Introduction

Jeholornis is a recently reported basal bird, which appears to be less advanced than any other known bird except for Archaeopteryx. Its stomach was found to contain over 50 seeds of unknown plants, representing the first direct evidence for seed-eating adaptation in the Mesozoic (Zhou and Zhang 2002a).

One of the most remarkable features of Jeholornis is its unreduced long skeletal tail. Except for Archaeopteryx and Jeholornis, the only other bird known to have a long skeletal tail is Rahonavis from the Late Cretaceous of Madagascar (Forster et al. 1998); however, this was not completely preserved, and hence the exact number of its caudal vertebrae remains unknown. The holotype of Jeholornis preserved 22 caudal vertebrae; however, the fact that there are only two short caudal vertebrae before the 20 elongated caudal vertebrae raises suspicions that the tail was probably not completely preserved. The two new specimens of Jeholornis described here have preserved a nearly completely articulated tail comprising more caudal vertebrae than that of the holotype.

Both new specimens are from the Jiufotang Formation in Chaoyang, western Liaoning, northeast China (Fig. 1A,B), where the holotype of Jeholornis and the associated feathered dromaeosaurs (Norell et al. 2002; Xu et al. 2003) and birds such as Sapeornis (Zhou and Zhang 2002b), Longipteryx (Zhang et al. 2001) and Yanornis (Zhou and Zhang 2001) have all been discovered. They are housed in the Institute of Vertebrate Paleontology and Paleoanthropology (IVPP) in Beijing. One is a nearly completely articulated individual (IVPP V13553) and the second lacks the forelimb and pectoral girdle (IVPP V13550). Both specimens are significantly smaller than the holotype and, since many juvenile features can be observed (such as the less well-defined extremities of long limb bones, the unfused vertebrae, relatively large skull), they probably represent two juvenile individuals. In other major features and proportions they are consistent with the description of Jeholornis prima, and thus they are classified to the same taxon.

Fig. 1A–C.
figure 1

Two new specimens of Jeholornis prima. A an incomplete skeleton (IVPP V13350); B a nearly complete skeleton (IVPP V13353); C fan-shaped distal tail feather (IVPP V13350)

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These new materials also provide much new information about other aspects of this basal bird, such as the scapula, coracoid, thoracic vertebrae, synsacrum, pneumaticity of the postcranial bones, complete pedal digits and impression of feathers (see Fig. 1).

The exact age of the bird-bearing Jiufotang Formation is unknown; however, it is generally believed to be Aptian (Wang and Zhou 2002), which is slightly younger than the Santana Formation of Brazil (Albian).

Comparison between Jeholornis and Archaeopteryx

In the skull, the most distinctive difference between Jeholornis and Archaeopteryx is the reduction of the teeth (see Electronic Supplementary Material). In Archaeopteryx, teeth are present in the premaxilla, maxilla and dentary (Martin 1991; Wellnhofer 1992). However, there are only three very small teeth present in the lower jaw of the holotype (IVPP V13274). In the IVPP V13350 specimen, two small teeth are present in the lower jaw, but none are present in the premaxilla or maxilla, as is also the case in the IVPP V13553 specimen. Both the upper and lower jaws of Jeholornis are shorter, deeper and more robust than in Archaeopteryx, indicating its specialized seed-eating adaptation (Zhou and Zhang 2002a). Both birds share a large triangle-shaped antorbital fenestra. The lachrymal of Jeholornis has two fenestrae that are absent in Archaeopteryx.

The neck of Jeholornis is as short as in Archaeopteryx and is probably composed of fewer than 10 cervical vertebrae. In both birds the cervical ribs are present. The number of the thoracic vertebrae is 14, similar to that of Archaeopteryx (Martin 1991). Pneumatic foramina are observed in a number of thoracic vertebrae of Jeholornis (Fig. 2A). Pneumaticity has also been reported in cervical and thoracic vertebrae of Archaeopteryx (Britt et al. 1998).

