Wulong bohaiensis: Iridescent plumage in a juvenile Dromaeosaur from the Jehol Biota.

Melanosomes are organelles within the cells of Vertebrates within which the pigment melanin is stored. The first fossil melanosomes were described in 2008, since when they have been recorded in a range of fossil taxa, with the different shape of different melanosomes being used to make inferences about the colour of a variety of extinct Animals. One notable group to which this methodology has been applied is Mesozoic Birds, enabling palaeontologists to determine that some of the remarkable colouration, and therefore presumably colour-related behaviour, seen in modern Birds was already present in the Mesozoic. 

One notable feature found in the plumage of a variety of Bird groups today is iridescence, a visual effect achieved by the coherent scattering of light at certain frequencies as it passes through the barbules of feathers, where layers of specially modified melanosomes are present. This works because melanin and keratin have different refractive indexes to both one-another and to air, enabling the bending of light at certain wavelengths in consistent ways. This is sometimes used to aid the camouflaging effect of the Bird's plumage, as in the case of the iridescent green plumage on the backs of Hummingbirds, it is more commonly used in displays and signalling between Birds.

Iridescence and plumage colour has been determined for a number of ancient Bird species, but feathers are also known in non-Avian Dinosaurs, with the most famous examples being the Jehol Biota from the Early Cretaceous of northeastern China, where a very large number of feathered Dinosaurs have been found. The feathers of these Jehol Dinosaurs are generally considered to be too modified by burial compression and thermal alteration, as well as oxidation after exposure, which has largely removed the kerogen matrix from which the fossils are made, leaving the majority of the fossils as (very detailed) rock impressions. This might seem to be an obstacle to the reconstruction of colour and iridescence in these fossils, but much of the work that has been done with fossil melanosomes has been based upon the shape of these structures, rather than their chemistry, which has allowed for the reconstruction of both non-iridescent structural colouration and iridescence in the plumage of Enatornithine Birds and non-Avian Paravian Dinosaurs (the Paravia is the group that includes Birds, Dromaeosaurs, and Troodontids).

All known iridescent nanostructures within feathers are found within the barbules (filaments projecting from the barbs of feathers), structures which appeared in early Maniraptorans (the group which includes Alvarezsaurs, Therizinosaurs, Oviraptosaurs, and Paravians), and to have been refined within the Paravians, and the presence of iridescence in a variety of Paravians could imply that the appearance of barbules may have been linked to iridescence.

It is highly likely that colouration has played an important role in the evolution of Birds and their ecology, and that the accumulating body of data on melanosomes in early Birds might provide insight into this. However, if non-Avian Paravians also had pigmented and iridescent plumage, then their evolution and ecology is equally likely to have been influenced by this. At the moment we have very little information on the colouration of these Dinosaurs, but potentially, if it can be collected, it may be possible to tell how their colouration changed as they reached maturity, and if their colouration was sexually dimorphic. To do this for any species of Dinosaur, a large dataset would be necessary, with numerous specimens with preserved feathers, reflecting both sexes and a range of ages. 

In a paper published in the journal Acta Palaeontologica Polonica on 13 June 2023, Angus Croudace of the School of Geosciences at the University of Edinburgh, Caizhi Shen of the Dalian Natural History Museum, Junchang Lü of the Institute of Geology of the Chinese Academy of Geological Sciences, Stephen Brusatte, also of the School of Geosciences at the University of Edinburgh, and Jakob Vinther of the School of Earth Sciences at the University of Bristol, reconstruct the plumage colouration of a specimen, DNHM D2933, of Wulong bohaiensis, an Early Cretaceous feathered Microraptorine Dromaeosaurid from the Jehol Biota of Liaoning, China.

Previous studies of the skeleton of DNHM D2933 have determined that it was a juvenile, about one year old when it died and still growing, making it the first juvenile non-Avian Dinosaur to have the colour of its plumage determined, as far as Croudace et al. are aware.  In order to determine the colouration, and iridescence, of the specimen, Croudace et al. used a statistical approach to the determining of the purpose of preserved melanosomes from different parts of the body. This works because different coloured melanosomes are known to be different in shape. Eumelanin-rich melanosomes are large and oblate and produce black colours, while pheomelanin-rich melanosomes are smaller and more ovoid, producing ginger or brown colours. Iridescent melanosomes are typically hollow or flat.

Dromaeosaurid Dinosaur Wulong bohaiensis (DNHM D2933), from Shangheshou, Chaoyang, Liaoning, China, Early Cretaceous Jiufotang Formation with a minimum age of 120.3 million years (A₁). Samples 1–16 were labelled by Stephen Brusatte while taking samples at the museum. Illustration by Jakob Vinther (A₂) to show distinct plumage groupings on Wulong bohaiensis (DNHM D2933). For clarity, in this illustration only the samples with successful melanosome preservation are labelled. Preservation on each of the excluded samples was not sufficient for study. Croudace et al. (2023).

Samples from DNHM D2933 were examined under a scanning electron microscope from several angles in order to establish the measurements of individual melanosomes. Since these 'melanosomes' are impressions rather than the original structures, it is impossible to determine whether-or-not they were hollow in life. However, the majority of the melanosomes observed appear to be to narrow to have been hollow. The density with which the melanosomes were packed, which has an effect on colour intensity, was not assessed.

Preserved melanosome imprints characteristic of each sample from the Dromaeosaurid Dinosaur Wulong bohaiensis (DNHM D9233) from Shangheshou, Chaoyang, Liaoning, China, Early Cretaceous Jiufotang Formation with a minimum age of 120.3 million years. All melanosome imprints are from solid and cylindrical melanosomes. Preservation on samples 7 and 14 is less clear. Three distinctive types of melanosome morphology were found on sample 15. Each was measured separately and treated as different samples for analysis (15a/15b/15c). Croudace et al. (2023).

Different types of melanosomes were observed on different parts of the body of the Dinosaur, enabling Croudace et al. to build up a picture of the distribution of colours its plumage, by comparison to a database of melanosomes from the plumage of modern Birds. Based upon this, Wulong bohaiensis is presumed to have been largely grey in colour, with patches of highly iridescent feathers on its forelimb and hindlimb remiges. 

Reconstruction of the Dromaeosaurid Dinosaur Wulong bohaiensis (DNHM D2933), from Shangheshou, Chaoyang, Liaoning, China, Early Cretaceous Jiufotang Formation with a minimum age of 120.3 million years. This illustration broadly depicts iridescent plumage on the limbs and grey feathers on the body. It should be noted that the full extent of the iridescence has been extrapolated in the creation of this illustration, based on the evidence provided by a small but significant distribution of iridescent samples across several limbs of the fossil. Robert Nicholls in Croudace et al. (2023).

Wulong bohaiensis is the fifth non-avian Paravian Dinosaur in which iridescence has been described (the others being Microraptor, Caihong, Bohaiornis, and Eoconfuciusornis) and the first juvenile. Two previously described species, Microraptor and Caihong, have also had the colour of their plumage determined, with both thought to be predominantly black.

The presence of iridescence in the feathers of non-Avian Dinosaurs lends support to the proposal that feathers evolved before flight, and originally had a quite different purpose, such as signalling, being later co-opted as flying aids. However, it is possible that the common ancestor of the Paravians was at least partially airborne, and that feathers were later co-opted for signalling in different groups. 

