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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Keratinous beaks in Confuciusornithiform Birds.

The beaked rostrum is one of the most distinctive features of Birds, present in all living species and exhibiting an enormous diversity of form and size relative to the body. Although this morphological diversity is commonly associated with various feeding strategies, the actual relationship between shape and function is far more complex. In some extant Birds the rhamphotheca, the keratinous sheath that covers the edentulous bony rostrum and together form the beak, forms specialised structures such as filters (e.g. Flamingos) and 'teeth' (e.g. Mergansers) that facilitate certain feeding behaviors. In addition to its primary role in feeding, the beak has evolved a myriad of other functions including sound production (e.g. billclattering/culmen knocking in Storks), warfare (e.g., Toucans, Long-billed Hermit Hummingbirds), thermoregulation (e.g. Toucans), and inter and intraspecific signaling (e.g. Toucans, American Goldfinches, King Penguins). The keratinous beak is a dynamic feature, it grows continuously as it is also constantly worn away through use and can change in size, shape, and colour in response to seasonal differences in functional requirements.

A keratinous beak was absent in the earliest bird, Archaeopteryx, which had a fully toothed rostrum. Tooth reduction and an edentulous rostrum evolved numerous times during the Mesozoic evolution of Aves given the phylogenetic distribution of edentulous clades and clades containing edentulous taxa. The oldest and most basal occurrence of a toothless rostrum in Aves is in the Early Cretaceous basal Pygostylian clade, the Confuciusornithiformes, in the oldest and most primitive member of this clade, Eoconfuciusornis from the 131 million years old Huajiying Formation. Tooth loss also evolved independently at least once in the diverse Ornithothoracine clade, the Enantiornithes, as evidenced by the edentulous Gobipteryx minuta. Tooth loss is far more common in the Enantiornithine sister-clade the Ornithuromorpha, the clade that includes Modern Birds. Several Early Cretaceous Ornithuromorphs preserve edentulous rostra: Archaeorhynchus, Eogranivora, Xinghaiornis, Schizooura, and Dingavis. The phylogenetic distribution of these taxa strongly suggests that tooth loss most likely evolved independently in each lineage and thus numerous times in this clade alone. Complete tooth loss in Mesozoic Birds has been linked to herbivory, which is also suggested in some data from non-Avian Dinosaurs.

In addition, some Ornithuromorphs (e.g. Yanornis, Yixianornis) possess a rostrum that is only edentulous at the tip of the premaxillae, caudally followed by teeth. This edentulous tip, which ventrally articulates with the edentulous Avian predentary, is inferred to have been covered by a small rhamphotheca. The entire premaxilla is edentulous in the Early Cretaceous Iteravis, and in the Late Cretaceous Ornithurine Ichthyornis, and the Hesperornithiformes. However, the pattern of tooth loss in the Ornithuromorpha was not a straight-forward rostro-caudal reduction as previously hypothesized. Mengciusornis, a Schizoourid Ornithuromorph closely related to the edentulous Schizooura, possesses teeth only in the premaxilla, indicating that tooth loss in Ornithuromorphs proceeded both rostro-caudally and caudo-rostrally. 

Like an edentulous rostrum, presumably rhamphothecae also evolved multiple times during the Cretaceous evolution of Birds associated with each new occurrence of tooth loss or reduction. Although the absence of teeth is readily identifiable, actual traces of the rhamphothecae are rarely preserved in the fossil record. So far among Mesozoic Aves traces of the rhamphotheca have only been reported in four specimens referable to the Early Cretaceous basal Pygostylian clade, the Confuciusornithiformes: the holotype of Eoconfuciusornis zhengi, the holotype of Confuciusornis dui, and two referred specimens of Confuciusornis sanctus. More Avian specimens from the Jehol Group are referable to the Confuciusornithiformes than to any other clade. A large number of described specimens boast well-preserved soft tissues most commonly in the form of feathers and keratinous ungual sheaths. Most specimens are recovered from the Yixian Formation and referred to Confuciusornis sanctus. Confuciusornis sanctus is without a doubt the fossil Bird known from the greatest number of specimens in the world, with thousands reportedly known and scattered throughout collections primarily in China but also elsewhere. Most other Jehol Birds with fully edentulous rostra are known from a single specimen (e.g. Xinghaiornis, Eogranivora) with the definite exception of Archaeorhynchus, which is known from five specimens, none of which preserve traces of the rhamphotheca.

