RESEARCH

PALEONTOLOGY paleomagnetics and chemical abrasion iso- tope dilution thermal ionization mass spec- Exceptional continental record of biotic recovery trometry (CA-ID-TIMS) U-Pb-dated volcanic ash (20). For comparison, ages using an al- after the –Paleogene mass extinction ternative age model based on work in the Denver Basin (18) are also provided in data S1 T. R. Lyson1*, I. M. Miller1, A. D. Bercovici1,2, K. Weissenburger1, A. J. Fuentes3, W. C. Clyde3, to S14. The study area contains an exceptionally J. W. Hagadorn1, M. J. Butrim4, K. R. Johnson2, R. F. Fleming1, R. S. Barclay2, dense vertebrate (299 localities) and megafloral S. A. Maccracken2,5, B. Lloyd6, G. P. Wilson7, D. W. Krause1,8, S. G. B. Chester9,10,11 (65 localities) record, with fossils occurring at >150 stratigraphic levels in the ~250-m-thick We report a time-calibrated stratigraphic section in Colorado that contains unusually complete sequence (Fig. 1). The extensive and nearly con- fossils of mammals, , and plants and elucidates the drivers and tempo of biotic recovery tinuous outcrop belt spans the last ~100 thou- during the poorly known first million years after the Cretaceous–Paleogene mass extinction sand years (ka) of the Cretaceous and the first (KPgE). Within ~100 thousand years (ka) post-KPgE, mammalian taxonomic richness doubled, ~1 million years (Ma) of the Paleocene. It in- and maximum mammalian body mass increased to near pre-KPgE levels. A threefold increase in cludes four North American Land Mammal maximum mammalian body mass and dietary niche specialization occurred at ~300 ka post-KPgE, Age (NALMA) interval zones, four palynostra- concomitant with increased megafloral standing species richness. The appearance of additional tigraphic biozones, three magnetochron bound- large mammals occurred by ~700 ka post-KPgE, coincident with the first appearance of Leguminosae aries, two U-Pb radiometric dates, and the (the bean family). These concurrent plant and mammal originations and body-mass shifts coincide palynologically defined K–Pg boundary, yield- with warming intervals, suggesting that climate influenced post-KPgE biotic recovery. ing a locally derived, high-resolution chrono- Downloaded from stratigraphic framework (Fig. 1, figs. S2 to S5, and supplementary materials) (20). Together, he Cretaceous–Paleogene (K–Pg) bound- separated by long temporal gaps, complete ver- these data provide an unprecedented opportu- ary marks Earth’s most recent mass ex- tebrate fossils are exceptionally rare, and age nity to assess the biotic recovery of a terrestrial tinction, when >75% of species, including control is variable (10–17). The Williston Basin ecosystem after the KPgE. T nonavian dinosaurs, went extinct (1). In has the most comprehensive fossil record with Vertebrate fossils in the Corral Bluffs suc- http://science.sciencemag.org/ the terrestrial realm, the mass extinction excellent age control, but the vertebrate speci- cession are unusually complete for this time was followed by a radiation of modern clades, mens are fragmentary (10, 12, 13). The San Juan period, are found in a range of depositional particularly placental mammals (2), crown Basin preserves a well-studied early Paleocene environments, and represent a diversity of birds (3), and angiosperms (4). The drivers vertebrate record but does not record the taxa and body sizes (Figs. 1 and 2). Most are (5–8)andtempo(9, 10)oftheK–Pg mass K–Pg boundary itself (16). Moreover, overlying three-dimensionally preserved in hydroxy- extinction (KPgE) have been hotly debated, Paleocene rocks only contain two vertebrate apatite concretions and are found in all ob- and the patterns of terrestrial recovery in the fossil–bearing horizons in the first 1 million served facies, often as articulated skeletons first million years after the KPgE remain poorly years post-KPgE (16). The Hanna Basin K–Pg or skulls with intact delicate structures such as understood. The extinction of all large-bodied section is rich in fragmentary vertebrate middle ear and hyoid elements (Fig. 2). Among