Feathers in modern Birds play a variety of roles, with signalling to other members of their species being important. In many modern Birds, iridescence plays an important part of such behaviour, often playing a role in courtship rituals. However, in such species, iridescence is typically only present in adults of reproductive age, not juveniles or subadults. DNHM D2933 is assessed to be a juvenile Dromaeosaur, about a year old, but still with some growing to do. In some Animals, reproduction can occur before the maximum size is reached, though in modern Birds of comparable size to Wulong bohaiensis, the best available analogue for reproductive behaviour, reproduction does typically occur until the individual is several years old, despite the fact that modern Birds typically reach their full size during their first year of life. This makes it unlikely that DNHM D2933 was reproductively active, and therefore unlikely that its iridescence was linked to mating behaviour. Some modern Birds, notably Corvids, develop iridescent feathers before reaching reproductive age. In these Birds, iridescence appears to be linked to the ability to recognise members of their own species, often as individuals (Corvids typically have quite complex social lives).

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Confuciusornis shifan: A new species of Confuciusornithid Bird from the Early Cretaceous Jehol Biota.

The Confuciusornithids are a group of Birds known from the Early Cretaceous Jehol Biota. Unlike earlier Jurassic Birds, they have both a pygostyle (short tail made from fused bones) and a beak, key features we associate with modern Birds, although they are not closely related, being considered to be the sister group to the Ornithothoraces, the group which comprises both the Euornithes ('True Birds'; the group to which all modern Birds belong) and the Enatiornithes ('Opposite Birds'; the most commonly preserved group of fossil Birds from the Cretaceous, which were generally toothed rather than beaked). Although these Birds are only known from a single fossil lagerstatten, thousands of individual specimens with a temporal range of about 15 million years (the Jehol Biota comprises three succeeding formations, the Dabeigou, Yixian and Jiufotan), which have been assigned to five genera and eleven species (although some of these assignments are debatable), giving us a degree of understanding of the group.

In a paper published in the journal Communications Biology on 21 December 2022, Renfei Wang of the College of Earth Sciences at Jilin University, and the Key Laboratory for Evolution of Past Life in Northeast Asia at the Paleontological Museum of Liaoning, Dongyu Hu, also of the Key Laboratory for Evolution of Past Life in Northeast Asia at the Paleontological Museum of Liaoning, Meisheng Zhang, also of the College of Earth Sciences at Jilin University, Shiying Wang, again of the Key Laboratory for Evolution of Past Life in Northeast Asia at the Paleontological Museum of Liaoning, Qi Zhao of the Key Laboratory of Vertebrate Evolution and Human Origins at the Institute of Vertebrate Paleontology and Paleoanthropology of the Chinese Academy of Sciences, Corwin Sullivan of the Department of Biological Sciences at the University of Alberta, and the Philip J. Currie Dinosaur Museum, and Xing Xu, once again of the Key Laboratory for Evolution of Past Life in Northeast Asia at the Paleontological Museum of Liaoning, and the Key Laboratory of Vertebrate Evolution and Human Origins at the Institute of Vertebrate Paleontology and Paleoanthropology, and of the Center for Vertebrate Evolutionary Biology at Yunnan University, describe a new species of Confuciusornithid Bird from the Xiaotaizi Village exposure of the Jiufotang Formation in  Jianchang County, Liaoning Province.

The new species is placed in the genus Confuciusornis, and given the specific name shifan, which means 'paragon of all teachers', and is an honorific applied to Confucius, and also refers to the 70th anniversary of the opening of Shenyang Normal University (瀋陽師範大學 or Shenyang Shifan Daxue). The species is described from a single specimen, PMoL-AB00178, which is a nearly complete and mostly articulated skeleton, preserved on a single slab.

Confuciusornis shifan holotype (PMoL-AB00178). (a) Photograph. (b) Schematic line drawing. cav caudal vertebra, cev cervical vertebra, fu furcula, ga gastralia, lc left coracoid, ldIII left manual digit III, lfe left femur, lh left humerus, lil left ilium, lis left ischium, lm left manus, lp left pes, lra left radiale, lr left radius, ls left scapula, lt left tibiotarsus, lu left ulna, lul left ulnare, ma mandible, pu pubis, py pygostyle, r rib, rc right coracoid, rdcIII claw of right manual digit III, rfe right femur, rfi right fibula, rh right humerus, ris right ischium, rm right manus, rp right pes, rra right radiale, rr right radius, rs right scapula, rt right tibiotarsus, ru right ulna, rul right ulnare, sk skull, sy synsacrum, tv thoracic vertebra. Arrow indicates the position from which the histological section of the right femur was taken. Scale bars is 2 cm. Wang et al. (2022).

Examination of the skeleton of Confuciusornis shifan indicates that it is an adult specimen, with all neurocentral sutures are closed without any trace, the sacral vertebrae are completely fused together to form a synsacrum, and nearly all of the compound bones (e.g., the metacarpus, tibiotarsus, and metatarsus) are fully formed. Examination of a cross section of the right femur revealed four lines of arrested growth (indicative of seasonal pauses in growth, similar to tree rings), which is considered indicative of having reached the final adult size in a Confuciusornithid.

Osteohistological section of Confuciusornis shifan holotype (PMoL-AB00178). Sample was taken from the midshaft of the right femur. ICL inner circumferential layer, OCL outer circumferential layer. Arrows indicate lines of arrested growth. Scale bar is 100 μm. Wang et al. (2022).

Despite this, Confuciusornis shifan is small for a Confuciusornithid Bird, with an estimated body mass of 174 g (around the size of a large Thrush or small Dove), with only one species, Changchengornis hengdaoziensis, having a smaller adult specimen (with an estimated body mass of 138 g).

The pygostyle is one of the defining features of modern Birds, but was absent in the long-tailed Birds of the Jurassic, with the Cretaceous-Recent Birds which share this characteristic being considered to comprise a single clade, the Pygostylians. In more advanced members of the group, such as the Sapeornithids, Pengornithid Enantiornithines, and Ornithuromorphs, this is a short, plough-shaped structure, but in earlier members of the group, including the Confuciusornithids, Jinguofortisids, and the majority of Enantiornithines, the pygostyle was longer and rod-shaped. It has generally been assumed that this longer pygostyle comprises a larger number of bones than the pygostyle of modern Birds, although the structure is seldom preserved well enough to be able to count the co-ossified bones which make it up. However, the pygostyle of Confuciusornis shifan is perforated (thought to be the result of incomplete fusion between adjacent neural arches), which leaves the intervertebral foramina (gaps between vertebrae) visible. The specimen has ten intervertebral foramina, implying a minimum of eleven vertebrae are fused, more than has previously been recorded in any Confuciusornithid Bird (the previous record-holder was a juvenile specimen of Confuciusornis sanctus with eight), and significantly more than is known from any non-Confuciusornithid Pygostylian Bird, with 5-6 being typical in even early members of the group.

Selected axial elements of Confuciusornis shifan holotype (PMoL-AB00178). (a) Cervical vertebrae. (b) Synsacrum. (c) Pygostyle. sy synsacrum. Arrows in (b) and (c) indicate the longitudinal ridge on the ventral surface of the synsacrum and the positions of foramina along the pygostyle, respectively. Scale bars are 0.5 cm in (a) and (c) and 1 cm in (b). Wang et al. (2022).

