Did the dinosaur extinction lead to the evolution of larger mammals?

Photo by Mark Byzewski, image of Corral Bluffs

Editor's Introduction

Exceptional continental record of biotic recovery after the Cretaceous–Paleogene mass extinction

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Sixty-six million years ago, an asteroid impact triggered a mass extinction event, known as the K-Pg extinction, that killed off the planet’s dinosaurs. Fossils, discovered by Tyler Lyson et. al., revealed that following the K-Pg extinction, mammals evolved to fill the ecological niches no longer filled by dinosaurs. Using a well-preserved fossil record in Colorado, the researchers documented the evolution of larger mammals with unprecedented detail. What geological and biological events correlate with this increase in size? How might flowering plants and evolved teeth have resulted in the rise of mammals?

Paper Details

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Original title
Exceptional continental record of biotic recovery after the Cretaceous–Paleogene mass extinction
Original publication date
Vol. 366, Issue 6468, pp. 977-983
Issue name


We report a time-calibrated stratigraphic section in Colorado that contains unusually complete fossils of mammals, reptiles, and plants, and elucidates the drivers and tempo of biotic recovery during the poorly known first million years after the Cretaceous–Paleogene mass extinction (KPgE). Within ~100 thousand years (ka) post-KPgE, mammalian taxonomic richness doubled and maximum mammalian body mass increased to near pre-KPgE levels. A three-fold increase in maximum mammalian body mass and dietary niche specialization occurred at ~300 ka post-KPgE, concomitant with increased megafloral standing species richness. The appearance of additional large mammals occurred by ~700 ka post-KPgE, coincident with the first appearance of Leguminosae (bean family). These concurrent plant and mammal originations and body mass shifts coincide with warming intervals, suggesting climate influenced post-KPgE biotic recovery.



A stepwise recovery. After an asteroid wiped out much of life on Earth, mammals—responding to changes in plants—grew in size and diversity surprisingly quickly. (Graphic: Denver Museum of Nature & Science, Adapted by C. Bickel/Science).



The Cretaceous–Paleogene (K–Pg) boundary marks Earth’s most recent mass extinction, when over 75% of species, including non-avian dinosaurs, went extinct (1). In the terrestrial realm, the mass extinction was followed by a radiation of modern clades, particularly placental mammals (2), crown birds (3), and angiosperms (4). The drivers (58) and tempo (910) of the K–Pg mass extinction (KPgE) have been hotly debated and the patterns of terrestrial recovery in the first million years after the KPgE remain poorly understood. The extinction of all large-bodied vertebrates (5) undoubtedly impacted the post-KPgE taxonomic, ecologic, and body-mass diversification of various clades, but the lack of a well-studied fossil record has left the factors influencing ecosystem recovery unknown. Here we provide a detailed and temporally constrained terrestrial fossil record from this critical interval.

Fossils of terrestrial and freshwater organisms from the first million years after the KPgE are exceedingly rare worldwide, hindering our knowledge of post-KPgE taxonomic and ecological radiations. Thus far, the most fossiliferous sections from this time interval occur in the Williston, San Juan, Hanna, and Denver basins along the eastern margin of the Rocky Mountains in North America (1112). In all of these study areas, discontinuous outcrops result in composite stratigraphic sections, plant fossil localities are geographically widely spaced, vertebrate-bearing horizons are sparse and separated by long temporal gaps, complete vertebrate fossils are exceptionally rare, and age control is variable (1017). The Williston Basin has the most comprehensive fossil record with excellent age control, but the vertebrate specimens are fragmentary (101213). The San Juan Basin preserves a well-studied early Paleocene vertebrate record but does not record the K–Pg boundary itself (16). Moreover, overlying Paleocene rocks only contain two vertebrate fossil-bearing horizons within the first one million years post-KPgE (16). The Hanna Basin K–Pg section is rich in fragmentary vertebrate fossils, but has structurally complex strata and lacks a detailed chronostratigraphic framework (17). Finally, the Denver Basin has well-documented Cretaceous and Paleocene strata, a precisely dated K–Pg boundary, and abundant, geographically dispersed plant fossils, but, prior to this study, a sparse and fragmentary vertebrate fossil record (14151819).


Fig. S1 Study Area Map A map of the Denver Basin showing the locations of the four study areas discussed in the text. (Figure 1 from the research's Supplemental Materials).

