Microraptor
Microraptor (Greek, μικρός, "mīkros": "small"; Latin, "raptor": "one who seizes") is a genus of small, four-winged dromaeosaurid dinosaurs. Numerous well-preserved fossil specimens have been recovered from Liaoning, China. They date from the early Cretaceous Jiufotang Formation (Aptian stage), 125 to 120 million years ago. Three species have been named ("M. zhaoianus", "M. gui", and "M. hanqingi"), though further study has suggested that all of them represent variation in a single species, which is properly called "M. zhaoianus". Cryptovolans, initially described as another four-winged dinosaur, is usually considered to be a synonym of "Microraptor". Like "Archaeopteryx", well -preserved fossils of "Microraptor" provide important evidence about the evolutionary relationship between birds and earlier dinosaurs. "Microraptor" had long pennaceous feathers that formed aerodynamic surfaces on the arms and tail but also on the legs. This led paleontologist Xu Xing in 2003 to describe the first specimen to preserve this feature as a "four-winged dinosaur" and to speculate that it may have glided using all four limbs for lift. Subsequent studies have suggested that "Microraptor" was capable of powered flight as well. "Microraptor" was among the most abundant non-avialan dinosaurs in its ecosystem, and the genus is represented  by more fossils than any other dromaeosaurid, with possibly over 300 fossil specimens represented across various museum collections. History. Naming controversy. The initial naming of "Microraptor" was controversial, because of the unusual circumstances of its first description. The first specimen to be described was part of a chimeric specimen—a patchwork of different feathered dinosaur species ("Microraptor" itself, "Yanornis" and an as-of-yet undescribed third species) assembled from multiple specimens in China and smuggled to the USA for sale. After the forgery was revealed by Xu Xing of Beijing's Institute of Vertebrate Paleontology and Paleoanthropology, Storrs L. Olson , curator of birds in the National Museum of Natural History of the Smithsonian Institution, published a description of the Microraptor's tail in an obscure journal, giving it the name "Archaeoraptor liaoningensis" in an attempt to remove the name from the paleornithological record by assigning it to the part least likely to be a bird. However, Xu had discovered the remains of the specimen from which the tail had been taken and published a description of it later that year, giving it the name "Microraptor zhaoianus". Since the two names designate the same individual as the type specimen, "Microraptor zhaoianus  would have been a junior objective synonym of Archaeoraptor liaoningensis" and the latter, if valid, would have had priority under the International Code of Zoological Nomenclature. However, there is some doubt whether Olson in fact succeeded in meeting all the formal requirements for establishing a new taxon. Namely, Olson designated the specimen as a lectotype, before an actual type species was formally erected. A similar situation arose with "Tyrannosaurus rex" and "Manospondylus gigas", in which the former became a "nomen protectum" and the latter a "nomen oblitum" due to revisions in the ICZN rules that took place on December 31 , 1999. In addition, Xu's name for the type specimen ("Microraptor") was subsequently used more frequently than the original name; as such, this and the chimeric nature of the specimen would render the name "Archaeoraptor" a "nomen vanum" (as it was improperly described) and the junior synonym "Microraptor" a "nomen protectum" (as it's been used in more published works than "Archaeoraptor" and was properly described). Additional specimens. The first specimen referred to "Microraptor" represented a small individual and included faint feather remnants, but was otherwise not well preserved and lacked a skull. In 2002 Mark Norell et al. described  another specimen, BPM 1 3-13, which they did not name or refer to an existing species. Later that year Stephen Czerkas et al. named the specimen "Cryptovolans pauli", and referred two additional specimens (the first to show well-preserved feathers) to this species. The generic name was derived from Greek "kryptos", "hidden", and Latin "volans", "flying". The specific name, "pauli", honors paleontologist Gregory S. Paul, who had long proposed that dromaeosaurids evolved from flying ancestors. The type specimens of "C. pauli" were collected from the Jiufotang Formation, dating from the early Albian and now belong to the collection of  the Paleontology Museum of Beipiao, in Liaoning, China. They are referred to by the inventory numbers LPM 0200, the holotype; LPM 0201, its counterslab (slab and counterslab together represent the earlier BPM 1 3-13); and the paratype LPM 0159, a smaller skeleton. Both individuals are preserved as articulated compression fossils; they are reasonably complete but partially damaged. Czerkas "et al." (2002) diagnosed the genus on the basis of having primary feathers (which in the authors' opinion made it a bird), a co-ossified sternum, a tail consisting of 28 to 30 vertebrae and a third finger with a short  phalanx III-3. Some of the feathers Czerkas described