A new Lower Cretaceous bird from China and tooth reduction in early avian evolution

Zhonghe Zhou, Fucheng Zhang Zhiheng Li

Abstract

A new avian genus and species, Zhongjianornis yangi gen. et sp. nov., is reported from the Lower Cretaceous lacustrine deposits of the Jiufotang Formation in Liaoning, northeast China. The new taxon is characterized by possessing the following combination of features: upper and lower jaws toothless, snout pointed, humerus with large and robust deltopectoral crest, second phalanx of the major manual digit longer than the first phalanx, unguals of the alular and major digits of similar length and significantly shorter than the corresponding penultimate phalanges, tibiotarsus slender and more than twice the length of the tarsometatarsus, and metatarsal IV longer than the other metatarsals. Phylogenetic analysis indicates that Zhongjianornis is phylogenetically basal to Confuciusornis and the dominant Mesozoic avian groups, Enantiornithes and Ornithurae, and therefore provides significant new information regarding the diversification of birds in the Early Cretaceous. It also represents the most basal bird that completely lacks teeth, suggesting that tooth loss was more common than expected in early avian evolution and that the avian beak appeared independently in several avian lineages, most probably as a response to selective pressure for weight reduction. Finally, the presence of a significantly enlarged humeral deltopectoral crest suggests that Zhongjianornis shares with other basal birds such as Jeholornis, Sapeornis and Confuciusornis a distinctive mode of adaptation for flight contrasting with that seen in more advanced birds, which instead possess an elongated sternum and a prominent keel.

1. Introduction

Over 30 genera of Early Cretaceous birds have been reported in the last two decades from the Lower Cretaceous of northeastern China (Chiappe 2007, Gao et al. 2008, Zhou et al. 2008, O'Connor et al. 2009), documenting a burst of avian diversification that followed the appearance of the earliest bird Archaeopteryx. These early birds occur in association with hundreds of exceptionally preserved feathered dinosaurs, early mammals, pterosaurs, amphibians, flowered plants and insects, which constitute the famous Jehol Biota (Benton et al. 2008; Zhang et al. 2008).

Recently, a relatively large bird was recovered from the Jiufotang Formation in Jianchang, western Liaoning. The new material is represented by a nearly complete and articulated skeleton. The new bird displays a combination of features that are unknown in any previously reported taxon; in particular, it represents the most basal avian that had completely lost teeth. The robust boomerang-shaped furcula and the large deltopectoral crest of the humerus are strongly reminiscent of Confuciusornis. The new discovery adds to our understanding of avian biodiversity in the Early Cretaceous.

2. Systematic paleontology

Aves Linnaeus, 1758.

Zhongjianornis yangi gen. et sp. nov.

(See figures 15).

Figure 1.

Holotype of Zhongjianornis yangi gen. et sp. nov. (IVPP V15900). Scale bar, 5 cm.

(a) Holotype: A nearly complete articulated skeleton with some poorly preserved feather imprints (Institute of Vertebrate Paleontology and Paleoanthropology collection, IVPP V15900).

(b) Etytomology: The genus and species names both honour the late Professor Zhongjian Yang (Chung-Chien Young), father of Chinese vertebrate paleontology and founder of the Institute of Vertebrate Paleontology and Paleoanthropology.

(c) Locality and horizon: Jianchang, Liaoning, northeastern China; Early Cretaceous Jiufotang Formation (He et al. 2004).

(d) Diagnosis: A pigeon-sized bird (table 1), distinguished from other early birds by possessing the following combination of features: toothless, snout pointed, humerus with a large and robust deltopectoral crest that is as wide as the humeral shaft and more than one-third the total length of the humerus, wing unguals small and slightly curved, metatarsal IV longer than II and III.

View this table:
Table 1.

Measurements of Zhongjianornis yangi gen. et sp. nov. (IVPP V15900).

