Naturwissenschaften DOI 10.1007/s00114-008-0499-0
ORIGINAL PAPER
The last polar dinosaurs: high diversity of latest Cretaceous arctic dinosaurs in Russia Pascal Godefroit & Lina Golovneva & Sergei Shchepetov & Géraldine Garcia & Pavel Alekseev
Received: 2 October 2008 / Revised: 28 November 2008 / Accepted: 3 December 2008 # Springer-Verlag 2008
Abstract A latest Cretaceous (68 to 65 million years ago) vertebrate microfossil assemblage discovered at Kakanaut in northeastern Russia reveals that dinosaurs were still highly diversified in Arctic regions just before the Cretaceous– Tertiary mass extinction event. Dinosaur eggshell fragments, belonging to hadrosaurids and non-avian theropods, indicate that at least several latest Cretaceous dinosaur taxa could reproduce in polar region and were probably year-round residents of high latitudes. Palaeobotanical data suggest that these polar dinosaurs lived in a temperate climate (mean annual temperature about 10°C), but the climate was apparently too cold for amphibians and ectothermic reptiles. The high diversity of Late Maastrichtian dinosaurs in high latitudes, where ectotherms are absent, strongly questions hypotheses according to which dinosaur extinction was a result of temperature decline, caused or not by the Chicxulub impact. Communicated by G. MAYR P. Godefroit (*) Department of Palaeontology, Royal Belgian Institute of Natural Sciences, rue Vautier 29, 1 000 Brussels, Belgium e-mail: Pascal.Godefroit@naturalsciences.be L. Golovneva : S. Shchepetov : P. Alekseev Komarov Botanical Institute, Russian Academy of Sciences, Prof. Popov street 2, St. Petersburg 197 376, Russia G. Garcia Institut International de Paléoprimatologie et Paléontologie Humaine, Evolution et Paléoenvironnements, Faculté des Sciences, CNRS UMR 6046–IPHEP, Université de Poitiers, 40 Avenue du Recteur Pineau, 86 022 Poitiers Cedex, France
Keywords Polar dinosaurs . Late Cretaceous . Extinction . Russia
Introduction Dinosaurs have often been portrayed as ‘tropical’ animals, sensitive to climatic fluctuations and living under the warm equable climates of the Mesozoic (see, e.g., Ginsburg 1986). However, recent discoveries of vertebrate assemblages at high latitudes show that dinosaurs could live close to the Mesozoic poles from the Early Jurassic until the Late Cretaceous, under climatic conditions, which, in any case, cannot be considered as tropical (Rich et al. 1997, 2002; Buffetaut 2004). The presence of dinosaurs in polar palaeoenvironments has important implications on the question of dinosaur extinction (Buffetaut 2004). Indeed, climate changes toward colder and/or more contrasted climates around the Cretaceous/Paleocene Boundary have often been put forward as one of the main causes for dinosaur extinction (see, e.g., Sloan 1976; Sloan et al. 1986; Officer et al. 1987; Landis et al. 1996). In this paper, we describe a Late Maastrichtian (68 to 65 million years ago) dinosaur fauna from Kakanaut in northeastern Russia, which demonstrates that polar dinosaurs were still highly diversified and well adapted to relatively cool climates just before the Cretaceous/Paleocene mass extinction event. Hadrosaurid and troodontid isolated teeth have previously been reported from this locality (Nessov and Golovneva 1990; Averianov and Sues 2007). In 2007, a new fossiliferous lens was found in the middle of the Kakanaut Formation. Bones, teeth, and eggshell fragments of dinosaurs were discovered after screen-washing of the sediments.