as primary were actually attached to the leg, rather than the arm. This, along with most of the other diagnostic characters, is also present in the genus "Microraptor", which was first described earlier than "Cryptovolans". However, BPM 1 3-13 has a longer tail, proportionately, than other "Microraptor" specimens that had been described by 2002, which have 24 to 26 tail vertebrae. Subsequent studies (and more specimens of "Microraptor") have shown that the features used to distinguish "Cryptovolans" are not unique, but are present to varying degrees across various specimens. In a  review by Phil Senter and colleagues in 2004, the scientists suggested that all these features represented individual variation across various age groups of a single "Microraptor" species, making the name "Cryptovolans pauli" and "Microraptor gui" junior synonyms of "Microraptor zhaoianus". Many other researchers, including Alan Feduccia and Tom Holtz, have since supported its synonymy. A new specimen of "Microraptor", BMNHC PH881, showed several features previously unknown in the animal, including the probably glossy-black iridescent plumage coloration. The new specimen also featured a bifurcated tailfan, similar in shape to previously known "Microraptor" tailfans except sporting a pair of long, narrow  feathers at the center of the fan. The new specimen also showed no sign of the nuchal crest, indicating that the crest inferred from the holotype specimen may be an artifact of taphonomic distortion. Numerous further specimens likely belonging to "Microraptor" have been uncovered, all from the Shangheshou Bed of the Jiufotang Formation in Liaoning, China. In fact, "Microraptor" is the most abundant non-avialan dinosaur fossil type found in this formation. In 2010, it was reported that there were over 300 undescribed specimens attributable to "Microraptor" or its close relatives among the collections of several Chinese museums, though many  had been altered or composited by private fossil collectors. Study and debate. Norell "et al." (2002) described BPM 1 3-13 as the first dinosaur known to have flight feathers on its legs as well as on its arms. Czerkas (2002) mistakenly described the fossil as having no long feathers on its legs, but only on its hands and arms, as he illustrated on the cover of his book "Feathered Dinosaurs and the Origin of Flight". In his discussion of "Cryptovolans" in this book, Czerkas strongly denounces Norell's conclusions; ""The misinterpretation of the primary wing feathers as being from  the hind legs stems directly to" [sic] "seeing what one believes and wants to see"". Czerkas also denounced Norell for failing to conclude that dromaeosaurs are birds, accusing him of succumbing to ""...the blinding influences of preconceived ideas."" The crown group definition of Aves, as a subset of Avialae, the explicit definition of the term "bird" that Norell employs, would definitely exclude BPM 1 3-13. However, he does not consider the specimen to belong to Avialae either. Czerkas's interpretation of the hindleg feathers noted by Norell proved to be incorrect the following year when additional specimens of "Microraptor  were published by Xu and colleagues, showing a distinctive hindwing" completely separate from the forelimb wing. The first of these specimens was discovered in 2001, and between 2001 and 2003 four more specimens were bought from private collectors by Xu's museum, the Institute of Vertebrate Paleontology and Paleoanthropology. Xu also considered these specimens, most of which had hindwings and proportional differences from the original "Microraptor" specimen, to be a new species, which he named "Microraptor gui". However, Senter also questioned this classification, noting that as with "Cryptovolans", most of the differences appeared to correspond with size, and likely age  differences. Two further specimens, classified as "M. zhaoianus" in 2002 ("M. gui" had not yet been named), have also been described by Hwang and colleagues. Czerkas also believed that the animal may have been able to fly better than "Archaeopteryx", the animal usually referred to as the earliest known bird. He cited the fused sternum and asymmetrical feathers, and argued that "Microraptor" has modern bird features that make it more derived than "Archaeopteryx". Czerkas cited the fact that this possibly volant animal is also very clearly a dromaeosaurid to suggest that the Dromaeosauridae might actually be a basal bird group , and that later, larger, species such as "Deinonychus" were secondarily flightless (Czerkas, 2002). The current consensus is that there is not enough evidence to conclude whether dromaeosaurs descended from an ancestor with some aerodynamic abilities. The work of Xu "et al." (2003) suggested that basal dromaeosaurs were probably small, arboreal, and could glide. The work of Turner "et al." (2007) suggested that the ancestral dromaeosaur could not glide or fly, but that there was good evidence that it was small-bodied (around 65 cm long and 600–700 g in mass). Description. With adult specimens estimated up to ) and with a  weight estimated up to , "Microraptor" was among the smallest-known non-avian dinosaurs. Holtz estimated it at . An estimate by Benson "et al." in 2012 was that "Microraptor" had a maximum length of . Aside from their extremely small size, "Microraptor" were among the first non-avialan dinosaurs discovered with the impressions of feathers and wings. Seven specimens of "M. zhaoianus" have been described in detail, from which most feather impressions are known. Unusual even among early birds and feathered dinosaurs, "Microraptor" is one of the few known bird precursors to sport long flight feathers on the legs as well as  the wings. Their bodies had a thick covering of feathers, with a diamond-shaped fan on the end of the tail (possibly for added stability during flight). Xu "et al." (2003) compared the longer plumes on "Microraptor"s head to those of the Philippine eagle. Bands of dark and light present on some specimens may indicate color patterns present in life, though at least some individuals almost certainly possessed an iridescent black coloration. Several anatomical features found in "Microraptor", such as a combination of unserrated and partially serrated teeth with constricted 'waists', and unusually long upper arm bones, are shared with  both primitive avians and primitive troodontids. "Microraptor" is particularly similar to the basal troodontid "Sinovenator"; in their 2002 description of two "M. zhaoianus" specimens, Hwang "et al." note that this is not particularly surprising, given that both "Microraptor" and "Sinovenator" are very primitive members of two closely related groups, and both are close to the deinonychosaurian split between dromaeosaurids and troodontids. Coloration. In March 2012, Quanguo Li "et al." determined the plumage coloration of "Microraptor" based on the new specimen BMNHC PH881, which also showed several other features previously unknown in "Microraptor". By analyzing the fossilized melanosomes (pigment cells) in  the fossil with scanning electron microscope techniques, the researchers compared their arrangements to those of modern birds. In "Microraptor", these cells were shaped in a manner consistent with black, glossy coloration in modern birds. These rod-shaped, narrow melanosomes were arranged in stacked layers, much like those of a modern starling, and indicated iridescence in the plumage of "Microraptor". Though the researchers state that the true function of the iridescence is yet unknown, it has been suggested that the tiny dromaeosaur was using its glossy coat as a form of communication or sexual display, much as in modern iridescent birds . Classification. The cladogram below follows a 2012 analysis by paleontologists Phil Senter, James I. Kirkland, Donald D. DeBlieux, Scott Madsen and Natalie Toth. Paleobiology. Wings and flight. "Microraptor" had four wings, one on each of its forelimbs and hindlimbs, somewhat resembling one possible arrangement of the quartet of flight surfaces on a tandem wing aircraft of today. It had long pennaceous feathers on arms and hands with legs and feet . The long feathers on the legs of "Microraptor" were true flight feathers as seen in modern birds, with asymmetrical vanes on the arm, leg, and tail feathers. As in modern  bird wings, "Microraptor" had both primary (anchored to the hand) and secondary (anchored to the arm) flight feathers. This standard wing pattern was mirrored on the hindlegs, with flight feathers anchored to the upper foot bones as well as the upper and lower leg. Though not apparent in most fossils under natural light, due to obstruction from decayed soft tissue, the feather bases extended close to or in contact with the bones, as in modern birds, providing strong anchor points. It was originally thought that "Microraptor" was a glider, and probably lived mainly in trees, because the hindwings anchored to  the feet of "Microraptor" would have hindered their ability to run on the ground. Some paleontologists have suggested that feathered dinosaurs used their wings to parachute from trees, possibly to attack or ambush prey on the ground, as a precursor to gliding or true flight. In their 2007 study, Chatterjee and Templin tested this hypothesis as well, and found that the combined wing surface of "Microraptor" was too narrow to successfully parachute to the ground without injury from any significant height. However, the authors did leave open the possibility that "Microraptor" could have parachuted short distances, as between closely spaced  tree branches. Wind tunnel experiments have demonstrated that sustaining a high-lift coefficient at the expense of high drag was likely the most efficient strategy for "Microraptor" when gliding between low elevations. "Microraptor" did not require a sophisticated, 'modern' wing morphology to be an effective glider. However, the idea that "Microraptor" was an arboreal glider relies on it to have regularly climbed or even lived in trees, when study of its anatomy have shown that its limb proportions fall in line with modern ground birds rather than climbers, and its skeleton shows none of the expected adaptations in animals specialized  for climbing trees. Describing specimens originally referenced as a distinctive species ("Cryptovolans pauli"), paleontologist Stephen Czerkas argued "Microraptor" may have been a powered flier, and indeed possibly a