3. Description

The holotype of Zhongjianornis yangi gen. et sp. nov. is a nearly complete articulated skeleton of an adult individual (figures 1 and 2). The skull is characterized by a pointed snout and toothless upper and lower jaws. The maxillary and nasal processes of the premaxilla form an angle of less than 30°. The two nasal bones are long and strap-like and seem to be slightly constricted in the middle part and to flare towards the posterior end. The frontal is large and domed. The posterior end of the maxillary process of the left premaxilla contacts the maxilla, which is massively built and shorter than the premaxilla. The maxilla articulates posteriorly with the long, rod-shaped jugal.

Figure 2.

Line drawing of the holotype of Zhongjianornis yangi gen. et sp. nov. (IVPP V15900). Abbreviations: ca, caudal vertebra; ce, cervical vertebra; co, coracoid; dI-1, first phalanx of alular digit; dII-1, first phalanx of major digit; dII-2, second phalanx of major digit; fe, femur; fi, fibula; fu, furcula; hu, humerus; il, ilium; is, ischium; mcI, alular metacarpal, mcII, major metacarpal; mcIII, minor metacarpal; mtI, metatarsal I; pd, pedal digits; pu, pubis; r, radius; sc, scapula; st, sternum; sy, synsacrum; ti, tibia; tmt, tarsometatarsus; tv, thoracic vertebra; u, ulna; up, uncinate process of rib. Scale bar, 5 cm.

A single occipital condyle is evident. Two flanges extend laterally from the posterior end of the basipterygoid process. A broad bone lying near the basipterygoid process is tentatively identified as a pterygoid, and a pair of slender bones between the nasal and maxilla is tentatively identified as the palatines.

The right mandible is well exposed in medial view. The dentary is strongly forked, with a long, straight ventral process and a short dorsal process that is slightly curved and nearly half the total length of the mandible. The angular appears massive, while the surangular is more slender. A triangular bone that tapers both anteriorly and posteriorly is recognized as the splenial, and a pair of slender rod-like bones is identified as hyoid elements (figure 3).

Figure 3.

(a) Skull of the holotype of Zhongjianornis yangi gen. et sp. nov. (IVPP V15900). (b) Line drawing of the holotype skull of Zhongjianornis yangi gen. et sp. nov. (IVPP V15900). Abbreviations: an, angular; ar, articular; bs, basisphenoid; de, dentary; fr, frontal; ju, jugal; ma, maxilla; na, nasal; pa, parietal; ?pal, ?palatine; pm, premaxila; ?pt, ?pterygoid; sa, surangular; sp, splenial bone. Scale bar, 1 cm.

The cervical vertebrae are ventrally exposed. The posterior cervicals seem to be more elongated than the anterior ones. Because of crushing, it is difficult to determine the type of central articulation. The thoracic vertebrae are incompletely preserved, and their number is difficult to determine. One of the thoracics, located near the synsacrum, can be seen to have an opisthocoelous centrum. The lateral surface of each thoracic centrum appears to be excavated.

The thoracic ribs appear to be slender. At least three of them display tightly associated uncinate process, which are expanded proximally but taper distally (figure 4a). No gastralia have been recognized, but it is unclear whether they are genuinely absent or simply not preserved.

Figure 4.

Close-up photos of Zhongjianornis yangi gen. et sp. nov. (IVPP V15900), showing (a) the thoracic ribs and uncinate processes, (b) the pectoral girdle, and (c) the hand. Abbreviations: dI-2, second phalanx of the alular digit; dII-3, third phalanx of the major digit; dIII-1, first phalanx of the minor digit; ul, ulnare; see figure 2 for other abbreviations. Scale bar, 1 cm.

The synsacrum is completely fused and exposed in the ventral view (figure 5a). However, its posterior end is obscured by the pelvis, and the transverse process of the last sacral is partly exposed through the acetabular opening. The number of sacral vertebrae is estimated to be no greater than eight.

Figure 5.

