Systematic palaeontology

Aves Linnaeus 1758

Ornithothoraces Chiappe 1995

Enantiornithes Walker 1981

Cruralispennia multidonta gen. et sp. nov.

Etymology. The generic name is derived from Latin ‘Cruralis’ and ‘penna’, referring to the unique feathers on the tibiotarsus; the specific name is derived from Latin ‘mult’ and ‘donta’, referring to the numerous dentary teeth.

Holotype. IVPP 21711 (housed at the Institute of Vertebrate Paleontology and Paleoanthropology), a nearly fully articulated partial skeleton with associated feathers preserved on a single slab (Fig. 1; Supplementary Table 1).

Figure 1: Cruralispennia multidonta holotype (IVPP V21711). (a) Photograph; (b) line drawing. ca, caudal vertebra; cv, cervical vertebra; il, ilium; is, ischium; lad, left alular digit; lco, left coracoid; lde, left dentary; lfe, left femur; lhu, left humerus; lmd, left major digit; lpd; left pedal digits; lra, left radius; lta, left tarsometatarsus; lti, left tibiotarsus; lul, left ulna; pu, pubis; py, pygostyle; qu, quadrate; rco, right coracoid; rfe, right femur; rhu, right humerus; rmd, right major digit; rpd, right pedal digits; rra, right radius; rsc, right scapula; rta, right tarsometatarsus; rti, right tibiotarsus; rul, right ulna; sk, skull; st, sternum; sy, synsacrum; tv, thoracic vertebra. The white circles (numbered 1–5) and box indicate the locations of the feather and histological samples, respectively. Scale bar, 10 mm. Full size image

Locality and horizon. The new specimen is collected from the Protopteryx-horizon of the Huajiying Formation at the Sichakou Basin, Fengning County, Hebei Province, northeastern China. Four other birds are reported from the same horizon, Eoconfuciusornis, Protopteryx, Eopengornis and Archaeornithura2,3,4,8. Stratigraphic correlation and isotopic dating place this horizon at 130.7 Myr ago, late Early Cretaceous5,7,9.

Diagnosis. A small enantiornithine with the following unique features: 14 dentary teeth; abbreviated, plough-shaped pygostyle with a pygostyle/tarsometatarsus length ratio of about 0.28; coracoid mediolaterally narrow with the sternal margin measuring only one-quarter of the proximo-distal length; sternum bearing a V-shaped caudal margin and two pairs of subequal caudal trabeculae; manus shorter than the humerus; postacetabular process of the ilium short and strongly ventrally directed; dorsal process of the ischium more distally placed; and pubis without a distal expansion.

Description

The skull is poorly preserved and partially disarticulated with only a few elements that are clearly identifiable (Fig. 2a,b). The short premaxillary corpus defines a 43° angle with the frontal process, which is considerably larger than in most other enantiornithines, for example, Protopteryx (28°), Parabohaiornis (26°) and Eoenantiornis (30°). Only two premaxillary teeth are visible, but poor preservation is likely obscuring the presence of additional teeth. Typically, enantiornithines have four premaxillary teeth10. The maxilla is triradiate in lateral view with a caudodorsally projecting dorsal process. Unlike in Pengornis11, the dorsal process is imperforate. The maxilla preserves traces of four maxillary teeth. The left frontal is exposed in ventral view; the caudal half is vaulted dorsally. A crescent-shaped element, displaced away from the cranial bones, probably represents the quadrate. It is identical to the laterally exposed left quadrate preserved in the holotype of Pengornis houi. As in most enantiornithines, a mandibular symphysis is absent. The left dentary is preserved in dorsal view (Fig. 2a). Fourteen dentary were present, more than in other known enantiornithine (for example, six to ten in bohaiornithids, two in Protopteryx4, six in Vescornis, three in Longipteryx) but similar to pengornithids (thirteen in Pengornis; Eopengornis was estimated to have 12–14 dentary teeth3). As in other basal birds with the exception of Archaeopteryx12, interdental plates are absent. All the dentary teeth are broken, missing their crowns to some extent. The outline of the base of the dentary teeth exhibits considerable variation, becoming progressively more buccolingually compressed caudal in the toothrow, with the width/length ratio declining from 0.85 to 0.43. In the fifth, sixth, tenth and twelfth through fourteenth teeth, the crowns are completely lost, revealing a large tooth pulp (an internal space housing the connective tissue and odontoblasts) occupying nearly the entire cross section of the tooth.

