A new confuciusornithid bird with a secondary epiphyseal ossification reveals phylogenetic changes in confuciusornithid flight mode

Abstract

The confuciusornithids are the earliest known beaked birds, and constitute the only species-rich clade of Early Cretaceous pygostylian birds that existed prior to the cladogenesis of Ornithothoraces. Here, we report a new confuciusornithid species from the Lower Cretaceous of western Liaoning, northeastern China. Compared to other confuciusornithids, this new species and the recently reported Yangavis confucii both show evidence of stronger flight capability, although the wings of the two taxa differ from one another in many respects. Our aerodynamic analyses under phylogeny indicate that varying modes of flight adaptation emerged across the diversity of confuciusornithids, and to a lesser degree over the course of their ontogeny, and specifically suggest that both a trend towards improved flight capability and a change in flight strategy occurred in confuciusornithid evolution. The new confuciusornithid differs most saliently from other Mesozoic birds in having an extra cushion-like bone in the first digit of the wing, a highly unusual feature that may have helped to meet the functional demands of flight at a stage when skeletal growth was still incomplete. The new find strikingly exemplifies the morphological, developmental and functional diversity of the first beaked birds.

Fig. 1. Confuciusornis shifan holotype (PMoL-AB00178).

a Photograph. b Schematic line drawing. cav caudal vertebra, cev cervical vertebra, fu furcula, ga gastralia, lc left coracoid, ldIII left manual digit III, lfe left femur, lh left humerus, lil left ilium, lis left ischium, lm left manus, lp left pes, lra left radiale, lr left radius, ls left scapula, lt left tibiotarsus, lu left ulna, lul left ulnare, ma mandible, pu pubis, py pygostyle, r rib, rc right coracoid, rdcIII claw of right manual digit III, rfe right femur, rfi right fibula, rh right humerus, ris right ischium, rm right manus, rp right pes, rra right radiale, rr right radius, rs right scapula, rt right tibiotarsus, ru right ulna, rul right ulnare, sk skull, sy synsacrum, tv thoracic vertebra. Arrow indicates the position from which the histological section of the right femur was taken. Scale bars: 2 cm.

Fig. 2. Osteohistological section of Confuciusornis shifan holotype (PMoL-AB00178).

Sample was taken from the midshaft of the right femur. ICL inner circumferential layer, OCL outer circumferential layer. Arrows indicate LAGs. Scale bar: 100 μm.

Fig. 3. Skull and mandible of Confuciusornis shifan holotype (PMoL-AB00178).

a Photograph. b Schematic line drawing. c close-up of the anterior margin of the orbit. an angular, ar articular, cmf caudal mandibular fenestra, d dentary, dp dorsal process of maxilla, f frontal, j jugal, l lacrimal, m maxilla, n nasal, o orbit, p parietal, pm premaxilla, q quadrate, rmf rostral mandibular fenestra, sa surangular, sp splenial. White rectangle in a indicates the region shown in c. A line drawing of the posterior half of the mandible of Confuciusornis sanctus IVPP V 13171 (drafted based on Fig. 1b in Wang et al.) is presented below the line drawing of the skull and mandible of Confuciusornis shifan; arrow indicates the ventral process of the surangular. Scale bars: 1 cm; note that c is not to scale.

Fig. 4. Selected axial elements of Confuciusornis shifan holotype (PMoL-AB00178).

a cervical vertebrae. b synsacrum. c pygostyle. sy synsacrum. Arrows in b and c indicate the longitudinal ridge on the ventral surface of the synsacrum and the positions of foramina along the pygostyle, respectively. Also see Supplementary Fig. 1 for a close-up of the distal part of the pygostyle. Scale bars: 0.5 cm in a, c; 1 cm in b.

Fig. 5. Pectoral and pelvic girdles of Confuciusornis shifan holotype (PMoL-AB00178).

a Pectoral girdle. b pelvic girdle. fu furcula, lc left coracoid, lil left ilium, lis left ischium, ls left scapula, pu pubis, rc right coracoid, rh right humerus, ris right ischium, rs right scapula. Scale bars: 1 cm.

Fig. 6. Relative proportions of the pectoral girdle and limb elements of the Confuciusornis shifan holotype (PMoL-AB00178) and other confuciusornithids.

Different gray shades indicate relative lengths of stylopodial, zeugopodial and metapodial limb segments from top to bottom, respectively. Values near the segments represent ratios of segment length to femoral length. All drawings scaled to a common, arbitrary femoral length.

Fig. 7. Selected limb elements of Confuciusornis shifan holotype (PMoL-AB00178).

a left carpometacarpus. b right carpometacarpus. c left alular metacarpal of the confuciusornithid specimen PMoL-AB00150. d right tarsometatarsus. Carpometacarpi are in palmar view, and tarsometatarsus is in cranial view. cb cushion-like bone, ep extensor process, pp pisiform process. Roman numerals in (d) identify metatarsals. Black arrow in (c) indicates the cranial distal condyle of the alular metacarpal; black and white arrows in (d) indicate the ridge-like process on metatarsal IV and the dorsal tubercle on metatarsal III, respectively. Scale bars: 0.25 cm.

Fig. 8. Cladogram of Mesozoic birds showing the systematic position of Confuciusornis shifan.

The strict consensus of the 192 most parsimonious trees recovered in the phylogenetic analysis performed in this study (length = 1404; consistency index = 0.277; retention index = 0.667). Bootstrap and Bremer values over the minimum threshold are given in normal font and bold italic font, respectively, near the nodes to which they pertain.

Fig. 9. Positions of estimated confuciusornithid specimens in a morphospace defined by wing loading (WL) and aspect ratio (AR) of extant birds with particular modes of flight.

Colored lines mark the areas of morphospace occupied by extant birds with particular modes of flight. The image of the morphospace was previously published by Serrano et al., and is used here with permission. Black circles indicate specimens which are holotypes of their respective species, unless only a specimen number is indicated. The specimens are numbered in descending order of estimated body mass.