SEARCH

SEARCH BY CITATION

Keywords:

  • avian;
  • Confuciusornis;
  • evolution;
  • primary feather;
  • wing shape

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

We examine the relationships between primary feather length (fprim) and total arm length (ta) (sum of humerus, ulna and manus lengths) in Mesozoic fossil birds to address one aspect of avian wing shape evolution. Analyses show that there are significant differences in the composition of the wing between the known lineages of basal birds and that mean fprim (relative to ta length) is significantly shorter in Archaeopteryx and enantiornithines than it is in Confuciusornithidae and in living birds. Based on outgroup comparisons with nonavian theropods that preserve forelimb primary feathers, we show that the possession of a relatively shorter fprim (relative to ta length) must be the primitive condition for Aves. There is also a clear phylogenetic trend in relative primary feather length throughout bird evolution: our analyses demonstrate that the fprim/ta ratio increases among successive lineages of Mesozoic birds towards the crown of the tree (‘modern birds’; Neornithes). Variance in this ratio also coincides with the enormous evolutionary radiation at the base of Neornithes. Because the fprim/ta ratio is linked to flight mode and performance in living birds, further comparisons of wing proportions among Mesozoic avians will prove informative and certainly imply that the aerial locomotion of the Early Cretaceous Confuciusornis was very different to other extinct and living birds.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

Other than bats and the extinct pterosaurs, birds are the only vertebrates to have evolved flapping flight. However, unlike bats and pterosaurs that both have a flexible flight membrane attached to elongate fingers, the wing surface in birds is made up of feathers, themselves firmly embedded in the bony wing skeleton. As a result, functional wing length is made up of forelimb bones (humerus, ulna/radius and manus) and the primary feathers (fprim) (Fig. 1). Although the phylogenetic distribution and functional morphology of components of the avian bony wing skeleton have been described (Gatesy & Middleton, 1997, 2007; Nudds et al., 2004a, 2007), the contribution of feather length to wing length in living birds has been largely ignored until recently (Nudds, 2007; Nudds et al., 2011). This is partly because fprim length data are not commonly collected: measurements of whole folded wings are often recorded by bird banders and ringers, whereas museum skins are almost always prepared with their wings folded flush against the body.

image

Figure 1.  Measurements used in this study (adapted from Nudds, 2007). Dashed line represents the midline of the bird’s body; on the left is Confuciusornis, the extremely abundant Early Cretaceous fossil bird, whereas on the right is a modern bird (to show overall differences in relative proportions). Abbreviations: bsemi, semispan; l, winglength; hum, humerus length; ul, ulna length; mn, manus length (carpometacarpus + first and second phalanx length in modern birds; carpometacarpus + longest digit precluding claws in fossil birds); and fprim, primary feather length (the end of distal digit to feather tip).

Download figure to PowerPoint

Under sampling of fprim length in extant taxa is unfortunate because ever increasing numbers of well-preserved fossil birds with complete feathering are now known from the Mesozoic (e.g. Elzanowski, 2002; Chiappe, 2007), especially from the Cretaceous of China (e.g. Zhou et al., 2005; Zhang et al., 2006; O’Connor et al., 2009). A growing number of nonavian theropod dinosaurs, close to the divergence of Archaeopteryx, are also now known to have had primary feathers on their forelimbs that may imply an aerial locomotion function (e.g. Xu et al., 2003; Hu et al., 2009; Xu & Guo, 2009), but not necessarily powered flight (Nudds & Dyke, 2010).

Thus, we now have the opportunity to assess the relative contribution of fprim to total arm length (ta) across the phylogenetic spectrum of avian evolution. Understanding changes in this proportion is important because the length of fprim relative to the whole wing is related to both flight mode and performance in extant birds. Nudds (2007) and Nudds et al. (2011) demonstrated that total wing length (l) and body mass also closely correlate to one another, scaling with an exponent close to 1/3. Within extant birds, tal1.08, indicating that fprim increases concomitant with a reduction in the contribution of the bony elements to overall wing length (Nudds, 2007). Thus, smaller birds, with faster wing-beat frequencies, tend to have longer primaries, whereas larger birds (often soarers) tend to have relatively shorter primaries (Nudds, 2007). These trends may also apply to the extensive fossil record of birds. Assessing wing shape in birds is an evolutionary question that has occupied biologists for hundreds of years (see review in Rayner, 1988): to understand the evolution of avian flight, we must also understand the development of wing proportions.