Close-up photos of Zhongjianornis yangi gen. et sp. nov. (IVPP V15900), showing (a) the pelvis and (b) the right foot. Abbreviations: mtII, metatarsal II; mtIII, metatarsal III; mtIV, metatarsal IV; pdI, pedal I; pdII, pedal II; pdIV, pedal IV; see figure 2 for other abbreviations. Scale bar, 1 cm.

The caudal series is incompletely preserved, although five caudal vertebrae are preserved in articulation posterior to the pelvis. A short rod-like chevron is associated with the most cranial of these vertebrae. The caudals are short and small, with short, flat transverse processes and apparently procoelous intercentral articulations. Near the right femur are a few more isolated caudals. One of them appears to be larger than the others and might possibly represent the pygostyle. Based on the morphology of the preserved caudals, it is probable that Zhongjianornis has only a short caudal series, although the presence of a pygostyle is questionable (figure 5a).

The left scapula is well preserved and articulates with the coracoid at an acute angle, while the left scapula and coracoid are more or less covered by the furcula and right coracoid (figure 4b). The elongate scapula is nearly as long as the humerus, with a curved and distally tapering shaft. The coracoid is also elongated and is a strut-like bone bearing a blunt acromion process. In contrast to ornithurine birds and at least one enantiornithine, Protopteryx (Zhang & Zhou 2000), the coracoid appears to lack a distinct procoracoid process. The sternal margin of the coracoid appears concave, with a maximum width less than half the length of the coracoid. The proximal part of the bone seems to bear a narrow supracoracoidal foramen.

The furcula is incompletely preserved and appears to lack a hypocleidum. Based on the available material, it can be reconstructed as having a robust boomerang-like shape, resembling the furculae of Archaeopteryx (Elzanowski 2002; Mayr et al. 2005), confuciusornithids (Hou et al. 1995; Chiappe et al. 1999) and other very basal birds. The furcula lacks grooves on its dorsal surface.

A thin bone between the right humerus and radius can be identified as an incompletely preserved sternum (one of the paired sternal plates), lying in proximity to the distal ends of some thoracic ribs. Although the outline of the whole sternum cannot be precisely reconstructed, this bone seems to be relatively short and more or less rounded, in contrast to elongated sterna of ornithurines. The sternum of Zhongjianornis also seems to lack a distinctly developed keel.

The forelimbs are exposed in dorsal view, and preserved in nearly complete articulation. The length ratio of the humerus + ulna + major metacarpal to the femur + tibiotarsus + metatarsal III is about 1.2, which is most similar to that of Jeholornis among known Mesozoic avians (Zhou & Zhang 2002). The humerus is robust, with a large deltopectoral crest that extends more than one-third the total length of the humerus. The deltopectoral crest is nearly as wide as the humeral shaft, with a rounded anterioproximal margin and a straight distal margin. The deltopectoral crest lacks a fenestra, in contrast to Sapeornis (Zhou & Zhang 2003) and confuciusornithids. The humeri of Zhongjianornis are straight and less twisted than in many more advanced birds. Proximally, the bicipital crest is prominent. The head of the humerus is not well exposed in either the right or the left forelimb, but seems not to be dorsally prominent. Distally, the humerus is slightly flared.

The ulna and radius are slightly longer than the humerus. The ulna is bow-shaped and is wider and more strongly curved than the radius. Distally the ulna seems to possess a semilunar external condyle. The right ulnare is preserved in association with the ulna and shows a distinctive metacarpal incision.

The carpometacarpus is only fused at the proximal end, where a prominent carpal trochlea is present. The alular metacarpal is not fused with the major metacarpal and is a slender bone lacking an extensor process. The minor metacarpal is only about half as wide as the major metacarpal. It is only slightly curved near its distal end and does not fuse distally with the major metacarpal although the two bones are closely appressed. The major and minor metacarpals extend distally to about the same level, in contrast to enantiornithines, in which the minor metacarpal extends further distally.