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Materials and methods Geological setting The Kakanaut Formation is exposed along the banks of Kakanaut River in the southeastern part of the Koryak Upland (Fig. 1; 62°54.1′ N, 177°07.5′ W). By Late Cretaceous time, the position of the North Pole was significantly closer to the Pacific Ocean, not far from the coast of northeastern Siberia, than it is today (Howarth 1981; Smith et al. 1994). Consequently, the Kakanaut area was located within the palaeo-Arctic Circle, at a palaeolatitude estimated between 70° and 75° N (Rich et al. 1997; Golovneva 2000). The Kakanaut Formation is a 1,000-m continental sequence of volcano–sedimentary rocks (Volobueva and Terekhova 1974; Golovneva 1994a). It overlies marine deposits containing the Maastrichtian ammonite Pachydiscus subcompressus and the Late Maastrichtian bivalve Shachmaticeramus kusiroensis (Zonova and Yazykova 1994; Yazykova 2004). The Kakanaut Formation is overlain by Danian marine sediments (Volobueva and Terekhova 1974; Golovneva 1994a). Because isolated dinosaur bones are distributed throughout the Kakanaut Formation, these deposits can be regarded as Late Maastrichtian in age. Palynological data confirm this age: Indeed, the Kakanaut Formation belongs to
Fig. 1 Sites of Late Cretaceous polar dinosaur finds in the northern hemisphere, with location of the Kakanaut locality. The base map shows the presumed configuration of the continents during the Late Cretaceous. Modified from Rich et al. 2002
the same Wodehouseia spinata–Aquilapollenites subtilis palynozone as the Udurchukan Formation, which is yielded a diversified hadrosaurid fauna in the Amur Region, southeastern Russia (Markevich and Bugdaeva 1997; Godefroit et al. 2004; Van Itterbeeck et al. 2005). The isolated bones, teeth, and eggshell fragments of dinosaurs described in the present paper were found in a fossiliferous lens, about 6-m long. The fine-grained sediments and the abundance of fish scales within the lens suggest a lowenergy freshwater environment in flat lowland. The predominance of tuff material in the lens indicates the close proximity of active volcanoes during deposition. Palaeoflora and palaoclimate of the Kakanaut Formation The palaeoflora of the Kakanaut locality has been extensively studied by Golovneva (1994a,b). With more than 50 recognized taxa, the Kakanaut Formation contains the richest Cretaceous palaeoflora from the Arctic region. Ginkgo (Fig. 2a) and the cycadophytes Encephalartopsis (Fig. 2d) and Nilssonia (Fig. 2e) are locally very abundant, often forming monodominant associations. The conifers are represented by the families Taxodiaceae (Fig. 2c), Cupressaceae, and Pinaceae) and by two taxa of uncertain affinities (Fig. 2b). Among the ten gymnosperm taxa identified in the Kakanaut Formation, four are regarded as evergreen. About 30 angiosperm taxa are represented at Kakanaut, and the following modern families can be confidently recognized (Golovneva 1994a,b): Rosaceae (Peculnea, Fig. 2f), Lauraceae (Cissites, Fig. 2g), Betulaceae (Corylus, Fig. 2i), Celastraceae (Celastrinites, Fig. 2j), Platanaceae (Platanus, Fig. 2k), Cercidiphyllaceae (Trochodendroides, Fig. 2l), and Fagaceae (Fagopsiphyllum). Seeds are also preserved in the locality (Fig. 2h). Entire-margined leaves, which potentially belonged to evergreen plants, represent 15% of the number of woody angiosperm leaves discovered in the Kakanaut Formation (Golovneva 2000). Above the Arctic Circle, the light regime was without any doubt an important seasonal factor that controlled the structure of vegetation. However, the influence of this factor is still uncertain. Experimental models demonstrate that the high concentration of atmospheric CO2 that prevailed at the end of the Cretaceous period would have increased the productivity of evergreen plants in polar regions (Royer et al. 2003). Climate Leaf Analysis Multivariate Program (Wolfe 1993) was performed using 31 leaf morphological characters in order to estimate the palaeoclimate of the Kakanaut area during Late Maastrichtian time. Mean annual temperature is estimated to have been about 10°C, and cold-month mean temperature apparently ranged between 0°C and 6°C. Mean annual precipitations, estimated between 1,500 and 1,700 mm, were relatively high and evenly distributed throughout the year (Golovneva 2000).