Here, we describe some basic changes in the relative proportions of the avian wing, with emphasis on fprim, from nonavian theropods through to modern birds (Neornithes). We draw on a data set of wing bone and feather measurements taken from fossils and focus on variation in the wing proportions of the especially well-known Early Cretaceous Confuciusornis (Confuciusornithidae) represented by hundreds of specimens that often include complete wings, to determine how fprim (relative to total arm length) has changed from basal birds to Neornithes.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

Measurements of wing bones and primary feathers were collected for a sample of Mesozoic birds, mostly in Chinese museums but some from primary literature, using digital calipers (rounded to the nearest mm) (n = 93; Data S1 in the Supporting Information). Measurements of living birds (50 species) were taken from Nudds et al. (2004a). We added selected measurements from the few nonavian theropod dinosaurs that are known to have had feathered forelimbs (i.e. Microraptor, Caudipteryx), although these encompass at least two diverse maniraptoran clades (n = 6). Measurements for the major forelimb bones as well as the length of the longest visible fprim were also taken, to sum to the total wing length (Fig. 1).

Analyses were conducted at the level of individual specimens binned into lineages defined by recent phylogenetic analyses (Fig. 2); because almost all taxa of Mesozoic birds are known from single specimens (> 95%; Dyke & Nudds, 2009; O’Connor & Dyke, 2010), or remain unassigned, treating specimens as species is a reasonable assumption for this analysis. We are aware that using specimens as single data points may artificially inflate sample size, but this is negligible because of the high proportion of single-specimen-taxa in our data set (see Data S1 in the Supporting Information). Lastly, we compared the fossil data to a larger set of living bird wing bone and fprim measurements (Nudds et al., 2011).

image

Figure 2.  Simplified consensus phylogenetic topology to show the relative positions of the six lineages we discuss. The nonavian theropods Caudipteryx and Microraptor were included in our analysis, as they preserve functional forelimb primary feathers.

Download figure to PowerPoint

Because we were concerned with describing patterns of variation in wing proportions among the known lineages of Mesozoic birds (Fig. 2; Data S1 in the Supporting Information), and thus tracking changes in the relative proportions of the components of wing length over time, an anova based on absolute deviations from the median was used (Bell, 1989; Sokal & Rohlf, 1995). As group variances are not statistically equal, a Welch and Brown–Forsythe test was also employed, and a Hochberg multiple test was used for post hoc multiple comparisons. All tests were conducted with spss software (spss v. 18.0.1, Chicago, IL, USA). The bulk of our fossil bird sample, chosen to capture complete wings with preserved fprim, lacks precise taxonomic assignment. Hence, a comparative analysis using independent contrasts was not conducted, because unresolved polytomies collapse to a single contrast value (Pagel, 1992). This means the data set here would provide insufficient data points to perform a meaningful comparative analysis controlling for phylogenetic effects using independent contrasts.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

Results of the one-way anova (F5,143 = 8.509, P < 0.001) and the Welch (F5,8.496 = 15.401, P <0.001) and Brown–Forsythe test (F5,49.453 = 12.059, P < 0.001) show that there are significant differences in mean wing proportions between the sampled lineages of basal birds (Fig. 3). Indeed, multiple comparisons show that the fprim lengths (relative to ta length) in Archaeopteryx and enantiornithines are shorter than they are in all other birds (Table 1). In other words, for a given ta length, members of these Mesozoic lineages had relatively shorter fprim comprising part of their wing lengths in comparison to their fossil and extant counterparts (Fig. 3). In contrast, fprim lengths in Confuciusornis are significantly longer than are those of any other Mesozoic fossil bird (F1,27 = 8.706, P < 0.01; F1,81 = 7.567, P < 0.01), although falling within the range of modern birds (Neornithes) (Nudds et al., 2011).

