichtian decline in suffered greater extinctions. These results imply that
total dinosaur species richness at either the global or the decreased diversity of large-bodied Maastrichtian
herbivores made their communities more vulnerable to will undoubtedly focus not only on the Spanish sections,
cascading extinctions. but on other units straddling the K–Pg boundary in
North America that are becoming better sampled, such
(2) Short-term trends as the Edmonton Group of Alberta, Canada (Eberth
et al., 2013).
Detailed intra-formational (sub-million-year timescale)
assessments of dinosaur biodiversity immediately pre-
ceding the K–Pg boundary are limited to the Western
Interior of the United States, and most focus on VII. DISCUSSION
documenting changes within the Hell Creek For-
mation (Sheehan et al., 1991, 2000; Pearson et al., (1) The tempo and causes of the dinosaur extinction:
2001, 2002) (Fig. 4). The first systematic study of an emerging view
Hell Creek dinosaur diversity used a 3-year field sur-
vey of in situ dinosaur macrofossils (Sheehan et al., The wealth of data accumulated over the past two
1991), and was later expanded to include microfos- decades is leading to an emerging picture of how
sils and non-dinosaurian vertebrates (Pearson et al., the Earth changed during the latest Cretaceous and
2001, 2002), to address some criticisms of the original how these changes affected dinosaurs. The tempo of
methods (Williams, 1994; Hurlbert & Archibald, 1995; the non-avian dinosaur extinction appears to have
Archibald, 1996). These studies found little support been sudden, at least in geological terms. Our current
for a decline in dinosaur species richness or ecological knowledge of the dinosaur fossil record provides no
diversity through the Hell Creek Formation, particu- indication of obvious long-term declines in global biodi-
larly when variations in sample size were accounted versity over the final 15 Myr of the Cretaceous (although
for (Fig. 4). A more recent, decade-long census of some North American herbivores did diminish in diver-
dinosaur macrofossils also found no change in the sity), no major dinosaur groups went extinct during this
diversity of large dinosaur taxa (primarily genera) time, and a diverse assemblage of abundant dinosaur
from the lower to the upper Hell Creek (Horner et al., species persisted until the very end of the Cretaceous in
2011). local faunas in North America and Europe. Whatever
The rarity of dinosaur fossils in the uppermost 3 m killed the dinosaurs seems to have been focused at the
of the Hell Creek Formation has historically been very end of the Maastrichtian, within a few hundred
taken as evidence that dinosaurs declined in abun- thousand years of the K–Pg boundary.
dance, or even went extinct, before the bolide impact The causes of the dinosaur extinction are more neb-
(Clemens, Archibald & Hickey, 1981; Williams, 1994; ulous, although new data help to better constrain
Archibald, 1996). Some workers, however, suggested and test possible scenarios. Long-term environmental
that this ‘three metre gap’ was an artefact caused changes through the Campanian and Maastrichtian,
by sampling (Sheehan et al., 2000) or preservational such as sea-level fluctuations, likely affected the ecologi-
factors, including acidic leaching associated with the cal structure of dinosaur communities, at least in North
impact (Retallack, Leahy & Spoon, 1987). Although the America. Loss of beta diversity, combined with reduc-
recent discovery of a ceratopsian fossil in a mudstone tion in species richness and morphological diversity
unit within the ‘gap’, about 15 cm below the K–Pg of large-bodied herbivores, perhaps due to the regres-
boundary, provides strong evidence that dinosaurs sion of the WIS in the Maastrichtian and a resultant
probably witnessed the impact at the end of the change in habitat distribution (Archibald, 1996; Gates,
Cretaceous (Lyson et al., 2011), this does not shed Prieto-Márquez & Zanno, 2012), may have made Maas-
light on changes in community composition, relative trichtian dinosaur communities more susceptible to cas-
abundances, or other aspects of dinosaur biodiver- cading extinctions (Mitchell et al., 2012) caused by a
sity over this presumably short terminal Cretaceous catastrophic extrinsic forcing factor, such as an impact
interval. or large-scale volcanism. These long-term environmen-
South of the Hell Creek area, dinosaurs maintained tal changes may have restructured dinosaur communi-
diversity and abundance, without any sign of decline, ties at the regional level in North America, but current
throughout the latest Cretaceous in the Ferris Forma- evidence does not support a major influence on global
tion of Wyoming (Lillegraven & Eberle, 1999). Further biodiversity through the latest Cretaceous, suggesting
afield, in the Tremp Basin of Spain, dinosaurs remained they are not the driving force behind the dinosaur
common and diverse throughout the Maastrichtian, extinction.
with no noticeable decline or local extinctions before Instead, current evidence indicates that the dinosaur
the K–Pg boundary (Riera et al., 2009; Vila et al., 2013). extinction was abrupt, which evokes the bolide impact
However, precise dating of these deposits is problematic as the potential major driver. What is less clear at
and diversity trends have not been analysed with the this stage is how Deccan volcanism affected dinosaurs
same statistical rigour and stratigraphic precision as the during the immediate run-up to the impact. Existing
Hell Creek studies (Pearson et al., 2002). Future work data on dinosaur diversity, richness, and community
structure in the last few hundred thousand years of (Archibald, 2011; Slater, 2013). Mammals evolved rea-
the Cretaceous—when the voluminous second Deccan sonable ecological diversity during the Jurassic and Cre-
pulse occurred—are not robust enough to tease apart taceous (Luo, 2007), but compared to extant species
the differential effects of Deccan-induced environmen- were generally small. All mammal groups were severely
tal change versus the direct effects of the impact on affected by the end-Cretaceous extinction, particularly
dinosaurs. It is clear that the major dinosaur species per- metatherians (marsupials and their fossil relatives)
sisted in the Hell Creek (and probably Spain) during the (Williamson et al., 2012; Wilson, 2013), larger-bodied
second Deccan phase, up until the K–Pg boundary and species, and those with specialized diets (Wilson, 2013).