The largest single collection of Confuciusornithiformes is that of the Shandong Tianyu Museum of Nature in Pingyi, China. The collection boasts 603 specimens, all of which consist of partial to nearly complete mostly articulated skeletons. It has been reported that 273 of these specimens preserve soft tissue in the form of feathers. A survey of this collection identified only two specimens preserving traces of the soft tissue of the beak.

In a paper published in the journal Frontiers in Earth Science on 16 September 2020, Xiaoting Zheng of the Institute of Geology and Paleontology at Linyi University, and the Tianyu Natural History Museum of Shandong, Jingmai O’Connor of the Key Laboratory of Vertebrate Evolution and Human Origins at the Institute of Vertebrate Paleontology and Paleoanthropology, and the Chinese Academy of Sciences Center for Excellence in Life and Paleoenvironment, Yan Wang and Xiaoli Wang, also of the Institute of Geology and Paleontology at Linyi University, and the Tianyu Natural History Museum of Shandong, Yin Xuwei and Xiaomei Zhang, again of the Tianyu Natural History Museum of Shandong, and Zhonghe Zhou, also of the Key Laboratory of Vertebrate Evolution and Human Origins at the Institute of Vertebrate Paleontology and Paleoanthropology, and the Chinese Academy of Sciences Center for Excellence in Life and Paleoenvironment, describe the two beaked specimens from the collection of the Tianyu Natural History Museum, and compare them to other specimens preserving traces of the rhamphotheca with regards to shape and mode of preservation.

603 specimens belonging to the Confuciusornithiformes in the collection of the Tianyu Natural History Museum were surveyed for preserved rhamphothecae. This feature was identified in two previously undescribed specimens, STM13-133 and STM13-162. As in all specimens preserving this feature, the traces are visible under normal light. These two specimens were studied using a Leica binocular microscope and photographed using a Canon EOS 5DS. Measurements were taken using Fiji (ImageJ) 2.0. Figures and illustrations were generated using Adobe CC 2018.

 

Confuciusornis sp. STM13-133: (A) main slab; (B) counter-slab. Scale bar equals two centimetres. Zheng et al. (2020).

Specimen STM13-133 consists of a nearly complete and articulated individual preserved with feather impressions in a slab and counter-slab. STM13-133 can be readily identified as Confuciusornis based on the robust edentulous rostrum, stout boomerang shaped furcula lacking a hypocleidium, massive perforated deltopectoral crest on the humerus, and characteristic manual morphology with reduced major digit ungual. Where unbroken, the bones are preserved white with cracks distinctly visible in black. Where the bones are broken they are reveal a reddish colouration indicative of iron oxidative taphonomic processes. The feathers are preserved primarily as reddish impressions with the rachis clearly visible as a gap in some primaries. In the distal half of the left wing the barbs are preserved a pale white-pink color. In addition to the wings, in which impressions of the primaries, secondaries, and some coverts are fairly well-preserved, body feathers are preserved on the dorsal and ventral margins of the skull, ventral surface of the neck, left lateral surface of the body, and near the right knee. The keratinous sheaths covering the manual and pedal claws are  mostly not preserved although the sheath covering the left minor digit ungual is partially preserved as a reddish stain.

The skull is preserved in left lateral view. Although the general shape of the skull is well-preserved, the cranial bones themselves are very poorly preserved, with most elements preserved as reddish voids or elements torn in half between the slab and counter-slab. The traces of the rhamphotheca appear to consist of four distinct parts, suggesting that the rhamphotheca covering the upper jaw and the rhamphotheca covering the lower jaw each consisted of two elements. This is evident from the morphology of the preserved traces themselves and further suggested by the fact that short feathers appear to extend nearly to the rostral tip of the rostrum (approximately, only the rostral 4 mm of the premaxillary corpus lack feathers) and toward the tip of the mandibular symphysis. However, it cannot be ruled out that these 'separate parts' of the rhampthothecae are not the result of post-mortem breakage.

 

Close up of the skull of Confuciusornis STM13-133: (A) photograph; (B) close up of the rhamphothecal traces (C), interpretative drawing of (B). Dark gray indicates poorly preserved bone, light gray indicates bone preserved as voids, orange indicates the traces of the rhamphothecae, and blue indicates feather traces. Anatomical abbreviations: de, dentary; en, external nares; fp, frontal process of the premaxilla; fr, feathers; l?, possible left side of the rhamphotheca; mx, maxilla; pm, premaxilla; r?, possible right side of the rhamphotheca; rh, rhamphotheca. Zheng et al. (2020).