This has interesting implications for the evolution of the Avian tail. Both Confuciusornis shifan and Confuciusornis sanctus have seven free caudal (tail) vertebrae in addition to the fused vertebrae of the pygostyle, giving Confuciusornis shifan a total caudal vertebrae count of eighteen. Five to eight free caudal vertebrae seems to be typical of early Pygostylian Birds, with 5–6 in Jinguofortisids, 6–8 in Enantiornithines, and 5–7 in early Ornithuromorphs (modern Birds have 5-6). The exception appears to be the Sapeornithids, which are thought to have about 12. Since the pygostyle typically comprises another 5-6 vertebrae, this means that most Pygostylian Birds have a total of no more than 14 caudal vertebrae, with the exception of the Confuciusornithids and Sapeornithids, which have about 18. This is still less than in the non-Pygostylian Birds, with Archaeopteryx having 21-23 free caudal vertebrae, and Jeholornis having 27. This implies a general tendency towards a reduction of the number of caudal vertebrae in Pygostylian Birds, with exceptions in groups such as the Confuciusornithids and Sapeornithids, and possibly the Enantiornithines (which had a long pygostyle, presumably made up of a higher number of fused vertebrae, although no actual data is available). It is known that at least some of the long-pygostyled Birds used this structure to support large, ornamental tail feathers, whereas the shorter plough shaped pygostyles of more advanced groups are used to support retractable tail fans, which greatly increase aerodynamic lift and maneuverability. 

Typical Confuciusornithids have long wings with strongly asymmetrical flight feathers, strut-like coracoids, a keeled sternum, and enlarged major manual digits, all features which have been used to argue that they were strong flyers, although some functional analyses have suggested that their capabilities would have been more limited, and it is generally accepted that their flight capacity would have been weaker than modern Birds, or even Early Cretaceous Ornithothoracines.

Although clearly closely related to Confuciusornis sanctus, Confuciusornis shifan shows some flight adaptations dissimilar to those seen in other Confuciusornithids. Typical Confuciusornithids have an elongated forearm, giving an increased wing-area, a useful adaptation to long-distance flight. Confuciusornis shifan is significantly smaller than most Confuciusornithids, and shows enlargement of many of the skeletal processes to which muscles would have attached. This would have given greater control over the tips of the wings during flight, increasing maneuverability during flight.

Selected limb elements of Confuciusornis shifan holotype (PMoL-AB00178). (a) Left carpometacarpus. (b) Right carpometacarpus. (c) left alular metacarpal of the confuciusornithid specimen PMoL-AB00150. (d) Right tarsometatarsus. Carpometacarpi are in palmar view, and tarsometatarsus is in cranial view. cb cushion-like bone, ep extensor process, pp pisiform process. Roman numerals in (d) identify metatarsals. Black arrow in (c) indicates the cranial distal condyle of the alular metacarpal; black and white arrows in (d) indicate the ridge-like process on metatarsal IV and the dorsal tubercle on metatarsal III, respectively. Scale bars are 0.25 cm. Wang et al. (2022).

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Cokotherium jiufotangensis: A new species of Eutherian Mammal from the Early Cretaceous Jehol Biota of China.

Eutherian Mammals (or Placental Mammals) represent the largest Mammal group alive today. Molecular clock analysis suggests that thy diverged from the Marsupials during the Jurassic, which is supported by the oldest known Eutherian Mammal fossil, Juramaia sinensis, coming from the Late Jurassic Tiaojishan Formation of Liaoning Province in China. However, the fossil record of early Eutherians is sparse, with only Juramaia sinensis known from the Jurassic, and a only a few examples, such as Eomaia, Acristatherium, Ambolestes, Sasayamamylos, Sinodelphys, and Prokennalestes coming from the Early Cretaceous. This makes it hard to make solid predictions about the relationships between these early Eutherian species, with the discovery of new species often leading to the reassessment of the importance of features used to define the group (for example Sinodelphys was considered the earliest known Marsupial until 2018, when a re-evaluation of the group following the discovery of Ambolestes zhoui lead to it being classified as a Eutherian.

In a paper published in the Philosophical Transactions of the Royal Society Series B: Biological Sciences on 7 February 2022, Hai-Bing Wang of the Key Laboratory of Vertebrate Evolution at the  Institute ofVertebrate Paleontology and Paleoanthropology, the Centre for Excellence in Life and Paleoenvironment of the Chinese Academy of Sciences, and the Key Laboratory of Palaeobiology and Stratigraphy at the Nanjing Institute of Geology and Palaeontology, Simone Hoffmann of the  Department of Anatomy at the New York Institute of Technology, Dian-Can Wang of the Department of Oral and Maxillofacial Surgery at Peking University, and Yuan-Qing Wang, also of the Key Laboratory of Vertebrate Evolution at the  Institute of Vertebrate Paleontology and Paleoanthropology, and the Centre for Excellence in Life and Paleoenvironment of the Chinese Academy of Sciences, and of the College of Earth and Planetary Sciences at the University of Chinese Academy of Sciences, describe a new species of Eutherian Mammal from the Early Cretaceous Jehol Biota of Liaoning Province, China.

The new species is described from a single specimen collected from the Jiufotang Formation at the Sihedang Site in Lingyuan City, and has an estimated age of 120 million years. It is named Cokotherium jiufotangensis, where 'Cokotherium' is intended to honour the late Chuan-Kui Li for his  contributions to our understanding of the evolution of early Mammals, and 'jiufotangensis' means 'from Jiufotang'.

Holotype specimen of Cokotherium jiufotangensis (IVPP V23387). (a) Skeleton of Cokotherium jiufotangensis; (b) skull in ventrolateral view; (c) forelimb mainly in lateral view; (d) virtual reconstruction of the skull in dorsolateral view; (e) virtual reconstruction of the skull in ventrolateral view. Right side indicated by (r), left side indicated by (l). (d) and (e) at same scale. ap, angular process; as, alisphenoid; bh, basihyal; c, lower canine; C, upper canine; C2, axis (cervical vertebra 2); ca, capitate; ci, crista interfenestralis; cl, clavicle; cot, coronoid tubercle; cp, coronoid process; ct, centrale; cv, cervical vertebrae; d, dentary; eh, epihyal; fc, fenestra cochleae; fr, frontal; fv, fenestra vestibuli; gf, glenoid fossa; h, humerus; ha, hamate; if, infraorbital foramen; ju, jugual; lc, lacrimal; lcf, lacrimal foramen; lu, lunate; mac, mandibular condyle; maf, masseteric fossa; max, maxilla; mc, metacarpals; na, nasal; oc, occipital condyle; omc, ossified Meckelian cartilage; pa, parietal; pgf, postglenoid fossa; pgp, postglenoid process; ph, phalanges; pi, pisiform; pmx, premaxilla; po, postorbital process; pr, promontorium; ptf, posttemporal foramen; r, radius; s, scapular; sc, scaphoid; sh, stylohyal; sf, stapedius fossa; sq, squamosal; st, sternum; T, thoracic vertebrae; td, trapezoid; th, thyrohyal; tm, trapezium; tq, triquetrum; u, ulnar. Wang et al. (2022).

