ENANTIORNITHES

Contents

Enantiornithes

Etymology

Discovery

The Quality of the Fossils

Enantiornithine Development and Growth

Systematics

References

Enantiornithes

'Enantiornithes' is an extinct group of flying Protobirds. They were the most abundant and diverse avialans (see Avialae) of the Mesozoic. Almost all retained teeth and clawed hands, like other primitive birds. Enantiornithines are thought to have left no living descendants.
The current consensus is that 'Enantiornithes' is a sister group to Aves. This means that Enantiornithines are a successful experiment in bird evolution, but one that diversified entirely separately from the lineage leading to modern birds (Chiappe & Walker, 2002). This consensus has been challenged in some studies, so that it is possible that enantiornithines may actually represent successive outgroups on the lineage leading to modern birds (Clarke & Norell, 2002. Elzanowski, 1995).
Enantiornithines were more advanced than ''Archaeopteryx'' or ''Confuciusornis'', but more primitive than all living birds (Neornithes), perhaps following an intermediate evolutionary path. Over 40 species have been named, but some names represent only single bones, so it is likely that not all are valid. They have been found in both inland and marine sediments, suggesting that they were an ecologically diverse group. Enantiornithine fossils appear to include waders, swimmers, fish - catchers, and hook - beaked raptors. The smallest are described as sparrow-sized, but some were much larger, such as ''Avisaurus'', which had an estimated wingspan of 1.2 meters (4 ft).

Etymology

The word “Enantiornithes” means ‘opposite birds’. This term was coined by Cyril Walker in his landmark paper; ''New subclass of birds from the Cretaceous of South America'' (1981). Walker does not give a formal treatment of his etymology, so it is unclear what feature or features are "opposite". There is some confusion about this matter among other writers.
Feduccia (1996, pp. 142) states that;
"The birds are so named because, among many distinctive features, there is a unique formation of the triosseal canal and the metatarsals are fused proximally to distally, the opposite of that in modern birds"
Feduccia's point about the tarsometatarsus is logical and true but in fact Walker, who established the term, does not say this. Walker never described the fusion of the tarsometatarsus as opposite, but rather as "Only partial". Also, it is not certain that enantiornithines had triosseal canals, since no fossil preserves an articulated example (Chiappe & Walker, 2002. pp.250-251). Moreover, Walker (1981, pp. 51) seems to state his real reason for using the word "opposite";
"Perhaps the most fundamental and characteristic difference between the Enantiornithes and all other birds is in the nature of the articulation between the scapula (Fig. 2a, C) and the coracoid, where the 'normal' condition is completely reversed."
This refers to an anatomical feature - the articulation between the scapula and coracoid – which has a concave-convex configuration that is the inverse of that of modern birds. Specifically, in Enantiornithes, the scapular facet of the coracoid is a convex knob and the coracoidal facet of the scapula is a concave dish - shaped excavation to receive it. In neornithes the scf is a round pit, which receives the tct, or coracoidal tubercle of the scapula (Hope, 2002).

Discovery

The first enantiornithines to be discovered were incorrectly referred to modern bird groups. They were first recognized as a distinct subclass by C.A. Walker, in 1981, based on some partial remains from the Late Cretaceous Period of what is now Argentina. In the 1990s, more complete enantiornithines were discovered and it was demonstrated that a few previously found birds (''Iberomesornis'', ''Cathayornis''/''Sinornis'') had enantiornithine features.
Enantiornithines have been found in North America, South America, Europe, Asia, and Australia. Known fossils attributable to this group are exclusively Cretaceous and it is believed that enantiornithines became extinct at the same time as their non-avian dinosaur relatives. One biogeographic study in the 1990s suggested that the distribution of enantiornithines implies a Middle Jurassic origin for the clade, but this theory has not been widely accepted by paleoornithologists; a Late Jurassic/Early Cretaceous origin is easier to reconcile with the fossil record. The earliest known enantiornithines are from the Early Cretaceous) of Spain (e.g. ''Noguerornis'', a basal genus) and China (e.g. ''Eoenantiornis'', a more derived genus) and the latest from the Late Cretaceous of North and South America (e.g. ''Avisaurus''). The widespread occurrence suggests that the Enantiornithes were able to cross oceans on their own power; they are the first bird lineage with a global distribution.

