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First Species of Enantiornithes from Sihedang Elucidates Skeletal Development in Early Cretaceous Enantiornithines

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Journal of Systematic Palaeontology ISSN: 1477-2019 (Print) 1478-0941 (Online) Journal homepage: http://www.tandfonline.com/loi/tjsp20 First species of Enantiornithes from Sihedang elucidates skeletal development in Early Cretaceous enantiornithines Han Hu & Jingmai K. O'Connor To cite this article: Han Hu & Jingmai K. O'Connor (2017) First species of Enantiornithes from Sihedang elucidates skeletal development in Early Cretaceous enantiornithines, Journal of Systematic Palaeontology, 15:11, 909-926, DOI: 10.1080/14772019.2016.1246111 To link to this article: https://doi.org/10.1080/14772019.2016.1246111 View supplementary material Published online: 14 Nov 2016. Submit your article to this journal Article views: 284 View related articles View Crossmark data Citing articles: 3 View citing articles Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tjsp20 Journal of Systematic Palaeontology, 2017 Vol. 15, No. 11, 909–926, http://dx.doi.org/10.1080/14772019.2016.1246111 First species of Enantiornithes from Sihedang elucidates skeletal development in Early Cretaceous enantiornithines Han Hu a,b* and Jingmai K. O’Connora aKey Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 142 Xizhimenwai Street, Beijing 100044, China; bUniversity of Chinese Academy of Sciences, 19A Yuquan Road, Beijing 100049, China (Received 1 April 2016; accepted 19 September 2016; published online 14 November 2016) The Sihedang locality of the Lower Cretaceous Yixian Formation is the only recognized ornithuromorph-dominated locality in the Jehol Group of north-eastern China. Here we report on the first enantiornithine from this locality and erect a new taxon Monoenantiornis sihedangia gen. et sp. nov. The holotype and only specimen preserves a rare ontogenetic stage in which the intermedium is ossified but free from the other proximal tarsals and the tibia, consistent with the pattern of ossification that occurs in neornithines. In order to explore the pattern of skeletal development in the enantiornithines, we select several published specimens inferred to represent different ontogenetic stages and document their degree of fusion in five key compound bones and the sterna. This provides a preliminary hypothesis for the sequence in which compound bones form in Early Cretaceous enantiornithines. From this hypothesis, most known specimens can be categorized into four major ontogenetic stages: all the compound bones unfused; synsacrum and pygostyle fused; tarsals fused; tibiotarsus and carpometacarpus formed. http://zoobank.org/urn:lsid:zoobank.org:pub:347485CA-87E6-4834-BEB5-687B6798644E Keywords: Aves; Mesozoic; Enantiornithes; ontogeny; skeletal development Introduction recognizable, such as Longipterygidae, Bohaiornithidae and Pengornithidae (Zhou 2014). The Early Cretaceous Jehol Biota in north-eastern China Recently, a new locality in the Yixian Formation was contains the most diverse recognized Mesozoic avifauna. discovered at Sihedang near Lingyuan, in western Liaon- Thousands of exceptionally preserved bird fossils have ing. Initial reports described the Sihedang avifauna as been uncovered from these deposits, accounting for half consisting of a single ornithuromorph taxon, Iteravis the known diversity of Mesozoic birds so far. The Jehol huchzermeyeri (Zhou et al. 2014). This is unusual Biota occurs in the lower Huajiying Formation (130.7 amongst Early Cretaceous localities, in which enantiorni- Ma), the middle Yixian Formation (125 Ma) and the upper thines typically dominate in both numbers and diversity. Jiufotang Formation (120 Ma) (Swisher et al. 2002;He Four additional ornithuromorphs have been reported from et al. 2004, 2006; Zhou 2014), together recording over the Sihedang locality: a new species of Gansus (Liu et al. 10 million years of early avian evolution. Enantiornithes 2014) and three longirostrine taxa: Juehuaornis zhangi (Aves: Ornithothoraces) is considered to be the dominant (Wang et al. 2015), Dingavis longimaxilla (O’Connor avian clade in the Cretaceous and the first major avian et al. 2016) and Changzuiornis ahgmi (Huang et al. radiation. The Protopteryx horizon of the Huajiying For- 2016). In addition, the holotype of Xinghaiornis lini, mation represents the second oldest known avian-bearing which was initially described as from the Sihetun locality deposit in the world and contains the earliest record of (Wang et al. 2013), may also be from the Sihedang local- the Enantiornithes. It records the first stage with low ity (O’Connor et al. 2016). The only other known orni- diversity in the evolution of the Jehol Biota, with