The specimen is a partial skeleton with a complete skull, forelimbs and part of the trunk and hindlimbs, which is preserved on a single slab of material. The dorsal and right lateral portions of the skull are obscured by the rock-matrix, but could be observed by computerised tomographic imaging.

Cokotherium jiufotangensis has an ossified Meckelian cartilage, something seen in modern Eutherians, but not previous Early Cretaceous examples such as Eomaia, Prokennalestes, Hovurlestes or Ambolestes. This had led to speculation that early members of the group retained a cartilaginous Meckelian sulcus into adult life, as was the case in the contemporary Eutriconodontan and Zhangheotheriid Mammals. 

Furthermore, this cartilage is reduced in size, which likely indicates that the middle ear bones have become detached from it, a key development of the ear in modern Mammals, which is not seen in the Eutriconodontans. The ear bones are separated from the Mecklian cartilage in some Zhangheotheriids, although only by a small gap, and this may also be the case in Cokotherium jiufotangensis.

Jaws and dentition of Cokotherium jiufotangensis (IVPP V23387). (a) Right upper jaw in lateral view; (b) right upper jaw in occlusal view; (c) left P5-M3 in occlusal view; (d) left p5-m3 in occlusal view; (e) right mandible with the ossified Meckelian cartilage (yellow) and hyoid bones (blue) in medial view; (f) right mandible with the ossified Meckelian cartilage (yellow) and hyoid bones (blue) in lateral view; (g) right mandible in dorsal view; (h) left mandible in dorsal view; (i) left mandible in lateral view showing unerupted canine. Right side indicated by (r), left side indicated by (l). (e)-(i) at same scale. ap, angular process; bh, basihyal; c, lower canine; C, upper canine; cot, coronoid tubercle; cp, coronoid process; DP, deciduous upper premolar; eh, epihyal; end, entoconid; hcd, hypoconid; hcld, hypoconulid; i, lower incisor; I, upper incisor; m, lower molar; M, upper molar; mac, mandibular condyle; maf, masseteric fossa; mdf, mandibular foramen; mec, metacone; med, metaconid; mef, mental foramen; omc, ossified Meckelian cartilage; p, lower premolar; P, upper premolar; pac, paracone; pacl, paraconule; pad, paraconid; pas, parastyle; pmc, post-metacrista cusp; pps, preparastyle; prc, protocone; prd, protoconid; sh, stylohyal; stc, stylocone; th, thyrohyal; uc, unerupted lower left canine. Wang et al. (2022).

Wang et al. were also able to reconstruct the inner ear of Cokotherium jiufotangensis in three dimensions using computerised tomographic scanning, the first time this has been done for an Early Cretaceous Eutherian Mammal (although the morphology of part of the inner ear has been described in Prokennalestes, a Eutherian from the Early Cretaceous of Inner Mongolia).

The  cochlear canal of Cokotherium jiufotangensis comprises a single coil (i.e. 360°). This is similar to the state in most later Cretaceous Eutherian Mammals, with greater coiling seen in most modern Mammals as well as some Cretaceous Zhelestids. Many other features of the ear, including  a secondary crus commune, the base of a secondary osseous lamina, the primary osseous lamina and a bony cribriform plate, are similar to those in both later Cretaceous and modern Eutherian Mammals, confirming these arose early in the history of the group.

Inner ear of Cokotherium jiufotangensis (IVPP V23387). (a) Position of inner ear (green), veins (blue), and nerves (yellow) in ventral view of cranium; (b) endocast of right and left inner ear (green), veins (blue), and nerves (yellow) in same ventral view; (c) cross section through left inner ear showing internal structures of cochlear canal; (a-c) at same scale. Endocast of inner ear (grey), cochlear and vestibular nerves (yellow) in (d) ventral, (e) dorsal, (f) medial and (g) lateral views, anterior is down, all at same scale. am, ampulla; asc, anterior semicircular canal; ca, cochlear aqueduct; cc, crus commune; ci, crista interfenestralis; cn, cochlear nerve; co, cochlear canal; cp, cribriform plate; crp, crista parotica; fc, fenestra cochleae; fn, facial nerve; fv, fenestra vestibuli; gf, glenoid fossa; gg, geniculate ganglion; hf, hiatus Fallopii; ips, inferior petrosal sinus; jf, jugular fossa; lhv, lateral head vein; lsc, lateral semicircular canal; pl, primary osseous lamina; pr, promontorium; psc, posterior semicircular canal; scc, secondary crus commune; sff, secondary facial foramen; slhv, sulcus for lateral head vein; vca, vein of cochlear aqueduct; vn, vestibular nerve. Wang et al. (2022).

The earliest Eutherian Mammals generally have a larger number of teeth than modern members of the group, and consequently these teeth are closely packed together. Cokotherium jiufotangensis has a reduced number of both incisors and molars, and consequently a less densely packed dentition, a trait otherwise recorded in Eutherian Mammals from the Late Cretaceous onwards. It still has four premolars on each side of both the upper and lower jaws, but the hindmost premolars are starting to show signs of molarisation, another trait previously known only from later Eutherian species.

Despite these apparently derived traits, a phylogenetic analysis carried out by Wang et al. suggests that Cokotherium jiufotangensis is one of the most basal Eutherians known, and possibly outside the Theria (Eutherians plus Marsupials) altogether. However, it is possible that this placement is an artefact of the small number of early Eutherians known, and our subsequent poor understanding of the relationships between these early Mammals.

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Immature feathers in juvenile Enantiornithines from the Early Cretaceous Jehol Avifauna.

Most data concerning the integument of the non-neornithine Pennaraptora; the clade that includes all Dinosaurs (including Birds) with pennaceous feathers, comes from the Middle-Upper Jurassic Yanliao and Lower Cretaceous Jehol lagerstatten in northeastern China. Thousands of specimens have been collected from these volcano-lacustrine deposits, hundreds of which preserve traces of integument that are typically rare in the fossil record. These specimens have provided direct evidence of plumage patterns and melanosome-based colouration, revealed extinct feather morphotypes, and shed light on the evolution of individual feather tracts (e.g. crus, tail). Despite this wealth of data, many gaps remain in our understanding. The preserved plumage cannot be considered complete in any specimen, and the two-dimensional preservation of most specimens makes preserved traces difficult to interpret with certainty. Ontogenetic changes in plumage, non-melanosome based colouration, the location of apteryia and much more remain largely unexplored.

Most modern Birds begin with a natal plumage that is replaced, through molting, with a series of plumages (juvenal, pre-basic) until the first basic plumage of the subadult is acquired, and then go through another series of plumages (second basic, third basic) until the definitive basic plumage of the mature adult appears, which may take up to eight years in some species. As a new feather forms it pushes out the older feather so that molting and new feather formation are essentially a single process. Immature (developing) feathers are readily identifiable as they emerge, being encased in a tubular waxy sheath, which is completely removed through preening after the feather cells have died and dried allowing the curled feather vanes to unfurl into a planar structure revealing their pennaceous morphology. The sheath is a keratinised epithelial tube that forms separately from the feather in the outer epidermal collar. The presence of the sheath obscures observation of the feather structure within and gives the feather a narrow and solid appearance; the rachis and barbs are only visible where the sheath has been removed. Molting occurs in living Birds for two reasons: during early ontogeny exchanging natal, juvenal, pre-basic, and nondefinitive basic plumages; and as adults in the definitive molt cycle associated with an annual renewal of the basic plumage and seasonally associated with an alternate plumage related to breeding and more rarely, a supplemental plumage that provides camouflage. If a Bird goes straight from the juvenal to the definitive basic plumage, the molt strategy is considered simple. If these two plumages are separated by additional molts (first basic, etc.), the molt strategy is termed complex. When a feather is damaged it is not replaced until the next molt. However, immature feathers may occur outside these ontogenetic or annual molt cycles if a feather is lost entirely in which case it is immediately replaced; this feather replacement is not considered a molt.