Fig. 2A–H.
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Jeholornis prima. A Thoracic vertebrae in lateral view (IVPP V13353); B synsacrum in dorsal view (IVPP V13353); C proximal caudal vertebrae in lateral view (IVPP V13350); D scapula in dorsal view (IVPP V13553); E reconstruction of synsacrum in dorsal view (IVPP V13353); F reconstruction of scapula in lateral view (IVPP V13553); G reconstruction of coracoid in dorsal view (holotype, IVPP V13274); H reconstruction of sternum in dorsal view (holotype, IVPP V13274). Abbreviations: ac acromion, ch chevron, co coracoid, c1–c6 the first through sixth caudal vertebrae (the transition point is between the fifth and sixth), fu furcula, gl glenoid, hu humerus, il ilium, is ischium, pf pneumatic foramen, sc scapula, s1–s6 first through sixth sacral vertebrae, tp transverse process. Scale bars in parts E–H are 1 cm long

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IVPP V13553 preserved a complete synsacrum (Fig. 2B, E). It is composed of six fused sacrals in contrast to Archaeopteryx, which has five unfused sacrals (Martin 1991). The synsacrum is composed of seven sacral vertebrae in Sapeornis, Confuciusornis and Protopteryx (Zhang and Zhou 2000), eight in Cathayornis (Zhou 1995) and nine in Yanornis (Zhou and Zhang 2001).

The number of caudal vertebrae in Archaeopteryx has generally been believed to be between 21 and 23 (Wellnhofer 1992) although a smaller number has been proposed for the Solnhofen specimen (Elzanowski 2001). The holotype of Jeholornis has been reported with 22 caudal vertebrae, which lies in the same range of caudal vertebrae as Archaeopteryx. Surprisingly, the two new specimens have preserved a skeletal tail comprising more caudal vertebrae than that of Archaeopteryx. In the IVPP V13353 specimen, there are 20 elongated caudal vertebrae and four anterior short caudal vertebrae; combined to make a total of 24 caudal vertebrae (Fig. 1B). In the IVPP V13350 specimen, 22 elongated caudal vertebrae are preserved and there are five short caudal vertebrae preserved in articulation (Fig. 2C); the total number of the caudal vertebrae is therefore 27 (Fig. 1A), more than in any known Archaeopteryx specimen. The number of elongated caudal vertebrae after the transition point is between 20 and 22 in Jeholornis but is less than 20 in Archaeopteryx.

The tail of Jeholornis not only has more caudal vertebrae than that of Archaeopteryx, it is also relatively much longer than in Archaeopteryx. The tail is shorter than both the forelimb and hindlimb in Archaeopteryx; however, in Jeholornis the tail is about 125% and 158% of the length of the forelimb and hindlimb, respectively (Table 1).

Table 1. Comparison between Jeholornis and Archaeopteryx in ratios of some major skeletal element lengths
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The other major difference between Jeholornis and Archaeopteryx in the caudal series is that the chevrons of Jeholornis are much more elongated, and are connected along most of the caudal series, resulting in a more solid tail (Zhou and Zhang 2002a). In this aspect, it bears more resemblance to the dromaeosaurs (Norell and Makovicky 1999; Xu et al. 2000) than to any other bird.

Archaeopteryx has a short sternum, which lacks a lateral trabecula. Re-examination of the sternum of Jeholornis shows sutures between the two sternal plates, similar to some dromaeosaurs and probably Archaeopteryx too (P.A. Wellnhofer, personal communication). The sternum of Jeholornis also represents the most basal bird with a lateral trabecula (Fig. 2H) and, further, the lateral trabecula possesses a rounded fenestra (Zhou and Zhang 2002a).

The pelvis of Jeholornis is generally similar to that of Archaeopteryx in the degree of the posterior inclination of the pubis. However, the ischium of Jeholornis has a better-developed proximal dorsal process than in Archaeopteryx and, in this respect, it is more similar to enantiornithines and some other basal birds such as Sapeornis and Confuciusornis (Martin et al. 1998).

Compared with Archaeopteryx, Jeholornis shows many derived features related to flight adaptation. As in Confuciusornis (Chiappe et al. 1999), the scapula of Jeholornis has a dorso-laterally facing glenoid facet (Fig. 2D, F); in Archaeopteryx, the glenoid facet is laterally faced. The coracoid is strut-like in Jeholornis, while it is short and non-strut-like in Archaeopteryx and Sapeornis (Zhou and Zhang 2002b). The new materials indicate that Jeholornis also has a supracoracoid foramen (Fig. 2G), as does Archaeopteryx. The carpometacarpus is well fused proximally in Jeholornis, but is less well fused in Archaeopteryx. The third metacarpal of Jeholornis is strongly bow-shaped, providing a strong support for the attachment of the primary feathers.