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Fig. 2 Representative elements of the megaflora from the Kakanaut Fomation (Late Cretaceous, northeastern Russia). a Ginkgo ex gr. adiantoides (Ung.) Heer, BIN 1200-7. b Elatocladus smittiana (Heer) Seward, BIN 1200-19. c Sequoia minuta Sveshn., BIN 1200-34. d Encephalartopsis vassilevskajae Krassilov, Golovn. et Nessov, BIN 1200-15. e Nilssonia serotina Heer, BIN 1200. f Peculnea lancea
Golovn., BIN 1200-141. g Cissites kautajamensis Golovn, BIN 120059. h Carpolithes ceratops (Knowlt.) Bell, BIN 967-771. i Corylus ageevii Golovn., BIN 1200-397. j Celastrinites septentrionalis (Krysht.) Golovn., BIN 1200-103. k Platanus rarinervis Golovn., BIN 1200-76. l Trochodendroides grossidentata Golovn., BIN 120068. Scale bars=1 cm
Institutional abbreviations
important for both taxonomic and palaeoecological studies because they usually include most of the vertebrate taxa known as macrofossils in the studied area, as well as many taxa not preserved as larger fossils in the same deposit. They therefore provide a more accurate glimpse into the real vertebrate biodiversity of the beds in which they occur (Brinkman et al. 2005). Hadrosaurid teeth, characterized by their lanceolate crown, which bears a single strong median carina on its enameled side, are numerous (Fig. 3b). Hadrosaurids are the dominant dinosaurs in Late Maastrichtian deposits from southeastern Russia (Godefroit et al. 2004) and are also well represented in Late Cretaceous deposits from Alaska (Fiorillo and Gangloff 2001). Labiolingually compressed phylliform teeth, with an apical cusp and a series of secondary cusps along the edge
The following institutional abbreviations were used: BIN, Botanical Institute, Russian Academy of Sciences, St Petersburg (Russia) and ZIN, Zoological Institute, Russian Academy of Sciences, St Petersburg (Russia).
Results Dinosaur bones and teeth The fossil assemblage of the fossiliferous lens consists of a concentration of small (<5 cm), well-sorted, and multitaxic vertebrate remains dominated by dinosaur teeth and fish scales. Such vertebrate microfossil assemblages are very
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Fig. 3 Dinosaur fossils from the Kakanaut Formation (Late Cretaceous, northeastern Russia). a Scapula tentatively attributed to a basal ornithopod, ZIN PH107/1. b Hadrosaurid tooth, ZIN PH107/2. c Ankylosaurian tooth, ZIN PH107/3. d Neoceratopsian tooth in mesial or distal view, ZIN PH107/4. e The same as d in occlusal view. f troodontid tooth (‘Troodon’ morphotype), ZIN PH107/5. g Troodontid tooth (‘Urbacodon’ morphotype), ZIN PH107/6. h Dromaeosaurid
tooth (‘Dromaeosaurus’ morphotype) in lingual view, ZIN PH107/7. i the same as h in mesial view, the white arrow indicates the lingually twisted mesial carina. j Dromaeosaurid tooth (‘Saurornitholestes’ morphotype), ZIN PH107/8. k tyrannosaurid tooth, ZIN PH107/9. l the same as k, detail of the mesial denticles showing the blood grooves between denticles that extend obliquely toward the base of the crown. Scale bars: a–k=5 mm; l=1 mm
of the crown, belong to ankylosaurian dinosaurs (Fig. 3c). Because of the strong development of a denticulate cingulum on both sides of the crown, these teeth closely resemble those of the North-American nodosaurid Edmontonia (Coombs 1990). This genus was identified by teeth directly associated with a partial skull in late Campanian–early Maastrichtian deposits from southern Alaska (Gangloff 1995). However, the development of the cingulum is too variable among ankylosaurians to be regarded as a valid diagnostic character, and therefore, the teeth discovered at Kakanaut are attributed to indeterminate ankylosaurians (Coombs 1990). Four isolated teeth represent the first neoceratopsian remains discovered in Maastrichtian deposits outside North America (Fig. 3d, e). The enameled side of their low and bulbous crown bears a strong primary ridge, placed eccentrically, and also well-developed secondary ridges (see, e.g., You and Dodson 2004; Godefroit and Lambert 2007). The basal part of the crowns and the roots are not preserved; it is therefore impossible to identify them more precisely, even at family level. Two small scapulae (Fig. 3a) closely resemble those of basal ornithopods, particularly those of Hypsilophodon foxii