The Quality of the Fossils

Many enatiornithine fossils were found in fragmentary states, and some are known only from a single bone. Particularly exquisite specimens that are complete, in full articulation and with soft tissue preservation are known from Las Hoyas in Cuenca, Spain and the Yixian Formation in Liaoning, China.
''Eoalulavis'' (Sanz et al.,1995) was found to have the fragmentary exoskeletons of aquatic crustaceans preserved in its digestive tract.
Recently, palaeontologists in China found an enantiornithine fossil with flight feathers on its legs as well as its arms (Zhang & Zhou, 2004), similar to the four-winged dinosaur ''Microraptor''. However, the leg feathers of the enantiornithine differ from those of ''Microraptor'' in being shorter, and only extending down to the ankle rather than along the foot as in the four-winged dinosaur.

Enantiornithine Development and Growth

Described enantiornithine fossils include eggs (Mikhailov, 1991,1996), embryoes (Elzanowski, 1981), and hatchlings (Sanz et al., 1997).
An enantiornithine embryo, still curled in its egg, has been reported from the Yixian Formation (Zhou, Zhang, 2004). Together with the hatchlings assigned to Gobipteryx(Elzanowski, 1995), these finds demonstrate that enantiornithine hatchlings had the skeletal ossification, well - developed wing feathers and the large brain which may correlate with precocial or superprecocial development in birds of today. Thus, at least some enantiornithine birds probably hatched from the egg substantially developed and ready to run, forage, and even fly in a just a few days.
Analyses of enantiornithine bone histology have been conducted to determine the growth rates of the animals. One recent study of Concornis bones shows a growth pattern different from modern birds (Cambra-Moo et al. 2006). Although growth was rapid for some weeks after hatching - probably until fledging - this fairly small species did not reach adult size for a long time, probably several years. Other studies (Sanz et al. 1995) have shown that growth was slow, as it is in living precocial birds. Altricial birds, on the other hand, are known to reach adult mass quickly thanks to lavish parental feeding. Still other analyses (Chiappe, 1995) have interpreted the bone histology to indicate that enantiornithines may not have had fully avian endothermy, instead having an intermediate metabolic rate.

Systematics

Enantiornithes is the sister group to Aves, and together they form a clade called Ornithothoraces. Several phylogenic studies have recovered Enantiornithes as a monophyletic clade distinct from Aves. One phylogeny, though (Clarke & Norell, 2002) reduced the number of unique enantiornithine apomorphies to just four. This raises the possibility that the addition of new fossils could unite Enantiornithes and Aves into one monophyletic clade. If this proves to be true, then Enantiornithes is a paraphyletic "clade" and, thus, invalid. All enantiornithines would then be grouped in the next larger clade Ornithothoraces instead, and called "ornithothoracines".
Enantiornithine systematics undergo frequent revision. The version used here, although based on many sources, is provisional, and in need of revision in light of abundant new fossil discoveries. What appears fairly certain by now (Chiappe, 2002) is that there were subdivisions within Enantiornithes, including some minor basal lineages in addition to the Euenantiornithes. The details of the interrelationship of all these lineages, indeed the validity of most, is disputed, although the Avisauridae, for one example, seem likely to constitute a valid group. Phylogenetic taxonomists have hitherto been very reluctant, and justifiably so, to suggest delimitations of enantiornithine clades (Sereno, 2005).
Phylogeny based on Chiappe (1992) Chiappe & Calvo (1994), Kurochkin (1996), Zhou & Hou (2002), Chiappe & Walker (2002) and Haaramo (2006):
'SUBCLASS ENANTIORNITHES'

★ Basal Enantiornithes and Enantiornithes ''incerta sedis''

★
★ ''Dapingfangornis'' (Early Cretaceous)

★
★ ''"Liaoxiornis"'' (Early Cretaceous) - a ''nomen dubium''

★
★ Enantiornithes gen. et sp. indet. CAGS-IG-02-0901 (Xiagou Early Cretaceous of Mazongshan, China)

★
★ Enantiornithes gen. et sp. indet. CAGS-IG-04-CM-023 (Xiagou Early Cretaceous of Changma, China: Harris 2006)

★
★ ''Elsornis'' (Late Cretaceous)

★
★ Enantiornithes gen. et sp. indet. (Late Cretaceous of Cruzy, France: Buffetaut 1998)

★
★ Enantiornithes gen. et sp. indet. MCSNM V3882a (Late Cretaceous of Ouadi al Gabour, Lebanon)

★
★ Enantiornithes gen. et sp. indet. MZ unnumbered (Adamantina Late Cretaceous of Presidente Prudente, Brazil) - enantiornithiform?