the impact, suggesting that at least in North America Nonetheless, at least some representatives of many
Deccan volcanism did not cause any substantial change major groups, including metatherians and eutherians
in dinosaur species richness. However, volcanic-induced (placentals and fossil relatives), were able to endure.
environmental changes may have affected dinosaur These survivors proliferated rapidly after the dinosaur
communities in other ways during this time, such as extinction, forming diverse mammalian faunas in North
changes in population structure or community ecology, America no later than 400000 years into the Paleocene
or at regional scales that are currently undetectable in (Renne et al., 2013; Wilson, 2013), which set the stage
the fossil record. for the ensuing 66 Myr of mammalian dominance in ter-
Given the weight of current evidence, we hold here restrial ecosystems.
that the bolide impact was probably the fundamental
cause of the dinosaur extinction, though it does not
automatically follow that this event was also primarily (3) Future directions
responsible for the extinction of other taxa at the We identify the following as critical research objec-
K–Pg boundary. Longer term phenomena such as tives for the next decade: (i) better sampling of
sea-level-mediated faunal restructuring and shorter Campanian–Maastrichtian dinosaurs from outside
term Deccan-induced climate changes may have made North America, especially those within chron 29r.
latest Maastrichtian communities less resilient to (ii) Detailed intra-formational sampling, like that
the impact, as ‘press’ events before the sudden and achieved for the Hell Creek, of dinosaur-bearing K–Pg
catastrophic ‘pulse’ of the impact (Arens & West, sections elsewhere in North America (Edmonton
2008). But we hypothesize that without the impact, Group, San Juan Basin, Big Bend), Europe (south-
non-avian dinosaurs probably would not have com- ern France, Spain, Romania), Asia (Nanxiong Basin,
pletely died out. This hypothesis, however, must be Amur Region), India, and South America (Patago-
tested as more data come to light, especially concern- nia). (iii) Late Cretaceous dinosaur diversity analyses
ing the effects of Deccan volcanism on dinosaurian with shorter time bins based on a finer-scale level
ecosystems. of intra-formational sampling, like those conducted
by Mallon et al. (2012) and Eberth et al. (2013). (iv)
Improved radioisotopic dating of the Deccan eruptions
(2) What happened after the dinosaur extinction?
and increasingly constrained dates for North Ameri-
The dinosaur extinction was part of a mass extinc- can sections (Renne et al., 2013), to enable fine-scale
tion that devastated terrestrial and marine ecosystems correlations between diversity changes and volcanism.
(MacLeod et al., 1997). On land, many organisms liv- (v) Additional metre-scale studies of whole-community
ing alongside dinosaurs also went extinct, including ecological dynamics within the Hell Creek Formation,
non-neornithine birds (Longrich, Tokaryk & Field, such as have been carried out for contemporary mam-
2011), many lizards and snakes (Longrich, Bhullar & mals (Wilson, 2005). (vi) More long-term studies of
Gauthier, 2012), pterosaurs, and numerous crocodyli- how dinosaur ecology, not only diversity, changed over
forms (MacLeod et al., 1997). Conversely, aquatic the Campanian–Maastrichtian, and other periods of
freshwater tetrapods such as amphibians, turtles, and comparable length in dinosaur evolution. (vii) Work
choristodires experienced lower losses across the K–Pg focused on aspects of dinosaur biology that may explain
boundary (Archibald & Bryant, 1990; MacLeod et al., why they went extinct, and particularly why certain birds
1997). There is general agreement that organisms in survived whereas many bird-like feathered dinosaurs
freshwater ecosystems were less affected by the extinc- died off. (viii) More robust theoretical models of how
tion than those in terrestrial (non-aquatic) or marine global, geological-scale changes might have impacted
environments (Archibald & Fastovsky, 2004), possibly populations and local environments, and be detected
because freshwater food chains were more reliant within a single formation. (ix) Comparisons between
on detritus feeding than photosynthesis (Sheehan & dinosaur alpha- and beta-diversity patterns and those of
Hansen, 1986). other latest Cretaceous plants and animals, to identify
With the extinction of dinosaurs, which had been complementary or contradictory patterns that might
incumbent in many terrestrial niches for over 160 Myr, help to identify the specific kill mechanisms for the
mammals had the opportunity to diversify and radiate end-Cretaceous extinction.
VIII. CONCLUSIONS (8) There is much still to learn about the dinosaur
extinction, and advances in radioisotopic dating, the
(1) Over the past two decades, a wealth of new data and discovery of more latest Cretaceous dinosaur fos-
advances in analytical techniques have given new insights sils outside of North America, and additional work
into one of the great riddles of palaeontology: why the on dinosaur biology and ecology will be particularly
dinosaurs went extinct. These advances are leading to important in testing the ‘emerging consensus’ that we
an emerging consensus on when and why the non-avian identify here.
dinosaurs died out at the end of the Cretaceous.
