The discovery of gastric pellets in the basal troodontid Anchiornis sheds new light on the evolution of the avian digestive system. Previous studies have demonstrated that non-avialan theropods share with modern birds some salient features pertaining to feeding and digestion. Like carnivorous birds, carnivorous non-avialan theropods probably swallowed prey whole or in large chunks9, as indicated by stomach contents in several theropod fossils that include partial or even nearly complete skeletons of a variety of small vertebrates9,17,25,26,27. The presence of gastroliths in several phylogenetically disparate theropod groups, including ceratosaurs28, ornithomimosaurs29,30, and oviraptorosaurs31,32, suggests that theropods probably had a two-chambered stomach with a muscular gizzard3,10. However, relatively basal coelurosaurian theropods probably differed from most birds in several digestive features. For example, the compsognathids Sinocalliopteryx17 and Scipionyx18 might have possessed highly acidic anterior stomach chambers, as indicated by the occurrence in these taxa of strongly acid-etched bones as apparent preserved stomach contents18. Furthermore, the strong etching also suggests that these basal coelurosaurian theropods may have been characterized by relatively long gastric residence times similar to those of modern crocodilians33.

The Anchiornis gastric pellets described in this study are the only ones definitively known from any non-avialan theropod, though an isolated aggregation of bones from the Lower Cretaceous of Las Hoyas, Spain has been identified as a pellet from either a non-avialan theropod or a pterosaur19. If the lack of other documented fossil theropod pellets is not simply a preservational artefact, parsimony suggests that pellet regurgitation and the advanced digestive features (a two-chambered stomach, efficient anti-peristalsis, low stomach acidity and short gastric residence) implied by this phenomenon were absent in non-paravians and evolved at the base of Paraves. However, gastric pellets of any kind have rarely been reported in the fossil record20, particularly in circumstances that permit them to be assigned to particular taxa, so the possibility that pellets occurred in non-paravians but have not yet been successfully recovered and identified must be considered.

Although the evidence bearing on whether pellet regurgitation might have occurred in some non-paravians is scattered and largely circumstantial, some tentative conclusions can be drawn. The most important datum is the occurrence of bone fragments in coprolites attributable to the basal (non-maniraptoriform) coelurosaur Tyrannosaurus7,8,9, which implies that hard indigestible material was still being expelled via the cloaca rather than orally in taxa of this evolutionary grade. There is no known evidence of either gastric pellets or bone-bearing coprolites in the basal coelurosaurian clade Compsognathidae, or in the non-paravian maniraptoriform clades Ornithomimosauria, Alvarezsauroidea, Therizinosauroidea and Oviraptorosauria. However, an important consideration in evaluating whether any of these taxa are likely to have produced gastric pellets is their inferred diet. Compsognathids were clearly carnivorous, based on their dentition and the occurrence of vertebrate remains as stomach contents in some compsognathid specimens17,34,35,36. However, ornithomimosaurs, therizinosauroids and oviraptorosaurs are all characterized by reduced or lanceolate teeth and other craniomandibular indicators of herbivory, and some ornithomimosaurs and oviraptorosaurs also have gastric mills that likely represent an additional adaptation for plant-eating37. Although the teeth of alvarezsauroids are reduced in size, some maxillary teeth of the basal form Haplocheirus are recurved and serrated as in undoubtedly faunivorous theropods38,39, and insectivory has been suggested for derived members of the group40,41. Alvarezsauroids appear much less likely than other non-paravian maniraptorans to have been largely or entirely herbivorous, but even Haplocheirus lacked skull and dental features suggestive of classic theropod carnivory and was presumably restricted to prey much smaller than itself39.

Among extant birds, pellet regurgitation is characteristic of carnivores, piscivores and insectivores20. Herbivores presumably either digest their food completely, or expel indigestible material in the faeces. If this pattern was also characteristic of non-avian theropods, then ornithomimosaurs, therizinosaurs and oviraptorosaurs probably did not produce gastric pellets, given their inferred herbivory. However, the presence of gastric mills in some ornithomimosaurs and oviraptorosaurs suggests that a muscular, grinding gizzard was present ancestrally in maniraptoriforms3. Although a muscular gizzard is necessary in order to form gastric pellets, the presence of a gizzard does not necessarily imply that a given theropod was capable of the efficient antiperistalsis needed for pellet regurgitation. Because of the evidence for cloacal rather than oral expulsion of indigestible residue in tyrannosauroids7, efficient antiperistalsis was probably absent in non-maniraptoriform theropods, and this feature of the digestive system was probably also plesiomorphically absent in the herbivorous Ornithomimosauria. Alvarezsauroids, which are probably less closely related to birds than are therizinosauroids and oviraptorosaurs39, are the most basal faunivorous maniraptoriforms. Because no alvarezsauroid coprolites or pellets have ever been reported, it is uncertain whether they digested their prey completely, expelled indigestible material cloacally, or expelled indigestible material orally.