The phalangeal formula of the manus is unclear. The alular digit is slender and does not extend to the distal end of the major metacarpal, and the first phalanx is much longer than the second (the ungual). The major digit comprises three phalanges. The first phalanx is the most robust of all the manual phalanges, whereas the second phalanx is shorter and more slender than the first phalanx and the third phalanx (the ungual) is shorter still. The minor digit is not preserved on the right wing, and only the first phalanx seems to be preserved on the left. Thus, the phalangeal count of the minor digit is unclear. The unguals of the alular and major digits are only slightly curved and are about equal in length, both of them being significantly shorter than the non-ungual phalanges of the manus (figure 4c).

The right pelvis is exposed in the lateral view (figure 5a). Both ilia are preserved, with the right ilium overlapping much of the left. The ilium is mainly dorsoventrally extended, and its pre-acetabular portion is greater than its slightly tapering post-acetabular portion. The ischium is robust and curved posterodorsally, with a prominent ascending process that contacts the posterior end of the ilium. The posteriorly directed right pubis is preserved in articulation with the ilium. The rod-shaped shaft of the pubis is nearly straight along much of its proximal portion. The distal tip of the pubis is missing, but part of the pubic symphysis is preserved, although its length cannot be reconstructed. The proximal ischium and pubis are preserved in articulation with the ilium, forming a rounded acetabular foramen. No anti-trochanter is evident.

The hind-limb elements are preserved in almost complete articulation. The femur is robust and nearly straight. It lacks a distinct neck but has a prominent ball-shaped head, which lacks a capital fossa. The femur is about two-thirds the length of the tibiotarsus and is much longer than the tarsometatarsus.

The tibiotarsus is long and slender, with the proximal and distal ends more or less crushed. Proximally, the tibiotarsus does not appear to form a cnemial crest. Distally, the tibiotarsus is well fused, but both the internal and external condyles are somewhat crushed and their shapes cannot be readily determined. The needle-shaped fibula is not fused with the tibiotarsus and extends along about three-quarters of the length of the latter bone. The right tibiotarsus appears shorter than the left, but we suspect that this is an artificial condition resulting from faulty reconstruction of the specimen by the local farmer before the specimen was obtained by us. Part of the middle segment was probably missing, as can be judged from a crack at the middle tibiotarsus.

The tarsometatarsus is relatively short, measuring only about 0.39 times the length of the tibiotarsus, which distinguishes it from any other known early birds (table 2). The right tarsometatarsus is completely preserved, but the left one is missing its distal end. The tarsometatarsus appears to be well fused at its proximal end. Based on the admittedly imperfect distal portion of the right tarsometatarsus, metatarsal IV appears to be longer than II and III (figure 5b), in contrast to most other early birds. However, we are less certain about the relative widths of the three major metatarsals. Metatarsal I is short, with an expanded distal end and a pointed proximal end. It appears to articulate with a facet on metatarsal II. Metatarsal V is absent. The pedal digits are nearly completely preserved, although they are greatly compressed. Digit I is moderately long, with the ungual exceeding the first phalanx in length. Digit II has a short first phalanx and a relatively long second phalanx, which, however, is shorter than the ungual. Digit III is slightly wider than the other digits. The non-ungual phalanges of digit IV are subequal in length and relatively short compared with those of the other digits. All of the pedal unguals are long and curved.

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Table 2.

Measurements (mm) and proportions of selected limb elements of Zhongjianornis yangi (IVPP V15900) and some other early birds from China. l. and r. indicate left and right sides, respectively. Abbreviations are as in figures 2 and 5.