vertebrates (5) undoubtedly affected the post- fossils but has structurally complex strata vertebrate specimens preserved in concretions, KPgE taxonomic, ecologic, and body-mass di- and lacks a detailed chronostratigraphic mammalian, , and crocodilian crania on November 21, 2019 versification of various clades, but the lack of framework (17). Finally, the Denver Basin (Fig. 2, A to T) and turtle shells (Fig. 2, U to X) a well-preserved fossil record has left the fac- has well-documented Cretaceous and Paleo- are the most common. Individual fossils range tors influencing ecosystem recovery unknown. cene strata, a precisely dated K–Pg bound- in size from ~3 mm2 (isolated teeth) to larger Here, we provide a detailed and temporally ary, and abundant, geographically dispersed forms such as 1.5-m-long, articulated crocodil- constrained terrestrial fossil record from this plant fossils but, prior to this study, contains ian skeletons. Plant fossils also span the size critical interval. only a sparse and fragmentary vertebrate spectrum across all observed facies, includ- Fossils of terrestrial and freshwater orga- fossil record (14, 15, 18, 19). ing microscopic palynomorphs, seeds, leaves, nisms from the first million years after the KPgE roots, branches, in situ saplings, and even large are exceedingly rare worldwide, hindering our Corral Bluffs study area, Denver Basin, stumps and logs (Fig. 3). knowledge of post-KPgE taxonomic and eco- Colorado, USA We recognize 16 mammalian taxa, 8 of which logical radiations. Thus far, the most fossiliferous We developed a high-resolution stratigraphic are based on cranial remains, including the sections from this time interval occur in the framework in the Corral Bluffs study area first occurrence of the late Puercan (Pu3) in- Williston, San Juan, Hanna, and Denver basins (east of Colorado Springs), a single continuous dex taxon Taeniolabis taoensis (Fig. 2, K and L) along the eastern margin of the Rocky Moun- (physically traceable) ~27-km2 outcrop from from the Denver Basin. Cranial size and lower tains in North America (11, 12). In all of these the Denver Basin that preserves the biotic first molar area were used to estimate mam- study areas, discontinuous outcrops result recovery of a terrestrial ecosystem in the first malian body mass—an important feature that in composite stratigraphic sections; plant fos- million years post-KPgE (20) (Fig. 1 and fig. affects many aspects of the biology and ecol- sil localities are geographically widely spaced, S1). This stratigraphy is tied to the geomag- ogy of mammals (Fig. 4) (21). Given that there vertebrate-bearing horizons are sparse and netic polarity time scale (GPTS 2012) using appears to be bias toward large vertebrates

1Denver Museum of Nature & Science, 2001 Colorado Boulevard, Denver, CO 80205, USA. 2National Museum of Natural History, Smithsonian Institution, 10th Street and Constitution Avenue NW, Washington, DC 20560, USA. 3Department of Earth Sciences, University of New Hampshire, 56 College Road, Durham, NH 03824, USA. 4Department of Earth and Environmental Sciences, Wesleyan University, Exley Science Center 333, Middletown, CT 06459, USA. 5Department of Entomology, University of Maryland, College Park, 4291 Fieldhouse Drive, College Park, MD 20742, USA. 6Department of Geology, Colorado College, 14 E. Cache La Poudre Street, Colorado Springs, CO 80903, USA. 7Department of Biology, University of Washington, 251 Life Sciences Building, Seattle, WA 98195, USA. 8Department of Anatomical Sciences, Stony Brook University, 101 Nicolls Road, Stony Brook, NY 11794, USA. 9Department of Anthropology and Archaeology, Brooklyn College, City University of New York, 2900 Bedford Avenue, Brooklyn, NY 11210, USA. 10Department of Anthropology, The Graduate Center, City University of New York, 365 Fifth Avenue, New York, NY 10016, USA. 11New York Consortium in Evolutionary Primatology, 200 Central Park West, New York, NY 10024, USA. *Corresponding author. Email: [email protected]

Lyson et al., Science 366, 977–983 (2019) 22 November 2019 1of6 RESEARCH | RESEARCH ARTICLE s Ash bed NALMA Pollen zones Pollen Chron P-mag samples (Ma) (m) samples Pollen