Figure 2: Skull and thoracic vertebrae of C. multidonta (IVPP V21711). (a) Photograph, (b) and line drawing of the skull, (c) thoracic vertebrae; dto, dentary tooth; fro, frontal; jug, jugal; lag, lateral groove of centrum; lde, left dentary; max, maxilla; mep, medial process of surangular; mto, maxillary tooth; nas, nasal; nes, neural spine; pop, postzygapophysis; prm, premaxilla; prp, prezygapophysis; pto, premaxillary tooth; qua, quadrate; sun, surangular; thv1–4, preserved thoracic vertebra 1–4. Scale bars, 5mm. Full size image

The vertebral column is incomplete (Fig. 1). Four thoracic vertebrae remain in articulation (Fig. 2c). Although the centra are largely broken, impressions of their lateral surfaces are preserved, indicating that the lateral surface was excavated by a groove in life, a feature characteristic of the Enantiornithes13. Only two free caudal vertebrae are preserved (Fig. 1). The pygostyle is fully fused (Fig. 3a). Unexpectedly, the bone is more similar to that of ornithuromorphs than to the elongated form of other enantiornithines (Fig. 3b–f). The pygostyle is abbreviated, having a pygostyle/tarsometatarsus length ratio of 0.28. Similar pygostyle ratios are otherwise known only in ornithuromorphs among Early Cretaceous birds (for example, 0.29 in Yixianornis, 0.22 in Iteravis, 0.25 in Archaeorhynchus; Supplementary Table 2; Fig. 3h). In contrast, the pygostyle is more than half the length of the tarsometatarsus in most enantiornithines, for example, Vescornis (0.67), Protopteryx (0.69), Pterygornis (0.72) and Sulcavis (0.79), and in some cases even subequal to or longer than the latter element (for example, Parabohaiornis and the Longipterygidae14,15). Although the Pengornithidae is characterized by a proportionately short pygostyle3,16,17, pygostyle to tarsometatarsus ratios exceed 0.4 in all the known specimens. In more basal pygostylians (Fig. 3g), the same ratio is ∼0.68 in the Sapeornithidae, and in the Confuciusornithidae the robust pygostyle is subequal to or longer than the tarsometatarsus (Fig. 3h; Supplementary Table 2). In Cruralispennia, the pygostyle is broad at its proximal end, its dorsoventral height decreasing sharply distally forming a blunt, dorsally upturned distal margin (Fig. 3a). The dorsal margin of the bone is concave, and the ventral margin is convex. All these features are characteristic of the plough-shaped pygostyle of ornithuromorphs in lateral view (Fig. 3d–f)18. Multiple lines of evidence suggest that the dorsal curvature of the pygostyle is not the result of deformation: first, the basal avian pygostyle is a fairly robust and stout element, unlikely to be deformed, and no similar deformation has been reported in the pygostyle of specimens of Protopteryx and Eopengornis from the same locality or any other Jehol enantiornithine; second, the dorsal and ventral margins of the pygostyle are smooth and unbroken (Fig. 3a); and third, slender elements such as the delicate fibula and the pubis, which are more vulnerable to postmortem crushing than the pygostyle, show no sign of deformation, further reinforcing our interpretation that the plough-shaped morphology of the pygostyle is a genuine feature of this new taxon. In contrast, in most enantiornithines this element is more rod-like in lateral view with nearly straight dorsal and ventral margins (Fig. 3b,c); the dorsoventral height remains even along the proximal half of the element, and gently decreases towards the distal end, marking the end of the ventrolateral processes. Sometimes this transition is abrupt forming a distinct distal constriction of the pygostyle19, which is notably absent in Cruralispennia. The distinct, dorsally upturned distal end of the pygostyle in Cruralispennia and many ornithuromorphs is absent in all other known enantiornithines.

