Enantiornithes

Enantiornithes is an extinct group of primitive birds. They were the most abundant and diverse avialans of the Mesozoic. Almost all retained teeth and clawed hands, like other primitive birds. Enantiornithines are thought to have left no living descendants. See protobirds.

A consensus of scientific analyses indicates that Enantiornithes is one of two major sister groups of derived birds. The other group is the Ornithurae, which includes all living birds as a subset. This means that Enantiornithines are a successful experiment in bird evolution, but one that diversified entirely separately from the lineage leading to modern birds. This consensus has never been universally accepted and is being challenged by new studies, so that it is possible that enantiornithines may actually represent successive outgroups on the lineage leading to modern birds. See Apsaravis.

Most researchers place Enantiornithines in Aves, but those that use the more restricive definition of Aves put them lower in the Avialae. Enantiornithines were more advanced than Archaeopteryx or Confuciusornis, but in several respects more primitive than all living birds (Neornithes), perhaps following an intermediate evolutionary path. Due to the primitive features, some early studies placed Enantiornithes with Archaeopteryx in the clade Sauriurae, but only a few researchers still do.

Over 40 species of Enantiornithines 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). Enantiornithine birds went extinct at the K-T boundary, along with hesperornithine birds and all other non-avian dinosaurs, and many other life forms.

Etymology

"Enantiornithes" means "opposite birds", from Ancient Greek einantios (ἐνάντιος) "opposite" + ornithes (όρνιθες) "birds" . This term was coined by Cyril Walker in his landmark paper which established the group. Walker did not give a formal treatment of his etymology, and left it unclear what feature or features are "opposite". Elsewhere in his paper, however, Walker did state his real reason for using the term "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 [...] and the coracoid, where the 'normal' condition is completely reversed."

This refers to an anatomical feature - the articulation of the shoulder bones – 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 scapular facet of the coracoid is a round pit, which receives the coracoidal tubercle of the scapula - compare the human glenohumeral joint, where the scapula has a similar excavation, but to receive the humerus as the coracoid is absent in mammals.

Walker's ambiguity on his reason for naming the group led to some confusion about this matter among later researchers. For example, Alan Feduccia stated in 1996:

"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 correct, but Walker did not use this reasoning in his original paper. 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 this feature.

Discovery

The first enantiornithines to be discovered were incorrectly referred to modern bird groups. They were first recognized as a distinct lineage by C. A. Walker, in 1981, based on some partial remains from the late Cretaceous period of what is now Argentina. Since the 1990s, more complete enantiornithines were discovered and it was demonstrated that a few previously described birds (e.g. 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 more in line 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. Some might thus even have been migratory, but given the markedly warmer climate of the Mesozoic and the fact that the known Enantiornithes are regions that were subtropical if not tropical at that time, it seems hardly likely that at least the known diversity of these birds contains long-distance migrants.

Enantiornithine fossils

Many enantiornithine fossils were found in fragmentary states, and some taxa 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 (PRC). Eoalulavis was found to have the remains of exoskeletons of aquatic crustaceans preserved in its digestive tract.

Another interesting find from Las Hoyas was reported by Sanz et al. in 2001. The fossil includes the remains of four hatchling enantiornithine skeletons of three different species. They are substantially complete, very tightly associated, and show surface pitting of the bones that indicates partial digestion. The authors concluded that this association was a regurgitated pellet and, from the details of the digestion and the size, that the hatchlings were swallowed whole by a pterosaur or small theropod dinosaur. This was the first evidence that Mesozoic birds were prey animals, and that some Mesozoic ornithodires regurgitated pellets like owls do today.

Zhang and Zhou in 2004 described an enantiornithine fossil with wing-like feather tufts on its legs, similar to Archaeopteryx. Leg feathers are also reminiscent of the four-winged dinosaur Microraptor, however, in the enantiornithine differ from the feathers are shorter, more disorganized (do not clearly form a wing) and only extend down to the ankle rather than along the foot. Considered together, these not too closely-related animals suggest that auxiliary leg feathers may have been a recurring feature in the evolution and refinement of flight in theropods.

Life history

Described enantiornithine fossils include eggs, embryos, and hatchlings. An enantiornithine embryo, still curled in its egg, has been reported from the Yixian Formation. Together with the hatchlings assigned to Gobipteryx, these finds demonstrate that enantiornithine hatchlings had the skeletal ossification, well-developed wing feathers and the large brain which correlate with precocial or superprecocial pattern of development in birds of today. Thus, at least some enantiornithine birds probably hatched from the egg substantially developed and ready to run, forage, and possibly even fly in a just a few days. This, together with the fact that the most ancient lineages of modern birds - paleognaths and Galloanserae - are precocial, suggests that the precocial condtion is plesiomorphic and was common among Cretaceous birds.