The dorsal feathers are short, extend caudodorsally, and increase in height caudally until they disappear due to poor preservation (the layer of matrix preserving the soft tissue is chipped away in this region) just rostral to the level of the caudal margin of the external nares. From their rostral-most point until the cranial margin of the external nares the feathers appear to overlap the right frontal process of the premaxilla, however, it is likely that the basal portions of the feathers are not complete. Caudal to this point portions of the feather apices are preserved but not their basal portions, exposing a caudal portion of the rhamphotheca extending along the dorsal margin of the frontal process of the right premaxilla. This trace extends for approximately the length of the dorsal margin of the external nares with a fairly even thickness of 2.8 mm and ends rather abruptly just cranial to the caudal margin of the external nares suggesting it may be caudally incomplete.

The rhamphothecae extend rostrally from the premaxillae and dentaries just over 9 mm. From the rostral position of the feathers and the pre-rostral length of the rhamphothecal traces it may be that both the rhamphothecae and the feathers are displaced rostrally. The traces of the upper and lower rhamphothecae overlap obscuring the dorsoventral thickness of these traces although the tips of each can be distinguished, preserved very close to each other consistent with the closed morphology of the jaws. The upper rhamphotheca appears to consist of two separate parts. The dorsal margin of each part can be distinctly observed due to the fact these margins are preserved a darker color than the remaining rhamphothecal traces. The dorsal margins of the right and left portions depart from a single point, approximately demarcating an angle of 8. For most of their preserved length cranial to the premaxilla the dorsal margins extend caudally nearly parallel to each other, separated by a distance of 0.86 mm. Both traces are interrupted by the feathers on the dorsal (or dorsolateral) margin of the skull.

The rhamphothecae covering the mandible also appears to be formed by left and right parts, the tips of which are clearly preserved slightly offset from each other. This could be due to the notched morphology of the tip of the mandible itself. However, a faint line of darker reddish colour extends through the lower rhamphothecal traces parallel to the ventral margin, continuous with the offset tip of the presumably right half of the mandibular rhamphotheca. The mandibular rhamphothecae extend rostrally to approximately the same level as the premaxillary rhamphothecae. As preserved the traces have a maximum thickness of 2.47 mm just rostral to the mandibular symphysis. Caudally it steadily decreases in thickness disappearing just rostral to the level of the cranial margin of the external nares. Similar to the upper jaw, the presence of left and right elements forming the mandibular rhamphothecae is supported by submalar feathers that extend far rostrally, presumably extending between the two halves of the mandibular rhamphothecae. These ventral feathers begin just caudal to the rostral tip of the mandibular bones and are separated from the dentary by the preserved trace of the mandibular rhamphothecae. The feather traces are interrupted by poor preservation (the layer preserving the soft tissue is clearly not preserved, exposing a lower level of sediment) at the level of the external nares, but appear again at the level of the antorbital fenestra and continue caudally, continuous with feathers along the ventral surface of the neck.

STM13-162 represents a complete specimen preserved in lateral view in a slab and counter-slab. The specimen is preserved in an unusual position with all the limbs folded close to the body. Faint traces of feathers are visible around the skeleton including traces of the wings. The keratinous sheaths covering the manual and pedal unguals are preserved. Dark material in the orbit may be soft tissue traces of the eye. Like STM13-133, STM13-162 is referable to Confuciusornis based on the robust edentulous rostrum, stout boomerang shaped furcula lacking a hypocleidium, massive perforated deltopectoral crest on the humerus, and characteristic manual morphology with hypertrophied alular ungual and reduced major digit ungual. 

Confuciusornis sp. STM13-162 (main slab). Scale bar equals two centimeters. Zheng et al. (2020).