Figure 3: Pygostyle of C. multidonta in comparison with other basal birds. (a–e) photographs and line drawings of the pygostyle in lateral view: (a) Cruralispennia; (b) enantiornithine Pterygornis; (c) enantiornithine Concornis; (d) ornithuromorph Yixianornis; (e) ornithuromorph Bellulornis; (f) ornithuromorph Piscivoravis; (g) basal pygostylian Confuciusornis. (h) Pygostyle length (y-axis) plotted against tarsometatarsal length (x axis) to compare the relative length of the pygostyle between groups of Mesozoic birds, showing that the highly abbreviated pygostyle of Cruralispennia is distinct from other enantiornithines but comparable to that of the Ornithuromorpha. (i) Results of discriminant analysis as histogram showing the Enantiornithes and basal ornithuromorphs plotted along the axis that maximizes their pygostyle differences; the obtained discriminant function suggest that the pygostyle of Cruralispennia falls within the morphospace of the Ornithuromorpha. Full size image

The strut-like coracoid is considerably more slender than in other Early Cretaceous enantiornithines and basal birds (Fig. 4). The ratio of the sternal margin width to the proximo-caudal length is ∼0.26, significantly smaller than in other Jehol enantiornithines, for example, Protopteryx (0.45), Eopengornis (0.59), Eoenantiornis (0.56) and Pterygornis (0.52), with the exception of Vescornis. Notably, comparably narrow coracoids are common in Late Cretaceous enantiornithines such as Enantiornis and Neuquenornis20. As in all other enantiornithines with the exception of Protopteryx, neither a procoracoid nor a lateral process is developed. The proximal one-third of the coracoid is rod-like, after which the element rapidly expands mediolaterally up to the midpoint of the shaft. Along the sternal half of the coracoid the corpus has a nearly even mediolateral width although the medial and lateral margins are weakly concave (Fig. 4a–c). In comparison, in other enantiornithines the sternal corpus is typically fan-shaped, increasing in width until the sternal margin (Fig. 4d–f)13,20. The impression left by the coracoid indicates that the sternal half of the coracoid was excavated by a dorsal fossa, a feature widely distributed among enantiornithines13,21. In Late Cretaceous taxa with comparably narrow coracoids the dorsal excavation is much deeper than in Early Cretaceous enantiornithines including Cruralispennia20. The scapular acromion process is straight and projects proximodorsally (Fig. 4b), as in other enantiornithines except pengornithids11,17. The midpoint of the cranial margin of the sternum bears a small cranially projecting process (Fig. 4b,c), a structure probably homologous to the rostral spine of living birds22, and also known in the Enantiornithes23, but not widely present (absent in Protopteryx, Eopengornis, the Longipterygidae and the Bohaiornithidae; Fig. 4d,e). The caudal margin of the sternum bears two pairs of subequal trabeculae (Fig. 4c). The lateral trabeculae are caudolaterally oriented. As in Protopteryx and pengornithids, these lateral trabeculae lack a distinct distal expansion like that present in most other taxa15,16. The intermediate trabeculae are slightly more delicate and extend to nearly the same level as the lateral trabeculae, a feature unknown in the Enantiornithes but characteristic of the Ornithuromorpha. The condition in Cruralispennia is most reminiscent of the morphology in basal-most ornithuromorph Archaeorhynchus in which the subequal processes are elongate and strap-like (short in more derived taxa)24. In other enantiornithines the intermediate trabeculae are short and triangular, except Protopteryx, in which these processes are only faintly visible4, and pengornithids, in which they are absent3. Distally, the xiphial region of the sternum is V-shaped, as in the basal enantiornithines Protopteryx and pengornithids (Fig. 4c–e). In contrast, it narrows, forming a distinct xiphoid process in other enantiornithines (Fig. 4f)15,17. The caudal margin of the xiphial region defines an angle of 34°, which is more acute than observed in Protopteryx (41°) and pengornithids (40°–75°). As in pengornithids3,17, the xiphial region and the lateral trabecula terminate at the same level, but the former extends farther caudally in Protopteryx (Fig. 4c–e).