Corral Bluffs Study Area, Denver Basin, Colorado, USA

We developed a new high-resolution stratigraphic framework in the Corral Bluffs study area, a single continuous (physically traceable) (~27 km2) outcrop from the Denver Basin that preserves the biotic recovery of a terrestrial ecosystem in the first million years post-KPgE (20) (Fig. 1 and fig. S1). This stratigraphy is tied to the Geomagnetic Polarity Time Scale (GPTS 2012) using paleomagnetics and a CA-ID-TIMS U-Pb-dated volcanic ash (20). For comparison, ages using an alternative age model based on work in the Denver Basin (18) are also provided in data files S1 to S14. The study area contains an exceptionally dense vertebrate (299 localities) and megafloral (65 localities) record with fossils occurring at more than 150 stratigraphic levels in the ~250 m thick sequence (Fig. 1). The extensive and nearly continuous outcrop belt spans the last ~100 thousand years (ka) of the Cretaceous and first ~1 Ma of the Paleocene. It includes four North American Land Mammal Age (NALMA) interval zones, four palynostratigraphic biozones, three magnetochron boundaries, two U-Pb radiometric dates, and the palynologically defined K–Pg boundary, yielding a locally derived, high-resolution chronostratigraphic framework (Fig. 1, figs. S2 to S5, and supplementary materials) (20). Together, these data provide an unprecedented opportunity to assess the biotic recovery of a terrestrial ecosystem following the KPgE.


Fig. 1 Temporally calibrated stratigraphic, floral, and faunal data for the K–Pg interval in the Corral Bluffs study area (fig. S1). Stratigraphy is tied to the Geomagnetic Polarity Time Scale (GPTS 2012) using paleomagnetics and a CA-ID-TIMS U-Pb-dated ash (italicized dates) (20) (data file S1 and figs. S3 and S5). The composite lithostratigraphic log (figs. S2 to S5) is dominated by intercalated mudstone and sandstone, reflecting a variety of fluvial facies. Pollen zones (data file S3) are defined by diversification of Momipites spp. (fossil juglandaceous pollen) (Fig. 3I). The K–Pg boundary is demarcated by the decrease in abundance of Cretaceous pollen taxa (labeled as “K-taxa”) without recovery, and subsequent fern (Cyathidites spp.) spike (data file S2). Relative abundance (%) of fern (Cyathidites spp.) and palm (Arecipites spp.) (Fig. 3E) palynomorphs increased dramatically post-KPgE (data file S2); note palm pollen percentages are offset from scale by 20%. Standing richness of dicot morphospecies or megafloral standing richness is exclusive of species that occur at a single locality (data files S4 to S7). Leaf-estimated mean annual temperature (LMAT) calibrated with East Asian forests (data file S8 and fig. S6). Pink horizontal bars indicate hypothesized warming intervals. Estimated leaf mass per unit area (data files S9 and S10 and fig. S7); shown with box plots that represent the distribution of species-site pair means for each 30-m bin starting from the K–Pg boundary (supplementary materials). Boxplots are placed along the y-axis near each bin’s stratigraphic midpoint, repositioned for visibility. See data file S11 and supplementary materials for placement of NALMAs. Tick marks next to GPTS, pollen zones, megafloral standing richness, and NALMAs show stratigraphic placement of samples and fossil localities (supplementary materials).
Left-hand scales

Question: Why was it important for the authors to find the paleomagnetic zones (labeled Chron in the figure) in their study area?

Answer: This was how the age of the plant and animal specimens collected could be determined.


The time scale on the left of the figure ranges from 66.50 million years ago to 64.96 million years ago. The K-Pg boundary crosses figure 1 at about 66 million years ago. Next to the time scale is a record of the paleomagnetic samples collected and the associated changes in Earth’s magnetic poles, followed by a bar labeled with an Ash bed scale. This is a record of sediments deposited by water from pre- and post–K-Pg.

NALMA and pollen zones

Question: Notice the yellow and green vertical bars (almost acting as bookends of the graph). What is the difference between what is represented by the Wodehouseia spinata Zone, P1, P2, P3 and the Lancian, Puercan 1, Puercan 2, Puercan 3 axes?

Answer: The Wodehouseia spinata Zone, P1, P2, P3 axis on the left indicates the time frame for different pollen and spore zones. The Lancian, Puercan 1, Puercan 2, Puercan 3 axis on the right indicates the time frame for different North American Land Mammal Ages.



The pollen zones axis starts with the Wodehouseia spinata zone and moves upward through three different pollen zones. The Wodehouseia spinata zone in the United States and Canada marks the uppermost stage of the Cretaceous period/Mesozoic era. This zone is named for the most abundant pollen samples seen in those rock layers. The tick marks to the left of the axis bar indicate the age of the rock from which pollen samples were collected. There are a total of 11 Cretaceous and 54 Paleocene localities.