(2) Precise new 40 Ar/39 Ar radioisotopic dates place the
extinction of the dinosaurs at 66.043 ± 0.043 Ma, at the IX. ACKNOWLEDGEMENTS
same time as the Chicxulub impact and shortly after the
initiation of the most voluminous phase of the Deccan
This work was funded by NSF EAR-1325544 (S.L.B.,
eruptions in India.
T.E.W.) and EAR-1325552 (D.J.P.), a Marie Curie Career
(3) A major challenge in studying the dinosaur extinc-
Integration Grant EC 630652 (S.L.B.), and an Imperial
tion is a biased fossil record. Only North America
College Junior and Alexander von Humboldt Research
preserves a series of well-dated, temporally stacked
Fellowships (P.D.M.). We thank two anonymous referees
dinosaur-bearing rock units that cover the final ∼15 Myr
for their helpful comments and A. Cooper and W. Foster
of the Cretaceous, and only a single formation (the
for their editorial assistance.
Hell Creek Formation) includes a well-studied and
well-dated record of dinosaurs over the final ∼1 Myr
of the Cretaceous. This makes it difficult to test cer-
tain hypotheses about the timing and tempo of the X. REFERENCES
extinction.
(4) The latest Cretaceous world was volatile. Before Alroy, J. (2010a). Fair sampling of taxonomic richness and unbiased estimation
of origination and extinction rates. Paleontological Society Special Papers 16,
the Chicxulub impact occurred, there were dramatic 55–80.
changes in sea level and temperature, as well as two Alroy, J. (2010b). Geographical, environmental and intrinsic biotic controls on
phases of Deccan volcanism. Phanerozoic marine diversification. Palaeontology 53, 1211–1235.
Alroy, J. (2010c). The shifting balance of diversity among major marine animal
(5) There is no evidence for a global, long-term decline groups. Science 329, 1191–1194.
in the diversity of non-avian dinosaurs prior to their Alroy, J., Aberhan, M., Bottjer, D. J., Foote, M., Fürsich, F. T., Harries,
extinction, although some groups (the bulk-feeding her- P. J., Hendy, A. J. W., Holland, S. M., Ivany, L. C., Kiessling, W., Kosnik,
M. A., Marshall, C. R., McGowan, A. J., Miller, A. I., Olszewski, T. D.,
bivorous ceratopsids and hadrosaurids in North Amer- Patzkowsky, M. E., Peters, S. E., Villier, L., Wagner, P. J., Bonuso, N.,
ica) did experience a loss of diversity and morpholog- Borkow, P. S., Bernneis, B., Clapham, M. E., Fall, L. M., Ferguson, C.
A., Hanson, V. L., Krug, A. Z., Layou, K. M., Leckey, E. H., Nürnberg, S.,
ical disparity over the final ∼15 Myr of the Cretaceous. Powers, C. M., Sessa, J. A., Simpson, C., Tomašovych, A. & Visaggi, C. C.
Ecological food-web modelling suggests that these losses (2008). Phanerozoic trends in the global diversity of marine invertebrates.
would have made terminal Cretaceous (Maastrichtian) Science 321, 97–100.
Alvarez, W. (1997). T. rex and the Crater of Doom. Princeton University Press,
ecosystems more susceptible to cascading extinctions by Princeton.
an external forcing mechanism (such as a bolide impact) Alvarez, L. W., Alvarez, W., Asaro, F. & Michel, H. V. (1980). Extraterrestrial
relative to ecosystems from earlier in the late Cretaceous cause for the Cretaceous-Tertiary extinction. Science 208, 1095–1108.
Archibald, J. D. (1996). Dinosaur Extinction and the End of an Era. Columbia
(Campanian). University Press, New York.
(6) There is little evidence of any decline in dinosaur Archibald, J. D. (2011). Extinction and Radiation. Johns Hopkins University
species richness or ecological diversity during the final Press, Baltimore.
Archibald, J. D. & Bryant, L. J. (1990). Differential Cretaceous/Tertiary
∼1 Myr of the Cretaceous in the Hell Creek Formation. extinctions of nonmarine vertebrates; evidence from northeastern Montana.
The major dinosaur taxa persisted until very close to Geological Society of America Special Papers 247, 549–562.
the K–Pg boundary, including during ∼400000 years of Archibald, J. D. & Clemens, W. A. (1982). Late Cretaceous extinctions.
American Scientist 70, 377–385.
Deccan eruptions. Archibald, J. D., Clemens, W. A., Padian, K., Rowe, T., MacLeod, N., Barrett,
(7) Current evidence indicates that the dinosaur P. M., Gale, A., Holroyd, P., Sues, H.-D., Arens, N. C., Horner, J. R.,
Wilson, G. P., Goodwin, M. B., Brochu, C. A., Lofgren, D. L., et al. (2010).
extinction was abrupt in geological terms, suggesting Cretaceous extinctions: multiple causes. Science 328, 973.
that long-term temperature and sea-level trends were Archibald, J. D. & Fastovsky, D. E. (2004). Dinosaur extinction. In The
not a major factor in the extinction. The abruptness Dinosauria. Second Edition (eds D. B. Weishampel, P. Dodson and H.
