Early Cretaceous–Late Cretaceous, 130.7–66.0 Ma
|Fossil specimen of a bohaiornithid (Zhouornis hani)|
and see text
Enantiornithes is a group of extinct avialans ("birds" in the broad sense), the most abundant and diverse group known from the Mesozoic era. Almost all retained teeth and clawed fingers on each wing, but otherwise looked much like modern birds externally. Over 80 species of enantiornitheans have been named, but some names represent only single bones, so it is likely that not all are valid. Enantiornitheans became extinct at the Cretaceous–Paleogene boundary, along with hesperornithids and all other non-avian dinosaurs. Enantiornitheans are thought to have left no living descendants.
Discovery and naming
The first enantiornitheans to be discovered were incorrectly referred to modern bird groups. For example, the first known enantiornithean, Gobipteryx minuta, was originally considered a paleognath related to ostriches and tinamou. Enantiornitheans were first recognized as a distinct lineage, or "subclass" of birds, by Cyril A. Walker in 1981. Walker made this discovery based on some partial remains from the late Cretaceous period of what is now Argentina, which he assigned to a new genus, Enantiornis, giving the entire group its name. Since the 1990s, many more complete enantiornitheans were discovered, and it was determined that a few previously described "birds" (e.g. Iberomesornis, Cathayornis, and Sinornis) were also enantiornitheans.
The name "Enantiornithes" means "opposite birds", from Ancient Greek enantios (ἐνάντιος) "opposite" + ornithes (όρνιθες) "birds" . The name was coined by Cyril Alexander Walker in his landmark paper which established the group. In his paper, Walker explained what he meant by "opposite":
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 enantiornitheans, 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: Template:Bquote
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 enantiornitheans had triosseal canals, since no fossil preserves this feature.
As a group, the Enantiornithes are often referred to as "enantiornithines". However, several scientists have noted that this is incorrect, because following the standard rules for forming the names of animal groups, it implies reference only to the subfamily Enantiornithinae. Following the naming conventions used for modern birds as well as extinct groups, it has been pointed out that the correct term is "enantiornithean".
Origin and range
Enantiornitheans have been found on every continent except Antarctica. Fossils attributable to this group are exclusively Cretaceous in age, and it is believed that Enantiornitheans became extinct at the same time as their non-avialan dinosaur relatives. The earliest known enantiornitheans are from the Early Cretaceous of Spain (e.g. Noguerornis) and China (e.g. Protopteryx) and the latest from the Late Cretaceous of North and South America (e.g. Avisaurus and Enantiornis). The widespread occurrence of this group suggests that at least some enantiornitheans were able to cross oceans under their own power; they are the first known avialan lineage with a global distribution.
Many enantiornithean fossils are very fragmentary, and some species are only known from a piece of a single bone. Almost all specimens that are complete, in full articulation, and with soft tissue preservation are known from Las Hoyas in Cuenca, Spain and the Jehol group in Liaoning (China). Enantiornithean fossils have been found in both inland and marine sediments, suggesting that they were an ecologically diverse group. Enantiornitheans appear to have included waders, swimmers, granivores, insectivores, fishers, and raptors. The vast majority of enantiornithean species were small, between the size of a sparrow and a starling, while the largest members of this clade are Pengornis houi, Xiangornis shenmi and Zhouornis hani. At least a few much larger species may have existed, including a potentially crane-sized species known only from footprints in the Eumeralla Formation (and possibly also represented in the Wonthaggi Formation by a single furcula), which might belong to an enantiornithean.
Given their wide range of habitats and diets, the skulls of enantiornitheans varied considerably between species. Enantiornithean skulls combined a unique suite of primitive and advanced features. As in more primitive avialans 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 and had beaks.
As a very large group of birds, enantiornitheans displayed a high diversity of different body plans based on differences in ecology and feeding, reflected in an equal diversity of wing forms, many paralleling adaptions to different lifestyles seen in modern birds. In general, the wings of enantiornitheans were advanced compared to more primitive avialans like Archaeopteryx, and displayed some features related to flight similar to those found in the lineage leading to modern birds, the Ornithuromorpha. While most enantiornitheans had claws on at least some of their fingers, many species had shortened hands, a highly mobile shoulder joint, and proportional changes in the wing bones similar to modern birds. Like modern birds, enantiornitheans had alulas, or "bastard wings", small forward-pointing arrangements of feathers on the first digit that granted higher maneuverability in the air and aided in precise landings.