image

Figure 3.  Mean ratios between fprim length and ta length in six lineages of nonavian theropods and Mesozoic birds (Fig. 2). One-way anovas (F5,143 = 8.509, P < 0.001) and the Welch (F5,8.496 = 15.401, P < 0.001) and Brown–Forsythe test (F5,49.453 = 12.059, P < 0.001) show that mean ratios are significantly different between avian lineages. Mean ratios and 90% confidence intervals are: Caud (Caudipteryx): = 0.4900 (0.3994, 1.3794); Micro (Microraptor): = 0.5850 (0.4104, 0.7596); Arch (Archaeopteryx): = 0.5371 (0.4621, 0.6122); Conf (Confuciusornithidae): = 0.9233 (0.7874, 1.0592); Enant (enantiornithines): = 0.7415 (0.6935, 0.7894); and Ornith (Ornithurines): = 0.8891 (0.8344, 0.9438).

Download figure to PowerPoint

Table 1.   Results of Hochberg multiple comparisons.
I groupsJ groupsMean difference (I−J)SEP95% CI
  1. Bold indicates significance at P < 0.05.

ConfuciusornithidaeArchaeopteryx0.386190.090160.0010.1180–0.6544
Enantiornithines0.181860.052270.010.0264–0.3373
OrnithuromorphaArchaeopteryx0.351930.082990.0010.1050–0.5988
Enantiornithines0.147600.038600.0030.0328–0.2624

Based on outgroup comparisons with nonavian theropods known to have primary feathers, and so likely capable of aerial locomotion (at least gliding or parachuting) to some extent (i.e. Microraptor) (Nudds & Dyke, 2009, 2010), it is clear that the possession of relatively shorter fprim (compared to the rest of the arm) is the primitive condition for Aves (Fig. 2). These relatively shorter primaries are retained in Archaeopteryx, but following the divergence of Confuciusornis and its kin (Confuciusornithidae) in the Early Cretaceous, much longer feathers compared to the bones of the arms (up to 50% of total wing length) had evolved (Table 1 of Kaiser, 2007). Our survey shows that enantiornithines had relatively short fprim lengths, not significantly different to those of the basal-most bird Archaeopteryx (Table 1) and that these proportions are retained by basal ornithuromorphs such as Hongshanornis, Gansus, Yixianornis and Jianchangornis (Fig. 2). The relatively more elongate primaries that characterize Neornithes evolved later within this clade (Fig. 2).

A Lillilifors test showed that our fprim data for Confuciusornis are normally distributed (h = 0, P = 0.3405, kstat = 0.1397, critval = 0.1877). Thus, there is no evidence for size dimorphism within our data as has been suggested by previous authors based on bone proportions alone (Chiappe et al., 2008, 2010). Earlier workers have suggested that the skeletal proportions and the presence of tail feathers in this highly abundant Chinese bird are consistent with sexual size dimorphism within the known specimen sample (Peters & Peters, 2009, 2010).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

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.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

We thank Xiaoting Zheng and Zhonghe Zhou for collections access in China and Gary Kaiser, Colin Palmer, Al McGowan, Jingmai O’Connor, Allen Moore and three anonymous referees for helpful comments. X.W. is supported by a CSC Government Scholarship (to UCD).