only thuromorph-dominated locality is the Lower Cretaceous two primitive enantiornithines known: Protopteryx and Changma locality of the Xiagou Formation in Gansu, Eopengornis (Zhang & Zhou 2000; Wang et al. 2014). China. From the discovery of the similar Sihedang locality Enantiornithine diversity is much higher in both the youn- in the Yixian Formation, hypotheses regarding avian fau- ger Yixian and Jiufotang formations, with diverse families nal turnover based on the Changma locality likely need to *Corresponding author. Email: [email protected] Ó The Trustees of the Natural History Museum, London 2016. All rights reserved. Published online 14 Nov 2016 910 H. Hu and J. K. O’Connor be reassessed in light of potential ecological differences and minor metacarpals in Pterygornis, but this is thought (Zhou et al. 2014). to be an autapomorphy since it is absent in all other taxa; Here we describe a new fossil bird representing the first Wang et al. 2016), and the major and minor metacarpals enantiornithine reported from the Sihedang locality. The unfused distally, whereas the alular metacarpal is fused to specimen represents a new taxon, Monoenantiornis sihe- the major metacarpal which is fused distally to the minor dangia gen. et sp. nov. We conducted a cladistic analysis metacarpal in ornithuromorphs; the tibiotarsus is fully to determine its phylogenetic position relative to previ- formed; the distal tarsals are fused to the proximal ends of ously known Cretaceous birds. As the first enantiornithine metatarsals II–IV, which are unfused to each other reported from Sihedang, this new specimen provides criti- (O’Connor & Chiappe 2011). Late Cretaceous taxa show cal information regarding the perceived diversity of this increased fusion in certain regions such as the skull, pelvis avifauna. and tarsometatarsus. However, neither a fully fused tarso- The level of skeleton fusion and reduction in modern metatarsus nor a distally fused carpometacarpus is ever birds is much higher than in other animal groups, having known to occur in any enantiornithine taxa. evolved to reduce weight and reinforce the body for aerial The new specimen described here records a rarely pre- locomotion: skull elements are almost completely fused served and previously undocumented ontogenetic stage, and some are greatly reduced, such as the maxilla, lacri- and thus contributes to our understanding of the sequence mal and postorbital; several thoracic vertebrae fuse into of fusion in the development of compound bones in Early the notarium; thoracic and sacral vertebrae fuse into the Cretaceous enantiornithines. synsacrum; distal caudal vertebrae fuse into the pygostyle; the pelvic bones are fully fused; the sternum consists of a single element; the distal carpals and metacarpals are Institutional abbreviations fused into the carpometacarpus; the proximal tarsals are fused to the tibia forming the tibiotarsus; and the distal BMNH: Beijing Museum of Natural History, Beijing, tarsals are fused to the metatarsals, forming the tarsometa- China; CNU: Capital Normal University, Beijing, China; tarsus. In the postcranial skeleton of some living domestic DNHM: Dalian Natural History Museum, Dalian, Liaon- fowls, the synsacrum is the first element to begin to fuse, ing, China; GMV: National Geological Museum of China, but fusion in this element occurs for a relatively long Beijing, China; IVPP: Institute of Vertebrate Palaeontol- period. The proximal tarsals begin to fuse nearly at the ogy and Palaeoanthropology, Beijing, China; LPM: same time as the synsacrum. Next, the sternum is fused, Liaoning Palaeontology Museum, Shenyang, Liaoning, followed by the formation of the tibiotarsus and the tarso- China; NIGP: Nanjing Institute of Palaeontology and metatarsus. The elements of the carpometacarpus are the Geology, Nanjing, China; STM: Shandong Tianyu last to begin the fusion process (Hogg 1982). Museum of Nature, Shandong, China. All these compound elements are absent in the earliest and basalmost bird, Archaeopteryx (Andrzej 2002). Skele- tal fusions occur in basal birds in various combinations: Systematic palaeontology the carpometacarpus is partially fused at the proximal end in the long bony-tailed bird Jeholornis (Zhou & Zhang Class Aves Linnaeus, 1758 2002a); the premaxillae are fused to each other, and the Ornithothoraces Chiappe, 1995 scapula and coracoid are fused into the scapulocoracoid Enantiornithes Walker, 1981 in Confuciusornis (Chiappe et al. 1999); the pygostyle, Genus Monoenantiornis gen. nov. synsacrum, tibiotarsus, tarsometatarsus and carpometacar- Type species. Monoenantiornis sihedangia sp. nov. pus (alular metacarpal still free) are all formed in Sapeor- nis (Zhou & Zhang 2002b). Compared to these basal Diagnosis. As for the type and only species.
