Science

The Tanis event deposit in North Dakota (USA) is an exceptional seiche deposit preserving a rich thanatocoenosis (that is, a mass death assemblage) of latest Cretaceous biota at the top of the Hell Creek Formation. The majority of macrofossils encountered at the Tanis locality represent direct casualties of the K–Pg bolide impact that were buried within the impact-induced seiche deposit5. Tens of minutes after the impact, the seiche agitated large volumes of water and soil in the estuary of the Tanis river5. As the seiche proceeded upstream, it advected bones, teeth, bivalves, ammonites, benthic foraminifera (Extended Data Fig. 1a–c) and plant matter in the suspended load while impact spherules rained down from the sky5. Within the thanatocoenotic accumulation, abundant acipenseriforms—sturgeons and paddlefishes—became oriented along the seiche flow directions and buried alive with numerous impact spherules in their gills5 (Fig. 1, Extended Data Fig. 2a, b).

During the Maastrichtian (that is, the last age of the Cretaceous), the climate of present-day North Dakota involved four seasons that were documented in tree-ring records recovered from other Upper Cretaceous sites in the Hell Creek Formation12,13. Tanis was located at approximately 50° N during the latest Cretaceous and experienced distinct seasonality in rainfall and temperature14. Regional air temperatures were reconstructed to range from 4–6 °C in winter up to an average of about 19 °C in summer13,14. To uncover the season of the K–Pg bolide impact, we analysed osteohistological records of acipenseriform bone apposition in three paddlefish dentaries and three sturgeon pectoral fin spines that were excavated at the Tanis site in 2017 (Extended Data Fig. 1d–j). These skeletal elements preserve unaltered growth records from embryonic development up to death, making them highly suitable for life history reconstructions15,16.

Growth records of end-Cretaceous fishes

To trace appositional growth and pinpoint the season in which bone apposition terminated, we first assessed the preservation of bone growth patterns across the studied specimens. We prepared dermal bone slices of six acipenseriform specimens as microscopic slides and subjected these to osteohistological assessment, during which lines of arrested growth (LAGs) were easily recognized (Fig. 2). To corroborate the annual nature of the LAGs using virtual high-resolution osteohistology17,18, three-dimensional (3D) volumes were produced with propagation phase-contrast synchrotron radiation micro-computed tomography19 on beamline BM05 of the European Synchrotron Radiation Facility, France. The 3D nature of the synchrotron data enables optimal projection of the bone deposition pattern across multiple cross-sectional planes and resolved the exact relationship between seasonality and cyclical bone apposition in superb detail20. In addition, virtual osteohistology allowed us to visualize the seasonal fluctuations of osteocyte lacunar density and volume, which are poorly expressed in the physical 2D thin sections18 (Fig. 3c, d) . The osteohistological data (Figs. 2, 3, Extended Data Figs. 3–6) were complemented with an incremental carbon isotope record extracted from one of the paddlefish dentaries (VUA.GG.2017.X-2724).

The tomographic data show that impact spherules associated with the paddlefish skeleton are present exclusively in its gill rakers5 and are absent elsewhere in the preserved specimen (Fig. 1). The absence of impact spherules outside the gill rakers demonstrates that spherules were filtered out of the surrounding waters but had not yet proceeded into the oral cavity or further down the digestive tract, and had not impacted the fish carcases during perimortem exposure. Impact spherule accumulation in the gill rakers and the arrival of the seiche waves must therefore have occurred simultaneously5, which implies that the acipenseriforms were alive and foraging during the bolide impact and the last minutes of the Cretaceous.

Well-conserved bone growth archives

The degree of preservation of the sampled acipenseriform bones was assessed using micro-X-ray fluorescence (Methods, Extended Data Figs. 7–9), which would reveal potential taphonomic elemental exchange that may have affected the primary stable isotope composition. The micro-X-ray fluorescence maps show that Fe and Mn oxides are present in the bone vascular canals and surrounding sediments (Extended Data Fig. 8), but have not invaded the bone apatite (Ca5(PO4,CO3)3(OH,F,Cl)). Detrital components, characterized by high concentrations of K and Si, remain restricted to the sediment matrix (Extended Data Fig. 8f–j). The bone apatite conserves a highly homogeneous distribution of P and Ca (Extended Data Fig. 9), which corroborates the unaltered preservation of these apatitic tissues. Skeletal remains of the paddlefishes and sturgeons thus experienced negligible diagenetic alteration, probably as a consequence of rapid burial and possibly aided by early Mn and Fe oxide seam formation21,22. The exquisite 3D preservation of delicate structures, including non-ossified tissues that originally enveloped the brain (Extended Data Fig. 2c–f), further demonstrates the excellent preservation of the fossils and absence of taphonomic reorganization23.

Consistent records of a spring death

Paddlefish dentaries form through perichondral ossification around the Meckel’s cartilage24. Sturgeon pectoral fin spines consist of dermal bone—an intramembranous skeletal tissue that forms in the mesenchyme (mesodermal embryonic tissue)25. Unlike endochondral bone, perichondral and dermal bone do not originate through mineralization of cartilaginous precursors26,27,28 but grow exclusively through incremental bone matrix apposition by secretion of a row of osteoblasts24,26,27,28. The thickness of one annual growth mark cumulatively spans a thick (favourable) growth zone, a thinner (slowly deposited) annulus and, ultimately, a LAG20. Our microscopic and virtual osteohistological data consistently show that the six fishes perished (that is, stopped growing) while forming a growth zone shortly after a LAG was deposited (Figs. 2, 3, Extended Data Figs. 3–6), which coincides with an early stage of the favourable growth season20. The outermost cortices of all six acipenseriform individuals studied here also exhibit increasing osteocyte lacunar densities and sizes towards their periosteal surfaces (Fig. 3c, Extended Data Figs. 5, 6). In all specimens, this density remained lower than the highest densities and average sizes recorded in previous years (Fig. 3c, Extended Data Figs. 3–6, 10b). As osteocyte lacunar density and size patterns were consistently cyclical across the preceding years during which they peaked at the climaxes of the growth seasons, the last recorded growth season had thus not yet climaxed at the time of death (Figs. 2, 3, Extended Data Figs. 3–6, 10b).