The skull is preserved in lateral view. Although the skull is complete and it retains its general shape the bones are crushed with little to no clearly preserved anatomical details. Notably, the tip of the fused premaxillae are slightly but distinctly downturned. Traces of the rhamphothecae from both the upper and lower jaws are visible in both slabs but more clearly observed in the main slab. These traces appear to be slightly displaced from their natural positions. The upper rhamphotheca trace is displaced dorsally so that the ventral margin is not level with the ventral margin of the premaxilla. The traces extend 5.9 mm from the premaxillae with a total length of 26.8 mm, dorsally ending near the caudal margin of the external nares. The pre-rostral portion of the traces form a triangular impression, divided dorsally and ventrally by the fact the dorsal portion that is continuous with the trace extending caudally over the frontal processes of the premaxillae is much darker. The margin dividing the darker (dorsal) and lighter (ventral) traces is interpreted as the ventral margin of the trace of either the right or left upper rhamphotheca, with the opposing trace somewhat displaced ventrally, forming the lighter portion of the pre-rostral impression of the rhamphothecae.

 

Close up of the skull of Confuciusornis STM13-162: (A) photograph of slab; (B) photograph of counter slab; (C) interpretative drawing. Scale bars equal one centimetre. Zheng et al. (2020).

The trace of the mandibular rhampotheca extends 6.66 mm from the dentaries and has a total length of 19.02 mm. The traces have a fairly even thickness of 1.52 mm except where they taper away caudally.

Due to the rare preservation of the rhamphotheca in the fossil record, very little is known about this feature in extinct organisms. As such, each new specimen has the potential to provide new information. So far among Mesozoic Birds, data has only been recovered for the Cretaceous Confuciusornithiformes. Most birds collected in deposits corresponding to the Lower Cretaceous Yixian Formation are referable to this clade. Counter intuitively, the horny sheath or rhamphotheca that covers the rostrum in edentulous Birds is less likely to preserve than the more pliable feather integument. In a collection of 603 specimens of Confuciusornithiforms nearly half preserve feathers on some part of the body (273 specimens, 45%). In contrast, only two specimens preserve some trace of the beak, that is 0.33% of the collection. This percentage is likely exaggerated by at least two factors. First, most fossils in the Tianyu Natural History Museum collection are not fully prepared and what preparation has been done was conducted prior to being placed in the collections of the Tianyu Natural History Museum and was not done by professionals. This may make it more difficult to identify the subtle traces of the preserved rhamphothecae, which are proportionately small compared to traces of the plumage. Furthermore, these subtle traces may also have been lost during cursory non-professional preparation attempts. The rhamphothecal traces preserved in Confuciusornis IVPP V12352 are surrounded by clear marks of preparation; unfortunately, there is not enough data currently available to assess to what extent the morphology of these and other soft tissue traces are affected by the work of preparators. Second, as the collection was aggregated an emphasis may have been placed on acquiring feathered specimens, which are visually striking, but not on specimens preserving the rhamphotheca, a soft tissue feature that is less obvious and easily overlooked. Unsurprisingly, the two specimens preserving beak traces described by Zheng et al. also preserve feathers. Of the two new specimens, STM13-133 is the better preserved and offers the most significant new morphological information.

The appearance of the two new specimens STM13-133 and STM13-162 suggests very different modes of preservation, presumably contributing to the diversity of taphonomic processes that apparently lead to the preservation of rhampthothecae in Jehol specimens. Preservation is very different in in all six known specimens that record these traces, among these differences varying with respect to the quality of bone preservation (excellent in Eoconfuciusornis zhengi IVPP V11977 and Confuciusornis sanctus IVPP V12352) and preservation of feathers (preserved in all but Confuciusornis sanctus IVPP V12352). Notably, several specimens appear to preserve some non-keratinous soft tissue (e.g., probable eye tissue in STM13-162; abdominal tissues in Eoconfuciusornis zhengi IVPP V11977) indicative of exceptional preservation.

In STM13-133 the mandibular rhamphothecae extend rostrally to approximately the same level as the premaxillary rhamphothecae as in Confuciusornis dui IVPP V11553 and Confuciusornis sanctus BMNHC-PH986, whereas the premaxillary traces extend farther in Confuciusornis sanctus IVPP V12352 and STM13-162 and the mandibular traces extend farther in Eoconfuciusornis zhengi IVPP V11977. With the limited information available it is impossible to determine to what degree this is due to taphonomy vs. actual interspecific differences. The traces in the two Tianyu Natural History Museum specimens are much more comparable to those in Confuciusornis sanctus IVPP V12352, so far Confuciusornis dui IVPP V11553 is unique in having a rhamphotheca that is rostrally upturned and this may be a diagnostic feature of this taxon. However, the holotype and only known specimen has been lost making Confuciusornis dui a nomen dubium.