Feather emergence has not been convincingly documented in any Avian specimen from the rich Jehol Biota. However, immature feathers have been proposed to be present in a juvenile specimen of the Oviraptorosaur (Maniraptora: Pennaraptora) Similicaudipteryx, although this identification is not without controversy. The unusual feather traces preserved in Similicaudipteryx STM 4-1 were originally interpreted as representing a distinct feather morphotype, the so-called ‘proximally ribbon-like pennaceous feathers’. Interpreting two-dimensional fossilised traces is notoriously difficult and with only a single juvenile specimen of Similicaudipteryx available, it is difficult to weigh these two competing hypotheses. However, in this case disagreement may be exacerbated by confusing terminologies. Rishard Prum referred to the immature feathers in STM 4-1 as pin-feathers. This hypothesis was rejected by Xing Xu, Xiaoting Zheng and Hailu You based on the large size of the feather structures in question. Although widely used to refer to all immature feathers, the term pin-feather technically refers only to the early stages  of feather growth (early immature), when the developing feather is short and entirely encased in its sheath (and thus resembling a pin). At this stage the feather would most likely not be visible, blocked from view by other surrounding feathers, unless it belonged to the first incoming natal plumage of an altricial chick (born naked) or a complete molt (all feathers molting at the same time, rare in Neornithes). As the feather continues to elongate it becomes a blood quill, the mid-immature stage. The name derives from the richly vascularised pulp extending up to the pulp cap, where parts of the feather are completing their keratinisation. Late immature refers to the stage in which the distal half of the feather has emerged from the sheath, exposing the pennaceous vanes. A feather is considered mature when the pulp has receded into the calamus and the sheath has been completely removed. Therefore, the argument of Xing Xu, Xiaoting Zheng and Hailu You that the feathers in Similicaudipteryx STM 4-1 are too large to be pin-feathers (early immature) is technically correct. However, these feathers could still represent mid to late stage immature feathers.

Recently, integumentary data from the Jehol Lagerstätte is being supplemented by skeletal specimens with associated soft tissue three-dimensionally preserved in Cenomanian (approximately 99 million years old) age Burmese Amber. One such specimen, HPG-15-1, preserves a cylindrical structure protruding from the caudal region interpreted as an emerging rectrix in the early stages of development. Identification of this structure as an immature feather is facilitated by the three-dimensional preservation of remains in amber, whereas feather traces in compression fossils are obscured by overlap and their two-dimensional preservation. 

In a paper published in the journal Vertebrata PalAsiatica in January 2020, Jingmai O'Connor of the Key Laboratory of Vertebrate Evolution and Human Origins at the Institute of Vertebrate Paleontology and Paleoanthropology of the Chinese Academy of Sciences, and the Center for Excellence in Life and Paleoenvironment, Amanda Falk of Centre College, Wang Min, also of the Key Laboratory of Vertebrate Evolution and Human Origins at the Institute of Vertebrate Paleontology and Paleoanthropology of the Chinese Academy of Sciences, and the Center for Excellence in Life and Paleoenvironment, and Zheng Xiao-Ting of the Institute of Geology and Paleontology at Linyi University, and the Shandong Tianyu Museum of Nature, describe the preserved integument in four juvenile Enantiornithines from the Early Cretaceous Jehol Biota, which they interpret as mid to late immature feathers based on extensive comparison with immature feathers in extant Neornithines.

 

Immature feathers in juvenile Neornithines. (A) Late immature remiges in Pelecanus occidentalis LACM 86193; (B) mid to late immature remiges in Otus asio LACM 100682; (C) mid to late immature remiges in Turdus migratorius LACM 100338; (D)–(F) mid immature contour feathers in Tyto alba LACM 100815 (nestling). Note tubular (‘ribbon-like’ in compression fossils) appearance of the proximally sheathed portions of the developing feathers Abbreviations: fv. feather vane (exposed distal to the proximal developing portion of the feather still encased in the waxy sheath); sh. waxy sheath. Scale bars are 1 cm. O'Connor et al. (2020).

This identification informs on the interpretation of similar integumentary structures in other previously described Jehol specimens. Together with data from previously reported juvenile Enantiornithines, O'Connor et al. make several inferences regarding the molt pattern in at least some members of this diverse clade.

 

Illustration of the stages in feather development. (A) Pin feather, early immature stage; (B) blood-quill, mid-immature stage; (C) late immature stage; (D) mature feather. O'Connor et al. (2020).

IVPP V 15564 and V 14980 were studied using a Leica S4E stereo microscope and photographed under normal light using Canon 5D4 digital camera and a Dinolite AM4115ZT. STM 34-1 and STM 34-9 were photographed using a Canon EOS 5D Mark II. Measurements were taken using Fiji (ImageJ) v. 2.0.

Laser-stimulated fluorescence photography was performed using a Nikon D60 with an AF-S Micro NIKKOR 85 mm 1:3.5 G macro lens. The laser used was a 447 nm 400 mW blue Spartan laser pointer (Dragon Lasers) with a Thorlabs EDI-S20-MD mounted engineered diffuser. The diffuser produced a square dot-matrix pattern. During the long-exposure shot required for laser-stimulated fluorescence photography, the combined laser and diffuser were moved back and forth slightly to cover the entire specimen evenly in the light source; otherwise, the photograph showed only tiny dots of light and not a properly fluorescing fossil. To filter out the blue portion of the visible light spectrum, a Midwest Optical LP 470-52 Longpass filter was used.

 

Unusual tail feathers in juvenile Similicaudipteryx STM 4-1, line drawing of rectrices. Abbreviations: er. exposed rachis; otherwise as above. Scale bar is 1 cm O'Connor et al. (2020).

IVPP V 14980 consists of a fully articulated partial skeleton of a young juvenile, laterally preserved in a slab and counterslab. It can be assigned to the Enantiornithes based on the presence of a Y-shaped furcula, minor metacarpal that projects farther distally than the major metacarpal, and metatarsal IV that is more slender than metatarsals II and IV with the trochlea reduced to a single condyle. The specimen is considered a juvenile based on its proportionately large cranium with proportionately large orbit, unossified sternum, and the absence of fusion between the distal carpals and metacarpals, proximal tarsals and the tibia, and the distal tarsals and the tarsometatarsus. The remains of seven unusual feathers are visible in both slabs projecting from the caudal margin of the proximal carpometacarpus and the ulna. As preserved, the feathers are 2.7–5.1 mm long. Some of these remains are clearly missing their proximal ends and potentially the distal ends may also be incomplete. Barbs protrude from the distal 13%–53% of the feathers. Proximal to the visible barbs the feathers are solidly coloured, featureless (lacks indication of barbs or rachis), and narrow with parallel margins, overall having a strap-like or ‘ribbon-like’ appearance (‘ribbon-like’ is used here to describe the morphology of proximal portions of feathers that appear solidly colored and strap-like, meaning the width is constant, without evidence of structural elements such as barbs or a rachis; it does not refer to a specific extinct feather morphotype). These unusual feather traces are here interpreted as probable immature feathers.