★
★ Enantiornithes gen. et sp. indet. Patrick Mechin collection 606 (Late Cretaceous of Bastide-Neuve, France) - alexornithid? (Buffetaut ''et al.'' 2000)

★
★ Order Iberomesornithiformes (disputed)

★
★
★ Family Iberomesornithidae

★
★
★
★ ''Iberomesornis'' (Early Cretaceous)

★
★
★
★ ''Noguerornis'' (Early Cretaceous)

★ Superorder Euenantiornithes

★
★ Basal Euenantiornithes

★
★ ''Concornis'' (Early Cretaceous) - enantiornithiform?

★
★ ''Eoalulavis'' (Middle Cretaceous)

★
★ Euenantiornithes ''incerta sedis''

★
★ ''Boluochia'' (Early Cretaceous) - cathayornithid?

★
★ ''Cuspirostrisornis'' (Early Cretaceous)

★
★ Enantiornithes gen. et sp. indet. CAGS-IG-04-CM-007 (Xiagou Early Cretaceous of Mazongshan, China: Lamanna ''et al.'' 2006)

★
★ ''Eoenantiornis'' (Early Cretaceous)

★
★ ''Largirostrornis'' (Early Cretaceous)

★
★ ''Longchengornis'' (Early Cretaceous)

★
★ ''Longirostravis'' (Early Cretaceous)

★
★ ''Hebeiornis'' (Early Cretaceous) - possibly a ''nomen nudum''; if valid, includes ''Vescornis''

★
★ Enantiornithes gen. et sp. indet. RBCM.EH2005.003.0002 (Northumberland Late Cretaceous of Hornby Island, Canada: Morrison ''et al.'' 2005)

★
★ ''Gurilynia'' (Late Cretaceous) - enantiornithiform?

★
★ ''Halimornis'' (Late Cretaceous)

★
★ ''Lectavis'' (Late Cretaceous) - enantiornithiform?

★
★ ''Lenesornis'' (Late Cretaceous)

★
★ ''Yungavolucris'' (Late Cretaceous) - enantiornithiform?

★
★ Family Kuszholiidae (disputed)

★
★
★ ''Kuszholia'' (Late Cretaceous)

★
★ Order Aberratiodontuiformes (disputed)

★
★
★ Family Aberratiodontuidae

★
★
★
★ ''Aberratiodontus'' (Early Cretaceous)

★
★ Order "Cathayornithiformes" (disputed)

★
★
★ Family "Cathyornithidae"

★
★
★
★ ''Sinornis/Cathayornis'' (Early Cretaceous) - which name is correct is disputed

★
★
★
★ ''Eocathayornis'' (Early Cretaceous)

★
★ Order Alexornithiformes (disputed)

★
★
★ Family Alexornithidae

★
★
★
★ ''Alexornis'' (Late Cretaceous)

★
★
★
★ ''Kizylkumavis'' (Late Cretaceous)

★
★
★
★ ''Sazavis'' (Late Cretaceous)

★
★ Order Gobipterygiformes (disputed)

★
★
★ Family Gobipterygidae

★
★
★
★ ''Gobipteryx'' (Late Cretaceous)

★
★ Order Enantiornithiformes

★
★
★ Family Enantiornithidae (disputed)

★
★
★
★ ''Enantiornis'' (Late Cretaceous)

★
★
★ Family Avisauridae

★
★
★
★ ''Avisaurus'' (Late Cretaceous)

★
★
★
★ ''Neuquenornis'' (Late Cretaceous)

★
★
★
★ ''Soroavisaurus'' (Late Cretaceous)
Sometimes included in the Enantiornithes are the following taxa:

★ ''Longipteryx'' (Early Cretaceous) - euenantiornithine (own order)?

