Phylogenetic distribution of fprim length in Mesozoic birds
Our analyses demonstrate that the mean fprim/ta ratio increases among successive lineages of Mesozoic birds towards the crown of the tree and Neornithes (Fig. 3). This suggests the presence of a general phylogenetic trend in primary feather length throughout avian evolution. However, the range of fprim/ta lengths in enantiornithines and Neornithes is broad (Data S1 in the Supporting Information) (i.e. 0.32–1.16 in enantiornithines and 0.43–1.19 in Neornithes). This increasing range of fprim/ta ratios is likely linked to the enormous enantiornithine and neornithine radiations and subsequent expansion into a wide range of ecological niches (Nudds et al., 2004a; Dyke & Nudds, 2009). The low fprim/ta ratio in Archaeopteryx, (Fig. 3) is quite similar to that of nonavian theropods, indicating that the possession of relatively shorter fprim (compared to the rest of the arm) is the primitive condition for Aves. The fprim component of total wing length in Confuciusornithidae is the largest among the clades (Fig. 3), augmenting the list of unique characteristics (synapomorphies) known for this lineage and further suggesting a unique flight style (see below).
The wing and flight of Confuciusornis
The Early Cretaceous Chinese fossil bird Confuciusornis is known from thousands of specimens, yet its biology, including mode-of-flight, is contentious (Hou et al., 1995; Chiappe et al., 1999, 2008, 2009; Peters & Peters, 2009, 2010). One biomechanical analysis of the strength of their narrow primary feather rachises (Nudds & Dyke, 2010) and recent anatomical studies indicating restricted upstroke capabilities (Senter, 2006; Zhou & Zhang, 2007) suggest that Confuciusornis was not capable of vigorous flapping flight. Larger birds have both longer wings and shorter primaries relative to their body masses than smaller birds (Nudds, 2007; Nudds et al., 2011). Larger birds also have lower wing-beat frequencies than smaller birds (Nudds et al., 2004b) and tend to have flight styles involving soaring and gliding as opposed to the vigorous flapping of smaller birds (Nudds, 2007). Confuciusornis has relatively long primaries (a high fprim/ta ratio) and therefore, based on the extant bird fprim data, was a fast flapping flyer. However, very elongate, thin and narrow wings (Martin & Zhou, 1998; Chiappe et al., 1999; Peters & Ji, 1999; Zinoviev, 2009), narrow primary rachises (Nudds & Dyke, 2010) and anatomy indicating no flapping upstroke capability suggest that Confuciusornis was almost certainly a glider. This paradox of conflicting signals in the flight morphology of Confuciusornis, combined with its unique anatomical characters (e.g. pneumatic foramen and large deltopectoral crest of the humerus) (Hou et al., 1995; Chiappe et al., 1999), seen variously in the other members of Confuciusornithidae (Eoconfuciusornis, Changchengornis), perhaps hints at unusual flight behaviour not seen in extant birds.
Wing shape and wing kinematics of early birds
The relative lengths of individual primary feathers play a key role in forming bird wing shape (Dawson, 2005). Within the wing itself, differences in the ratios of underlying fprim (relative to the length of the total arm) are likely to relate to flight style. As a general rule, larger living birds that soar tend to have longer, pointed wings with relatively shorter primaries, whereas smaller birds that perform fast flapping favour short, rounded wings and have relatively longer primary feathers (Rayner, 1988; Pennycuick, 1989; Nudds & Bryant, 2000; Nudds, 2007).
Because relative lengths of feathers contribute to these differences in wing proportion (Nudds, 2007), one could argue that the primaries of Archaeopteryx are consistent with a wing more suited to soaring than to fast flapping. The wing kinematics of Archaeopteryx are still disputed (Yalden, 1970; Feduccia & Tordoff, 1979; Ruben,1991; Burgers & Chiappe,1999; Nudds & Dyke, 2010): slower flapping has been the consensus view for some time, as this basal bird likely lacked aspects of its bony skeleton (sternum) for the attachment of some flight muscles (Elzanowski, 2002; Wellnhofer, 2008). However, a recent study of likely lift force generating capabilities (Nudds & Dyke, 2010) showed that the primary feather rachises in Archaeopteryx were probably not strong enough for flapping flight. Although arguments exist concerning whether Archaeopteryx is a flapper or not, clearly, the flight ability of this fossil bird was very poor, consistent with the lack of flight muscles (Speakman, 1993; Elzanowski, 2002; Wellnhofer, 2008), the absence of a dorsal glenoid surface (Senter, 2006) and the weakness of its primary feather shafts (Nudds & Dyke, 2010). This general conclusion is further reinforced by the relatively short primary feathers we report here.
The morphology of fossils, including the presence of aerodynamic control features such as an alula and wing-tip feather separation, suggests that some enantiornithine birds possessed more sophisticated flight abilities than Archaeopteryx (Sanz et al., 1996; Garner et al., 1999; Zhang & Zhou, 2000; O’Connor et al., 2009), although still limited when compared to the diversity seen in modern birds (Sanz & Ortega, 2002; Zhou & Zhang, 2007). Surveys of forelimb proportions have also shown that these birds fall within the range of extant taxa and thus likely possessed at least some of the flight styles of their living counterparts (Dyke & Nudds, 2009). Among enantiornithines, specimens with high fprim/ta ratios (> 0.8) account for 30% of the total sample with ratios in Longipteryx chaoyangensis and Dalingheornis liweii larger than one. This may suggest that various wing shapes, likely dominated by short and rounded types, existed within enantiornithines although their relatively shorter average fprim length could be used to imply a more limited flapping ability compared with Neornithes.
In summary, there appears to be an evolutionary trend towards relatively longer primaries (mean fprim/ta ratio) in successive lineages of Mesozoic avians. The notable exception is the Confuciusornithidae, which have exceptionally long primary feathers for their wing lengths. Confuciusornis has the primary fprim/ta ratio of modern fast flapping birds, but paradoxically the primary feather strength (Nudds & Dyke, 2010) and other morphological features (Martin & Zhou, 1998; Chiappe et al., 1999; Peters & Ji, 1999; Senter, 2006; Zhou & Zhang, 2007; Zinoviev, 2009) of a glider. The exact flight style of Confuciusornis remains an enigma, but it appears unlikely that it was a vigorous flapping flyer. Although fprim/ta is a useful character for identifying flight abilities, clearly in some cases, information from other traits is also required. Finally, the range of fprim/ta in enantiornithines and neornithines is broad a likely consequence of their rapid radiations into a broad range of ecological niches.