Notably, in the five specimens in which both skull and femur length can be measured the skull is proportionately much larger in specimens of greater body size. Interpretations are obscured by the taxonomic diversity of these Confuciusornithiforms. However, at least Eoconfuciusornis zhengi IVPP V11977 is regarded as a subadult. This may suggest that the skull becomes proportionately longer in mature individuals. A proportionately short rostrum is a common indicator of ontogenetic immaturity. This also suggests that ontogeny is not a factor that plays into preservation of the rhamphotheca since this feature is preserved in both subadult and adult specimens.

Ichthyornis and Hesperornis were described as having osteological correlates that indicate the presence of compound rhamphothecae with the upper jaws covered by a premaxillary nail, culminicorn and paired latericorns and the lower jaw rhamphothecae consisting of a mandibular nail and paired ramicorns. This in turn was used to infer that the presence of compound rhamphothecae covering the rostrum is plesiomorphic to the crown clade. However, a recent comprehensive description of the skull of Ichthyornis based on multiple new specimens indicates that osteological features of compound rhamphothecae, i.e. a nasolabial groove on the upper jaw and mentolabial grooves on the mandibles, are in fact absent. Only a premaxillary nail is inferred to be present in this taxon based on the presence of numerous neurovascular foramina on the rostral portion of the edentulous premaxilla, presumably accentuating the hooked morphology of this element. A mandibular nail was absent but a small keratinous sheath likely covered the outer surface of the predentary bone present in these non-Neornithine Ornithurines, thus the condition in Hesperornis and Ichthyornis represents a primitive rhamphothecal morphology not present in Neornithines (the predentary being a feature restricted to non-Neornithine Ornithuromorphs).

An edentulous rostrum covered by rhamphothecae in the Confuciusornithiformes evolved independently from that in Ornithurines like Ichthyornis, Enantiornithines like Gobipteryx, basal Ornithuromorphs like Archaeorhynchus and Eogranivora, and other stem lineages that display some form of tooth reduction and thus may have had small beaked portions of the rostrum similar to Ichthyornis (e.g. Jeholornis, Sapeornis). Therefore, it would not be unexpected to find morphological differences in this feature between Cretaceous Avian clades. In most Neornithines the caudal extent of the rhamphothecae of the upper jaw is approximated by the caudal extent of the maxillary process of the premaxilla. If Confuciusornithiforms shared this condition with Neornithines it would suggest that the ventral and lateral portion of the rhamphotheca below the external nares would be rostrally limited due to the fact that the maxilla makes up a majority of the facial margin. It cannot be determined if the ventral margin of the rhamphotheca ends level with the premaxillomaxillary contact since the ventral margin below the premaxilla is not preserved in any specimen and similarly the lateral portions of the rhamphotheca are also not preserved (presumably lost during preparation). However, Zheng et al. suggest it is more likely that Confuciusornithiforms differed from Neornithines in this feature and that the rhamphotheca extended onto the maxilla in Confuciusornithiforms. This is supported by the fact that the maxilla, like the premaxilla and dentary, also bears pits and grooves indicative of neurovasculature. Compared to the premaxillary body and the rostral portion of the dentary, the maxilla is dominated by grooves and pits are less common. These pits and grooves are only present on the premaxillary process of the maxilla suggesting the caudalmost extension of the rhamphotheca on the upper jaw was the caudal margin of the external nares, which is partially enclosed caudally by the nasal process of the maxilla that divides this element into premaxillary and jugal processes. Notably there are no osteological correlates (pits, grooves) that support the caudal extension of the rhamphotheca along the dorsal surface of the skull although the presence of the rhamphotheca is demonstrated by direct evidence in several specimens (IVPP V12352, STM13-133).

 

Possible reconstructions of the skull integument in Confuciusornis: (A) the rhamphotheca is limited to the premaxilla as in neornithines, and the cranial feathers extend only as far rostrally as the rhamphotheca; (B) the upper rhamphotheca is reconstructed extending along the premaxillary process of the maxilla and the dorsal cranial feathers are reconstructed extending rostrally, possibly medially between the two halves of the rhamphotheca as suggested by STM13-133. Zheng et al. (2020).