Figure 4: Shoulder and forelimb of C. multidonta and some enantiornithines. (a) Photograph, (b) and line drawing of Cruralispennia, IVPP V21711; (c–f) reconstruction (not to scale) of the coracoids and sternum in Cruralispennia (c), Protopteryx (d), Eopengornis (e) and Parabohaiornis (f). ap, acromion process; dp, deltopectoral crest; lad, left alular digit; lam, left alular metacarpal; lco, left coracoid; lhu, left humerus; lmd, left major digit; lmm, left major metacarpal; lra, left radius; lt, lateral trabecula; lul, left ulna; mt, intermediate trabecula; op, olecranon process; rco, right coracoid; rhu, right humerus; rra, right radius; rs, rostral spine; rsc, right scapula; rul, right ulna; st, sternum; xp, xiphoid process. The white arrowhead in a indicates the circular fossa on the proximocranial surface of the humerus. The lateral margin of the distal half of the coracoid in Cruralispennia is weakly concave (red arrow in c), in contrast to the strong convex form in other enantiornithines (red arrows in d–f). The sternum of Cruralispennia bears a rostral spine, a structure not present in most enantiornithines (black arrowheads in d–f). Scale bar, 10 mm. Full size image

The forelimb is short relative to the hindlimb, with an intermembral index (humerus+ulna/femur+tibiotarsus) of 0.97. In contrast, the forelimb is longer in most other enantiornithines (for example, 1.10 in Protopteryx, 1.29 in Eopengornis, 1.42 in Pengornis, 1.15 in Parabohaiornis). The robust humerus is shorter than the ulna. The humeral head is concave cranially and its proximal margin is concave centrally, and a circular fossa is developed on the midline of the proximocranial surface (Fig. 4a), features characteristic of the Enantiornithes13. The small deltopectoral crest is narrow, less than half of the midshaft width, and extends only along the proximal quarter of the humerus. The ulna is robust, bowed proximally, and has a well-developed blunt olecranon process (Fig. 4a,b). As in more derived birds, the hand (carpometacarpus+major digit) is shorter than the humerus, whereas the hand is longer in contemporaneous basal enantiornithines Protopteryx and Eopengornis, and more basal birds (for example, Archaeopteryx, Sapeornis and Confuciusornis3,4,25,26). As in pengornithids and most other enantiornithines25, the alular digit is reduced so that its proximal phalanx ends proximal to the distal end of the major metacarpal (Fig. 4a,b), whereas the two elements terminate at the same level in Protopteryx4.

The pelvic bones (ilium, ischium and pubis) are poorly preserved. The postacetabular process of the ilium is short and strongly ventrally directed, distinguishable from other enantiornithines (see Supplementary Note 1 for detailed description; Supplementary Fig. 1). The tibiotarsus measures ∼116% of the femoral length. Like most other enantiornithines15, the proximal end of the fibula is triangular and the shaft rapidly tapers so that distally the bone is thin and delicate, terminating near the midpoint of the tibiotarsus (Fig. 1; Supplementary Fig. 2). In basal enantiornithines Protopteryx and the Pengornithidae, the fibula is unreduced and nearly reaches the lateral condyle of the tibiotarsus3,16. No free distal tarsals are recognized, and metatarsals II–IV appear to be fused only proximally (Supplementary Fig. 2). The tarsometatarsus is gracile and elongate, measuring 85% of the tibiotarsus (typically closer to half of the tibiotarsus length in most enantiornithines). Metatarsal III is clearly the longest. The trochlea of metatarsal I appears to have articulated above the level of the other metatarsal trochlea. The pedal digits are disarticulated. The non-ungual phalanges are gracile with deep collateral ligamental fovea. The claws are recurved with well-developed flexor processes and lateral surfaces deeply excavated by a deep neurovascular sulcus (Supplementary Fig. 2).

