Enantiornithines

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. Over 50 species of Enantiornithines have been named, but some names represent only single bones, so it is likely that not all are valid. Enantiornithine birds went extinct at the K-Pg boundary, along with hesperornithine birds and all other non-avian dinosaurs, and many other life forms. Enantiornithines are thought to have left no living descendants.

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 branch of 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.

Most researchers place Enantiornithines in Aves, but those that use the more restrictive 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 modern 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.

Discovery and naming
The first enantiornithines to be discovered were incorrectly referred to modern bird groups. They were first recognized as a distinct lineage by Cyril 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.

"Enantiornithes" means "opposite birds", from Ancient Greek einantios (ἐνάντιος) "opposite" + ornithes (όρνιθες) "birds". The name was coined by Walker in his landmark paper which established the group. In his paper, Walker explained what he meant by "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 socket joint that is the reverse of that of modern birds. Specifically, in enantiornithines, the facet where the scapula (shoulder blade) meets the coracoid (the primary bone of the shoulder girdle in vertebrates other than mammals) is a convex knob and the corresponding point on the shoulder blade is concave and dish-shaped. In modern birds, the way the joint articulates is reversed.

Walker was not clear on his reasons for giving this name in the Etymology section of his paper, and this ambiguity led to some confusion 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 (the combined upper foot and ankle bone) 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.

Description
Many enantiornithine fossils are found in highly fragmentary states, and some taxa are known only from a piece of 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). 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 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).

Skull
Given their wide range of habitats and diets, the skulls of enantiornithines varied considerably between species. Enantiornithine skulls combined a unique suite of primitive and advanced characteristics. As in more basal birds like Archaeopteryx, they retained the postorbital bone and a small premaxilla, and most species had toothy jaws rather than toothless beaks. Only a few species, such as Gobipteryx minuta, were fully toothless.

Wing
As a very large group of birds, enantiornithines displayed a diversity of different body plans based on differences in ecology and feeding. The wings of enantiornithines were relatively advanced compared to basal birds, and Eoalulavis shows that at least some had an alula, or "bastard wing", granting higher maneuverability in the air. One enantiornithine fossil shows 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.

Tail
Clarke et al. (2006) surveyed all enantiornithine fossils then known and concluded that none had preserved tail feathers that formed a lift-generating fan, as in modern birds. They found that all birds outside of the ornithurae with preserved tail feathers had only short coverts or elongated paired tail plumes. Thus, they suggested that the development of the pygostyle in enantiornithes must have been a function of tail shortening, not the development of a modern tail feather anatomy. An ornithurine bird, Yixianornis, was reported by the authors as the earliest bird with a fan of tail feathers. However, in 2009, an enantiornithine called Shanweiniao was reported with four long tail feathers that overlapped each other, possibly forming a lift-generating surface similar to the tail fans of modern birds.

Origin and range
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. Protopteryx) 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 from regions that were subtropical if not tropical at that time, it seems unlikely that the known diversity of these birds contains long-distance migrants.

Diet
Given the wide diversity of skull shape among enantiornithines, many different dietary specializations must have been present among the group. Some forms, like Shenqiornis, had large, robust jaws suitable for eating hard-shelled invertebrates. In longipterygids, the snouts were long and thin with teeth restricted to the tip of the jaws, and they were likely mud-probers (small-toothed species) and fishers (large-toothed species). The short, blunt teeth of Pengornis were likely used to feed on soft-bodied arthropods.

A few specimens preserve actual stomach contents. Unfortunately, none of these preserve the skull, so direct correlation between their known diet and snout/tooth shape cannot be made. Eoalulavis was found to have the remains of exoskeletons of aquatic crustaceans preserved in its digestive tract. , and Enantiophoenix preserves corpuscles of amber among the fossilized bones, suggesting that this animal fed on tree sap, much like modern sapsuckers and other birds. The sap would have fossilized and become amber.

Predation
A specimen from Las Hoyas reported by Sanz et al. in 2001 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.

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. Juvenile specimens can be identified by a combination of factors: rough texture of their bone tips indicating portions which were still made of cartilage at the time of death, relatively small breastbones, large skulls and eyes, and bones which had not yet fused to one another. Some hatchling specimens have been given formal names, including "Liaoxiornis delicatus"; however, Luis Chiappe and colleagues considered the practice of naming new species based on juveniles detrimental to the study of enantionrithines, because it is nearly impossible to determine which adult species a given juvenile specimen belongs to, making any species with a hatchling holotype a nomen dubium.

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 patterns 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 condition 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
Enantiornithine classification and taxonomy has historically been complicated by a number of factors. In 2010, Mesozoic bird paleontologists Jingmai O'Connor and Gareth Dyke outlined a number of criticisms against the prevailing practices of scientists failing to describe many specimens in enough detail for others to evaluate thoroughly. Some species have been described based on specimens which are held in private collections, making further study or review of previous findings impossible. Because it is often unfeasible for other scientists to study each specimen in person given the worldwide distribution of the Enantiornithes, and due to the many uninformative descriptions which have been published on possibly important specimens, many of these specimens become "functional nomina dubia". Furthermore, many species have been named based on extremely fragmentary specimens, which would not be very informative scientifically even if they were described sufficiently. Over one-third of all named enantiornithine taxa are based on only a fragment of a single bone. O'Connor and Dyke argued that while these specimens can help expand knowledge of the time span or geographic range of the Enantiornithes and it is important to describe them, naming such specimens is "unjustifiable".