Nasolabial, culminolabial, and mentolabial grooves, features that indicate the divisions between the compound rhamphothecal elements in neornithines, are not visible in the skull bones of Confuciusornis. The premaxillary nail, the only portion of the neornithine rhamphotheca considered present in Ichthyornis, is rostrally restricted. At least along the dorsocranial margin the rhamphotheca is caudally extensive in Confuciusornis. The absence of a culminolabial groove may suggest that the rhamphotheca covering the tip of the premaxilla and frontal processes of the premaxilla were not separated into a premaxillary nail and culminocorn as in Neornithines with compound rhamphothecae. This is also supported by the morphology of the traces in IVPP V12352 in which the dorsal margin of the preserved rhampthothecal traces are smooth along their entirety. This suggests the condition in Confuciusornithiforms was more reminiscent of the simple rhamphotheca in many living birds in which the compound elements are entirely fused and grooves are absent. However, unlike in Neornithines, in which the premaxillary nail and mandibular nail are single elements, evidence from STM13-133 may suggest that the rhamphotheca covering the upper and lower jaws including the rostral-most portions may have been compound elements medially divided into left and right components.

 

A close up of the cranial half of the rostrum in Confuciusornis sanctus IVPP V12352 showing the pits and grooves that cover the premaxillary body, premaxillary process of the maxilla, and the rostral portion of the dentaries, inferred to reflect neurovasculature related to the presence of a keratinous beak. Scale bar equals five millimetres. Zheng et al. (2020).

Although STM13-133 is the only specimen to preserve evidence suggesting the Confuciusornithiform rhamphotheca was divided into right and left halves, it may be that only one side, presumably the side still buried in matrix (for example, the right in IVPP V12352), is preserved in most specimens due to the lateral exposure of the skull and or taphonomy, or that the two halves were tightly attached rostrally. The morphology in STM13-162 somewhat supports the interpretation at least that the upper rhamphotheca consisted of left and right halves but the weakly preserved traces provide no definitive information. However, without additional data it is impossible to rule out the alternative that the appearance of right and left components forming the rhamphotheca in STM13-133 is an artifact of preservation. Potentially the upper and lower rhamphothecae eere crushed and broken giving the appearance of consisting of two parts. Crushed, two-dimensional fossils often preserve fractures than can be misinterpreted as true morphologies.

A 2019 study by Amanda Falk, Jingmai O'Conner, Min Wang, and Zhonghe Zhou, discussed the differential preservation of various keratinous integumentary structures in the numerous described specimens of Confuciusornithiforms. Despite evidence that the rhamphotheca is the hardest of the beta-keratin integumentary structures, it is the least commonly preserved and notably there appears no pattern in the preservation of specific keratin structures. STM13-133 and STM-13-162 offer no information that elucidates this issue. Superficially, preservation appears very different between these two specimens, offering no clues as to the taphonomic conditions that are conducive to preservation of this feature. Differences in bone coloration hint at different mineralisation processes (iron oxidative processes were clearly part of the taphonomic history of STM13-133 as indicated by the reddish color where the bones are broken and the reddish stains forming the feather traces, but not STM13-162). Differences in preservation of the plumage also point to different modes of preservation; a large portion of the plumage is preserved in STM13-133 and these are mostly preserved as reddish stains, whereas the feathers in STM13-162 are only faintly preserved. The stark contrasting modes of preservation (evident from comparing the quality of preservation of structures such as bone and feathers and differences in mineral composition as superficially determined by differences in colour) between the two specimens confirms previous observations that preservation of the rhamphotheca is not limited to a very narrow set of specific chemical conditions. In the future, chemical analyses of specimens preserving rhamphothecal traces may shed light on the specific taphonomic processes and geochemical conditions conducive to the preservation of these traces.