The black lines and black circles represent pollen samples collected from various members of the walnut hickory family, specifically Momipites. Diversification of Momipites defined the pollen zones (indicated in yellow on the left).


Question: Why are the lines of the Momipites species different lengths? What does this difference in line length indicate?

Answer: As time passed, environmental conditions changed, niches opened, and Momipites evolved, eventually forming new genera filling open niches.

Pollen samples

The green line represents fern (Cyathidites spp.) pollen and the orange line indicates palm (Arecipites spp.) pollen. The datapoint circles indicate the age of the rock layers in which the pollen was found. In order to show both the fern and palm pollen spikes on the same axis, the authors note that the palm percentages start at 20% instead of 0%. The first palm datapoint circles (located between 66.500 and 66.398) indicate a relative abundance of about 30%, and the abundance of fern pollen at this time is about 10%.

Box plots

The green rectangles on the right-hand side of the figure are box plots. A box plot is a graphical representation of the concentration and spread of data. One box plot is constructed from five values: the minimum data value, the first quartile, the median value, the third quartile, and the maximum data value. To find the quartiles, the data are arranged from least to greatest, the median of the dataset is found by determining the middle value (dividing the data into halves), and the quartiles are determined by finding the median of the two halves. The spread of the data is shown through the horizontal distance between the smallest and largest value. The lines (sometimes called “whiskers”) extending outside the box indicate the variability outside the upper and lower quartiles.

During Puercan 2 (about 65.688 Ma), the box plot indicates the greatest leaf mass. Note that this is in a warming trend and that there is a spike in palm pollen.


Question: Which box plot shows the greatest uncertainty?

Answer: The one located at the boundary between Puercan 1 and 2. The error bars are greater than for any of the other box plots.

Vertebrate fossils in the Corral Bluffs succession are unusually complete for this time period, and are found in a range of depositional environments, and represent a diversity of taxa and body sizes (Figs. 1 and 2). Most are three-dimensionally preserved in hydroxyapatite concretions and are found in all observed facies, often as articulated skeletons or skulls with intact delicate structures such as middle ear and hyoid elements (Fig. 2). Among vertebrate specimens preserved in concretions, mammalian, turtle, and crocodilian crania (Fig. 2, A to T) and turtle shells (Fig. 2, U to X) are most common. Individual fossils range in size from ~3 mm2 (isolated teeth) to larger forms such as 1.5 m-long, articulated crocodilian skeletons. Plant fossils also span the size spectrum across all observed facies, including microscopic palynomorphs as well as seeds, leaves, roots, branches, and in situ saplings, and large stumps and logs (Fig. 3).


Fig. 2 Representative selection of vertebrate fossils. (A to R) Crania in dorsal and ventral views of Eoconodon coryphaeus [(A) and (B); DMNH.EPV.130976], Ectoconus ditrigonus [(C) and (D); DMNH.EPV.130985], Loxolophus sp. [(E) and (F); DMNH.EPV.132501], juvenile Ectoconus ditrigonus [(G) and (H); DMNH.EPV.132515], Carsioptychus coarctatus [(I) and (J); DMNH.EPV.95283], Taeniolabis taoensis [(K) and (L); DMNH.EPV.95284], cf. Navajosuchus [(M) and (N); DMNH.EPV.48541], Axestemys infernalis [(O) and (P); DMNH.EPV.132514], Palatobaena sp. [(Q) and (R); DMNH.EPV.134081], and (S and TCedrobaena putorius (DMNH.EPV.130982). (U to X) Turtle shells in dorsal and ventral views of Gilmoremys sp. [(U) and (V); DMNH.EPV.95454] and Hoplochelys sp. [(W) and (X); DMNH.EPV.95453]. All crania and shells to scale except for (W) and (X), which are scaled 1:2 compared to other specimens (10-cm scale bar).

Figure S1 (shown as a supplementary resource earlier in the paper) shows where these fossils were collected. These fossils made it possible to estimate the body mass of the post K-Pg animals. The teeth and cranial size were the primary sources of data used in body mass estimates in this study.

Tooth structure

Question: Based on the tooth structure of specimen D (Ectoconus ditrigonus), was it an herbivore or a carnivore?

Answer: Ectoconus ditrigonus was a terrestrial herbivore, about the size of a sheep.


Fossils can be extraordinarily fragile, yet encased in hard rock. Identifying, collecting, revealing, and studying fossils are all important aspects of a paleontologist’s work. The American Museum of Natural History has an extensive amount of information about fossil collecting and fossil preparation. Learn more on their Paleontology Portal.