Two fledgling enantiornithean wings have been found preserved in amber from deposits in Myanmar. These are the first complete Mesozoic dinosaur remains preserved this way (a few isolated feathers are otherwise known, unassigned to any species), and one of the most exquisitely preserved dinosaurian fossils known. The preserved wings show variations in feather pigment and prove that enantiornitheans had fully modern feathers, including barbs, barbules, and hooklets, and a modern arrangement of wing feather including long flight feathers, short coverts, a large alula and an undercoat of down.
One enantiornithean 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 enantiornithean 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.
Clarke et al. (2006) surveyed all enantiornithean 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 avialans outside of Euornithes (the clade they called Ornithurae) with preserved tail feathers had only short coverts or elongated paired tail plumes. They suggested that the development of the pygostyle in enantiornitheans must have been a function of tail shortening, not the development of a modern tail feather anatomy. These scientists suggested that a fan of tail feathers and the associated musculature needed to control them, known as the rectrical bulb, evolved alongside a short, triangular pygostyle, like the ones in modern birds, rather than the long, rod- or dagger-shaped pygostyles in more primitive avialans like enantiornitheans. Instead of a feather fan, most enantiornitheans had a pair of long specialized pinfeathers similar to those of the extinct Confuciusornis and certain birds-of-paradise.
However, further discoveries showed that at least among primitive enantiornitheans, tail anatomy was more complex than previously thought. One enantiornithean, Shanweiniao, is known to have had at least four long tail feathers that overlapped each other. It is possible that these formed a lift-generating surface similar to the tail fans of euornitheans, though the fan-like tail of this species may have evolved independently of the modern bird lineage. Chiappeavis, a primitive pengornithid enantiornithean, had a fan of tail feathers similar to that of more primitive avialans like Sapeornis, suggesting that this might have been the ancestral condition, with pinfeathers being a feature evolved several times in early avialans for display purposes. Another enantiornithean, Feitianius, also had an elaborate fan of tail feathers. More importantly, soft tissue preserved around the tail was interpreted as the remains of a rectrical bulb, suggesting that this feature was not in fact restricted to species with modern-looking pygostyles, but might have evolved much earlier than previously thought and been present in many enantiornitheans.
Given the wide diversity of skull shape among enantiornitheans, many different dietary specializations must have been present among the group. Some, 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. The sharp, recurved teeth and strongly hooked talons of bohaiornithids suggest that they were predators of small to medium-sized vertebrates.
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 from aquatic crustaceans preserved in its digestive tract, and Enantiophoenix preserved 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.
A fossil from Spain reported by Sanz et al. in 2001 included the remains of four hatchling enantiornithean 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 avialans were prey animals, and that some Mesozoic pan-avians regurgitated pellets like owls do today.
Known enantiornithean fossils include eggs, embryos, and hatchlings. An enantiornithean 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 enantiornitheans, 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 hatchling specimens of the Mongolian Gobipteryx and Gobipipus, these finds demonstrate that enantiornithean hatchlings had the skeletal ossification, well-developed wing feathers, and large brain which correlate with precocial or superprecocial patterns of development in birds of today. In other words, enantiornitheans probably hatched from the egg already well developed and ready to run, forage, and possibly even fly at just a few days old.
Analyses of enantiornithe bone histology have been conducted to determine the growth rates of these animals. A 2006 study of Concornis bones showed a growth pattern different from modern birds; although growth was rapid for a few weeks after hatching, probably until fledging, this small species did not reach adult size for a long time, probably several years. Other studies have all supported the view that growth to adult size was slow, as it is in living precocial birds (as opposed to altricial birds, which are known to reach adult size quickly). Studies of the rate of bone growth in a variety of enantiornitheans has shown that smaller species tended to grow faster than larger ones, the opposite of the pattern seen in more primitive species like Jeholornis and in non-avialan dinosaurs. Some analyses have interpreted the bone histology to indicate that enantiornitheans may not have had fully avian endothermy, instead having an intermediate metabolic rate.
Evidence of colonial nesting has been found in enantiornitheans, in sediments from the Late Cretaceous (Maastrichtian) of Romania. Evidence from nesting sites shows that enantiornitheans buried their eggs like modern megapodes, which is consistent with their inferred superprecocial adaptations.
Because many enantiornitheans lacked complex tails and possessed radically different wing anatomy compared to modern birds, they have been the subject of several studies testing their flight capabilities.