★ ''Protopteryx'' (Early Cretaceous of China)

★ ''Nanantius'' (Early and possibly Late Cretaceous) - enantiornithiform?

★ ''Abavornis'' (Late Cretaceous)

★ ''Horezmavis'' (Late Cretaceous of Kyzyl Kum, Uzbekistan) - gobipterygiform?

★ ''Gargantuavis'' (Late Cretaceous of S France)

★ ''Incolornis'' (Late Cretaceous)

★ ''Patagopteryx'' (Late Cretaceous)

★ Family Zhyraornithidae - enantiornithiform?

★
★ ''Zhyraornis'' (Late Cretaceous)

★ ''Catenoleimus''

★ ''Explorornis''.
The validity of the supposed Early Cretaceous euenantiornithine ''"Jibeinia"'' is disputed; the holotype seems lost. The Late Cretaceous taxon ''"Cerebavis"'' is based on an endocranial cast and while this is not diagnostic, it is different from modern birds and as far as can be told from Ornithurae in general.

References

★ 'Buffetaut', Éric (1998): First evidence of enantiornithine birds from the Upper Cretaceous of Europe: postcranial bones from Cruzy (Hérault, France). ''Oryctos'' '1': 127-130. HTML abstract

★ 'Buffetaut', Éric; Mechin, Patrick & Mechin-Salessy, Annie (2000): An archaic bird (Enantiornithes) from the Upper Cretaceous of Provence (southern France). ''C. R. Acad. Sci. Paris IIA - Sciences de la Terre et des planètes'' '331'(8): 557–561. (HTML abstract)

★ 'Cambra-Moo', Oscar; Delgado Buscalioni, Ángela; Cubo, Jorge; Castanet, Jacques; Loth, Marie-Madeleine; de Margerie, Emmanuel & de Ricqlès, Armand (2006): Histological observations of Enantiornithine bone (Saurischia, Aves) from the Lower Cretaceous of Las Hoyas (Spain). ''C. R. Palevol'' '5'(5): 685–691. PDF fulltext

★ 'Chiappe', Luis M. (1992): Enantiornithine (Aves) tarsometatarsi and the avian affinites of the Cretaceous Avisauridae. ''Journal of Vertebrate Paleontology'' '12'(3): 344-350.

★ 'Chiappe', Luis M. & 'Calvo', J. M. (1994): ''Neuquenornis volans'', a new Late Cretaceous bird (Enantiornithes: Avisauridae) from Patagonia, Argentina. ''Journal of Vertebrate Paleontology'' '14'(2): 230-246. HTML abstract

★ 'Chiappe, Luis M.' & 'Walker', C. A. (2002): Skeletal morphology and systematics of the Cretaceous Euenantiornithes (Ornithothoraces: Enantiornithes). ''In:'' Chiappe, Luis M. & Witmer, Lawrence M. (eds.): Mesozoic Birds: Above the Heads of Dinosaurs: 240-267. University of California Press, Berkeley. ISBN 0520200942

★ 'Chiappe, Luis M.' (1998): Wings over Spain - bird fossils - includes related article, ''Natural History'', Sept, fulltext

★ 'Clarke', Julia A.; Norell, Mark A. (2002) The Morphology and Phylogenetic Position of Apsarvais ukhaana from the Late Cretaceous of Mongolia. American Museum Novitates. No. 3387. American Museum of Natural History. Central Park West at 79th Street. New York, NY 10024.

★ 'Feduccia', Alan. (1996) the Origin and Evolution of Birds. Yale University. New Haven, Conn.

★ 'Haaramo', Mikko (2006): Mikko's Phylogeny Archive: †Enantiornithes. Version of 2006-APR-03. Retrieved 2006-OCT-02.