better flyer than "Archaeopteryx". He noted that the "Microraptor's" fused sternum, asymmetrical feathers, and features of the shoulder girdle indicated that it could fly under its own power, rather than merely gliding. Today, most scientists agree that "Microraptor" had the anatomical features expected of a flying animal, though it would have been a less advanced form of flight compared to birds. For example, some studies suggest the shoulder joint was too  primitive to allow a full flapping flight stroke. In the ancestral anatomy of theropod dinosaurs, the shoulder socket faced downward and slightly backward, making it impossible for the animals to raise their arms vertically, a prerequisite for the flapping flight stroke in birds. Studies of maniraptoran anatomy have suggested that the shoulder socket did not shift into the bird-like position of a high, upward orientation close to the vertebral column until relatively advanced avialans like the enantiornithes appeared. However, other scientists have argued that the shoulder girdle in some paravian theropods, including "Microraptor", is curved in such a way  that the shoulder joint could only have been positioned high on the back, allowing for a nearly vertical upstroke of the wing. This possibly advanced shoulder anatomy, combined with the presence of a propatagium linking the wrist to the shoulder (which fills the space in front of the flexed wing and may support the wing against drag in modern birds) and an alula, much like a "thumb-like" form of leading edge slot, may indicate that "Microraptor" was capable of true, powered flight. Other studies have demonstrated that the wings of "Microraptor" were large enough to generate the lift necessary  for powered launching into flight even without a fully vertical flight stroke. A 2016 study of incipient flight ability in paravians demonstrated that "Microraptor" was capable of wing-assisted incline running, as well as wing-assisted leaping and even ground-based launching. Stephen Czerkas, Gregory S. Paul, and others have argued that the fact "Microraptor" could fly and yet is also very clearly a dromaeosaurid suggests that the Dromaeosauridae, including later and larger species such as "Deinonychus", were secondarily flightless. The work of Xu and colleagues also suggested that the ancestors of dromaeosaurids were probably small, arboreal, and capable of  gliding, although later discoveries of more primitive dromaeosaurids with short forelimbs unsuitable for gliding have cast doubt on this view. Work done on the question of flight ability in other paravians, however, showed that most of them probably would not have been able to achieve enough lift for powered flight, given their limited flight strokes and relatively smaller wings. These studies concluded that "Microraptor" probably evolved flight and its associated features (fused sternum, alula, etc.) independently of the ancestors of birds. Hindwing posture. Sankar Chatterjee suggested in 2005 that, in order for "Microraptor" to glide or fly, the forewings and  hindwings must have been on different levels (as on a biplane) and not overlaid (as on a dragonfly), and that the latter posture would have been anatomically impossible. Using this biplane model, Chatterjee was able to calculate possible methods of gliding and determined that "Microraptor" most likely employed a "phugoid" style of gliding: launching itself from a perch, the animal would have swooped downward in a deep U-shaped curve and then lifted again to land on another tree. The feathers not directly employed in the biplane wing structure, like those on the tibia and the tail, could have been  used to control drag and alter the flight path, trajectory, etc. The orientation of the hindwings would also have helped the animal control its gliding flight. Chatterjee also used computer algorithms that test animal flight capacity to test whether or not "Microraptor" was capable of true, powered flight, as opposed to or in addition to passive gliding. The resulting data showed that "Microraptor" did have the requirements to sustain level powered flight, so it is theoretically possible that the animal flew, as opposed to gliding. Some paleontologists have doubted the biplane hypothesis, and have proposed other configurations. A 2010 study  by Alexander "et al." described the construction of a lightweight three-dimensional physical model used to perform glide tests. Using several hindleg configurations for the model, they found that the biplane model, while not unreasonable, was structurally deficient and needed a heavy-headed weight distribution for stable gliding, which they deemed unlikely. The study indicated that a laterally abducted hindwing structure represented the most biologically and aerodynamically consistent configuration for "Microraptor". A further analysis by Brougham and Brusatte, however, concluded that Alexander's model reconstruction was not consistent with all of the available data on "Microraptor" and argued that the  study was insufficient for determining a likely flight pattern for "Microraptor". Brougham and Brusatte criticized the anatomy of the model used by Alexander and his team, noting that the hip anatomy was not consistent with