4. Comparison and discussion

The new specimen represents a bird that is relatively large compared with other known birds from the Lower Cretaceous (table 1). It can be most readily distinguished from other taxa by the following features: skull with a pointed snout and toothless jaws, and robust humerus with a distinctively enlarged deltopectoral crest. Among Early Cretaceous birds of comparable or greater size, both Jeholornis and Sapeornis have a greater forelimb to hind-limb length ratio (Zhou & Zhang 2003). Jeholornis also has a unique skull adapted for seed-eating, with robust jaws bearing reduced teeth (Zhou & Zhang 2002). The skull of Sapeornis is adapted for herbivory, but still retains large teeth on the premaxilla, and the humerus of this taxon differs from that of Zhongjianornis in displaying a distinct fenestra on the deltopectoral crest. Furthermore, the femur and metatarsal III of Zhongjianornis are both significantly shorter in comparison to the tibiotarsus than those in Sapeornis.

The confuciusornithids are a group of birds from northeast China that are similar in size to Zhongjianornis, and they also resemble this taxon in having completely toothless jaws (Zhang et al. 2008). However, Zhongjianornis can be easily distinguished from confuciusornithids by its pointed snout and by the small size of the ungual of the alular manual digit (Hou et al. 1995; Chiappe et al. 1999). Furthermore, Zhongjianornis has a greater forelimb to hind-limb ratio than is seen in confuciusornithids (table 2).

Finally, the basal ornithurines Hongshanornis (Zhou & Zhang 2005) and Archaeorhynchus (Zhou & Zhang 2006) are two additional Chinese early birds that completely lack teeth. However, both are smaller than Zhongjianornis. Hongshanornis has far more slender limb bones, lacks an extremely large deltopectoral crest and displays a much smaller forelimb to hind-limb ratio. Archaeorhynchus, by contrast, is readily distinguishable from Zhongjianornis by its greater forelimb to hind-limb ratio. More advanced ornithurines such as Yixianornis and Yanornis (Zhou & Zhang 2001; Clarke et al. 2006) are toothed. All known enantiornithines from the Early Cretaceous of China have retained at least some teeth in the skull (Zhang & Zhou 2000; Zhou et al. 2005) and are often much smaller than Zhongjianornis. This is true even of the largest enantiornithine, Pengornis (Zhou et al. 2008), which also has greater forelimb to hind-limb and femur to tibiotarsus ratios than Zhongjianornis (table 2).

Phylogenetic analysis indicates that Zhongjianornis represents one of the most basal known birds. This taxon is more derived than Archaeopteryx, Sapeornis and Jeholornis, but is more basal than other known taxa including Confuciusornis and the two dominant Mesozoic avian groups, the enantiornithines and ornithurines (figure 6). The new discovery adds to the known diversity of Lower Cretaceous avian assemblages. Furthermore, it is notable that the most basal currently known avian taxa are all relatively large in comparison with the more derived enantiornithines, confirming that the evolution of improved powered flight was coupled with a size decrease on the lineage leading to enantiornithines. The new cladogram is generally consistent with a recent analysis by Zhou et al. (2008), except that Sapeornis occupies a more basal position than Jeholornis in the current analysis. This result is surprising, as it contrasts with all previous analyses. The new topology readily explains the presence of a primitive non-strut-like coracoid in Sapeornis, but would also suggest that the long skeletal tail in Jeholornis could have evolved secondarily.

Figure 6.

Phylogeny of Zhongjianornis yangi gen. et sp. nov. Phylogenetic analysis was conducted using NONA 2.0 and WinClada. All characters were unordered. A total of 205 morphological characters were used, following Zhou et al. (2008). The data matrix from Zhou et al. (2008) was used in a revised form. Tree length = 487; CI = 0.55; RI = 0.77. The cladogram is based on the strict consensus of four most parsimonious trees.