Osmólska), pp. 672–684. University of California Press, Berkeley.
evokes the Chicxulub impact as the most likely funda- Arens, N. C. & West, I. D. (2008). Press-pulse: a general theory of mass
mental cause of the extinction, although the coarseness extinction? Paleobiology 34, 456–471.
of the fossil record makes it difficult to test how Deccan Barrera, E. & Savin, S. M. (1999). Evolution of late Campanian-Maastrichtian
marine climates and oceans. Geological Society of America Special Papers 332,
volcanism may have affected dinosaurs during the final 245–282.
∼400000 years of the Cretaceous. Furthermore, longer Barrett, P. M., McGowan, A. J. & Page, V. (2009). Dinosaur diversity
term changes in sea level in North America may have led and the rock record. Proceedings of the Royal Society of London Series B 276,
2667–2674.
to the ecological restructuring that made Maastrichtian Beerling, D. J., Lomax, B. H., Royer, D. L., Upchurch, G. L. & Kump, L. R.
dinosaurs particularly susceptible to extinction. (2002). An atmospheric pCO2 reconstruction across the Cretaceous-Tertiary
boundary from leaf megafossils. Proceedings of the National Academy of Sciences of Hammer, O., Harper, D. A. T. & Ryan, P. D. (2001). Paleontological statistics
the United States of America 99, 7836–7840. software package for education and data analysis. Palaeontologica Electronica
Benton, M. J. (1990). Scientific methodologies in collision: the history of the 4(1), 1–9.
study of the extinction of the dinosaurs. Evolutionary Biology 24, 371–400. Hansen, H., Mohabey, D. & Toft, T. (2001). No K/T boundary at Anjar,
Benton, M. J. (2008). Fossil quality and naming dinosaurs. Biology Letters 4, Gujarat, India: evidence from magnetic susceptibility and carbon isotopes.
729–732. Journal of Earth System Science 110, 133–142.
Bhandari, N., Shukla, P., Ghevariya, Z. & Sundaram, S. (1995). Impact Hicks, J. F., Johnson, K. R., Obradovich, J. D., Tauxe, L. & Clark, D. (2002).
did not trigger Deccan volcanism: evidence from Anjar K/T boundary Magnetostratigraphy and geochronology of the Hell Creek and basal Fort
intertrappean sediments. Geophysical Research Letters 22, 433–436. Union formations of southwestern North Dakota and a recalibration of the
Brown, C. M., Evans, D. C., Campione, N. E., O’Brien, L. J. & Eberth, D. A. age of the Cretaceous-Tertiary boundary. Geological Society of America Special
(2013). Evidence for taphonomic size bias in the Dinosaur Park Formation Papers 361, 35–55.
(Campanian, Alberta), a model Mesozoic terrestrial alluvial-paralic system. Hildebrand, A. R., Penfield, G. T., Kring, D. A., Pilkington, M., Camargo,
Palaeogeography, Palaeoclimatology, Palaeoecology 372, 108–122. A., Jacobsen, S. B. & Boynton, W. V. (1991). Chicxulub crater: a possible
Brusatte, S. L., Butler, R. J., Prieto-Márquez, A. & Norell, M. A. (2012). Cretaceous/Tertiary boundary impact crater on the Yucatan Peninsula,
Dinosaur morphological diversity and the end-Cretaceous extinction. Nature Mexico. Geology 19, 867–871.
Communications 3, 804 (doi: 10.1038/ncomms1815). Hofmann, C., Feraud, G. & Courtillot, V. (2000). 40Ar/39Ar dating of
Brusatte, S. L., Nesbitt, S. J., Irmis, R. B., Butler, R. J., Benton, M. mineral separates and whole rocks from the Western Ghats lava pile: further
J. & Norell, M. A. (2010). The origin and early radiation of dinosaurs. constraints on duration and age of the Deccan traps. Earth and Planetary Science
Earth-Science Reviews 101, 68–100. Letters 180, 13–27.
Campione, N. E. & Evans, D. C. (2011). Cranial growth and variation in edmon- Hong, S. K. & Lee, Y. I. (2012). Evaluation of atmospheric carbon dioxide
tosaurs (Dinosauria: Hadrosauridae): implications for latest Cretaceous mega- concentrations during the Cretaceous. Earth and Planetary Science Letters
herbivore diversity in North America. PLoS ONE 6(9), e25186. 327-328, 23–28.
Carrano, M. (2008). Taxonomy and classification of non-avian Dinosauria. Horner, J. B., Goodwin, M. B. & Myhrvold, N. (2011). Dinosaur census
Paleobiology Database Online Systematics Archive 4. reveals abundant Tyrannosaurus and rare ontogenetic stages in the Upper
Chenet, A.-L., Courtillot, V., Fluteau, F., Géerard, M., Quidelleur, X., Cretaceous Hell Creek Formation (Maastrichtian), Montana, USA. PLoS ONE
Khadri, S. F. R., Subbarao, K. V. & Thordarson, T. (2009). Determina- 6(2), e16574.
tion of rapid Deccan eruptions across the Cretaceous-Tertiary boundary using Huber, B. T., Norris, R. D. & MacLeod, K. G. (2002). Deep-sea paleotempera-
paleomagnetic secular variation: 2. Constraints from analysis of eight new ture record of extreme warmth during the Cretaceous. Geology 30, 123–126.
sections and synthesis for a 3500-m-thick composite section. Journal of Geophys- Hurlbert, S. H. & Archibald, J. D. (1995). No statistical support for sudden
ical Research 114, B06103. (or gradual) extinction of dinosaurs. Geology 23, 881–884.