 

Juvenile Enantiornithine IVPP V 14980 preserving probable immature feathers. (A) Slab A; (B) slab B; (C) close up of boxed area marked in (A) showing details of the immature feathers along the distal ulna and proximal carpometacarpus; (D) slab B under laser-stimulated fluorescence; (E) boxed region in (D) enlarged to show details of the immature feathers under normal lightAbbreviations: if. immature feathers; other abbreviations as above. Scale bars are 1 cm. O'Connor et al. (2020).

Previously described with regards to preserved sternal ossifications, IVPP V 15564 consists of a nearly complete and articulated juvenile Enantiornithine ventrally exposed preserved in a slab and counter-slab. The remains of three proximally narrow feathers with distal barbs are visible on the dorsal margin of the left humerus with traces of another three feathers projecting from the caudal margin of the distal left ulna and wrist. These are interpreted as probable immature feathers. Two incomplete remiges are preserved cranially projecting from the manus; one preserves only the calamus region and the other preserves approximately the proximal 33%–50% of the feather. Their proximal ends are featureless but barbs can be faintly observed for most of the preserved length of the more complete remix. The probable immature feathers on the humerus extend from the distal end of the deltopectoral crest to just before the mid-point of this element, measuring 6.3–8.5 mm in length. Barbs visibly protrude in approximately the distal half (41%–58%) of the feather. The feathers preserved near the wrist are shorter (2.8–4.3 mm). Barbs are only visible protruding in the distal most portion (14%–18%) of the feathers. V 15564 additionally preserves a pair of elongate ‘rachis-dominated’ tail feathers. The feather remains are only faintly preserved along the proximal three-quarters and darkly preserved distally. The feather remains are roughly equal in width for their entire length, being featureless throughout, and flexed so that they are ventrally concave. This unusual preservation may suggest that these tail feathers are also immature.

 

Juvenile enantiornithine IVPP V 15564 preserving probable immature feathers. (A) Slab A; (B) left forelimb, enlarged from boxed region indicated in (A); (C) boxed region in (B) enlarged to show detail of the immature feathers on the proximal humerus; (D) possible late stage developing tail feathers, boxed region indicated in (A) under laser-stimulated fluorescence. Abbreviations: rm. remige; other abbreviations as above. Scale bars are 1 cm. O'Connor et al. (2020).

Previously described with regards to ossification patterns in Enantiornithines, STM 34-1 represents a nearly complete and articulated juvenile laterally exposed preserved in a slab and counterslab. Mature primaries are preserved on the right wing; mature secondaries can be observed on the left wing. Body feathers are preserved along the dorsal margin of the body from the braincase to the free caudal vertebrae, ventral to the pygostyle, and on the tibiotarsus. Dense feathering is preserved associated with both humeri and the cranial margin of the wing. The body feathers appear to be immature although interpretations are obscured in most areas by the density of the preserved feathers (whereas identification is much clearer in IVPP V 15564 and V 14980 because the preserved feathers are very sparse with no overlap). The proximal portions of many of the body feathers are dark, featureless, narrow, and strap-like (parallel margins) whereas the distal most portions are lighter in colour and barbs are visible. This morphology is clearest in regions where the feather preservation is sparser, such as along the tibiotarsus. The overall morphology of the body feathers strongly resembles the immature feathers in some juvenile neornithines in which a majority of the feather remains sheathed and the feathers have a curved appearance and are oriented perpendicular to the body. The feathers in STM 34-1 are also reminiscent of the unusual feathers preserved in Cruralispennia V 21711.

 

Juvenile Enantiornithines preserving possible immature feathers. (A) STM 34-1 with mature remiges and densely preserved body feathers that appear to be immature; (B) STM 34-9 with sparsely preserved probable immature body feathers and a pair of rachis-dominated feathers; (C) close up of the area marked in (B) showing early and mid-immature stage feathers on the forelimb. Scale bars are 1 cm. O'Connor et al. (2020).

Described by Xiaoting Zheng, Xiaoli Wang, Jingmai O'Connor, and Zhonghe Zhou with regards to the morphology of the sternum, STM34-9 is a nearly complete and articulated juvenile Enantiornithine dorsally exposed preserved in a slab and counterslab. It is the only juvenile described by O'Connor et al. that is not from the Jiufotang Formation but from the older Yixian Formation. STM 34-9 has sparsely preserved body feathers located on the neck, wings and abdomen. These feathers have a solid appearance for most of their length with barbs visible distally in some of the better preserved feathers, suggesting the body feathers preserved in this specimen may be immature. A pair of ‘rachis-dominated’ tail feathers is also preserved. Similar to the body feathers these rectrices have a dark, solid appearance along the proximal two-thirds of their length. These tail feathers are poorly preserved but barbs appear to be visible along the distal third. The unusual preservation and curved appearance of these ‘rachis-dominated’ tail feathers may suggest they are immature.

 

Unusual feathers in Cruralispennia IVPP V 21711. (A) Photograph of the full slab; (B) close up of the unusual feathers on the tibiotarsus Scale bar in (A) equals 1 cm; scale bar in (B) equals 5 mm. Abbreviations as above. O'Connor et al. (2020).

Based on gross anatomical observations and comparison with living birds, O'Connor et al. suggest that the unusual integumentary structures in IVPP V 15564 and V 14980 that are proximally narrow with distally located barbs, appearing ‘ribbon-like’, are best interpreted as immature feathers partially encased in a waxy keratinous sheath. Similarly, they infer that the unusual morphology of the feathers in STM 34-1 and STM 34-9 may also be due to immaturity although conclusions are more equivocal due to the large degree of overlap in STM 34-1 and relatively poorer preservation in STM 34-9. In immature feathers the vanes are folded within the sheath, giving the feather a temporarily narrow, tubular appearance, in which rachis and barbs cannot be distinguished. Reduced into two-dimensional traces, this might appear ‘proximally ribbon-like’ and/or to superficially resemble a hypertrophied rachis. The rachis and barbs only become visible distally in mid and late stage immature feathers as the distal portions of the sheath dry out and begin to fall away or are removed by preening exposing the barbs and allowing the vanes to unfurl. The identification of immature feathers in juvenile enantiornithines is unsurprising. Living Birds go through a number of molts and plumages early in their ontogeny before reaching the definitive basic plumage characteristic of the mature adult.