Combining the new evidence from Anchiornis with previous information on theropod digestion suggests two plausible scenarios for the evolution of efficient antiperistalsis and the tendency to produce gastric pellets. One possibility is that efficient antiperistalsis is a primitive maniraptoran feature, which would imply that oral regurgitation occurred in at least some alvarezsauroids. Therizinosaurs and oviraptorosaurs would then have been capable of this type of antiperistalsis, at least plesiomorphically, but would probably have needed to resort to it only in unusual circumstances given their herbivorous diets. Anchiornis and at least some other faunivorous basal paravians, by contrast, would have used their inherited capacity for efficient antiperistalsis to rid themselves of bones and other indigestible prey residues through oral regurgitation. The alternative evolutionary possibility is that alvarezsauroids still lacked efficient antiperistalsis, which really did emerge at the origin of Paraves as suggested by the absence of known pellets from more basal theropods. It will be likely be impossible to judge between the two scenarios until alvarezsauroid coprolites and/or pellets are available for analysis.

The Anchiornis pellets described here are highly similar to those of modern birds. The bones and/or scales in all these pellets retain relatively smooth surfaces and show no signs of strong acid-etching, suggesting short gastric residence as in most modern birds20. In both temporal and phylogenetic terms, the basal troodontid Anchiornis represents the earliest theropod that can be shown to have possessed both a two-chambered stomach, efficient antiperistalsis, low stomach acidity and short gastric residence, suggesting that the highly efficient and specialized avian digestive system was plesiomorphically present in the Paraves or even the Maniraptora (Fig. 4). In particular, oral expulsion would have greatly improved digestive efficiency20, which could have helped provide the energy needed for aerial locomotion, and early paravians could perhaps also have slightly reduced their body mass by quickly expelling any ingested material that was resistant to digestion. A number of other features critical for aerial locomotion are also thought to have appeared at the base of the Paraves, including cerebral expansion and elaboration of visually associated brain regions42, forelimb enlargement16,43, and a more metabolically active physiology44. If such an efficient digestive system indeed originated at the base of the Paraves in connection with the above-mentioned biological innovations, it will provide further support for the appearance of aerial locomotion in basal paravians16,44,45.

Figure 4 Evolution of digestive features in theropod dinosaurs. A two-chambered stomach with muscular gizzard, possibly highly acidic anterior stomach chamber, and relatively long gastric residence time might have characterized most theropods, including basal coelurosaurians; a digestive system with relatively short residence time and efficient antiperistalsis to expel indigestible material orally might have originated at the base of Paraves; and some highly specialized digestive structures such as the crop might have originated at the base of the Pygostylia. Full size image

The presence of both terrestrial lizards and aquatic fish in the diet of Anchiornis suggests that this dinosaur was an opportunistic generalist hunter. Anchiornis would then have been broadly similar in its foraging behaviour to the dromaeosaurid Microraptor, which evidently fed on mammals, birds, and fish25,26,27. The presence of three lizard skeletons in the pellet of STM0-179 indicates that Anchiornis must have consumed three prey animals in rapid succession. Preserved stomach contents of a referred specimen of the compsognathid Sinocalliopteryx also include multiple prey items17.

However, the pellet contents of Anchiornis differ from the stomach contents of Microraptor and Sinocalliopteryx in including a particularly high proportion of fish, with five pellets of the six described here containing only fish scales. The preponderance of fish scales in gastric pellets attributable to Anchiornis, if taken at face value, suggests that fish formed an important or even predominant component of this dinosaur’s diet. This observation is surprising given that Anchiornis does not, based on comparisons to its living relatives, appear well suited to catching fish or even living in close proximity to water. Anchiornis has extensive feathering on the lower legs, including the toes, whereas extant near-shore or aquatic birds tend to have little plumage below the knee. Furthermore, Anchiornis has a relatively short snout, whereas fish-catching birds usually have long, slender bills.

Taken together, evidence from the newly reported pellets and from the morphology of Anchiornis, particularly when the latter is considered in the light of comparative data from extant birds, creates the seemingly paradoxical picture of an animal that had a mainly piscivorous diet but was nevertheless poorly adapted to catching fish. We suggest that this paradox may have a behavioural and/or taphonomic resolution. Behaviourally, Anchiornis may simply have been good enough at obtaining fish to thrive as a partial piscivore, despite appearing poorly suited to fishing. Taphonomically, some kind of bias may have favoured the preservation of fish-bearing pellets over those containing the remains of terrestrial vertebrates, so that the pellet evidence is not really representative of the normal diet of Anchiornis. Nevertheless, what can be stated definitively is that the diet of Anchiornis included both fish and lizards at least on an occasional basis, and that Anchiornis possessed a derived digestive system capable of forming and regurgitating pellets in an essentially avian manner.