Given the differential preservation of keratinous structures in various specimens, we hypothesize that the preservation of keratinous integumentary structures may not be related to properties of the keratin itself. The common preservation of feathers compared to the rhampthotheca may be due to the fact that the former is commonly melanised in Confuciusornithiforms, as demonstrated in multiple specimens. The addition of melanin to keratinous structures increases their relative hardness. Melanin is extremely resistant to decay and most preserved feathers in Jehol specimens that have been studied using scanning electron microscopy at most commonly melanosomes are preserved together with their impressions. This may be related to the fact that most Jehol specimens are preserved split between a slab and counter-slab; the act of splitting may be responsible for the formation of impressions of melanosomes in the surrounding matrix (whether consisting of degraded or petrified remnants of the feather keratin or sediment) just as voids are left by bones that remain in the opposite slab. The few studies in which only imprints or melanosomes were recovered may reflect limited sampling. However, even where only impressions of melanosomes were recovered, keratin was reportedly not preserved. Although understanding of feather preservation in the Jehol and other deposits is currently incomplete, available studies strongly suggest that a majority of feather traces contain preserved melanosomes. The rare preservation of the rhamphothecae in Confuciusornithiforms may suggest this structure was not melanised in most members of this clade (in Neornithines both melanic and non-melanic beak morphologies are present). The only known specimen of Confuciusornis dui preserves traces of the rhamphotheca and thus hypothetically it is possible the bill may have been melanised in this species. Unfortunately, this hypothesis cannot be tested since the specimen is lost. Alternatively, the bill may be seasonally melanised, like that of some extant Birds, and only preserved in individuals that died during this particular season. Although the overall scarcity of such traces (now six specimens reported out of purportedly thousands) suggests that the rhamphotheca was simply not melanised, it is possible to test these two hypotheses by sampling bill traces preserved in specimens of Confuciusornis and studying them using scanning electron microscopy in order to determine the presence or absence of preserved melanosomes. However, the rarity of these traces and their relatively limited surface area (compared to feathers) make it unlikely that this will be possible due to the destructive nature of scanning electron microscopy sampling. If Confuciusornithiforms had non-melanic rhamphothecae this would indicate the bill was lightly coloured, thus providing new data that will translate to more accurate reconstructions of this important clade of Cretaceous Birds.

A total of six Confuciusornithiforms preserving traces of the rhamphothecae have now been identified. Preservation is very different between all six specimens, thus providing no information pertaining to the specific taphonomic conditions that are conducive to the preservation of this feature. In the future, chemical analyses on all six specimens will hopefully elucidate the different diagenetic pathways that are conducive to preservation of the rhamphotheca, at least in Confuciusornithiforms. The rare preservation of rhamphothecae may suggest that the beak in Confuciusornithiforms was non-melanic and thus lightly coloured. Although it was reasonable to assume that the rhamphothecae would have a different morphology in each independent evolutionary origin of this feature, this study provides the first discussion of the differences between the rhamphothecae in non-Neornithine Ornithurines, Confuciusornithiforms, and Neornithines. In addition to having rhamphotheca that extends onto the maxilla, one specimen suggests that the Confuciusornis rhamphotheca may have been a compound structure consisting of right and left halves on both the upper and lower jaws. Osteological and soft tissue evidence suggests that the rhamphothecae covering the upper jaw extended dorsally and laterally to the caudal margin of the external nares. Notably, evidence from several specimens indicates that although pits and grooves may indicate the presence of a rhamphotheca, they do not correlate strictly with the extent of this feature as the frontal processes of the premaxilla lack pits and grooves but were clearly covered in rhamphotheca in Confuciusornithiforms.

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Saurophthirus laevigatus: A new species of Flea from the Early Cretaceous Yixian Formation of Liaoning Province, China.

Siphonaptera, commonly known as Fleas, are one of the widely known blood-sucking ectoparasitic Insects, comprising more than 2500 described species in 16 extant families. Up to now, the fossil Siphonaptera contain 16 species in five families from Cainozoic amber and Mesozoic compression fossils. All Cainozoic Fleas have been placed in two families, the Ctenophthalmidae and Pulicidae, while all Mesozoic Fleas, grouped in three families, the Pseudopulicidae, Saurophthiridae, and Tarwiniidae, which together form an extinct superfamily, the Saurophthiroidea, comprising nine species within five genera. Saurophthirus longipes, an unusual insect from the Early Cretaceous Zaza Formation of Baissa in Siberia, was described by Arnold Ponomarenko in 1976. He reported that its similarities with Fleas are piercing-sucking proboscis and soft distensible abdomen. A family of Saurophthiridae was established by Ponomarenko ten years later in 1986, including only this species. Another species of this family, Saurophthirus exquisitus, was described in 2013, based on three specimens, from the Early Cretaceous Yixian Formation of Liaoning Province, China, and it was suggested that the Saurophthiridae represent a transitional group from basal to extant Fleas. These fossil Fleas display some features seen in crown Fleas but are still considerably different from extant Fleas in many morphological characters, e.g., the absence of pronotal and genal ctenidia (comblike structures) on the body, the lack of the uniquely modified jumping hind legs, distinct ctenidia on the tibiae, more developed eyes, antennae with more than 15 segments, absence of laterally compressed abdomen, presence of medium body size, swollen hind coxae and partially extended male genitalia. These features indicate that Saurophthirus is more closely related to modern Fleas than to the Cretaceous genera Pseudopulex and Tarwinia.