Two-dimensionally preserved immature feathers appear superficially ‘ribbon-like’ for a significant portion of their proximal length. Similar ‘proximally ribbon-like’ (or ‘wirelike’) feather structures have been previously described in two specimens from the Jehol Biota, IVPP V 21711 the holotype of Enantiornithine Cruralispennia multidonta (inferred to be a subadult) and a juvenile specimen of the basal Oviraptorosaur Similicaudipteryx STM 4-1. Each taxon is currently inferred, at least by some, to possess a unique feather morphotype that is now extinct. Juvenile Similicaudipteryx STM 4-1 preserves rectrices that are described as ‘ribbon-like’ along their proximal two-thirds and normal pennaceous in appearance in the distal third, interpreted both as an unusual feather morphotype (the so-called proximally ribbon-like pennaceous feathers) and alternatively as pin-feathers. Cruralispennia V 21711 preserves feathers described as 'narrow and wire-like almost the entire length, only distally fraying into individual hair-like barbs that account for less than 10% the length of the feather', which were considered a distinct (and previously undescribed) feather morphotype in the original description. The feathers in Cruralispennia were originally described as present on the wrist and tibiotarsus. The feathers in V 21711 are densely preserved surrounding the skeleton. Although details of the plumage are heavily obscured by a high degree of overlap, re-examination suggests similar feather structures may additionally be present on other regions of the body (e.g. lateral body feathers). The descriptions of the feathers in both Similicaudipteryx STM 4-1 and Cruralispennia V 21711 is consistent with the unusual feathers preserved in the juvenile Enantiornithines described by O'Connor et al., as well as that of mid-immature feathers in extant Birds. Although two-dimensional preservation makes it nearly impossible to interpret feathers in compression fossils unequivocally, O'Connor et al. feel the unusual feather structures preserved in enantiornithines V 14980, V 15564, STM 34-1, STM 34-9, and V 21711 can best be interpreted as immature feathers based on the following lines of evidence:

First, these unusual feather structures co-occur with normal feathers throughout different tracts of the body in STM 34-1 and Cruralispennia V 21711. In extant Birds, feathers that are ornamental in structure and not just color typically occur in discrete regions, whereas the feathers here in question have a patchy distribution throughout many regions of the body consistent with a molt in which the entire plumage is in the process of being replaced so that immature feathers appear in every tract on the body. Filoplumes, specialised sensory feathers, occur throughout the plumage and have barbs only distal on the rachis, thus superficially resembling the purported immature feathers described here, although filoplumes differ in that they are very small and have a narrow, delicate rachis compared to normal feathers. The width of the proximally strap-like portion of the feathers in question is greater than the rachis of normal body feathers in other Jehol Birds making it unlikely that these are filoplumes. Furthermore, such a robust rachis would impede on the sensory function of the filoplume, which must be delicate in order to sense aerodynamic disturbances. It is unknown when such sensory feathers evolved in Aves (or a more inclusive clade of pennaraptorans), although it is unlikely (although not impossible) given their diminutive size in extant Birds, that these would be the only feather type to preserve in specimens such as V 14980. 

Second, the anatomical location of these feathers in Cruralispennia V 21711 (as well as V 14980, V 15564, STM 34-1, and STM 34-9) is inconsistent with the previous interpretation of these feathers in V 21711 as a unique morphotype of ornamental feather, wiry ornamental feathers projecting craniolaterally from the wrist would presumably impede flight. However, immature feathers in neornithines often protrude in unusual directions while incased in sheath, as also observed in STM 34-1.

Third, the large number of loose feathers associated with V 21711 supports interpretations this Bird was molting at the time of death and immature feathers would not be unexpected in juveniles such as V 14980, V 15564, STM 34-1, and STM 34-9, presumably exchanging their juvenal plumage for a more mature basic or pre-basic plumage. Immature feathers in the presumably subadult holotype of Cruralispennia multidonta, may be related to reproductive activity (ushering in an alternate plumage) or seasonal changes in plumage (supplemental plumage). However, the most likely interpretation is that they are part of an annual molt as alternate and supplemental plumages are comparatively less common within Neornithes.

An alternative interpretation is that these feathers might represent unusual taphonomic artifacts resultant from the lacustrine depositional environment since preservation in water can sometimes deform feathers. However, this interpretation is not supported given the selectiveness of the purported distortion throughout the plumage of STM 34-1 and V 21711. This also does not explain the frequency of such distortion in juvenile specimens.

Although without further material interpretations are tenuous, O'Connor et al. consider that the tail feathers in Similicaudipteryx STM 4-1 are also best interpreted as immature. As immature pennaceous feathers unfurl from their sheaths the proximal most portion of the exposed vane (at the distal-most portion of the sheath) forms a distinct V-shaped morphology that can also be clearly observed in STM 4-1. This feature is unfortunately not visible in the immature body feathers in juvenile Enantiornithines, probably due to their small size and poor preservation. The presence of immature feathers in the juvenile Similicaudipteryx STM 4-1 is almost certainly related to ontogeny and the appearance of the juvenal plumage. This is supported by the fact that all the immature tail feathers appear to be in the same stage of development, whereas in post-juvenal molts tail feathers are renewed in sequence beginning with the medial pair.

Juvenile Enantiornithines V 15564 and STM 34-9 both preserve a pair of elongate rectrices that appear unusual when compared to ‘rachis-dominated’ tail feathers preserved in subadult-adult specimens. In both specimens the tail traces are preserved in lateral view and the feathers are slightly curved. The feather remains are darkly coloured throughout their preserved length and largely featureless, whereas in the 'proximally ribbon-like' portion of ‘rachis-dominated’ tail feathers (which consists of rachis) preserved in subadult or adult specimens of Confuciusornis and Enantiornithines the proportionately wide rachis is typically observed as an empty space demarcated laterally by faint dark margins that are distally continuous with the pennaceous vane, and marked by a medial stripe (e.g. Confuciusornis V 13156, Eopengornis STM 24-1, Enantiornithine indet. GSGM-07-CM-001). In the entire preserved portion of the ‘rachis-dominated’ tail feathers in V 15564 and STM 34-9 these features are not visible. Instead the entire feather is preserved dark and 'ribbon-like' although the proximal two thirds is considerably lighter. Furthermore, the ‘rachis-dominated’ tail feathers preserved in all previously described specimens including other juveniles (e.g. UFRJ-DG 031 Av and STM 34-7) are perfectly straight, whereas the feathers in V 15564 and STM 34-9 are distinctly flexed. This featureless morphology and curvature may suggest the RDFs in V 15564 and STM 34-9 are still encased in the keratinous feather sheath (mid to late immature feathers). In this interpretation, the darker distal portion is presumably the vaned, melanosome bearing portion of the ‘rachis-dominated’ tail feather. The ornamental tail feathers in the pin-tailed Ornithuromorph Archaeorhynchus STM 7-11 appear similarly solid and featureless and may also be immature feathers. 

The only previous report of immature Avian feathers in the Cretaceous fossil record is a developing rectrix preserved protruding from the tail region in an Enantiornithine neonate preserved trapped in amber (HPG-15-1). This is considered one of the paired ‘rachis-dominated’ tail feathers commonly found in Enantiornithines, with the second feather in the pair poorly preserved, bent back against the body. The developing rectrix is preserved in a cylindrical sheath with very short barbs just visible beginning to protrude from the distal tip. Parts of the sheath appear to have been taphonomically lost but because of its small size and inclusion in amber, which is cloudy in some parts, details of the developing feather inside are not visible. Despite these limitations, three-dimensional preservation makes it much easier to interpret the fossilized integumentary structures and the observed morphology is fully consistent with early-immature stage developing feathers in extant birds. Loss of the sheath and exposure of the distally projecting barbs while the feather is still so immature is probably abnormal and a result of entrapment in amber and subsequent taphonomic processes. The fact the developing tail feathers are early immature suggests that HPG-15-1 represents an earlier ontogenetic stage than V 15564 and STM 34-9, in which the immature ‘rachis-dominated’ tail feathers are proportionately much longer (i.e. more mature). This also suggests that juvenile Enantiornithine STM 34-7 is more mature than HPG-15-1, V 15564, and STM 34-9 with regards to plumage, given that the preserved ‘rachis-dominated’ tail feathers are mature (fully developed). However, it is possible that these feathers appeared at different times in different Enantiornithine lineages and therefore any inference regarding ontogenetic maturity based on plumage is at this time tentative at best.