Among previously reported beaked birds from the Mesozoic of China, confuciusornithids represent the most basal forms to display this advanced feature. Jeholornis and Sapeornis have greatly reduced their teeth, but in neither of these taxa are teeth completely lacking (Zhou et al. 2005; Zhou & Zhang 2007). All known Chinese enantiornithines are also toothed, although some of them, including Longipteryx (Zhang et al. 2001), Longirostravis (Hou et al. 2004) and Shanweiniao (O'Connor et al. 2009), have their teeth restricted to the premaxilla and anterior dentary. Among known basal ornithurines, both Hongshanornis and Archaeorhynchus are completely toothless. An analysis of 31 avian genera from the Lower Cretaceous of China shows that seven of them are edentulous (table 3), and most are either completely toothed (i.e. teeth present in premaxilla, maxilla and dentary) or partially toothed (i.e. teeth absent on either one or two of the same three bones). The avian assemblage from the Lower Cretaceous of China documents a transition from completely toothed birds in the Late Jurassic to completely toothless ones in the Cenozoic.

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Table 3.

List of 31 known avian genera from the Lower Cretaceous of China.

The new bird also represents the most basal form to completely lose its teeth, although tooth loss undoubtedly occurred independently in several early avian lineages. Among known toothless birds, Confuciusornis is the next most advanced. We assume that tooth loss in both cases was probably owing to selective pressure for a reduction in body weight, and it would be especially advantageous to reduce the weight of the head rather than, for instance, the trunk, because the former is further from the centre of gravity. Many ornithurines that retained teeth, such as Yanornis and Yixianornis, also appear to have been strong flyers, and the selection pressure for weight reduction was probably less severe in these taxa.

The great variations in jaw and rostral morphology that existed among early birds may also suggest that significant trophic differentiation played a key role in the explosive radiation of birds approximately 20 million years after Archaeopteryx (Chiappe & Walker 2002; Chiappe 2007; Zhou & Zhang 2007).

Zhongjianornis appears to retain a boomerang-shaped furcula like those of more basal avians and non-avian theropods. Unlike Archaeopteryx, Jeholornis and Sapeornis, it possesses well-developed uncinate processes, as in Confuciusornis and more derived taxa.

The humerus has a robust deltopectoral crest, much as in confuciusornithids, but lacks a fenestra of the kind seen in Sapeornis and most confuciusornithids. Zhang et al. (2008) showed that a remarkably enlarged humeral deltopectoral crest represents an adaptation for increasing flight capability between 131 and 120 Ma for confuciusornithids. It is notable that both Jeholornis and Sapeornis have a large deltopectoral crest, a condition unknown in enantiornithine and ornithurine birds (Zhou & Zhang 2001; Clarke & Norell 2002; Clarke et al. 2006). Besides, none of these most basal birds possesses an elongated sternum or a prominent sternal keel. The presence of a large deltopectoral crest in these basal birds probably compensated to some extent for the lack of an elongate, keeled sternum.

The proportions of the hind-limb and pes, as well as the shapes of the pedal unguals, seem to indicate an arboreal habit for Zhongjianornis. For instance, metatarsal III is only about 0.39 times as long as the tibiotarsus, a smaller ratio than in other known Early Cretaceous birds. The ratio of the length of the femur to that of the tibiotarsus is 0.68, also a smaller value than is typical of Early Cretaceous birds. The pedal unguals are all long and curved, and significantly longer than other phalanges. The hand of Zhongjianornis still retains some primitive features, such as the presence of a long major digit in which the second phalanx is longer than the first. However, it is also notable that the wing unguals seem to be relatively reduced and less curved than in more basal birds such as Jeholornis, Sapeornis and Confuciusornis, possibly indicating that they have lost their former presumed role in climbing.

Acknowledgements

We are grateful to Corwin Sullivan for reading the manuscript and providing many suggestions. We also thank Xiaolin Wang for help in the field, Yan Li for fossil preparation and Wei Gao for photos. This research was funded by the Major Basic Research Projects (2006CB806400) of MST of China and the National Natural Science Foundation of China (40121202).

Footnotes

  • One contribution to a Special Issue ‘Recent advances in Chinese palaeontology’.

    • Received May 23, 2009.
    • Accepted June 19, 2009.

References

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