The entire skeleton is surrounded by the carbonized remains of feathers with the exception of the rostrum and feet (Fig. 1). The neck feathers are longer along the dorsal margin than the ventral margin. The body feathers appear to be hair-like and rachis-less, as in most other Jehol birds27,28. The partially folded left wing preserves several bilaterally asymmetrical remiges (Fig. 5a), although the overlap between feathers prevents an accurate assessment of their number. As preserved the feathers are shorter than in other enantiornithines, measuring only twice the length of the manus. The most striking integumentary feature is the crural feathers, best preserved on the right tibiotarsus (Fig. 5f,g). Feathers on the femur are obscured by overlap with feathers from other parts of the body. As in other enantiornithines, feathers are absent on the tarsometatarsus. An array of at least 14 feathers is preserved along the entire length of the right tibiotarsus. These feathers are heavily overlapped but two dissociated feathers clearly preserve the morphology of their proximal and distal ends (Fig. 5g). The two feathers measure 12.1 and 15.8 mm in length, with a subequal width of ∼0.25 mm. They are preserved curved and tapered at the proximal end. The feathers are narrow and wire-like almost the entire length, only distally fraying into individual hair-like barbs that account for <10% the length of the feather (Fig. 5h). The distal hair-like barbs run parallel to each other, similar to other rachis-less body feathers. Whereas in pennaceous feathers the barbs project off a central shaft, and the two vanes form a herringbone structure. Individual barbs cannot be identified in the proximally wire-like portion of any of the fourteen preserved crural feathers, suggesting that the proximal wire-like portion is likely the result of the fusion of individual barbs forming a rachis-like structure. The rachis differs from that in other fossil feathers27,28,29 in that the wire-like portion is proportionally longer than in the down-like body feathers and substantially narrower than in basal birds with an elongated rachis (for example, pennaceous feathers and other morphotypes; 0.37–0.67 mm in Archaeopteryx30, 1.06 mm in Confuciusornis31; 2.02 mm in Eopengornis). Furthermore, in some feathers from the Jehol biota and especially those from the same locality of Cruralispennia, the rachis appears dark in colour often bounded by light vanes laterally28. In the crural feathers preserved in Cruralispennia the rachises are preserved a uniform dark colour. This new feather morphology, proximally wire-like part with a short filamentous distal tip (PWFDTs), differs from all modern feathers and has not been previously observed in non-avian dinosaurs or basal birds (Fig. 5h–k)27,28,29,32. Approximately ten PWFDT-like feathers are preserved projecting from the cranial margin of the left wing (Fig. 5a), suggesting that this feather type is not restricted to the hindlimb. Although these feathers share some features with the proximally ribbon-like pennaceous tail feathers preserved in a juvenile oviraptorosaur Similicaudipteryx, individual barbs are readily identifiable along the distal third of the rectrices in the latter and they form pennaceous vanes29. Experimental studies have begun to uncover the molecular pathways responsible for the diversity of modern feather morphologies32,33. Bone morphogenetic protein 4 (BMP4) promotes barb fusion and rachis formation, whereas sonic hedgehog (Shh) induces apoptosis of the marginal plate epithelia to form individual barbs33. The wire-like portion in PWFDTs is likely the result of the overexpression of BMP4 and/or suppression of Shh, notably the same pathways regarded as being responsible for the formation of rachis-dominated rectrices28.

Figure 5: Plumage of C. multidonta and leg feather morphotype of basal birds (IVPP V21711). (a) Left wing of Cruralispennia with inset showing the distal ends of remiges under higher magnification; (b) SEM image of wing samples (location indicated by the circle in a) showing the melanosomes (white arrowhead); (c) tail feathers of Cruralispennia; (d) SEM image of tail feather samples (circle in c); (f) right tibiotarsus feathers with two disassociated feathers (g); (e) SEM image of crural feather sample (circle in f); (h–k) reconstructed the known leg feathers in basal birds: (h,i) proximally wire-like with filamentous distal tips (PWFDTs) crural feather of Cruralispennia; (j) model of a pennaceous leg feather; (k) modern of a down-like leg feather; (l) distribution of leg feather morphotypes among basal birds based on information from literature34 and the present study (note that feather size is exaggerated). (a,c,f) Scale bars, 10 mm, and (b,d,e) Scale bars, 2 μm. Full size image