★ 'Harris', Jerald D.; Lamanna, Matthew C.; You, Hai-lu; Ji, Shu-an & Ji, Qiang (2006): A second enantiornithean (Aves: Ornithothoraces) wing from the Early Cretaceous Xiagou Formation near Changma, Gansu Province, People's Republic of China. ''Canadian Journal of Earth Sciences'' '43'(5): 547–554. PDF fulltext

★ 'Hope', Sylvia. The Mesozoic record of Neornithes (modern birds). ''In:'' Chiappe, Luis M. & Witmer, Lawrence M. (eds.): Mesozoic Birds: Above the Heads of Dinosaurs: pp. 339-388. University of California Press, Berkeley. ISBN 0520200942

★ 'Kurochkin', E. (1996): A new enantiornithid of the Mongolian Late Cretaceous, and a general appraisal of the Infraclass Enantiornithes (Aves). Paleontological Institute, Moscow, 60 pp.

★ 'Lamanna', Matthew C.; You, Hai-lu; Harris, Jerald D.; Chiappe, Luis M.; Ji, Shu-an; Lü, Jun-chang & Ji, Qian (2006): A partial skeleton of an enantiornithine bird from the Early Cretaceous of northwestern China. ''Acta Palaeontologica Polonica'' '51'(3): 423–434. PDF fulltext

★ 'Morrison', Kurt; Dyke, Gareth J. & Chiappe, Luis M. (2005): Cretaceous fossil birds from Hornby Island (British Columbia). ''Canadian Journal of Earth Sciences'' '42'(12): 2097–2101. HTML abstract

★ 'Norell', Mark A.; Clarke, Julia A. (2001) Fossil that fills a critical gap in avian evolution. Nature Vol. 409 11 January 2001 pp. 181 - 184

★ 'Sanz', J.L., Bonaparte, J.F. (1992). A new order of birds (Class Aves) from the Lower Cretaceous of Spain; pp. 39-49 in; Papers in Avian Paleontology, Honoring Pierce Brodkorp. Science Series 36. Natural history Museum of Los Angeles County, Los Angeles.

★ 'Sanz', J.L., Chiappe, L.M.,Buscalioni, A.D. (1995). The Osteology of Concornis lacustris (Aves:Enantiornithes) from the Lower Creataceous of Spain and a reexamination of its phylogenetic relationships. American Museum Novitates 3133:1-23.

★ 'Sanz', J.L., Chiappe, L.M., Pérez-Moreno, B.P., Buscalioni, A.D., Moratalla, J.F., Ortega, F., Poyato-Ariza, F.J.(1996)A new Lower Creatceous bird from Spain: implications for the evolution of flight. Nature 382:442-445.

★ 'Sanz', J.L., Chiappe, L.M., Pérez-Moreno, B.P., Moratalla, J.F., Hernández-Carrasquilla, F. Buscalioni, A.D., Ortega, F., Poyato-Ariza, F.J., Rasskin-Gutman, D., Martínez-Delclós, X. (1997) A nestling bird from the Early Cretaceous of Spain:implications for avian skull and neck evolution. Science 276:pp.1543-1546.

★ 'Sereno', P. C. (2005): ''TaxonSearch: Stem Archosauria''. Version 1.0, 2005 November 7. Retrieved 2006-OCT-02.

★ 'Walker', C. A. (1981): New subclass of birds from the Cretaceous of South America. ''Nature'' '292': 51-53. {DOI|10.1038/292051a0}} (HTML abstract)

★ ''Zhang'', Fucheng; Zhou, Zhonghe. (2004): Leg feathers in an Early Cretaceous bird. Nature 21 October 2004 Vol. 431 pp. 925.

★ 'Zhou', Z. & 'Hou', L.-H. (2002): The Discovery and Study of Mesozoic Birds in China. ''In'' Chiappe, Luis M. & Witmer, Lawrence M. (eds.): Mesozoic Birds: Above the Heads of Dinosaurs: 160-183. ISBN 0520200942

★ 'Zhou', Z. & 'Zhang', F. (2004) A Precocial Avian Embryo from the Lower Cretaceous of China. ''Science'' , 22 October 2004. vol. 36, # 5696, pp. 653.

★ 'Zhou', Z. & 'Zhang', F. (2005): Discovery of an ornithurine bird and its implication for Early Cretaceous avian radiation. ''PNAS'' '102'(52): 18998-19002. PDF fulltext Supporting Information