Clemens, W. A., Archibald, J. D. & Hickey, L. M. (1981). Out with a whimper Ivanov, B. A. (2005). Numerical modeling of the largest terrestrial meteorite
not a bang. Paleobiology 7, 293–298. craters. Solar System Research 39, 381–409.
Colbert, E. H. (1961). Dinosaurs: their Discovery and their World. E. P. Dutton and Jay, A. E., Niocaill, C. M., Widdowson, M., Self, S. & Turner, W. (2009).
Co., New York. New palaeomagnetic data from the Mahabaleshwar Plateau, Deccan Flood
Courtillot, V. E. & Renne, P. R. (2003). On the ages of flood basalt events. Basalt Province, India: implications for the volcanostratigraphic architecture
Comptes Rendus Geoscience 335, 113–140. of continental flood basalt provinces. Journal of the Geological Society 166, 13–24.
Dessert, C., Dupre, B., François, L. M., Schott, J., Gaillardet, J., Chakra- Jiang, X.-J., Liu, Y.-Q., Ji, S.-A., Zhang, X.-L., Xu, L., Jia, S.-H., Lü, J.-C., Yuan,
pani, G. & Bajpai, S. (2001). Erosion of Deccan Traps determined by river C.-X. & Li, M. (2011). Dinosaur-bearing strata and K/T boundary in the
geochemistry: impact on the global climate and the 87Sr/86Sr ratio of seawa- Luanchuan-Tantou Basin of western Henan Province, China. Science China
ter. Earth and Planetary Science Letters 188, 459–474. Earth Sciences (doi:10.1007/s11430-011-4186-1 (2011)).
Dodson, P. (1996). The Horned Dinosaurs. Princeton University Press, Princeton. Keller, G. (2012). The Cretaceous-Tertiary mass extinction, Chicxulub impact,
Eberth, D. A., Evans, D. C., Brinkman, D. B., Therrien, F., Tanke, D. and Deccan volcanism. In Earth and Life (ed. J. A. Talent), pp. 759–793.
H. & Russell, L. S. (2013). Dinosaur biostratigraphy of the Edmonton Springer, New York.
Group (Upper Cretaceous), Alberta, Canada: evidence for climate influence. Koenig, A. E., Lucas, S. G., Neymark, L. A., Heckert, A. B., Sullivan, R. M.,
Canadian Journal of Earth Sciences 50, 701–726. Jasinski, S. E. & Fowler, D. W. (2012). Direct U-Pb dating of Cretaceous and
Evans, D. C., Schott, R. K., Larson, D. W., Brown, C. M. & Ryan, M. J. (2013). Paleocene dinosaur bones, San Juan Basin, New Mexico: COMMENT. Geology
The oldest North American pachycephalosaurid and the hidden diversity of 40, e262.
small-bodied ornithischian dinosaurs. Nature Communications 4, 1828 (doi: Kring, D. A. (2007). The Chicxulub impact event and its environmental conse-
10.1038/ncomms2749). quences at the Cretaceous-Tertiary boundary. Palaeogeography, Palaeoclimatol-
Fassett, J. E. (2009). New geochronologic and stratigraphic evidence confirms ogy, Palaeoecology 255, 4–21.
the Paleocene age of the dinosaur-bearing Ojo Alamo Sandstone and Animas Li, L. & Keller, G. (1998). Abrupt deep-sea warming at the end of the
Formation in the San Juan Basin, New Mexico and Colorado. Palaeontologia Cretaceous. Geology 26, 995–998.
Electronica 12(3A), 1–146. Lillegraven, J. A. & Eberle, J. J. (1999). Faunal changes through Lancian and
Fassett, J. E., Heaman, L. M. & Simonetti, A. (2011). Direct U-Pb dating Puercan time in southern Wyoming. Journal of Paleontology 73, 691–710.
of Cretaceous and Paleocene dinosaur bones, San Juan Basin, New Mexico. Lillegraven, J. A. & Ostresh, L. M. (1990). Late Cretaceous (earliest Campa-
Geology 39, 159–162. nian/Maastrichtian) evolution of western shorelines of the North American
Fastovsky, D. E., Huang, Y., Hsu, J., Martin-McNaughton, J., Sheehan, P. M. Western Interior Seaway in relation to known mammalian faunas. Geological
& Weishampel, D. B. (2004). Shape of Mesozoic dinosaur richness. Geology Society of America Special Papers 243, 1–30.