In Archaeopteryx the forelimb is about the same length as the hindlimb; however, in Jeholornis the forelimb is about 126% that of the hindlimb (Table 1); the manus in Jeholornis is also relatively much shorter and robust than in Archaeopteryx (see Electronic Supplementary Material).

The two new specimens of Jeholornis preserved completely articulated pes. Although the hallux is reversed and the claws are large and curved, indicative of arboreal capability, the toe proportions are not characteristic of more advanced perching birds with distinctively longer penultimate phalanges ( Zhou and Farlow 2001). It is notable that the first digit is short compared with Archaeopteryx with a relatively small claw. A free tarsal in IVPP V13553 is probably a juvenile feature.

Feather impressions are not preserved in the holotype of Jeholornis, but are found in both the IVPP V13550 and IVPP V13553 specimens. In the IVPP V13550 specimen, the tail feathers are relatively well preserved (Fig. 1C). It is notable how the long tail feathers are attached to the distal caudal vertebrae in a way very similar to that of non-avian theropods Caudipteryx (Ji et al. 1998) and Microraptor (Xu et al. 2003), i.e., they form a more or less fan-shaped rectrice at the distal end of the tail. It is probably noteworthy that both Caudipteryx and Microraptor have been suggested to be flightless birds by some researchers (Feduccia 1999; L.D. Martin, personal communication). In the IVPP V13553 specimen, wing feathers are relatively well preserved (Fig. 1B). The exact number of the primary and secondary feathers is difficult to estimate, but the wing feathers are asymmetric and long.

Discussion

Jeholornis is undoubtedly one of the most important discoveries of early birds after Archaeopteryx, as it is only the second known bird with a complete long tail (which also bears much resemblance to dromaeosaurs, demonstrating a close relationship between birds and dromaeosaurs regardless of whether dromaeosaurs are dinosaurs or secondarily flightless birds).

The number of sacral vertebrae of Jeholornis (6) is larger than that in Archaeopteryx (5), but fewer than in other known birds, and may represent a link between the most primitive bird and those more advanced forms such as Sapeornis, Confuciusornis and Protopteryx, which have seven sacrals.

Jeholornis has more caudal vertebrae (maximum of 27) than Archaeopteryx (maximum of 23) and this may imply that the common ancestor of birds had at least 27 caudal vertebrae. The tail of Jeholornis is also much longer than that of Archaeopteryx (Table 1). It has been proposed that Archaeopteryx probably represents a side-branch in early avian evolution (Martin 1983; Hou et al. 1996; Feduccia 1999). The discovery in Jeholornis of a much longer tail comprising more caudal vertebrae than in Archaeopteryx appears to lend further credence to this hypothesis.

Despite of the primitive appearance of Jeholornis, shared with Archaeopteryx in the caudal half of the body (i.e., the pelvis, the hindlimb and the caudal vertebrae), it shows a surprisingly advanced cranial half of the body, which is more derived than in Archaeopteryx, thus confirming a mosaic pattern of morphological evolution common in early birds. These advanced character states include: a scapula with a dorso-laterally exposed glenoid facet, a strut-like coracoid, a sternum with a lateral trabecula with a fenestra; a wing having a well fused carpometacarpus, bowed metacarpal III and a shortened and more robust digit II, which is more suitable for attachment of the primary feathers.

Pneumaticity has been recognized in the skull, cervical and thoracic vertebrae and pelvis of Archaeopteryx (Britt et al. 1998; Christiansen and Bonde 2000). Jeholornis has not only preserved pneumaticity in various thoracic vertebrae but also in the sternum. The sternum, together with the furcula, is part of a respiratory cycling mechanism between the lungs and the air sacs (Jenkins et al. 1988). The pneumatic sternum may indicate the presence of the interclavicular sac in Jeholornis.

Sternal fenestrae are present in all known ornithurine birds such as Yanornis and Yixianornis (Zhou and Zhang 2001) and most modern birds, but it has not been reported in any dinosaur or enantiornithine bird, although the sternum of enantiornithine Concornis is perforated by several foramina (Sanz et al. 1995). The development of the interclavicular sac in Jeholornis is related either to its powerful flying ability or its large size, as large flying birds generally have well-developed pneumatic bones, while small fliers have only a few or none (Welty 1982).