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Mesozoic Aviary Takes Form COMMENTARY Mesozoic aviary takes form Alan Feduccia* Department of Biology, University of North Carolina, Chapel Hill, NC 27599-3280 hen I attempted a modern synthesis of avian evolution in 1980 (1), I told the then science editor at Harvard WUniversity Press that I thought the in- formation on avian evolution was com- ing in so sluggishly that there would be little need for a quick revision. Was I ever wrong! By the early 1980s, the revelation of the presence of volant pa- leognaths in the Northern hemisphere Paleogene (2) provided compelling evi- dence that ratites were not ancient pas- sengers on drifting continents, but the product of a post-Cretaceous–Tertiary radiation from ancestors that for the most part flew to their respective conti- nents. In the same year, an initially muted epiphany appeared with the dra- matic discovery by Cyril Walker (3) of the existence of a completely unknown subclass of Mesozoic birds, which he called the enantiornithines, or opposite birds, so-called because the fusion of their tarsal elements was the opposite of that of ornithurine (modern-type) birds; Fig. 1. Simplified diagram of putative phylogenetic relationships of the major groups of the Mesozoic they also possess a distinctive arrange- aviary discussed here (and excluding the more problematic avian microraptors and flightless bird Cau- ment of the bones of the shoulder girdle dipteryx). The time of branching of the ornithurines remains a major question. (Modified from ref. 15.) and a unique sternum. The story of Mesozoic birds became complicated by the discovery in 1985, by Russian col- issue of PNAS, Zhou continued his re- Mesozoic. He included the enantiorni- league Evgeny Kurochkin (4), of Ambi- markable discoveries with colleague thines along with Archaeopteryx within a ortus, a Lower Cretaceous archaic but Fucheng Zhang (8), describing one of subclass Sauriuriae, as distinctive from modern-type ornithurine (carinate) bird the most dramatic discoveries from the the subclass Ornithurae, or birds of with an advanced flight apparatus. How- Chinese Early Cretaceous, a complete modern aspect. [The skull of Archae- ever, Walker’s discovery was followed by skeleton of Hongshanornis, the earliest opteryx is extremely similar to that of the discovery of additional enantiorni- known beaked ornithurine bird (archaic enantiornithines, particularly Cathayornis thine or opposite birds from the Lower but modern-type bird), coeval with op- (11).] Since then, archaic birds that do Cretaceous of Spain (5). In addition, at posite birds (enantiornithines) from the not fit clearly into a taxonomic group the 1992 meeting of the Society of same deposit. Hongshanornis was a small have been described, including the prim- Avian Paleontology and Evolution in bird with strong flying capability and itive beaked bird Confuciusornis, the Frankfurt, Germany, a young Chinese shows again the antiquity of modern seed-eating bird Jeholornis (with only paleontology graduate student appeared avian flight architecture, only some 20 three small teeth in the lower jaw), and for the first time and dazzled the con- or so million years after the earliest Sapeornis (with no lower jaw teeth), ference participants with discoveries of a known bird, the urvogel Archaeopteryx, thus bringing into question the exact major radiation of opposite birds from as well as size reduction characteristic of position of Archaeopteryx. Nevertheless, the Early Cretaceous of China, repre- more modern lineages. with the present description of the orni- sented by some 20 individual specimens Given the fact that the number of thurine Hongshanornis, the evidence belonging to at least three distinctive new species of Mesozoic birds discov- appears overwhelming that ‘‘Early Cre- taxa. Zhonghe Zhou’s discovery (6) was ered during the past decade more than taceous bird evolution highlights a to lead the way to one of the most dra- triples those described during the past distinctive dichotomy between enantior- matic breakthroughs in avian evolution 200 years, one can begin to have some nithines and ornithurines, the two major that followed during the ensuing years. degree of confidence in reconstructing avian groups of the Mesozoic’’ (ref. 8; This window on the Early Cretaceous their history. Although a number of dis- see also Fig. 1), a proposal that has via the Chinese Jehol Biota ranks with parate interpretations have appeared, a been only weakly contradicted by a only a handful of such deposits, includ- fairly clear picture emerges from the ing the Late Jurassic Solnhofen Lime- ongoing controversy. In 1983 and later stone, that has given us relatively in 1995, Martin (9, 10) noted the dis- Conflict of interest statement: No conflicts declared. complete pictures of the biota of a par- tinctiveness of the enantiornithines from See companion