32, 877–880. Lloyd, G. T. (2012). A refined modelling approach to assess the influence of
Fastovsky, D. E., Huang, Y., Hsu, J., Martin-McNaughton, J., Sheehan, P. M. sampling on palaeobiodiversity curves: new support for declining Cretaceous
& Weishampel, D. B. (2005). Shape of Mesozoic dinosaur richness: comment dinosaur richness. Biology Letters 8, 123–126.
and reply. Geology 33, e74–e75. Lloyd, G. T., Davis, K. E., Pisani, D., Tarver, J. E., Ruta, M., Sakamoto, M.,
Fastovsky, D. E. & Sheehan, P. M. (2005). The extinction of the dinosaurs in Hone, D. W. E., Jennings, R. & Benton, M. J. (2008). Dinosaurs and the
North America. GSA Today 15, 4–10. Cretaceous terrestrial revolution. Proceedings of the Royal Society of London Series
Gates, T. A., Prieto-Márquez, A. & Zanno, L. E. (2012). Mountain building B 275, 2483–2490.
triggered Late Cretaceous North American megaherbivore dinosaur radia- Lofgren, D. L., Hotton, C. L. & Runkel, A. C. (1990). Reworking of
tion. PLoS ONE 7(8), e42135. Cretaceous dinosaurs into Paleocene channel deposits, upper Hell Creek
Godefroit, P., Golovneva, L., Shchepetov, S., Garcia, G. & Alekseev, P. Formation, Montana. Geology 18, 874–877.
(2009). The last polar dinosaurs: high diversity of latest Cretaceous arctic Longrich, N. R., Bhullar, B.-A. S. & Gauthier, J. A. (2012). Mass extinc-
dinosaurs in Russia. Naturwissenschaften 96, 495–501. tion of lizards and snakes at the Cretaceous-Paleogene boundary. Proceed-
Goldin, T. J. & Melosh, H. J. (2009). Self-shielding of thermal radiation by ings of the National Academy of Sciences of the United States of America 109,
Chicxulub impact ejecta: firestorm or fizzle? Geology 37, 1135–1138. 21396–21401.
Gradstein, F. M., Ogg, J. G., Schmitz, M. & Ogg, G. (2012). The Geologic Time Longrich, N. R., Tokaryk, T. T. & Field, D. J. (2011). Mass extinction of birds at
Scale 2012. Elsevier, Amsterdam. the Cretaceous-Paleogene (K-Pg) boundary. Proceedings of the National Academy
Grossman, E. L. (2012). Oxygen isotope stratigraphy. In The Geologic Time Scale of Sciences of the United States of America 108, 15253–15257.
2012 (eds F. M. Gradstein, J. G. Ogg, M. Schmitz and G. Ogg), pp. 181–206. Lucas, S. G., Sullivan, R. M., Cather, S. M., Jasinski, S. E., Fowler, D. W.,
Elsevier, Amsterdam. Heckert, A. B., Spielmann, J. A. & Hunt, A. P. (2009). No definitive evidence
of Paleocene dinosaurs in the San Juan Basin. Palaeontologia Electronica 12(8A), Russell, D. A. (1984). The gradual decline of the dinosaurs—fact or fallacy?
1–10. Nature 307, 360–361.
Luo, Z.-X. (2007). Transformation and diversification in early mammal evolu- Sant, D. A., Mathew, G., Khadkikar, A. S., Gogte, V. & Gundurao, T. K.
tion. Nature 450, 1011–1019. (2003). Co-existent cristobalite and iridium at 65 Ma, Anjar Intertrappeans,
Lyson, T. R., Bercovici, A., Chester, S. G. B., Sargis, E. J., Pearson, D. & Kachchh, western India. Cretaceous Research 24, 105–110.
Joyce, W. G. (2011). Dinosaur extinction: closing the ‘3 m gap’. Biology Letters Scannella, J. B. & Horner, J. R. (2010). Torosaurus Marsh, 1891, is Triceratops
7, 925–928. Marsh, 1889 (Ceratopsidae: Chasmosaurinae): synonymy through ontogeny.
MacLeod, N., Rawson, P. F., Forey, P. L., Banner, F. T., Boudagher-Fadel, Journal of Vertebrate Paleontology 30, 1157–1168.
M. K., Bown, P. R., Burnett, J. A., Chambers, P., Culver, S., Evans, S. E., Schulte, P., Alegret, L., Arenillas, I., Arz, J. A., Barton, P. J., Bown, P. R.,
Jeffery, C., Kaminski, M. A., Lord, A. R., Milner, A. C., Milner, A. R., Bralower, T. J., Christeson, G. L., Claeys, P., Cockell, C. S., Collins,
Morris, N., Owen, E., Rosen, B. R., Smith, A. B., Taylor, P. D., Urquhart, G. S., Deutsch, A., Goldin, T. J., Goto, K., Grajales-Nishimura, J. M.,
E. & Young, J. R. (1997). The Cretaceous-Tertiary biotic transition. Journal of et al. (2010). The Chicxulub asteroid impact and mass extinction at the
the Geological Society of London 154, 265–292. Cretaceous-Paleogene boundary. Science 327, 1214–1218.
Mallon, J. C., Evans, D. C., Ryan, M. J. & Anderson, J. S. (2012). Megaherbivo- Self, S., Widdowson, M., Thordarson, T. & Jay, A. E. (2006). Volatile
rous dinosaur turnover in the Dinosaur Park Formation (upper Campanian) fluxes during flood basalt eruptions and potential effects on the global
of Alberta, Canada. Palaeogeography, Palaeoclimatology, Palaeoecology 350-352, environment: a Deccan perspective. Earth and Planetary Science Letters 248,
124–138. 518–532.
Mannion, P. D., Upchurch, P., Carrano, M. T. & Barrett, P. M. (2011). Sereno, P. C. (1999). The evolution of dinosaurs. Science 284, 2137–2147.