A late-stage Enantiornithine embryo from the Jehol Lagerstätte (IVPP V 14238) preserves traces of developing remiges (flight feathers of the wing) described as 'feather sheets'; given that the Enantiornithine is unhatched, these feathers are very likely mid to late stage immature feathers. Their large size precludes them from being early immature feathers. These feather traces and the plumage in HPG-15-1 strongly suggest that members of the Enantiornithes were born fully fledged and capable of flight soon after hatching, somewhat resembling the super-precocial Megapodes, the only group of Neornithines in which neonates are similarly born fledged and capable of flight. Megapodes do not fly immediately, requiring nearly two days to dig themselves out of their mounds during which they preen off their feather sheaths and let their feathers dry. Similarly, hatchling Enantiornithines would have had to wait until their feather sheaths were removed and their feathers dry before attempting flight. Although ecological and behavioural differences clearly exist between Enantiornithines and Megapodes (e.g. Enantiornithines were arboreal and not mound-nesters), Megapodes represent the precocial extreme in extant Neornithines and thus the closest analogue for Enantiornithine development, for which all evidence indicates a form of extreme precociality.

O'Connor et al. do not consider the sparse plumage preserved in specimens such as V 15564, V 14980, and STM 34-9 to reflect the in vivo condition and thus to represent evidence of sparse altricial-like plumage in some juvenile Enantiornithines. Rather, they consider the sparse plumage to be a preservational artifact. This inference is supported by the fact the skeleton in these and all known juvenile Enantiornithine specimens are similarly well ossified, which is strongly suggestive of precocial development. Although O'Connor et al. cannot begin to explain the selectivity of the feather preservation in these specimens, they tentatively suggest that the presence of a feather sheath may in some circumstances have aided in the preservation of some of these feathers. Taphonomy is an incredibly complex subject with every possible subdivision of an organism (from organs to cells, and from the plumage to individual feathers and feather parts) representing a unique chemical microenvironment subject to different forms of preservation, producing specimens with vastly different degrees and forms of preservation. However, attempting to account for these preservational differences is clearly beyond the scope of their current work.

The juvenal plumage is marked by the first appearance of pennaceous feathers. The presence of pennaceous feathers upon hatching indicates the absence of a downy natal plumage, which was also suggested for Similicaudipteryx and may represent the primitive Pennaraptoran condition. Most living Birds have one, in some cases more, natal plumage. All evidence for the Enantiornithes currently indicates a form of super-precociality (hatching fledged with a high degree of skeletal ossification, fairly slow post-natal growth), which excludes the presence of a natal plumage based on the presence of pennaceous remiges in hatchlings. A similar pattern is observed in Megapodes, which hatch with fully pennaceous plumage and achieve their adult plumage within several weeks in some species, before they reach adult size. The juvenile Enantiornithine trapped in amber, HPG-15-1, indicates that although the wings consisted of fully developed remiges, the juvenal plumage in at least some lineages consisted of a sparse coat of primitive feather morphotypes covering other parts of the body, and was thus very different from the juvenal plumage of super precocial Neornithines (i.e. that of Megapode neonates), and unlike that of any extant Bird.

IVPP V 15564, V 14980, STM 34-1, and STM 34-9 probably capture one of the first posthatching molts. V 15564, STM 34-9, and HPG-15-1 preserve what appear to be developing ‘rachis-dominated’ tail feathers. The presence of this feature in several juvenile specimens, including fully formed feathers in STM34-7 and UFRJ-DG 031 Av, clearly indicates these ornamental tail feathers appear at a very early ontogenetic stage. Evidence from HPG-15-1 suggests that ‘rachis-dominated’ tail feathers may appear in the first post-hatching molt in at least one Enantiornithine lineage. If sexually-dimorphic tail ornaments appear in the first molt, it suggests that Enantiornithines had only two plumages and went immediately from the juvenal plumage into the adult basic plumage in their first molt. Similarly, Megapodes hatch without their tail feathers, which appear after two weeks in the Brush-turkey (Alectura lathami), achieving basic plumage within four weeks of hatching. In contrast, most extant Birds require several annual molts before they achieve the definitive basic plumage. This suggests that Enantiornithine molting patterns were much simpler than that of most Neornithines, suggesting the complexity observed in the crown clade is limited to a subset of Avians crown-ward of the Enantiornithes and may have co-evolved with rapid growth strategies in the Ornithuromorpha, in which reproductive maturity follows skeletal maturity (Enantiornithines show the opposite condition). However, given the paucity of relevant data in the fossil record it is unlikely we will ever fully understand molting strategies in Stem Birds and their early evolution in crown Aves with any great certainty.

In other juvenile Enantiornithines STM 34-2 and STM 34-7 the plumage is well preserved but immature feathers are not observed. The identification of immature feathers in some juvenile specimens and their clear absence in others (e.g., STM 34-2, 34-7) has the potential to inform on the relative age of a particular specimen. However, when comparing degree of sternal ossification between specimens with the presence or absence of immature feathers, no pattern is apparent. Previous attempts to correlate degree of sternal ossification with other signs of maturity (e.g. size) have also failed to identify any useful patterns. This is unsurprising given the apparent diversity in growth strategies gleaned from the results of sporadic histological studies of Enantiornithines as well as the variation in molt patterns observed in living Birds that most likely would have also been present to some degree in Enantiornithines. The utility of immature feathers to assess maturity is likely further exasperated by the fact that immature feathers are ephemeral features and thus it may be that they are rarely captured by the fossil record. In taxa in which this is a slow, drawn out process lasting months, evidence of molting is less obvious and may not be detectable in the halo of overlapping feathers that most often surrounds the skeleton in compression fossils in which feathers are preserved. However, the greatest factor preventing the use of feathers to assess maturity is the differential preservation of feathers between specimens, which at this time cannot be accounted for.

The preserved integument of four juvenile Enantiornithines is described. Unusual traces are morphologically consistent with their interpretation as immature feathers. Detailed examination of gross morphology and comparison with extant birds suggests that some reported proximally ribbon-like (or wire-like) feather morphotypes may in fact represent immature feathers partially encased in sheaths. However, at this time, all interpretations of delicate integumentary structures strictly drawn from observations from compression fossils should be regarded as equivocal. In the future it may be possible to lend further support to this hypothesis through histochemistry or advanced viewing techniques (e.g. scanning electron microscopy). The sum of the currently available evidence suggests that Enantiornithines had simple molt patterns compared to living Birds, potentially only possessing the juvenal plumage they hatched with and the basic plumage of the adult, which appears far prior to the advent of both reproductive and skeletal maturity.

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