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information
  • Bell, G. 1989. A comparative method. Am. Nat. 133: 553571.
  • Burgers, P. & Chiappe, L.M. 1999. The wing of Archaeopteryx as a primary thrust generator. Nature 399: 6062.
  • Chiappe, L.M. 2007. Glorified Dinosaurs. Wiley, New York.
  • Chiappe, L.M., Ji, S., Ji, Q. & Norell, M.A. 1999. Anatomy and systematics of the Confuciusornithidae (Aves) from the late Mesozoic of northeastern China. Bull. Am. Mus. Nat. Hist. 242: 189.
  • Chiappe, L.M., Marugán-Lobón, J., Ji, S. & Zhou, Z. 2008. Life history of a basal bird: morphometrics of the Early Cretaceous Confuciusornis. Biol. Lett. 4: 719723.
  • Chiappe, L.M., Marugán-Lobón, J. & Chinsamy, A. 2010. Comment on Peters & Peters Palaeobiology of the Cretaceous bird. Biol. Lett. 6: 529530.
  • Dawson, A. 2005. The scaling of primary flight feather length and mass in relation to wing shape, function and habitat. Ibis 147: 283292.
  • Dyke, G.J. & Nudds, R.L. 2009. The fossil record and limb disparity of enantiornithines, the dominant flying birds of the Cretaceous. Lethaia 42: 248254.
  • Elzanowski, A. 2002. Archaeopterygidae (Upper Jurassic of Germany). In: Mesozoic Birds: Above the Heads of Dinosaurs (L.M.Chiappe & L.M.Witmer, eds), pp. 129159. University of California Press, Berkeley.
  • Feduccia, A. & Tordoff, H.B. 1979. Feathers of Archaeopteryx: asymmetric vanes indicate aerodynamic function. Science 203: 10211022.
  • Garner, J.P., Taylor, G.K. & Thomas, A.L.R. 1999. On the origins of birds: the sequence of character acquisition in the evolution of avian flight. Proc. R. Soc. Lond. B 266: 12591266.
  • Gatesy, S.M. & Middleton, K.M. 1997. Bipedalism, flight, and the evolution of theropod locomotor diversity. J. Vert. Paleontol. 17: 308329.
  • Gatesy, S.M. & Middleton, K.M. 2007. Skeletal adaptations for flight. In: Fins into Limbs: Evolution, Development, and Transformation (B.K.Hall, ed.), pp. 269283. The University of Chicago Press, Chicago.
  • Hou, L.-H., Zhou, Z.-H., Gu, Y.-C. & Zhang, H. 1995. Confuciusornis sanctus, a new Late Jurassic sauriurine bird from China. China. Sci. Bull. 40: 15451551.
  • Hu, D.-Y., Hou, L.-H., Zhang, L.-J. & Xu, X. 2009. A pre-Archaeopteryx troodontid from China with long feathers on metatarsus. Nature 461: 640643.
  • Kaiser, G.W. 2007. The Inner Bird: Anatomy and Evolution. pp. 386. UBC Press, Vancouver.
  • Martin, L.D. & Zhou, Z.-H. 1998. Confuciusornis sanctus compared to Archaeopteryx lithographica. Naturwissenschaften 85: 286289.
  • Nudds, R.L. 2007. Wing-bone length allometry in birds. J. Avian Biol. 38: 515519.
  • Nudds, R.L. & Bryant, D.M. 2000. The energetic cost of short flights in birds. J. Exp. Biol. 203: 15611572.
  • Nudds, R.L. & Dyke, G.J. 2009. Forelimb posture in dinosaurs and the evolution of the avian flapping flight-stroke. Evolution 63: 9941002.
  • Nudds, R.L. & Dyke, G.J. 2010. Narrow primary feather rachises in Confuciusornis and Archaeopteryx suggest poor flight ability. Science 328: 886889.
  • Nudds, R.L., Dyke, G.J. & Rayner, J.M.V. 2004a. Forelimb proportions and the evolutionary radiation of Neornithes. Proc. R. Soc. B 271: S324S327.
  • Nudds, R.L., Taylor, G.K. & Thomas, A.L.R. 2004b. Tuning of Strouhal number for high propulsive efficiency accurately predicts how wingbeat frequency and stroke amplitude relate and scale with size and flight speed in birds. Proc. R. Soc. B 271: 20712076.