Crural feathers are commonly present in both basal and modern birds. In Archaeopteryx, Sapeornis, Confuciusornis and some enantiornithines, the crural feathers are pennaceous with symmetrical vanes (Fig. 5l)15,30,34,35. In some enantiornithines and in Yanornis, the only Early Cretaceous ornithuromorph preserving leg feathers, the crural feathers are short and have a downy appearance similar to other body feathers (Fig. 5k)34, distinct from PWFDTs. In living birds with well-developed crural feathers, such as raptors, the feathers are pennaceous and may offer aerodynamic benefits as air brakes, allowing raptors to achieve a steeper descent when attacking prey36. In some other birds such as owls, the feathers have a downy morphology and even extend onto the pedal digits, serving as protection against prey and or thermal insulation37. In the absence of pennaceous vanes it is unlikely that the PWFDTs in Cruralispennia would have provided much aerodynamic utility. Unfortunately, it is notoriously difficult to ascertain feather function in fossil birds, and possible functions of PWFDTs in Cruralispennia include, but are not limited to, insulation, heat shielding, and social signalling. In fact, elongated feathers tend to be proximally narrow, which reduces drag, making it possible to be ornamental but designed to mitigate aerodynamic cost (possible function for PWFDT), similar to the ‘racket-plumes’ in the tails of some birds38.

Five feather samples, from the skull, right and left wings, tail, and tibiotarsus (Fig. 1), were analysed using scanning electron microscopy (SEM). These feather samples consist of densely packed aligned three-dimensional sub-micrometric bodies (Fig. 5b,d,e; Supplementary Fig. 3), which are interpreted as fossilized melanosomes in following with recent studies39,40. These microstructures are mostly identified as eumelanosomes based on their elongate, rod shape (0.91–2.61 μm long; 136–473 nm wide)39. The proportions of the eumelanosomes vary between sampled regions: the eumelanosomes of the tail are the largest (1.92–2.61 μm long; 380–512 nm wide; Fig. 5e); the eumelanosomes of the skull have the largest aspect ratio (long axis to short axis) averaging 7.14, followed closely by the eumelanosomes in the wings and tail (Supplementary Fig. 3); whereas the crural feathers show the smallest aspect ratio averaging 3.86 (Fig. 5e). Melanosome geometry and feather colour are highly correlated40,41, and thus the crural feathers most likely represent a different colour from other body parts. This may suggest that these unusual feathers were used in display.

The bone tissue of the humerus was sampled to investigate the age of IVPP V21711 and form of growth that characterizes Cruralispennia. The transverse section of the humerus is avascular, mainly composed of a thick layer of parallel-fibered bone tissue bounded internally by an inner circumferential layer (ICL)42 and externally by an outer circumferential layer (OCL)42 (Fig. 6; Supplementary Fig. 4). The medullary cavity is lined by the ICL, which consists of avascular lamellar bone tissue of endosteal origin. The ICL is thin, about one-sixth of the total width of the cortex. A few flattened osteocyte lacunae can be observed. In the middle parallel-fibered layer, the osteocyte lacunae become progressively flatter and more highly parallel organized towards the periosteum. The OCL consists of lamellar bone with a small number of flattened osteocyte lacunae. Growth marks such as lines of arrested growth (LAGs) or annuli are absent. The presence of an ICL and OCL together is widely regarded to indicate that active bone deposition has ceased42,43, suggesting that growth was complete or nearly complete in IVPP V21711 at the time of its death. Previously osteohistological studies indicate that enantiornithines took several years to reach adult size after which they continued to grow very slowly, evident from the preservation of LAGs in the thick middle layer of more rapidly formed bone and closely spaced rest lines in the slowly formed OCL42,44. The absence of rest lines in the OCL suggests that IVPP V21711 was a subadult at the time of death. The absence of LAGs in the middle layer suggests that unlike other enantiornithines but similar to Confuciusornis and derived ornithuromorphs45,46, Cruralispennia reached near adult size within a year. This suggests that derived growth strategies evolved very early in the Enantiornithes, although the persistence of slower growing lineages even into the Late Cretaceous, reveals that the Enantiornithes were diverse in their developmental strategies42,44. However, compared with other fast-growing avian lineages (woven or fibrolamellar bone tissue), the bone tissue in Cruralispennia is parallel-fibered and avascular, indicating that the bone tissue still formed more slowly than in Confuciusornis or ornithuromorphs45,46.