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: 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. Another study supports that growth to adult size was slow, as it is in living precocial birds. Altricial birds on the other hand are known to reach adult size quickly thanks to lavish parental feeding. Still other analyses have interpreted the bone histology to indicate that enantiornithines may not have had fully avian endothermy, instead having an intermediate metabolic rate.

Classification

Phylogeny

Enantiornithes is the sister group to Ornithurae or Ornithuromorpha depending on the taxonomic authority, and together they could form a clade called Ornithothoraces. Most phylogenetic studies have recovered Enantiornithes as a monophyletic group distinct from the modern birds and their closest relatives. The 2002 phylogenetic analysis by Clarke and Norell, though, reduced the number of enantiornithine autapomorphies to just four. This raises the possibility that the discovery of new fossils could unite Enantiornithes and the birds closer to living species into one clade. If this proves to be true, then Enantiornithes is a paraphyletic taxon and thus phylogenetically invalid. All enantiornithines would then be united in the next larger clade Ornithothoraces instead, and called "ornithothoracines". (see Apsaravis for more on the possible invalidation of Enantiornithes)

On the other hand, Confuciusornis might be closer to Enantiornithes than to living birds rather than about equally distinct from both, which in turn would render the Ornithothoraces meaningless too. In that case, the Pygostylia would apply, but that taxon, too, is ill-defined. Altogether, the radiation of the early truly avian lineages (as opposed to "dinobirds" like Archaeopteryx or Dalianraptor) presents a highly confusing picture at present, and while the deep divergence between Enantiornithes and Neornithes seems for real, the relationships of these two and other Cretaceous groups like Hesperornithes or Liaoningornithiformes is not well resolved.

Enantiornithine systematics are also highly provisional. The version used here, although based on many sources, is only tentative, and in need of revision in light of abundant new fossil discoveries. What appears fairly certain by now is that there were subdivisions within Enantiornithes possibly including some minor basal lineages in addition to the more apomorphic Euenantiornithes. The latter may be a clade or an evolutionary grade (and hence are also of questionable validity). 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.

Taxonomy

Subclass Enantiornithes

• Basal Enantiornithes and Enantiornithes incerta sedis
• Dapingfangornis (Early Cretaceous)
• "Liaoxiornis" (Early Cretaceous) - a nomen dubium
• Pengornis (Jiufotang Early Cretaceous of Dapingfang, China)
• 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)
• Elsornis (Late Cretaceous)
• Enantiornithes gen. et sp. indet. (Late Cretaceous of Cruzy, France)
• 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?
• Order Iberomesornithiformes (disputed)
• Family Iberomesornithidae
• Iberomesornis (Early Cretaceous)
• Noguerornis (Early Cretaceous)
• Superorder Euenantiornithes
• Basal Euenantiornithes
• Eoalulavis (Early Cretaceous)
• Euenantiornithes incerta sedis
• Boluochia (Early Cretaceous) - cathayornithid?
• Concornis (Early Cretaceous) - cathayornithid? enantiornithiform?
• Cuspirostrisornis (Early Cretaceous)
• Enantiornithes gen. et sp. indet. CAGS-IG-04-CM-007 (Early Cretaceous)
• 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 (Late Cretaceous)
• Gurilynia (Late Cretaceous) - enantiornithiform?
• Halimornis (Late Cretaceous)
• Lectavis (Late Cretaceous) - enantiornithiform?
• Lenesornis (Late Cretaceous)
• Neuquenornis (Late Cretaceous) - cathayornithid? avisaurid?
• Yungavolucris (Late Cretaceous) - enantiornithiform?
• Family Kuszholiidae (disputed)
• Kuszholia (Late Cretaceous)
• Order Cathayornithiformes (disputed)
• Family Alethoalaornithidae
• Alethoalaornis (Early Cretaceous of Liaoning, China)
• 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)
• Soroavisaurus (Late Cretaceous)

Sometimes included in the Enantiornithes are the following taxa:

• Aberratiodontus (Early Cretaceous) - euenantiornithine (own order)?
• Longipteryx (Early Cretaceous) - euenantiornithine (own order)?
• Paraprotopteryx (Yixian Early Cretaceous of Fengning, China)
• Protopteryx (Early Cretaceous of China)
• Wyleyia (Early Cretaceous) - basal?
• Nanantius (Early -? Late Cretaceous) - enantiornithiform?
• Abavornis (Late Cretaceous) - euenantiornithine?
• Catenoleimus (Late Cretaceous)
• Explorornis (Late Cretaceous) - euenantiornithine?
• Horezmavis (Late Cretaceous of Kyzyl Kum, Uzbekistan) - gobipterygiform?
• Gargantuavis (Late Cretaceous)
• Incolornis (Late Cretaceous) - euenantiornithine?
• Patagopteryx (Late Cretaceous)
• Dalingheornis
• Family Zhyraornithidae - enantiornithiform?
• Zhyraornis (Late Cretaceous)

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