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    New Bohaiornis-like bird from the Early Cretaceous of China: enantiornithine interrelationships and flight performance Luis M. Chiappe1, Meng Qingjin2, Francisco Serrano1,3, Trond Sigurdsen1,4, Wang Min5, Alyssa Bell1 and Liu Di2 1 Dinosaur Institute, Natural History Museum of Los Angeles County, Los Angeles, CA, USA 2 Beijing Museum of Natural History, Beijing, China 3 Spanish Royal Academy of Sciences, Madrid, Spain 4 Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA 5 Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China ABSTRACT During the last decade, several Bohaiornis-like enantiornithine species—and numerous specimens—have been recognized from the celebrated Jehol Biota of northwestern China. In this paper, we describe the anatomy of another “bohaiornithid” species from the 125 million-year-old Yixian Formation of Liaoning Province, China. The new taxon differs from previously recognized “bohaiornithids” on a number of characters from the forelimb and shoulder girdle. We also provide a new phylogenetic framework for enantiornithine birds, which questions the monophyly of the previously recognized bohaiornithid clade and highlights ongoing challenges for resolving enantiornithine interrelationships. Additionally, we offer the first assessment of the flight properties of Bohaiornis-like enantiornithines. Our results indicate that while “bohaiornithids” were morphologically suited for flying through continuous flapping, they would have been unable to sustain prolonged flights. Such findings expand the flight strategies previously known for enantiornithines and other early birds. Submitted 8 March 2019 8 September 2019 Accepted Subjects Evolutionary Studies, Paleontology, Taxonomy Published 25 October 2019 Keywords Evolution of flight, Jehol Biota, Birds, Enantiornithes, Cretaceous Corresponding authors Luis M.
  • Precocial Spectrum for Social Complexity in Mammals and Birds – a Review Isabella B

    Precocial Spectrum for Social Complexity in Mammals and Birds – a Review Isabella B

    Scheiber et al. Frontiers in Zoology (2017) 14:3 DOI 10.1186/s12983-016-0185-6 REVIEW Open Access The importance of the altricial – precocial spectrum for social complexity in mammals and birds – a review Isabella B. R. Scheiber1*, Brigitte M. Weiß2,3, Sjouke A. Kingma1 and Jan Komdeur1 Abstract Various types of long-term stable relationships that individuals uphold, including cooperation and competition between group members, define social complexity in vertebrates. Numerous life history, physiological and cognitive traits have been shown to affect, or to be affected by, such social relationships. As such, differences in developmental modes, i.e. the ‘altricial-precocial’ spectrum, may play an important role in understanding the interspecific variation in occurrence of social interactions, but to what extent this is the case is unclear because the role of the developmental mode has not been studied directly in across-species studies of sociality. In other words, although there are studies on the effects of developmental mode on brain size, on the effects of brain size on cognition, and on the effects of cognition on social complexity, there are no studies directly investigating the link between developmental mode and social complexity. This is surprising because developmental differences play a significant role in the evolution of, for example, brain size, which is in turn considered an essential building block with respect to social complexity. Here, we compiled an overview of studies on various aspects of the complexity of social systems in altricial and precocial mammals and birds. Although systematic studies are scarce and do not allow for a quantitative comparison, we show that several forms of social relationships and cognitive abilities occur in species along the entire developmental spectrum.