Traditionally, they have been considered inferior flyers, due to the shoulder girdle anatomy being assumed to be more primitive and unable to support a ground-based launching mechanism, as well as due to the absence of rectrices in many species.
However, several studies have shown that they were efficient flyers, like modern birds, possessing a similarly complex nervous system and wing feather ligaments. Additionally, the lack of a complex tail appears to not have been very relevant for avian flight as a whole - some extinct birds like lithornids also lacked complex tail feathers but were good flyers, and they appear to have been capable of a ground based launching.
Due to the difference in sternal and shoulder girdle anatomy, many enantiornitheans used a flight style unlike that of any modern bird species[clarification needed], though more typical flight styles were present as well.
Some researchers classify enantiornitheans, along with the true birds, in the class Aves. Others use the more restrictive crown group definition of Aves, and place enantiornitheans in the more inclusive group Avialae. Enantiornitheans were more advanced than Archaeopteryx, Confuciusornis, and Sapeornis, but in several respects they were more primitive than modern birds, perhaps following an intermediate evolutionary path.
A consensus of scientific analyses indicates that Enantiornithes is one of two major groups within the larger group Ornithothoraces. The other ornithothoracine group is Euornithes or Ornithuromorpha, which includes all living birds as a subset. This means that enantiornitheans were a successful branch of avialan evolution, but one that diversified entirely separately from the lineage leading to modern birds.
Enantiornithean classification and taxonomy has historically been complicated by a number of factors. In 2010, 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 enantiornithean species 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".
Enantiornithes is the sister group to Euornithes, 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 enantiornithean autapomorphies to just four.
Enantiornithean systematics are highly provisional and notoriously difficult to study, due to the fact hat enantiornitheans tend to be extremely homoplastic, or very similar to each other in most of their skeletal features due to convergent evolution rather than common ancestry. What appears fairly certain by now is that there were subdivisions within enantiornitheans possibly including some minor basal lineages in addition to the more advanced 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 enantiornithean clades.
One such delineation named the Euenantiornithes, was defined by Chiappe (2002) as comprising all species closer to Sinornis than to Iberomesornis. Because Iberomesornis is often found to be the most primitive or basal enantiornithean, Euenantiornithes may be an extremely inclusive group, made up of all Enantiornithes except for Iberomesornis itself. Despite being in accordance with phylogenetic nomenclature, this definition of Euenantiornithes was severely criticized by some researchers, such as Paul Sereno, who called it "a ill-defined clade [...] a good example of a poor choice in a phylogenetic definition".
The taxonomic list of enantiornithean groups presented here follows a summary published by Thomas R. Holz, Jr. in 2011, except in cases where noted.
- Primitive Enantiornithes
- Dalingheornis (China)
- Dapingfangornis (China)
- Elsornis (Mongolia)
- Eoalulavis (Spain)
- Feitianius (China)
- Gobipipus (Mongolia)
- Holbotia (China) 
- Houornis (China)
- Iberomesornis (Spain)
- Jibeinia (China)
- Liaoningornis (China)
- Paraprotopteryx (China)
- Protopteryx (China)
- Qiliania (China)
- Sazavis (Uzbekistan)
- Xiangornis (China)
- Yuanjiawaornis (China) 
- Primitive Euenantiornithes
- Abavornis (Uzbekistan)
- Alethoalaornis (China)
- Alexornis (Mexico)
- Catenoleimus (Uzbekistan)
- Cathayornis (China)
- Cratoavis (Brazil) 
- Dunhuangia (China) 
- Enantiornis (Argentina)
- Eocathayornis (China)
- Explorornis (Uzbekistan)
- Flexomornis (Texas)
- Fortunguavis (China) 
- Grabauornis (China)
- Gracilornis (China)
- Gurilynia (Mongolia)
- Huoshanornis (China)
- Incolornis (Uzbekistan)
- Kuszholia (Uzbekistan)
- Kizylkumavis (Uzbekistan)
- Largirostrornis (China)
- Lectavis (Argentina)
- Lenesornis (Uzbekistan)
- Liaoxiornis (China)
- Longchengornis (China)
- Martinavis (Argentina/France/New Mexico)
- Nanantius (Australia)
- Noguerornis (Spain)
- Otogornis (China)
- Parvavis (China)
- Pterygornis (China) 
- Sinornis (China)
- Yungavolucris (Argentina)
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