Fig. 3 Representative selection of plant fossils. (A) In situ tree stump. (B to E) Palm fossils—in-situ stump (B), frond (C), flower (D; DMNH.EPI.45594), and Arecipites sp. pollen grain (E). (F and G) Most common smooth and toothed dicot morphospecies—(F) “Rhamnus” goldiana (DMNH.EPI.52262) and (G) Platanites marginata (DMNH.EPI.23281). (H and I) Walnut family flower and pollen—Cyclocarya sp. (DMNH.EPI.52272) and Momipites tenuipolus pollen grains preserved as a dyad (H). (J) Legume seedpod (DMNH.EPI.45540). (K) Legume leaflet (DMNH.EPI.45576). Rock hammer handle = 38 cm in (A) to (C); (D), flower is 5 mm wide; (E), pollen grain is 42 μm long; (I), each pollen grain has a 20 μm diameter; leaflet in (K) is scaled 2:1 compared to (J) (5-cm scale bar).
Sizing specimens

In these photos, the size of the specimens in A, B, and C is compared to a known object, a rock hammer measuring 38 cm. Knowing the size of the rock hammer provides an idea of scale and dimension. Specimen J is shown alongside a physical 5-cm scale bar. Different scale bars are shown as size references in F, G, and H. The size of pollen grains (E and I) is provided. These are all techniques used by scientists when providing information about the size of objects.

LMA traits

Leaf mass per unit area (LMA) for different plant species was calculated in this study. Leaves with low LMA are known to be thin and have high rates of photosynthesis, short lifespans, and high nutritional value. Leaves with high LMA are thick and have low rates of photosynthesis, long lifespans, and low nutritional value. Legumes are known to be nutrient rich.


Question: A narrow legume pod is shown in J and a leaflet in K. Upon close analysis, what traits would you expect the legume to exhibit? Why?

Answer: It would be thin and fragile and have a high rate of photosynthesis, a short lifespan, and high nutritional value. The legume pod and leaflet have a low LMA.

Plant evolution

The plant species pictured in Figure 3 were able to flourish and evolve following the extinction of many Cretaceous plant species. As a result of the asteroid impact, terrestrial habitats were greatly altered. This resulted in many plant groups, including pine, spruce, and fir trees, suffering a loss in diversity. They were not adapted to the new physical environment.

Not as many flowering plant groups suffered. Above the K-Pg boundary, flowering plants, such as those pictured in Figure 3, underwent a rapid increase in diversity. They adapted to and filled niches vacated by extinct plant species.

Why plants?

Question: If the researchers were looking for data to support that mammals increased in body mass after the K-Pg extinction event, why were they interested in what was happening at the same time with plant species?

Answer: Photosynthesis is the process that converts the sun’s energy into chemical energy. Animals rely on photosynthetic organisms, primarily plants in a terrestrial ecosystem, as a source of nutrients and energy. If plants were becoming more nutrient- and energy-rich, they would support greater numbers of mammals with larger body masses.

We recognize sixteen mammalian taxa, eight of which are based on cranial remains, including the first occurrence of the late Puercan (Pu3) index taxon Taeniolabis taoensis (Fig. 2, K and L) from the Denver Basin. Cranial size and lower first molar area were used to estimate mammalian body mass – an important feature that impacts many aspects of the biology and ecology of mammals (Fig. 4) (21). Given that there appears to be bias toward large vertebrates in our dataset (supplementary materials and data file S11), we focused on maximum mammalian body mass. The largest bodied mammals disappear at the K–Pg boundary (10) and returned to near pre-KPgE levels within 100 ka after the K–Pg boundary (Fig. 4). Subsequent shifts in maximum mammalian body mass occurred at the Pu1/Pu2 and near the Pu2/Pu3 transitions, ~300 and ~700 ka post-KPgE, respectively (Fig. 4). In addition, the pattern and abundance of vertebrates preserved in all paleoenvironments suggest that by ~700 ka post KPgE the largest mammals (25+ kg) were spatially partitioned across the landscape. We observe a strong pattern of association between taxa and facies (Fig. 4) indicating that baenid turtles (Fig. 2, Q to T) and Taeniolabis taoensis (Fig. 2, K and L) lived in or near river channel margins whereas chelydroid turtles (Fig. 2, W and X) and the large periptychid mammals Ectoconus ditrigonus (Fig. 2, C, D, G, and H) and Carsioptychus coarctatus (Fig. 2, I and J) primarily occupied distal portions of the floodplain (Fig. 4).