Phylogeny
Enantiornithes is the sister group to Ornithurae or Ornithuromorpha depending on the taxonomic authority, and together they 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.

Enantiornithine systematics are 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 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 to suggest delimitations of enantiornithine clades.

Cau and Arduini, 2008

Zhou, Zhang and Li, 2010a

O'Connor, Gao and Chiappe, 2010b

You et al., 2010d

Taxonomy
Subclass Enantiornithes


 * Basal Enantiornithes and Enantiornithes incerta sedis
 * "Cathayornis" chabuensis (Early Cretaceous of Chabu, China) – cathayornithid?
 * Dapingfangornis (Early Cretaceous)
 * 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)
 * Huoshanornis (Early Cretaceous) – Euenantiornithes?
 * "Liaoxiornis" (Early Cretaceous) – a nomen dubium
 * Pengornis (Early Cretaceous)
 * Qiliania (Xiagou Early Cretaceous)
 * Elsornis (Late Cretaceous) – close to Flexomornis?
 * 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?
 * Flexomornis (Late Cretaceous) – close to Elsornis?
 * Order Iberomesornithiformes
 * Family Iberomesornithidae
 * Enantiornithes gen. et sp. indet. CAGS-IG-07-CM-001
 * Iberomesornis (Early Cretaceous)
 * Noguerornis (Early Cretaceous)
 * Superorder Euenantiornithes
 * Basal Euenantiornithes
 * Eoalulavis (Early Cretaceous)
 * Euenantiornithes incerta sedis
 * Bohaiornis (Early Cretaceous)
 * Cuspirostrisornis (Early Cretaceous)
 * Eoenantiornis (Early Cretaceous)
 * Elbretornis (Late Cretaceous)
 * Enantiornithes gen. et sp. indet. CAGS-IG-04-CM-007 (Early Cretaceous)
 * Enantiornithes gen. et sp. indet. RBCM.EH2005.003.0002 (Late Cretaceous)
 * Gurilynia (Late Cretaceous) – enantiornithiform?
 * Hebeiornis (Early Cretaceous) – possibly a nomen nudum; see Vescornis and Jibeinia
 * Martinavis (Late Cretaceous)
 * Largirostrornis (Early Cretaceous)
 * Lectavis (Late Cretaceous) – enantiornithiform?
 * Lenesornis (Late Cretaceous)
 * Longchengornis (Early Cretaceous)
 * Yungavolucris (Late Cretaceous) – enantiornithiform?
 * Family Kuszholiidae (disputed)
 * Kuszholia (Late Cretaceous)
 * Order Alexornithiformes (disputed)
 * Family Alexornithidae
 * Alexornis (Late Cretaceous)
 * Kizylkumavis (Late Cretaceous)
 * Sazavis (Late Cretaceous)
 * Order Protopterygiformes
 * Family Protopterygidae
 * Protopteryx (Early Cretaceous)
 * Order Longipterygiformes
 * Family Longipterygidae
 * Boluochia (Early Cretaceous)
 * "Camptodontus" (Jiufotang Early Cretaceous of Chaoyang City, China)
 * Longipteryx (Early Cretaceous)
 * Longirostravis (Early Cretaceous)
 * Rapaxavis (Jiufotang Early Cretaceous of Chaoyang City, China)
 * Shanweiniao (Yixian Early Cretaceous of China)
 * Order Cathayornithiformes
 * Family Alethoalaornithidae
 * Alethoalaornis (Early Cretaceous of Liaoning, China)
 * Family Cathyornithidae
 * Cathayornis (Early Cretaceous)
 * Eocathayornis (Early Cretaceous)
 * Sinornis (Early Cretaceous)
 * Order Gobipterygiformes
 * Family Gobipterygidae
 * Gobipteryx (Late Cretaceous)
 * ? Jibeinia (Early Cretaceous)
 * Vescornis (Early Cretaceous)
 * Order Enantiornithiformes
 * Family Enantiornithidae (disputed)
 * Enantiornis (Late Cretaceous)
 * Family Avisauridae
 * Avisaurus (Late Cretaceous)
 * Bauxitornis (Late Cretaceous)
 * Concornis (Early Cretaceous)
 * Enantiophoenix
 * Halimornis (Late Cretaceous)
 * Intiornis (Late Cretaceous)
 * Neuquenornis (Late Cretaceous)
 * Soroavisaurus (Late Cretaceous)

Sometimes included in the Enantiornithes are the following taxa:
 * Aberratiodontus (Early Cretaceous) – euenantiornithine (own order)?
 * Dalingheornis (Yixian Early Cretaceous of Dawangzhangzi, China)
 * Paraprotopteryx (Yixian Early Cretaceous of Fengning, 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)
 * Family Zhyraornithidae – enantiornithiform?
 * Zhyraornis (Late Cretaceous)

The three taxa "Jibeinia", "Vescornis", and "Hebeiornis", may be synonyms. (See the three articles for details on the confusion). If so, "Jibeinia" was published in 1997, "Vescornis"was described in 2004, and "Hebeiornis"was published in 1999 but it may not have been an adequate description. Therefore, if the three names truly do describe the same Genus, the senior synonym of the three would be "Jibeinia". Unfortunately, Dr. Hou reported the holotype of Jibeinia lost in 2001.

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.