Testing the effect of the rock record on diversity: a multidisciplinary approach Sheehan, P. M., Fastovsky, D. E., Barreto, C. & Hoffmann, R. G. (2000).
to elucidating the generic richness of sauropodomorph dinosaurs through Dinosaur abundance was not declining in a ‘3 m gap’ at the top of
time. Biological Reviews 86, 157–181. the Hell Creek Formation, Montana and North Dakota. Geology 28,
Marsh, O. C. (1882). Classification of the Dinosauria. American Journal of Science 523–526.
23, 81–86. Sheehan, P. M., Fastovsky, D. E., Hoffmann, R. G., Berghaus, C. B. &
Matsui, T., Imamura, F., Tajika, E., Nakano, Y. & Fujisawa, Y. (2002). Gabriel, D. L. (1991). Sudden extinction of the dinosaurs: family-level
Generation and propagation of a tsunami from the Cretaceous-Tertiary patterns of ecological diversity during the latest Cretaceous, upper Great
impact event. Geological Society of America Special Papers 356, 69–77. Plains, U.S.A. Science 254, 835–839.
Miller, K. G., Kominz, M. A., Browning, J. V., Wright, J. D., Mountain, G. Sheehan, P. M. & Hansen, T. A. (1986). Detritus feeding as a buffer to extinction
S., Katz, M. E., Sugarman, P. J., Cramer, B. S., Christie-Blick, N. & Pekar, at the end of the Cretaceous. Geology 14, 868–870.
S. F. (2005). The phanerozoic record of global sea-level change. Science 310, Slater, G. J. (2013). Phylogenetic evidence for a shift in the mode of
1293–1298. mammalian body size evolution at the Cretaceous-Palaeogene boundary.
Mitchell, J. S., Roopnarine, P. D. & Angielczyk, K. D. (2012). Late Creta- Methods in Ecology and Evolution 4, 734–744.
ceous restructuring of terrestrial communities facilitated the end-Cretaceous Sloan, R. E., Rigby, J. K., Van Valen, L. M. & Gabriel, D. L. (1986). Gradual
dinosaur extinction and simultaneous ungulate radiation in the Hell Creek
mass extinction in North America. Proceedings of the National Academy of Sciences
Formation. Science 234, 1173–1175.
of the United States of America 109, 18857–18861.
Smit, J. (1999). The global stratigraphy of the Cretaceous-Tertiary boundary
Nordt, L., Atchley, S. & Dworkin, S. (2003). Terrestrial evidence for two
impact ejecta. Annual Review of Earth and Planetary Sciences 27, 75–113.
greenhouse events in the latest Cretaceous. GSA Today 13, 4–9.
Smit, J. & Hertogen, J. (1980). An extraterrestrial event at the
Padian, K. & Chiappe, L. M. (1998). The origin and early evolution of birds.
Cretaceous-Tertiary boundary. Nature 285, 198–200.
Biological Reviews 73, 1–42.
Sullivan, R. M. (2006). The shape of Mesozoic dinosaur richness: a reassess-
Pearson, D. A., Schaefer, T., Johnson, K. R. & Nichols, D. J. (2001).
ment. New Mexico Museum of Natural History and Science Bulletin 35, 403–405.
Palynologically calibrated vertebrate record from North Dakota consistent
Tobin, T. S., Ward, P. D., Steig, E. J., Olivero, E. B., Hilburn, I. A.,
with abrupt dinosaur extinction at the Cretaceous-Tertiary boundary. Geology
Mitchell, R. N., Diamond, M. R., Raub, T. D. & Kirschvink, J. L. (2012).
29, 39–42.
Extinction patterns, 𝛿 18 O trends, and magnetostratigraphy from a southern
Pearson, D. A., Schaefer, T., Johnson, K. R., Nichols, D. J. & Hunter,
high-latitude Cretaceous-Paleogene section: links with Deccan volcanism.
J. P. (2002). Vertebrate biostratigraphy of the Hell Creek Formation in
Palaeogeography, Palaeoclimatology, Palaeoecology 350-352, 180–188.
southwestern North Dakota and northwestern South Dakota. Geological Society
Upchurch, P., Mannion, P. D., Benson, R. B. J., Butler, R. J. & Carrano,
of America Special Papers 361, 145–167. M. T. (2011). Geological and anthropogenic controls on the sampling of the
Peppe, D. J., Evans, D. A. D. & Smirnov, A. V. (2009). Magnetostratigraphy terrestrial fossil record: a case study from the Dinosauria. Geological Society of
of the Ludlow Member of the Fort Union Formation (Lower Paleocene) in London, Special Publication 358, 209–240.
the Williston Basin, North Dakota. Geological Society of America Bulletin 121, Vavrek, M. J. & Larsson, H. C. E. (2010). Low beta diversity of Maastrichtian
65–79. dinosaurs of North America. Proceedings of the National Academy of Sciences of the
Pope, K. O., Baines, K. H., Ocampo, A. C. & Ivanov, B. A. (1997). Energy, United States of America 107, 8265–8268.
volatile production, and climatic effects of the Chicxulub Cretaceous/Tertiary Vila, B., Oms, O., Fondevilla, V., Gaete, R., Galobart, A., Riera, V. &
impact. Journal of Geophysical Research 102, 21645–21664. Canudo, J. I. (2013). The latest succession of dinosaur tracksites in Europe:
Renne, P. R., Deino, A. L., Hilgen, F. J., Kuiper, K. F., Mark, D. F., Mitchell, hadrosaur ichnology, track production and palaeoenvironments. PLoS ONE
W. S., Morgan, L. E., Mundil, R. & Smit, J. (2013). Time scales of critical 8(9), e72579.
events around the Cretaceous-Paleogene boundary. Science 339, 684–687. Wang, S. C. & Dodson, P. (2006). Estimating the diversity of dinosaurs.