Fig. 4 Timeline of expansion of maximum body mass and niche space in earliest Paleocene mammals correlated with diversification and origination of key plant groups and warming intervals. Post-KPgE “disaster” ecosystems occur for less than 100 ka, ecosystem “recovery” occurs between ~100–300 ka, and overall post-KPgE ecosystem equilibrium occurs within ~300 ka. Mammalian body mass estimated based on cranial and lower first molar dimensions of specimens recovered from Pu1–Pu3 intervals (data files S13 and S14 and figs. S8 and S9). Data from Corral Bluffs study area (yellow) except for Pu1 mammals, which come from adjacent outcrops in the Denver Basin (West Bijou (no fill; orange), South Table Mountain (blue), and Alexander Locality (green)) and Didelphodon from North Dakota (red) (data files S13 and S14 and supplementary materials). Not plotted is distribution of other large (10–100+ kg) vertebrates (e.g., turtles, crocodilians, dinosaurs) found throughout the section (Fig. 1). Pink, blurred horizontal bars represent hypothesized warming intervals interpreted from LMAT. Niche partitioning graph showing environmental distribution of vertebrate groups (data file S12): CarsioptychusEctoconus, and chelydroid turtles predominantly associated with floodplain and ponded water facies; baenid turtles and Taeniolabis predominantly in river channel complexes and proximal to medial crevasse splay facies. FAD = first appearance datum.

Natural selection drives competing species into different niches. Over time, each species develops different patterns of resource use. This results in a change in their ecological niches, reduces competition, and allows for successful coexistence.


Question: Eoconodon (cranium 7) and Taeniolabis (cranium 8) coexisted during the Puercan 3 (700,000 to 1 Ma). Examine the illustrations of their skills and also their photographs in Figure 1, Eoconodon in 1A and 1B, and Taeniolabis in 1K and 1L. How can you tell that these mammals did not compete for food?

Answer: Eoconodon appears to have large, sharp canines. Its tooth structure and arrangement indicate that it was carnivorous. Taeniolabis has fewer teeth and lacks pronounced canines. Its large incisors appear to be better suited for shearing off plant leaves.


Question: Why is it important to indicate where warming trends occurred? How are these trends related to the rise of mammals?

Answer: With each warming trend, the diversity of plants and mammals increases. The change in the physical environment, temperature, sunlight, precipitation, etc., favored different variations and opened new niches.


As plant species evolved, so did the animals that fed on them. Animals that had specialized diets pre-KPgE could not find food after the asteroid impact. During the initial “disaster” ecosystems period, animals that were generalists were still able to eat. Later into the recovery period (shown on the right-hand brown bar labeled “Post-KPgE timeline” in Figure 4), plants became more diversified. Eventually, some mammal species became specialists, resulting in body mass increases in some species.

We recognize 233 plant morphospecies in our study area (supplementary materials). Despite lower sampling of Cretaceous strata (11 Cretaceous localities vs. 54 Paleocene localities), richness of dicotyledonous (dicot) leaf morphospecies from raw species counts at localities in the last ~100 ka of the Cretaceous (-18–0 m; 7 localities, 777 specimens, most speciose locality n = 31) and the first ~100 ka of the Paleocene (0–20 m; 6 localities, 1,019 specimens, most speciose locality n = 13) indicates that earliest Paleocene dicot diversity was less than half that of the latest Cretaceous (fig. S6). Additionally, 46% of Cretaceous dicot leaf morphospecies that occur at more than one site do not occur in any of our Paleocene localities. A comparable study with similar time bins from the Williston Basin estimated 57% extinction in dicot leaf morphospecies at the KPgE (22). Leaf mass per area (LMA), a proxy for carbon investment and ecological strategy in plants (23), decreased in both maximum and minimum values across the K–Pg boundary (Fig. 1 and fig. S7) consistent with a shift to faster growth strategies. Megafloral standing richness and LMA are lowest in the earliest Paleocene, but exceed pre-KPgE levels within ~300 ka (Fig. 1 and fig. S7).

Following the KPgE, many angiosperm clades diversified (4). The Corral Bluffs section preserves the oldest known occurrence of the Leguminosae, or bean family, as evidenced by fossil seedpods and leaflets dated to 65.35 Ma (Fig. 3, J and K). The oldest previously recognized legume (24) is based on wood and leaflets (25) from early Paleocene rocks of Argentina (26), whereas the earliest legume seedpods are not recognized until the late Paleocene (~58 Ma) of Colombia (27). Our discovery supports (i) a nearly synchronous first appearance of legumes in North America and southern South America; (ii) a rapid diversification for the group in the earliest Paleocene (24); and (iii) their apparent origination in the Western Hemisphere.