(Galton 1974) and Jeholosaurus shangyuanensis (Xu et al. 2000): The ventral articular head is craniocaudally expanded, the glenoid forms a large crescent-like depression supported dorsally by a prominent buttress, and the scapular blade is relatively short and expanded distally. In hadrosaurid babies and embryos of similar size, the ventral head of the scapula is less expanded, and the scapular blade is proportionally longer (Horner and Currie 1994). However, those characters cannot be regarded as strictly synapomorphic for basal ornithopods because they can be separately observed in other dinosaur lineages. For that reason, these scapulae are only tentatively attributed to indeterminate basal ornithopods, pending further evidences. Ornithischians were therefore well diversified in Arctic regions by Late Maastrichtian times. Comparisons with the Late Maastrichtian Hell Creek ornithischian assemblage in Montana and North and South Dakota (Russell and Manabe 2002) reveal that only pachycephalosaurids are apparently not represented at Kakanaut. On the other hand, pachycephalosaurids are represented in the Late Campanian of the North Slope of Alaska (Gangloff et al. 2005; Sullivan 2006). Because pachycephalosaurids usually form minor components of Late
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Cretaceous dinosaur faunas, it cannot be excluded that their apparent absence in the Kakanaut Formation represents a collecting bias. Five theropod dental morphotypes can also be identified at Kakanaut. One specimen closely resembles the fragmentary troodontid tooth previously discovered at Kakanaut and tentatively referred to as Troodon cf. formosus (Nessov and Golovneva 1990; Averianov and Sues 2007): its distal carina bears nine large and hooked denticles, with pointed tips turned upward (Fig. 3f). On this new specimen, it is clear that the mesial carina is not serrated. In Troodon, only the posterior mandibular teeth lack denticles on the mesial carina (Currie et al. 1990). In any case, such tooth morphology is widely distributed among troodontids and cannot be regarded as diagnostic at generic level (Averianov and Sues 2007). Another tooth from Kakanaut is tentatively attributed to a troodontid theropod (Fig. 3g). With its inflated, slightly recurved, and unserrated crown, it resembles the dentary teeth of Byronosaurus jaffei (Makovicky et al. 2003) and Urbacodon itemirensis (Averianov and Sues 2007). Dromaeosaurid teeth are also well represented by two morphotypes. The first group resembles the teeth of Dromaeosaurus albertensis (Currie et al. 1990): the crown is proportionally high and narrow, the mesial carina is characteristically twisted lingually, denticles are smallest at the ventral and dorsal ends of both the mesial and distal carinae, and each denticle is relatively broad and chisel-like in shape (Fig. 3h, i). The other morphotype more closely
resembles the teeth of Saurornitholestes langstoni (Currie et al. 1990): the crown is much compressed laterally, there is a great disparity in size between the mesial and distal denticles, apical denticles are hooked towards the tip of the crown, and the interdenticle slits are deep (Fig. 3j). Larger theropod teeth can be attributed to tyrannosaurid theropods (Currie et al. 1990). They are stouter and less compressed laterally than those of troodontids or dromaeosaurids. The denticles are wide and do not curve toward the tip of the crown but do possess sharp ridges of enamel along the midline (Fig. 3k). They are best characterized by the diagnostic blood grooves between denticles that extend obliquely toward the base of the crown (Fig. 3l). With five morphotypes, the biodiversity of isolated theropod teeth is therefore the same in the Kakanaut Formation as in younger, Late Campanian to Early Maastrichtian, tooth-based theropod faunas discovered in lower latitudes in North America (Currie et al. 1990; Rowe et al. 1992; Fiorillo and Currie 1994). Only four theropod dental morphotypes have been identified in the Campanianâ&#x20AC;&#x201C; Maastrichtian Prince Creek Formation of Alaska (Fiorillo and Gangloff 2000). Although it is limited, the fossil sample recovered from the Kakanaut Formation shows that fairly diverse dinosaur taxa were apparently able to live under polar conditions by Late Maastrichtian time. There is no indication at all that polar dinosaur faunas became impoverished by Late Maastrichtian time, just before the Cretaceousâ&#x20AC;&#x201C;Tertiary extinction event.