article on page 18998 in issue 52 of volume ticular time in the past and has revealed the ornithurines, and their worldwide 102. a relatively complete fauna of the world Cretaceous distribution indicated that *E-mail: [email protected]. of the Early Cretaceous (7). In a recent they were the dominant landbirds of the © 2005 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0509970102 PNAS ͉ January 3, 2006 ͉ vol. 103 ͉ no. 1 ͉ 5–6 Downloaded by guest on September 26, 2021 taxon from the Late Cretaceous (12), at endothermy) adapted this clade for the in front of the dentaries, previously a time when homoplasy may be at play. physiologically demanding shore-line known only in late Cretaceous ornithu- These two major clades of the Age of ecosystem. Physiological differences may rines (ichthyornithiforms and hesperor- Reptiles were also distinctive in many also explain why the enantiornithines nithiforms), and this character is very other ways, and notably studies of long- became extinct along with the dinosaurs likely a synapomorphy of the clade, bone histology show that enantiorni- at the end of the Cretaceous, whereas although it is also an independent thines and more basal birds still retained character uniting the dinosaurian clade growth rings, grew slowly, and were Ornithischia. likely ectothermic to a large degree. In Bone histology of To date, there is simply no evidence, contrast, the bone histology of Creta- either structural or biological, for the ceous ornithurines is similar to that of Cretaceous ornithurines existence of any form of protofeather modern birds, devoid of growth rings (14). Nevertheless, thanks to the careful (13). Such bone growth is suggestive of is similar to that work of Zhou and Zhang (8) and oth- ers, the field of Mesozoic birds has an endothermic physiology, a corollary made great strides, and the current dis- of strong flight and migratory ability, of modern birds. covery will go a long way toward clarify- perhaps associated with a shore-line ing what has been a murky picture of habitat in Cretaceous ornithurines. In- the avian past. We can now minimally the ornithurines by the end of the Cre- terestingly, Hongshanornis shows skeletal say that the aviary of the Age of Rep- features that indicate a shore-dwelling taceous had produced the font of the tiles comprised a number of basal habitat, conforming to what we know of modern, post-Cretaceous–Tertiary, avian groups, but was characterized by two many of the other Mesozoic ornithu- radiation. major clades, the archaic land birds or rines, especially the late Cretaceous ich- It is also clear that teeth were re- enantiornithines (opposite birds), and thyornithiforms and hesperornithiforms. duced and replaced by a beak several the primitive ornithurines (birds of mod- All but one of the enantiornithines is times in the Cretaceous ornithurines, ern aspect), the totality of which pro- known from lacustrine or terrestrial as well as in some primitive lineages duced an ancient adaptive radiation with habitats. Although speculative, it may be (Confuciusornis). In addition, another a surprising morphological diversity, that the advanced physiology of orni- revelation is that Early Cretaceous or- analogous in many respects to the diver- thurines (advanced flight capability and nithurines possessed a predentary bone sity of modern birds. 1. Feduccia, A. (1980) The Age of Birds (Harvard 6. Zhou, Z. (1995) Cour. Forschungsinst. Senckenberg 10. Martin, L. D. (1995) Cour. Forschungsinst. Senck- Univ. Press, Cambridge, MA). 181, 9–22. enberg 181, 23–36. 2. Houde, P. & Olson, S. L. (1981) Science 214, 7. Chang, M.-M. (2003) The Jehol Biota: The Emer- 11. Martin, L. D. & Zhou, Z. (1997) Nature 389, 1236–1237. gence of Feathered Dinosaurs, Beaked Birds, and 556. 3. Walker, C. A. (1981) Nature 292, 51–53. Flowering Plants (Shanghai Scientific and Techni- 12. Clarke, J. A. & Norell, M. A. (2002) Am. Mus. 4. Kurochkin, E. N. (1985) Cretaceous Res. 6, 271–278. cal Publishers, Shanghai). Novitates 3387, 1–46. 5. Sanz, J. L. & Bonaparte, J. F. (1992) in A New 8. Zhou, Z. & Zhang, F. (2005) Proc. Natl. Acad. Sci. 13. Chinsamy-Turan, A. (2005) The Microstructure of Order of Birds (Class Aves) from the Lower Creta- USA 102, 18998–19002. Dinosaur Bone (John Hopkins Univ. Press, Balti- ceous of Spain, Los Angeles County Museum of 9. Martin, L. D. (1983) in Perspectives in Ornithol- more). Science Series, ed. Campbell, K. E. (Los Angeles ogy, eds. Brush, A. H. & Clark, G. A., Jr. 14. Feduccia, A., Lingham-Soliar, T. & Hinchliffe, County Museum of Science, Los Angeles), Vol. (Cambridge Univ. Press, Cambridge, U.K.), pp. J. R. (2005) J. Morphol. 266, 125–166. 36, pp. 39–49. 291–338. 15. Zhou, Z. (2004) Naturwissenschaften 91, 455–471. 6 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0509970102 Feduccia Downloaded by guest on September 26, 2021.
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