Relative changes in leaf-estimated mean annual temperature (LMAT) (Fig. 1, fig. S6, and supplementary materials) from our section track paleotemperature proxies from sections elsewhere in the world. Corral Bluffs experienced a 4.6 °C cooling (22.1 ± 2.7 °C 1SE to 17.5 ± 3.4 °C 1SE) during the last ~100 ka of the Cretaceous, comparable to cooling estimates derived from LMAT (28) and carbonate-clumped isotopes (29) from the Williston Basin, and δ18O of benthic foraminifera from the South Atlantic (30). For the first time, we corroborate (31) a warm interval immediately post-K–Pg in a terrestrial section. Here we observe a 5.1 °C warming event (17.5 ± 3.4 °C 1SE to 22.6 ± 3.5 °C 1SE) occurred from the K–Pg boundary through the first ~60 ka of the Paleocene, similar to the ~5 °C in ~100 ka warming pulse inferred from δ18O of phosphatic fish scales from the El Kef K–Pg section of Tunisia (31). A second ~150 ka interval (65.80–65.65 Ma) shows an initial warming of 2.2 °C (21.1 ± 3.3 °C 1SE to 23.3 ± 2.9 °C 1SE) over ~30 ka, sustained temperatures for ~50 ka, and then 3.0 °C cooling (22.7 ± 2.8 °C 1SE to 19.7 ± 3.1 °C 1SE) over ~70 ka at the top of magnetochron C29r. This event corresponds with the Danian C2 carbon isotopic excursion and inferred warming interval observed in marine (32) and terrestrial (33) strata. Sampling between these warming intervals is limited and an alternative hypothesis is a general warming trend from the K–Pg boundary to the magnetochron C29r/29n boundary. A third 2.9–3.2 °C warming pulse (18.0 ± 3.3 °C 1SE to 20.9 ± 3.0 °C 1SE to 17.7 ± 3.5 °C 1SE) over ~10 ka is tentatively recognized ~700 ka post-KPgE.


Paleotemperature and Ecosystem Recovery

The timing of these warming intervals corresponds with changes in plant richness and taxonomic composition and, likely due to additional food sources, coincident shifts in mammalian taxonomic composition, ecologic diversification, and expansion in the range of maximum mammalian body mass (Fig. 4). A mammalian taxonomic increase has been documented elsewhere in the Denver Basin, within the first 100 ka of the Paleocene, from nine species found in the earliest Pu1 faunas to 21 species found in later Pu1 faunas (3435). Maximum mammalian body mass increased through this interval to near pre-KPgE levels, from the largest known Lancian mammal (~8 kg) to the largest known Pu1 mammal (~6 kg), coincident with the first post-KPgE warming episode (Fig. 4 and figs. S8 and S9). The Pu1/Pu2 transition occurred ~300 ka after the KPgE and was marked by the appearance of varied and large (20+ kg) periptychid mammals. The appearance of larger-bodied periptychid mammals, particularly the herbivorous, hard-object feeder Carsioptychus coarctatus (Fig. 2, I and J) (3738), marks a notable dietary niche specialization in the earliest Paleocene moving from the largely omnivorous/insectivorous diet found in Pu1 mammals (39) to a more herbivorous diet found in some Pu2 mammals. This dietary shift is correlated with a three-fold increase in maximum mammalian body mass compared to Pu1 faunas (Figs. 1 and 4 and figs. S8 and S9). The Pu1/Pu2 transition was coincident with the onset of a high plateau in megafloral standing richness, an increase of LMA beyond pre-KPgE levels, a doubling of the diversity of Momipites spp. [fossil juglandaceous (walnut family) pollen (Fig. 3I)], and the second early Paleocene warming interval (Figs. 1 and 4). The diversification of Juglandaceae taxa with small, winged seeds to later taxa with larger wingless seeds is hypothesized to reflect a transition from wind to animal transport (36). This hypothesis is supported by the close correlation between diversification reflected in fossil juglandaceous pollen and the appearance of several large herbivorous periptychid mammals whose specialized and enlarged premolars are thought to be for hard-object feeding (3738). Finally, the appearance of legumes co-occurred with a tentatively recognized short warming pulse and shift in maximum mammalian body mass. Specifically, two large-bodied mammals appear within ~700 ka post-KPgE (Fig. 4) – the herbivorous multituberculate Taeniolabis taoensis (~34 kg) and the omnivorous triisodontid archaic ungulate Eoconodon coryphaeus (~47 kg) (Fig. 2, A and B). These data suggest that earliest Paleocene warming pulses may have played an important role in post-KPgE ecosystem recovery, perhaps by facilitating immigration and/or in situ co-evolution of flora and fauna.