In a paper published in the journal Acta Palaeontologica Polonica on 21 February 2020, Yanjie Zhang of the College of Life Sciences at Capital Normal University, Chungkun Shih, also of the College of Life Sciences at Capital Normal University, and of the Department of Paleobiology at the Smithsonian National Museum of Natural History, Alexandr Rasnitsyn of the Palaeontological Institute of the Russian Academy of Sciences, and Dong Ren and Taiping Gao, again of the College of Life Sciences at Capital Normal University, describe a new species of Saurophthirus from from the Yixian Formation of Liaoning Province, China, which produces Insects ranging in age from about 128.2 to 121.6 million years, with the majority of the specimens dated to about 125 million years ago (Early Cretaceous).

The new species is named  Saurophthirus laevigatus, meaning 'smooth' in Latin. It is described from a single, male, specimen with body almost perfectly fusiform and 9.8 mm long excluding antennae, almost completely-preserved ventral view, slightly dorsoventrally compressed. 

Saurophthirid Flea Saurophthirus laevigatus, male (holotype, CNU-SIP-LL2015001) from the Early Cretaceous Yixian Formation of Northeastern China. (A) Part, habitus in general view (A₁), line drawing (A₃), enlargement of antenna (A₂), details of genitalia (A₄), (A₅); 7, 8, 9, the seventh to ninth abdominal segments. (B) Counterpart, general view (B₁), enlargements of claws (B₂), (B₃), arrows. (A₅) photographed under alcohol. Scale bars: (A₁), (B₁) 1 mm; (A₃) 2 mm; (A₂), (A₄), (A₅), (B₂), (B₃) 0.5 mm. Zhang et al. (2020).

Extant Fleas display peculiar morphological characters including relatively small body-size, laterally compressed body, the uniquely modified jumping middle and hind legs. However, the morphological characters of the stem-group Fleas are primitive compared to the crown Fleas. The fossil Fleas known from the Mesozoic possess the following features to support their Flea affinity: the piercing-sucking mouthparts with serrate stylets to penetrate thick and body coverings; relatively large body with long but thin legs and scythe-shaped claws for living on a large surface; body and legs with stiff spines and setae all directed backward imply that they adapted to fix and move on a surface covered with hairs or feathers. Each of the above features separately can be probably found in some other insect groups. However, for insects having all these characters combined, they were most likely adapted to blood sucking of vertebrate host with outgrowths like hairs or feathers. Saurophthirids have been suggested to resemble crown-group Fleas. The new species has the 'transitional' characters of Saurophthiridae and particularly genus Saurophthirus, including the medium body size, short piercing-sucking stylet mouthparts, slender legs (enlarged hind coxae) and the half-retracted male genitalia.

Up to now, three families, four genera with seven fossil species of basal Flea insects have been reported from the Cretaceous of Australia, Russia, and the Northeastern China. In contrast to the species from the Jurassic, the taxa from the Cretaceous have a higher degree of richness, suggesting the Cretaceous is an important stage of evolutionary radiation after the origination of basal Fleas in the Jurassic.

For ectoparasitic insects living in feathers of feathered Dinosaurs, Pterosaurs, or Birds or in hairs of Mammals, their small body size would have provided advantage for concealment in the host and reduced probability for being detected and removed by the host. Furthermore, Zhang et al. consider that the reason for decreasing body size of basal Fleas was to reduce the blood intake and minimize Flea’s demand for food and energy inputs. The blood consumption of the flea is positively correlated with its weight, and the blood consumption of female Fleas are significantly higher than males. The blood consumption of the female Cat Flea, Ctenocephalides felis, per day is equivalent to 15.15 times of their body weight. So, Zhang et al. believe that the Early Cretaceous Fleas, especially the transitional Fleas, became smaller in order to avoid host detection and reduce blood intake, which is the adaptation to ectoparasitic life in the early stage of evolution. 

In addition, the evolution of the male genitalia is clearly indicated in fossils. The basal taxa from the Jurassic have entirely exposed genitalia with broad gonostylus articulated at apex to form a wide clasping organ, in contrast to the half-retracted genitalia from the Early Cretaceous. Therefore, Zhang et al.  believe that the new species with more retracted genitalia might have provided concealment and protection.

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