170 P3 C28r Mammals Other vertebrates Dinosaurs K-taxa Momipites inaequali tenuipolus M. wyomingensis M. M. dilatus M. leffingwelli M. M. waltmanensis M. M. anellus M. triorbicularis M. Arecipites spp. (palm) Megafloral localities Megafloral 64.960 spp. Cyathidites (fern) 65.000 160 LMAT (°C) Range through 150 10 15 20 25 140 Puercan 3 130

120

110 P2 Warming? (~3°C)

100

90

65.500 Downloaded from 80

70 Puercan 2 C29n 65.688 60 Warming (~2–3°C) 50

40 http://science.sciencemag.org/

30 P1 20

10 Warming (~5°C) Puercan 1 66.040 Fern spike K–Pg 0

-10

-20 10 20 30 40 20 40 60 80 100 120 66.253 Megafloral standing Leaf mass per unit area -30 2

-40 richness (g/m ) on November 21, 2019 -50 Lancian 66.398 C29r -60 -70 Wodehouseia spinata Zone Wodehouseia 66.500 C30n 0 20 40 60 0 20 40 60 80 100 (%) (%)

Fig. 1. Temporally calibrated stratigraphic, floral, and faunal data for the are offset from scale by 20%. Standing richness of dicot morphospecies or K–Pg interval in the Corral Bluffs study area (fig. S1). Stratigraphy is megafloral standing richness is exclusive of species that occur at a single tied to the GPTS 2012 using paleomagnetics (P-mag) and CA-ID-TIMS U-Pb- locality (data S4 to S7). Leaf-estimated mean annual temperature (LMAT) datedash(italicizeddates)(20) (data S1 and figs. S3 and S5). The composite calibrated with East Asian forests (data S8 and fig. S6). Horizontal pink shading lithostratigraphic log (figs. S2 to S5) is dominated by intercalated mudstone indicates hypothesized warming intervals. Estimated leaf mass per unit area and sandstone, reflecting a variety of fluvial facies. Pollen zones (data S3) (data S9 and S10 and fig. S7) is shown with box plots that represent the are defined by diversification of Momipites spp. (fossil juglandaceous pollen) distribution of species-site pair means for each 30-m bin (supplementary (Fig. 3I). The K–Pg boundary is demarcated by the decrease in abundance materials). Box plots are placed along the y axis near each bin’sstratigraphic of Cretaceous pollen taxa (labeled “K-taxa”) without recovery, and the midpoint and are repositioned for visibility. See data S11 and supplementary subsequent fern (Cyathidites spp.) spike (data S2). Relative abundance (%) materials for placement of NALMAs. Tick marks for P-mag, pollen zones, of fern (Cyathidites spp.) and palm (Arecipites spp.) (Fig. 3E) palynomorphs megafloral standing richness, and NALMAs show stratigraphic placement of increased considerably post-KPgE (data S2); note that palm pollen percentages samples and fossil localities (supplementary materials). in our dataset (supplementary materials and Pu3 transitions, ~300 and ~700 ka post-KPgE, baenid (Fig. 2, Q to T) and T. taoensis data S11), we focused on maximum mammalian respectively (Fig. 4). In addition, the pattern (Fig. 2, K and L) lived in or near river channel body mass. The largest-bodied mammals dis- and abundance of vertebrates preserved in all margins, whereas chelydroid turtles (Fig. 2, appeared at the K–Pg boundary (10) and re- paleoenvironments suggest that by ~700 ka W and X) and the large periptychid mammals turned to near pre-KPgE levels within 100 ka post-KPgE, the largest mammals (25+ kg) were Ectoconus ditrigonus (Fig. 2, C, D, G, and H) after the K–Pg boundary (Fig. 4). Subsequent spatially partitioned across the landscape. We and Carsioptychus coarctatus (Fig. 2, I and J) shifts in maximum mammalian body mass observe a strong pattern of association be- primarily occupied distal portions of the flood- occurred at the Pu1–Pu2 and near the Pu2– tween taxa and facies (Fig. 4), indicating that plain (Fig. 4).

Lyson et al