The evolution of the modern avian digestive system: insights from paravian fossils from the Yanliao and Jehol biotas

Abstract

The avian digestive system, like other aspects of avian biology, is highly modified relative to other reptiles. Together these modifications have imparted the great success of Neornithes, the most diverse clade of amniotes alive today. It is important to understand when and how aspects of the modern avian digestive system evolved among neornithine ancestors in order to elucidate the evolutionary success of this important clade and to understand the biology of stem birds and their closest dinosaurian relatives: Mesozoic Paraves. Although direct preservation of the soft tissue of the digestive system has not yet been reported, ingested remains and their anatomical location preserved in articulated fossils hint at the structure of the digestive system and its abilities. Almost all data concerning direct evidence of diet in Paraves comes from either the Upper Jurassic Yanliao Biota or the Lower Cretaceous Jehol Biota, both of which are known from deposits in north-eastern China. Here, the sum of the data gleaned from the thousands of exceptionally well-preserved fossils of paravians is interpreted with regards to the structure and evolution of the highly modified avian digestive system and feeding apparatus. This information suggests intrinsic differences between closely related stem lineages implying either strong homoplasy or that diet in each lineage of non-ornithuromorph birds was highly specialized. Regardless, modern digestive capabilities appear to be limited to the Ornithuromorpha, although the complete set of derived feeding related characters is restricted to the Neornithes.

Reply to Li et al. “IsOculudentavisa bird or even archosaur?”

“…As clearly stated in the etymology 1 , the name Oculudentavis was not derived to mean a bird with bird-like tooth and eye morphology as described by Li et al, but rather a bird with a toothed eye, referring to the dentition below the eye that also occurs, although less extensively, in Ichthyornis 6 . Although in the future new information may prove we are incorrect in our original interpretation and Oculudentavis may be added to the list of taxa whose names have become misnomers (e.g., Oviraptor, Piscivorenantiornis) 15,16 , this is in no way due to gross negligence, but rather due to the fact that Oculudentavis may represent an outstanding case of convergent evolution between squamates and birds, the likes of which biologists have rarely seen before. Li et al do not provide conclusive support for their alternative interpretation of Oculudenatvis, and their hypothesis is only supported in the absence of avians in the phylogenetically broader cladistic analysis presented here (Fig.…”

Trophic shift and the origin of birds

“…Living birds are toothless, and they swallow their food whole, which is temporally stored in their crop and then grinded up by their muscular gizzard. Fossil evidence shows that the specialization of the digestive system occurs in multiple lineages of ancestral birds (Zhou et al 2010;Zheng et al 2011;Zheng et al 2014;Chiappe and Qingjin 2016;Wang et al 2016b;O'Connor 2019;O'Connor and Zhou 2020) (Fig. 3).…”

“…Fossil evidence shows that ever since the origin of birds from the Late Jurassic, they underwent adaptive radiation to diversified dietary niches in the Cretaceous, with herbivorous (e.g., fruits and seeds), piscivorous, and insectivorous diets found (Zhou and Zhang 2002;Zhou et al 2003;Benton 2015;Chatterjee 2015;Chiappe and Qingjin 2016;Ksepka et al 2019;O'Connor 2019;O'Connor and Zhou 2020). In particular, seed and/or fruit eating are suggested in many ancestral bird lineages, such as Jeholornis, Sapeornis, Hongshanornis, and Yanornis (Zhou and Zhang 2002;Zheng et al 2011;Benton 2015;Chatterjee 2015;Chiappe and Qingjin 2016;Mayr 2017;Ksepka et al 2019;O'Connor 2019;O'Connor and Zhou 2020). This suggests that seed and/or fruit eating may have been relatively common during the early evolution of birds and that this herbivorous adaptation may play a vital role in the early evolution of birds (Zanno and Makovicky 2011;Zheng et al 2011;Chatterjee 2015;Wang et al 2016a).…”

“…;Benton 2015;Chatterjee 2015;Mayr 2017). Among these maniraptoran theropods, many of them, including most dromaeosaurids and derived troodontids, show carnivory(Zanno et al 2009;O'Connor et al 2011;Xu et al 2011;Zanno and Makovicky 2011;Brusatte 2012;Han et al 2014;Chatterjee 2015;Button et al 2017;Mayr 2017;O'Connor 2019;O'Connor et al 2019;O'Connor and Zhou 2020) (Fig. 3).…”

“…Given the possible arboreality and gliding lifestyle of ancestral birds, while there are many potential predators, such as carnivorous theropods, carnivorous mammals (e.g., Repenomamus), snakes (e.g., Sanajeh) and crocodylomorphs, in the Mesozoic terrestrial ecosystem (Brusatte 2012; Matsukawa et al 2014), four lines of evidence may suggest that one group of carnivorous theropods-maniraptorans (e.g., dromaeosaurids)-is likely one of the main predators of ancestral birds, as proposed previously (Gong et al 2010; O'Connor et al 2011; Chatterjee 2015). Primarily, a wealth of small feathered maniraptorans, such as Aurornis, Anchiornis, Bambiraptor, Buitreraptor, Changyuraptor, Eosinopteryx, Jinfengopteryx, Microraptor, Rahonavis, and Xiaotingia, are found to have hallmark anatomical characteristics indicative of their capability of gliding flight or even some forms of powered flight (Han et al 2014; Xu et al 2014; Benton 2015; Chatterjee 2015; Chiappe and Qingjin 2016; Mayr 2017; Sullivan et al 2017; Pei et al 2020), and many of these volant maniraptorans, such as Microraptor, Anchiornis, and Changyuraptor, show predatory features(Zanno et al 2009;Gong et al 2010;O'Connor et al 2011;Xu et al 2011;Zanno and Makovicky 2011;Brusatte 2012;Han et al 2014;Button et al 2017;Mayr 2017;O'Connor 2019;O'Connor et al 2019;O'Connor and Zhou 2020), representing one of the potential aerial predators of ancestral birds. The predation pressure from these aerial predators may be more significant than those ground predators given the arboreality and gliding lifestyle of ancestral birds.…”