Discovery of a rare arboreal forest-dwelling flying reptile (Pterosauria, Pterodactyloidea) from China

Background

Discussion

This recently discovered pterosaur species can be referred to the Pterodactyloidea based on several features such as the confluent naris and antorbital fenestra, a long wing metacarpal, a reduced tail, and the pedal digit V lacking elongated phalanges and reduced to a tiny metatarsal (length 0.8 mm) (9, 10). To establish the phylogenetic position of Nemicolopterus crypticus, we performed a cladistic analysis using the dataset published by Wang et al. [ref. 4; see supporting information (SI) Appendix]. The result was rather surprising, because the most extraordinary aspect of this species is the absence of the synapomorphic features of the main pterodactyloid clades. Regarding the Archaeopterodactyloidea (Fig. 4), Nemicolopterus crypticus lacks the rounded posterior region of the skull and the elongated midcervical vertebrae that diagnose this group. It has the posterior part of the skull elongated but lacks any crest such as the laterally compressed parietal crest present in Feilongus and the Gallodactylidae (4, 9). Nemicolopterus crypticus shows a nasal process, but this structure differs from the archaeopterodactyloid condition by being placed medially but not laterally. The nasal process of Nemicolopterus seems to be unique by being much shorter than the medial nasal process as reported in Anhanguera (1, 11) and Sinopterus dongi (12) and longer than the knob-like structure present in Thalassodromeus sethi (13) and Pteranodon (14). Last, Nemicolopterus crypticus is toothless, and all members of the Archaeopterodactyloidea bear teeth.

The toothless condition is widespread among the Dsungaripteroidea. Nemicolopterus crypticus also shares with dsungaripteroids the presence of a dorsal pneumatic foramen on the proximal articulation of the humerus (Fig. 2).

The cladistically more basal dsungaripteroid pterosaur group is the Nyctosauridae, characterized by having a long wing metacarpal more than double the length of the humerus (15). Although the wing metacarpals are not completely preserved in Nemicolopterus crypticus, the length ratios between the humerus and the second and third wing phalanges differ remarkably from that of Nyctosaurus, which has longer phalanges, and allows us to confidently infer that the Chinese taxon lacks the extremely elongated wing metacarpal condition. Nemicolopterus crypticus also does not show the particularly hatched-shaped deltopectoral crest of the humerus that is displaced further down the shaft as observed in nyctosaurids. Some authors further argued that Nyctosaurus has only three wing phalanges (15). If correct, this feature would be another difference from the plesiomorphic condition (e.g., four wing phalanges) as observed in Nemicolopterus.

Nemicolopterus is more closely related to the Ornithocheiroidea (a clade that groups all more derived pterodactyloids) relative to the Nyctosauridae by possessing the articulation between the skull and mandible positioned under the anterior half of the orbit, which in other pterosaurs is displaced further backwards. Nemicolopterus, however, lacks several ornithocheiroid features such as a parietal crest and a pneumatic foramen on the lateral side of the cervical vertebral centrum. Moreover, the Chinese taxon lacks the diagnostic features of the Pteranodontoidea, such as the warped deltopectoral crest and the scapula shorter than the coracoid (9).

Nemicolopterus crypticus also does not display the diagnostic features of the Dsungaripteridae such as the small rounded orbit that is positioned very high in the skull, the presence of a suborbital opening, the posteroventral expansion of the maxilla and the characteristic dentition of Dsungaripterus and “Phobetor” (1, 16). It also cannot be regarded as a member of the Azhdarchidae, which show extremely elongated midcervicals with reduced neural spines (17, 18) and a deep coracoidal flange (19). It shares with the Tapejaridae the presence of a thin and apparently subvertical lacrimal process but lacks the large premaxillary sagittal crest, the large nasoantorbital fenestra, the distinct pear-shaped orbit, and the broad tubercle at the ventroposterior margin of the coracoid (20).