Renne, P. R. & Goodwin, M. B. (2012). Direct U-Pb dating of Cretaceous and Proceedings of the National Academy of Sciences of the United States of America 103,
Paleocene dinosaur bones, San Juan Basin, New Mexico: COMMENT. Geology 601–605.
40, e259. Weimer, R. J. (1984). Relation of unconformities, tectonics, and sea-level
Retallack, G. J., Leahy, G. D. & Spoon, M. D. (1987). Evidence from paleosols changes, Cretaceous of Western Interior, USA. Memoir of the American Associ-
for ecosystem changes across the Cretaceous/Tertiary boundary in eastern ation of Petroleum Geologists 36, 7–35.
Montana. Geology 15, 1090–1093. Weishampel, D. B., Dodson, P. & Osmólska, H. (2004). The Dinosauria. Second
Riera, V., Oms, O., Gaeta, R. & Galobart, A. (2009). The end-Cretaceous Edition. University of California Press, Berkeley.
dinosaur succession in Europe: the Tremp Basin record (Spain). Palaeogeogra- Wignall, P. B. (2001). Large igneous provinces and mass extinctions.
phy, Palaeoclimatology, Palaeoecology 283, 160–171. Earth-Science Reviews 53, 1–33.
Roberts, E. M., Deino, A. L. & Chan, M. A. (2005). 40Ar/39Ar age of the Wilf, P., Johnson, K. R. & Huber, B. T. (2003). Correlated terrestrial and
Kaiparowits Formation, southern Utah, and correlation of contemporaneous marine evidence for global climate changes before mass extinction at the
Campanian strata and faunas along the margin of the Western Interior Basin. Cretaceous-Paleogene boundary. Proceedings of the National Academy of Sciences
Cretaceous Research 26, 307–318. of the United States of America 100, 599–604.
Robinson, N., Ravizza, G., Coccioni, R., Peucker-Ehrenbrink, B. & Norris, Williams, M. E. (1994). Catastrophic versus noncatastrophic extinction of the
R. (2009). A high-resolution marine 187Os/188Os record for the late dinosaurs: testing, falsifiability, and the burden of proof. Journal of Paleontology
Maastrichtian: distinguishing the chemical fingerprints of Deccan volcanism 68, 183–190.
and the KP impact event. Earth and Planetary Science Letters 281, 159–168. Williamson, T. E., Brusatte, S. L., Carr, T. D., Weil, A. & Standhardt, B. R.
Royer, D. L. (2006). CO2-forced climate thresholds during the Phanerozoic. (2012). The phylogeny and evolution of Cretaceous-Paleogene metatherians:
Geochimica et Cosmochimica Acta 70, 5665–5675. new cladistic analysis and description of new early Paleocene specimens from
Royer, D. L. (2014). Atmospheric CO2 and O2 during the Phanerozoic: tools, the Nacimiento Formation, New Mexico. Journal of Systematic Palaeontology 10,
patterns, and impacts. Geochemistry Treatise (Second Edition) 6, 251–267. 625–651.
Wills, M. A., Briggs, D. E. G. & Fortey, R. A. (1994). Disparity as an XI. SUPPORTING INFORMATION
evolutionary index: a comparison of Cambrian and recent arthropods.
Paleobiology 20, 93–131.
Wilson, G. P. (2005). Mammalian faunal dynamics during the last 1.8 million Additional supporting information may be found in the
years of the Cretaceous in Garfield County, Montana. Journal of Mammalian
Evolution 12, 53–76. online version of this article.
Wilson, G. P. (2013). Mammals across the K/Pg boundary in northeast- File S1. Dataset and Fig. S1 showing Campanian and
ern Montana, U.S.A.: dental morphology and body-size patterns reveal Maastrichtian dinosaur occurrence records and rar-
extinction selectivity and immigrant-fueled ecospace filling. Paleobiology 39,
429–469. efied and Shareholder Quorum Subsampling diversity
Wolbach, W. S., Lewis, R. S. & Anders, E. (1985). Cretaceous extinctions: statistics.
evidence for wildfires and search for meteoritic material. Science 230, 167–170.
Wolfe, J. A. & Upchurch, G. R. (1987). North American nonmarine climates File S2. R file with data and code for Shareholder
and vegetation during the Late Cretaceous. Palaeogeography, Palaeoclimatology, Quorum Subsampling analysis.
Palaeoecology 61, 33–77.
(Received 5 December 2013; revised 7 June 2014; accepted 16 June 2014 )

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Biol. Rev. (2014), pp. 000–000.

The extinction of the dinosaurs

Key words: dinosaurs, end-Cretaceous, mass extinction, Cretaceous–Paleogene, extinctions, macroevolution,

* Address for correspondence (Tel: +44 01316506039; E-mail: [email protected]).

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

Epoch Age Ma Chron

10 15 20 30 34 38 42 46 19 23 27 7 11 15 7 11 15 5 45 85 0 3000 600 900 1200

Age Dinosaur species MAT Deccan Global sea

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

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