The transition from an ecosystem characterized by a small-bodied mammalian fauna, post-“disaster” ferns, and low diversity plant communities to one exhibiting a larger-bodied mammalian fauna and more ecologically and taxonomically complex forests mirrors modern post-disaster ecological successions, but on a much longer timescale (typically 104–105 years for recoveries from global mass extinctions versus 10–102 years for modern local-regional ecological recoveries) (40). The overall and long-term recovery we observe has recently been described as an aspect of “Earth system succession” (40). This concept proposes that global ecological succession following mass extinctions is intrinsically paced by the interactions of the biosphere and geosphere, both of which may be knocked out of equilibrium (40). The low-diversity, small-bodied mammalian fauna and low-diversity forests dominated by ferns and palms, often indicative of ecological disequilibrium, suggest that a period of ecosystem disequilibrium lasted for up to ~100 ka post-KPgE in our research area. A period of ecosystem “recovery” followed ~100 – 300 ka post-KPgE when megafloral diversity steadily increased. At ~300 ka post-KPgE we see several additional signs of ecosystem “recovery”, including i) the increase and then plateau of megafloral standing richness; ii) LMA exceeding pre-KPgE levels; iii) diversification of Juglandaceae, a potentially energy-rich food source for mammals; and iv) the first significant taxonomic diversification, dietary specialization (e.g., increased herbivory), and increase in maximum body mass of mammals (Pu1/Pu2). Finally, spatial niche partitioning, appearance of several additional large (30+kg) mammals, and expansion of mammalian body mass disparity continues through ~700 ka at the Pu2/Pu3 boundary, all further indications of ecosystem “recovery.” These changes are correlated with the arrival of plant taxa (e.g., legumes) that would have offered mammals new calorie-dense food sources. Taken together, our record places time estimates on the patterns of biotic recovery in Earth system succession and demonstrates that several aspects of ecosystem “recovery” occurred within ~300 ka post-KPgE (Fig. 3).

The pattern of warming pulses correlated with biotic change during the earliest Paleocene demonstrates a strong relationship between the biosphere and geosphere. The Deccan Traps of the Indian subcontinent represent repeated and voluminous volcanic eruptions (>106 km3 of magma) during the post-KPgE Earth system succession (67). These eruptions might have induced warming pulses via the release of greenhouse gases (e.g., CO2) (7). Recent work on the timing of these eruptions (67) places ~70% of the total volume within the 300–400 ka window roughly coincident with the earliest Paleocene warming pulse(s) observed at Corral Bluffs and the temporally correlated shifts in biotic recovery (Figs. 1 and 4). Although not a feedback of the biosphere-geosphere system, Deccan eruptions likely influenced atmospheric chemistry, in turn shaping Earth system succession and post-KPgE ecosystem recovery (Fig. 4). Detailed records of post-mass extinction biotic recovery, such as the one presented here, will provide a critical framework for predicting ecosystem recovery following mass extinction events including the one we currently face (41).




Materials and Methods

Supplementary Text

Figs. S1 to S9

Table S1

Data Files S1 to S14


References (42123)



1. D. M. Raup, J. J. Sepkoski Jr., Science 215, 1501-1503 (1982).

2. M. A. O'Leary et al.Science 339, 662-667 (2013).

3. R. O. Prum et al., Nature 526, 569-573 (2015).

4. S. Magallón, L. L. Sánchez-Reyes, S. L. Gómez-Acevedo, Ann. Bot. 123, 491-503 (2019).

5. P. Schulte et al., Science 327, 1214-1218 (2010).

6. B. Schoene et al.Science 363, 862-866 (2019).

7. C. J. Sprain et al., Science 363, 866-877 (2019).

8. J. D. Archibald et al., Science 328, 973, author reply 975-976 (2010).

9. D. A. Pearson et al., "Vertebrate biostratigraphy of the Hell Creek formation in southwestern North Dakota and northwestern South Dakota" in The Hell Creek Formation and the Cretaceous-Tertiary Boundary in the Northern Great Plains: An Integrated Continental Record of the End of the Cretaceous (Geological Society of America Special Paper, vol. 361, 2002), pp. 145-167.

10. G. P. Wilson, "Mammalian extinction, survival, and recovery dynamics across the Cretaceous-Paleogene boundary in northeastern Montana, USA" in Through the End of the Cretaceous in the Type Locality of the Hell Creek Formation in Montana and Adjacent Areas (Geological Society of America Special Paper, ed. 503, 2014), pp. 365-392.