Nemicolopterus crypticus shows some particular morphological features not reported in pterosaurs before. Among those is the presence of a well developed posterior process on the femur, situated above the articulation with the tibia (Fig. 3c). This process has a triangular shape and likely supported tendons or muscles that connected the femur and tibia (possibly reaching the foot), strengthening the movement of the lower part of the leg (and foot). The penultimate phalanges of the foot are curved ventrally to a degree not reported in any other pterosaur, particularly on the first and fourth digits. This species also shows that the penultimate phalanx of the fourth digit is longer than the first, a feature previously unknown in the Pterodactyloidea and only reported in the anurognathids Jeholopterus (21) and Anurognathus (22). The unguals are laterally compressed and dorsoventrally expanded with the flexor tubercle deeper and larger than in some primitive pterosaurs such as Rhamphorhynchus (22), archaeopterodactyloids [e.g., Pterodactylus (1, 23)] and in the more derived Anhanguera (11) and Pteranodon (14). Despite not having a reversed hallux like birds or the odd, hallux-like pedal digit present in drepanosaurids [Triassic diapsid reptiles (24)], the odd curved condition of the penultimate phalanges, which are the largest in the foot, is strongly indicative of arboreal habits of Nemicolopterus crypticus. This interpretation is corroborated with studies of phalanges of extinct sloth lemurs that concluded that arboreal species have more strongly curved phalanges than their terrestrial relatives (25). Furthermore, having the penultimate pedal phalanges longer than their neighboring proximal phalanges is a feature typically associated with arboreal capacity in birds (e.g., ref. 26) and also strengthens the present arboreal hypothesis for this flying reptile. Although other pterosaurs, particularly the more primitive anurognathids (e.g., Jeholopterus), were also regarded as having an arboreal lifestyle, Nemicolopterus is the pterodactyloid pterosaur to present the best adaptation for developing this lifestyle.

The wing span of the holotype and only known specimen of Nemicolopterus crypticus is estimated to be ≈250 mm, making it one of the smallest flying reptiles recovered so far. This small size raises the question about its ontogenetic age. Although the growth pattern of this previously undescribed species is not known, there are some comparisons that can be made with other pterosaurs known by more complete ontogenetic series, mainly the archaeopterodactyloid species from the Solnhofen Limestone, Southern Germany. This deposit has yielded the smallest flying pterosaurs recorded in the literature so far and are considered juveniles of the genus Pterodactylus (and related taxa). The smallest specimen has a wingspan of only 180 mm and is regarded as a hatchling that was a few weeks old when it died (1). The skeleton of that specimen is very delicate with several parts not ossified, such as the sternum and some pedal phalanges. Other juvenile specimens of Pterodactylus were also found in the Solnhofen Limestone and differ from more mature individuals by the lack of ossification in some parts of the skeleton, particularly the pedal phalanges and the tarsal elements (9). This lack of ossification was also observed in one juvenile specimen tentatively referred to as Germanodactylus cristatus (27) and seems to have been widespread in at least the Solnhofen pterodactyloid fauna. Although showing signs of immaturity with several cranial and postcranial elements unfused, which are indicative of juvenile pterosaurs (11, 28), Nemicolopterus crypticus has all skeletal elements well ossified, including the pedal phalanges, the tarsal elements, and the epiphyses of long bones (e.g., humerus). Furthermore, the gastralia and the sternum, which tend to be fragile and badly preserved in juveniles, are well ossified in this specimen (Figs. 2 and 3). Therefore, it can be concluded that the sole specimen of this small pterosaur represents a young individual, but not a hatchling that had just left the egg. How much it might have grown is not clear, but in any case, it is the smallest pterosaur specimen recovered from the Liaoning deposits (and Asia) so far, even smaller than the embryo of a toothed pterodactyloid recently found in the Yixian Formation, whose wing span was estimated to be 270 mm (29).

Nemicolopterus crypticus presents the best adaptations for an arboreal lifestyle found in any pterosaur, particularly in the Pterodactyloidea. It is very likely that this pterosaur represents a lineage of arboreal creatures that lived and foraged for insects in the gymnosperm forest canopy of Northeast China during the Early Cretaceous.

Another interesting aspect of this animal is its phylogenetic position. Nemicolopterus crypticus is undoubtedly a basal dsungaripteroid and in the sister-group relationship with the Ornithocheiroidea. The latter includes the most derived pterosaurs (9), some reaching gigantic sizes with wingspans of >6 m [e.g., Pteranodon (1)] and also Quetzalcoatlus (30), which has a wingspan of ≈10 m and is regarded as the largest flying animal of all time. The phylogenetic position of Nemicolopterus crypticus suggests that the Ornithocheiroidea originated from crestless and toothless small insectivorous arboreal forms. Although not conclusive, the fact that this primitive dsungaripteroid is found in Asia suggests that this continent could have played a major role in the evolution of the derived pterosaurs constituting the Ornithocheiroidea.

Last, because of its arboreal lifestyle, Nemicolopterus crypticus can be considered a rarity among pterosaurs, and its preservation further demonstrates the uniqueness of the fossil lagerstätten that constitute the Jehol Biota.

Supplementary Material