The inferred annual growth cycles are independently corroborated by a stable carbon isotope (𝛿13Csc) archive that recorded several years of seasonal dietary fluctuations in growing bone. Paddlefish VUA.GG.2017.X-2724 also yielded, in addition to this 𝛿13Csc archive, an oxygen isotope (𝛿18Osc) record across the final six years of its life (Supplementary Data Table 1, Extended Data Fig. 10a, Methods). The low and constant 𝛿18Osc values in VUA.GG.2017.X-2724 reflect exclusive inhabitation of freshwater environments by the paddlefishes. This implies that their osteohistological records must have captured seasonal variability rather than, for example, migration between saline and freshwater habitats. Although modern sturgeons are known to have anadromous lifestyles29,30, this remains to be confirmed for the fossil sturgeons at Tanis, as isotopic data from sturgeon pectoral fin spines could not be secured (Methods, ‘Micromill’). Notably, the osteohistological records of all our sturgeons and paddlefishes converge on the same annual growth phase, despite their potential different lifestyles.

Like their modern-day relatives, the latest Maastrichtian paddlefishes of Tanis were filter feeders that presumably consumed copepods and other zooplankton29,30,31. These fishes probably experienced an annual feeding pattern, determined by fluctuating food availability, that peaked between spring and autumn31. During maximum productivity, ingested zooplankton enriches the growing skeleton of filter-feeding fishes with 13C relative to 12C32,33. Thus, the cyclically elevated 13C/12C ratios in paddlefish VUA.GG.2017.X-2724 (Fig. 3a) reflect distinct episodes of high food availability and consumption. Carbon isotope records across the growth record of Paddlefish VUA.GG.2017.X-2724 indicate that peak annual growth rate was not yet attained and the feeding season had thus not yet climaxed—corroborating a boreal spring death.

Implications for selective K–Pg survival

The Chicxulub bolide impact caused a global heat pulse that ignited widespread wildfires9,34. After this heat wave, the last boreal spring of the Mesozoic transitioned to a global impact winter10. Although a June timing for the K–Pg impact has been suggested on the basis of palaeobotanical indications for anomalous freezing in this region (Wyoming, USA)35, the palaeobotanical identities, taphonomic inferences and stratigraphic assumptions underlying that conclusion have since all been refuted36,37,38,39. Moreover, post-impact cooling happened in the first months to decades following the K–Pg impact10, which renders proxies registering post-impact freezing conditions asynchronous with the impact event itself.

A suite of impact-induced phenomena contributed to the K–Pg extinction on differing timescales40,41. In the days to months following the impact, its instantaneous effects, such as intense infrared radiation caused by ejecta reentry34, resulting wildfires9,34 and the spread of sulfurous aerosols leading to acid precipitation42 must have predominantly afflicted the exposed continental environments. Although negotiating these hostile conditions would not have guaranteed survival, an early clade-wide eradication would always have meant immediate extinction41.

The seasonal timing of the catastrophic end-Cretaceous bolide impact places the event at a particularly sensitive stage for biological life cycles in the Northern Hemisphere. In many taxa, annual reproduction and growth take place during spring. Species with longer incubation times, such as non-avian reptiles, including pterosaurs and most dinosaurs, were arguably more vulnerable to sudden environmental perturbations than other groups43 (for example, birds). Southern Hemisphere ecosystems, which were struck during austral autumn, appear to have recovered up to twice as fast as Northern Hemisphere communities44, consistent with a seasonal effect on biotic recovery.

Subterranean sheltering conceivably contributed to the cynodont survival of the Permo-Triassic (PT) crisis45. Similarly, large-scale wildfires raging across the Southern Hemisphere9,34,41 may have been evaded by hibernating mammals that were already sheltered in burrows34,41 in anticipation of austral winter. Additional modes of seasonal dormancy, torpor and/or aestivation, which are nowadays practised by various mammals46,47 as well as certain amphibians, birds and crocodilians48, could have facilitated further underground survival. In the aftermath of the K–Pg event, ecological networks collapsed from the bottom up. Floral necrosis9 and extinction immediately affected species dependent on primary producers, while some animals capable of exploiting alternative resources—for example, certain birds and mammals49,50—persisted.

Conclusions

Seasonal timing of the Chicxulub impact in boreal spring and austral autumn will aid in further calibrating evolutionary models exploring the selectivity of the K–Pg extinction and the asymmetry in extinction and recovery patterns between the two hemispheres. Decoupling short- and long-term effects of the bolide impact on the K–Pg mass extinction will also aid in identifying extinction risks and modes of ecological deterioration caused by the forthcoming global climate change. The uniquely constrained Tanis site5 offers valuable proxies for reconstructing the environmental, climatological and biological conditions that prevailed locally when the Mesozoic ended.