other dromaeosaurs. In most dromaeosaurids, features of the hip bone prevent the legs from splaying horizontally; instead, they are locked in a vertical position below the body. Alexander's team used a specimen of "Microraptor" which was crushed flat to make their model, which Brougham and Brusatte argued did not reflect its actual anatomy. Later in 2010, Alexander's team responded to these criticisms, noting  that the related dromaeosaur "Hesperonychus", which is known from complete hip bones preserved in three dimensions, also shows hip sockets directed partially upward, possibly allowing the legs to splay more than in other dromaeosaurs. Ground movement. Due to the extent of the hindwings onto most of the animal's foot, many scientists have suggested that "Microraptor" would have been awkward during normal ground movement or running. The front wing feathers would also have hindered "Microraptor" when on the ground, due to the limited range of motion in the wrist and the extreme length of the wing feathers. A 2010 study  by Corwin Sullivan and colleagues showed that, even with the wing folded as far as possible, the feathers would still have dragged along the ground if the arms were held in a neutral position, or extended forward as in a predatory strike. Only by keeping the wings elevated, or the upper arm extended fully backward, could "Microraptor" have avoided damaging the wing feathers. Therefore, it may have been anatomically impossible for "Microraptor" to have used its clawed forelimbs in capturing prey or manipulating objects. Implications. The unique wing arrangement found in "Microraptor" raised the question of whether the evolution of  flight in modern birds went through a four-winged stage, or whether four-winged gliders like "Microraptor" were an evolutionary side-branch that left no descendants. As early as 1915, naturalist William Beebe had argued that the evolution of bird flight may have gone through a four-winged (or "tetrapteryx") stage. Chatterjee and Templin did not take a strong stance on this possibility, noting that both a conventional interpretation and a tetrapteryx stage are equally possible. However, based on the presence of unusually long leg feathers in various feathered dinosaurs, "Archaeopteryx", and some modern birds such as raptors, as well  as the discovery of further dinosaurs with long primary feathers on their feet (such as "Pedopenna"), the authors argued that the current body of evidence, both from morphology and phylogeny, suggests that bird flight did shift at some point from shared limb dominance to front-limb dominance and that all modern birds may have evolved from four-winged ancestors, or at least ancestors with unusually long leg feathers relative to the modern configuration. Feeding. In 2010 researchers announced that further preparation of the type fossil of "M. zhaoianus" revealed preserved probable gut contents. These consisted of mammalian bones, including a  possible skull, limb, and vertebral fragments and also a whole foot. The foot skeleton is similar to those of "Eomaia" and "Sinodelphys". It corresponds to an animal with an estimated snout to vent length of and a mass of . The unguals of the foot are less curved than in "Eomaia" or "Sinodelphys", indicating that the mammal could climb but less effectively than in the two latter genera. In the December 6, 2011 issue of "Proceedings of the National Academy of Sciences", Jingmai O'Connor and coauthors described a "Microraptor" specimen containing bird bones in its abdomen, specifically a partial wing and  feet. Their position indicate that the dinosaur swallowed a tree-perching bird whole. In 2013 researchers announced that they had found fish scales in the abdominal cavity of a "Microraptor" specimen. This new finding corrects the previous position that "Microraptor" hunted only in an arboreal environment. They also argued that the specimen showed a probable adaptation to a fish-eating diet: the good preservation of the mandible shows that the first three teeth were inclined anterodorsally, a character often associated with piscivory. "Microraptor" was an opportunistic feeder, hunting the most common prey in both arboreal and aquatic habitats. In 2019 , a new genus of scleroglossan lizard ("Indrasaurus") was described from a specimen found in the stomach of a "Microraptor". The "Microraptor" apparently swallowed its prey head first, a behavior typical of modern carnivorous birds and lizards. The "Indrasaurus" bones lacked marked pitting and scarring, indicating that the "Microraptor" died shortly after eating the lizard and before significant digestion had occurred. Unlike its fellow paravian "Anchiornis", "Microraptor" has never been found with gastric pellets, despite the existence of four "Microraptor" specimens that preserve stomach contents. This suggests that "Microraptor" passed indigestible fur, feathers, and bits of bone in its droppings instead  of producing pellets. Based on the size of the scleral ring of the eye, it has been suggested "Microraptor" hunted at night. However, the discovery of iridescent plumage in "Microraptor" has cast doubt on this conclusion, as no modern birds that have iridescent plumage are known to be nocturnal.