11. D. J. Nichols, K. R. Johnson, Plants and the K-T boundary, (Cambridge University Press, MA, 2008).

12. D. L. Lofgren et al., "Paleocene biochronology in the Puercan through Clark-forkian Land Mammal Ages" in Late Cretaceous and Cenozoic Mammals of North American: Biostratigraphy and Geochronology, (Columbia University Press, New York, New York, 2004), pp. 43-105.

13. K. R. Johnson, "Megaflora of the Hell Creek and lower Fort Union Formations in the western Dakotas: vegetational response to climate change, the Cretaceous-Tertiarty boundary event, and rapid marine transgression" in The Hell Creek Formation and the Cretaceous-Tertiary Boundary in the Northern Great Plains: An Ingegrated Continental Record of the End of the Cretaceous, (Geological Society of America Special Paper, vol. 361, 2002), pp. 329-391.

14. R. G. Raynolds, K. R. Johnson, Rocky Mt. Geol. 38, 171-181 (2003).

15. J. J. Eberle, Rocky Mt. Geol. 38, 143-169 (2003).

16. T. E. Williamson, The Beginning of the Age of Mammals in the San Juan Basin, New Mexico: Biostratigraphy and Evolution of Paleocene Mammals of the Nacimiento Formation (New Mexico Museum of Natural History and Science Bulletin ed. 8, 1996).

17. J. A. Lillegraven, J. J. Eberle, J. Paleontol. 73, 691-710 (1999).

18. W. C. Clyde et al., Earth Planet. Sci. Lett. 452, 272-280 (2016).

19. M. Deschesne, R. G. Raynolds, P. E. Barkmann, K. J. Johnson, "Denver Basin Geologic Maps: Bedrock Geology, Structure and Isopach Maps of the Upper Cretaceous through Paleogene Strata between Greeley and Colorado Springs, Colorado," Colorado Geological Survey, 15 (2011).

20. A. J. Fuentes et al., Constructing a timescale of biotic recovery across the Cretaceous-Paleogene boundary, Corral Bluffs, Denver Basin, Colorado. bioRxiv:10.1101/636951 (2019).

21. S. S. Hopkins, "Estimation of body size in fossil mammals" in Methods in Paleoecology: Reconstructing Cenozoic Terrestrial Environments and Ecological Communities (Springer, 2018), pp. 7-22.

22. P. Wilf, K. R. Johnson, Paleobiology 30, 347-368 (2004).

23. B. Blonder et al.PLOS Biol. 12, e1001949 (2014).

24. M. Lavin, P. S. Herendeen, M. F. Wojciechowski, Syst. Biol. 54, 575-594 (2005).

25. M. Brea et al.Alcheringa32, 427-441 (2008).

26. E. E. Comer et al.Palaios 30, 553-573 (2015).

27. S. L. Wing et al.Proc. Natl. Acad. Sci. U.S.A. 106, 18627-18632 (2009).

28. P. Wilf, K. R. Johnson, B. T. Huber, Proc. Natl. Acad. Sci. U.S.A. 100, 599-604 (2003).

29. T. S. Tobin, G. P. Wilson, J. M. Eiler, J. H. Hartman, Geology 42, 351-354 (2014).

30. J. S. K. Barnet et al., Geology 46, 147-150 (2017).

31. K. G. MacLeod, P. C. Quinton, J. Sepúlveda, M. H. Negra, Science 360, 1467-1469 (2018).

32. F. Quillévéré, R. D. Norris, D. Kroon, P. A. Wilson, Earth Planet. Sci. Lett. 265, 600-615 (2008).

33. I. Gilmour et al., Geology 41, 783-786 (2013).

34. E. L. Dahlberg, J. J. Eberle, J. J. Sertich, I. M. Miller, Rocky Mt. Geo. 51, 1-22 (2016).

35. M.D. Middelton, E. W. Dewar, "New Mammals from the early Paleocene Littleton fauna (Denver Formation, Colorado)" in Paleogene Mammals (New Mexico Museum of Natural History and Science Bulletin, vol. 26, 2004), pp. 59-80.

36. K. D. Rose, The Beginning of the Age of Mammals. (Johns Hopkins University Press, Baltimore, Maryland, 2006).

37. J. D. Archibald, "Archaic undulates ("Condylarthra")" in Evolution of Tertiary Mammals of North America: Volume 1: Terrestrial Carnivores, Ungulates, and Ungulate Like Mammals. (Cambridge University Press, MA, 1998).

38. E. W. Dewar, PaleoBios 23, 1-19 (2003).

39. B. H. Tiffney, Ann. Mo. Bot. Gard. 71, 551-576 (1984).

40. P. Hull, Curr. Biol. 25, R941-R952 (2015).

41. A. D. Barnosky et al., Nature 471, 51-57 (2011).