Fig. 4 Fragmentary dinosaur eggshells from the Kakanaut Formation (Late Cretaceous, northeastern Russia). a Radial thin section in nonpolarized light of a spheroolithid eggshell, ZIN PH107/10; observe the unevenly distributed pore canals (p) corresponding to prolatocanaliculate type, the white arrow indicates the altered fishbone lines. b Radial view under SEM of a spheroolithid eggshell, ZIN PH107/11, showing the spheroolithid microstructure with fan-shaped shell units and no distinct mammillary layer. c Outer surface elements of a spheroolithid eggshell, ZIN PH107/12, consisting of irregular nodes
and sinuous ridges, typical of sagenotuberculate ornamentation. d Radial view under SEM of a prismatoolithid eggshell, ZIN PH107/13; note the bi-layered structures with an external recrystallized layer (RL); the black arrow marks the approximate limit between the mammillary (ML) and prismatic (PL) layers. e Microscopic view under non-polarized light of the radial thin section of a prismatoolithid eggshell, ZIN PH107/14. f Microscopic view under polarized light with a distinct columnar extinction pattern of the same as e
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Dinosaur eggshell fragments Partially recrystallized dinosaur eggshell fragments have also been discovered in the fossiliferous lens at Kakanaut. This is the first time that dinosaur eggshells are reported in polar regions. Spheroolithid eggshells, attributed to hadrosaurids (Zelenitsky 2000), are most numerous. Their shell structure consists of an imperfectly spherulitic layer (thickness, 1.24–1.54 mm) and of irregular pore canals (Fig. 4a, b). The accretion lines inside the crystalline units are almost horizontal and sometimes crisscrossed by altered structures in a fish-bone pattern (Fig. 4a). Their external ornamentation forms a lineariform and mottled pattern with the pore system (Fig. 4c). Prismatoolithid eggshells, assigned to non-avian theropod dinosaurs (Zelenitsky 2000; Varricchio et al. 2002), have also been identified at Kakanaut. They are composed of interlocking shell columns that overlay a well-pronounced inner mammillary layer (Fig. 4d–f). The contact between these two distinct structural layers is gradual, giving this eggshell type a prismatic character. Their thickness varies between 0.96 to 1.24 mm, depending on their preservation. Indeed, some fragments are covered by an external diagenetic layer (Fig. 4a). Their pore openings are isolated, and their outer surface is not ornamented. The discovery at Kakanaut of hadrosaurid and non-avian theropod eggshell fragments definitely proves that at least some polar dinosaurs could reproduce at high latitude. This is a further argument suggesting that polar dinosaurs could stay at high latitudes throughout the year and were adapted to survive through periods of prolonged darkness during the polar night, feeding on evergreen gymnosperms and angiosperms.
Discussion The composition of the Kakanaut dinosaur assemblage superficially resembles that from the Hell Creek Formation in western North America (Russell and Manabe 2002). On the other hand, it is markedly different form the Late Maastrichtian faunas discovered in northeastern China and southeastern Russia. In this area, herbivorous dinosaurs were largely dominated by lambeosaurine hadrosaurids, nodosaurids and sauropods were also represented, whereas ceratopsians were apparently completely absent (Godefroit et al. 2004; Van Itterbeeck et al. 2005). Such a contrasted distribution suggests an important provincialism of the dinosaur faunas in Eurasia during the Late Maastrichtian. It means that the global biodiversity of the latest Cretaceous dinosaurs is probably largely underestimated in the current state of our knowledge. Therefore, previous scenarios about gradual dinosaur extinction, based on the evolution of local
dinosaur faunas in Western North America (see, e.g., Sloan 1976; Sloan et al. 1986), are probably completely biased. The remains of terrestrial, cold-blooded forms such as amphibians, turtles, lizards, and crocodilians, which constitute a major part of more southern vertebrate assemblages, are conspicuous by their absence throughout the Kakanaut Formation. This is also the case in Campano–Maastrichtian vertebrate assemblages from Alaska (Clemens and Nelms 1993; Rich et al. 2002). On the other hand, typical ectothermic reptiles were well represented in Arctic North America from the mid-Cretaceous until the Turonian– Coniacian, when higher temperatures prevailed (Parrish et al. 1987; Tarduno et al. 1998). Therefore, it can be hypothesized that latest Cretaceous dinosaurs were able to withstand climatic conditions that were too harsh for typical ectothermic reptiles (Clemens and Nelms 1993; Buffetaut 2004). The high diversity of dinosaurs and the concomitant absence of typical ectothermic reptiles in Arctic regions during the Late Maastrichtian therefore invalidate theories explaining the extinction of non-avian dinosaurs by a temperature decline, caused or not by the Chicxulub impact. Indeed, non-avian dinosaurs disappeared from all the continents and all the ecosystems at the end of the Maastrichtian, whereas typical ectothermic reptiles, which were apparently less resistant to cold, were only little affected at the Cretaceous–Tertiary Boundary (Buffetaut 2004). On the other hand, the high diversity of non-avian dinosaurs in Arctic regions during the Late Maastrichtian is not incompatible with the impact hypothesis. It is often hypothesized that, after the Chicxulub impact, the introduction of huge amounts of ‘dust’ in the atmosphere resulted in a drastic reduction of the photosynthetic activity during a prolonged period. The rapid but selective extinction of animals feeding on foliage lead to a food-chain collapse (Buffetaut 1990; Sheehan and Fastovsky 1992).Even though herbivorous dinosaurs were able to subsist on low-quality food during the annual polar night, it is unlikely that they could have survived a much longer darkness period following the Chicxulub impact, since food resources would not have been renewed because of enduring reduction of photosynthetic activity (Buffetaut 2004).
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