  • Nudds, R.L., Dyke, G.J. & Rayner, J.M.V. 2007. Avian brachial index and wing-kinematics: putting movement back into bones. J. Zool. 272: 218226.
  • Nudds, R.L., Kaiser, G.W. & Dyke, G.J. 2011. Scaling of avian primary feather length. PLoS ONE. 6: e15665. doi:10.1371/journal.pone.0015665.
  • O’Connor, J.K. & Dyke, G.J. 2010. A re-assessment of Sinornis santensis and Cathayornis yandica (Aves: Enantiornithes). Rec. Aust. Mus. 62: 720.
  • O’Connor, J.K., Wang, X.-R., Chiappe, L.M., Gao, C.-H., Meng, Q.-J., Cheng, X.-D. et al. 2009. Phylogenetic support for a specialized clade of Cretaceous enantiornithine birds with information from a new species. J. Verteb. Paleont. 29: 188204.
  • Pagel, M.D. 1992. A method for the analysis of comparative data. J. Theor. Biol. 156: 431442.
  • Pennycuick, C.J. 1989. Bird Flight Performance. A Practical Calculation Manual. Oxford University Press, Oxford.
  • Peters, W.S. & Ji, Q. 1999. Had Confuciusornis to be a climber? J. Ornithol. 140: 4150 (in German).
  • Peters, W.S. & Peters, D.S. 2009. Life history, sexual dimorphism and ‘ornamental’ feathers in the Mesozoic bird Confuciusornis sanctus. Biol. Lett. 5: 817820.
  • Peters, W.S. & Peters, D.S. 2010. Sexual size dimorphism is the most consistent explanation for the body size spectrum of Confuciusornis sanctus. Biol. Lett. 6: 531532.
  • Rayner, J.M.V. 1988. Form and function in avian flight. In: Current Ornithology (R.F.Johnston, ed.), pp. 166. Plenum Press, New York.
  • Ruben, J. 1991. Reptilian physiology and the flight capacity of Archaeopteryx. Evolution 45: 117.
  • Sanz, J.L. & Ortega, F. 2002. The birds from Las Hoyas. Sci. Prog. 85: 113130.
  • Sanz, J.L., Chiappe, L.M., Pérez-Moreno, B.P., Buscalioni, A.D. & Moratalla, J. 1996. A Lower Cretaceous bird from Spain: implications for the evolution of flight. Nature 382: 442445.
  • Senter, P. 2006. Scapular orientation in theropods and basal birds, and the origin of flapping flight. Acta Palaeontol. Polon. 51: 305313.
  • Sokal, R.R. & Rohlf, F.J. 1995. Biometry: The Principles and Practice of Statistics in Biological Research. W. H. Freeman and Company, New York.
  • Speakman, J.R. 1993. Flight capabilities in Archaeopteryx. Evolution 47: 336340.
  • Wellnhofer, P. 2008. Archaeopteryx der urvogel von Solnhofen. Verlag Dr Friedrich P feil, Muenchen, Germany.
  • Xu, X. & Guo, Y. 2009. The origin and early evolution of feathers: insights from recent paleontological and neontological data. Vertebr. Palasiat. 47: 311329.
  • Xu, X., Zhou, Z.-H., Wang, X.-L., Kuang, X.-W., Zhang, F.-C. & Du, X.-K. 2003. Four-winged dinosaurs from China. Nature 421: 335340.
  • Yalden, D.W. 1970. The flying ability of Archaeopteryx. Ibis 113: 349356.
  • Zhang, F.C. & Zhou, Z.H. 2000. A primitive enantiornithine bird and the origin of feathers. Science 290: 19551960.
  • Zhang, Z.-H., Hou, L.-H., Hasegawa, Y., O’Connor, J., Martin, L.D. & Chiappe, L.M. 2006. The first Mesozoic heterodactyl bird from China. Acta Geol. Sinica 80: 631635.
  • Zhou, Z.-H. & Zhang, F.-C. 2007. Mesozoic birds of China––a synoptic review. Front. Biol. 2: 114.
  • Zhou, Z.-H., Chiappe, L.M. & Zhang, F.-C. 2005. Anatomy of the Early Cretaceous bird Eoenantiornis buhleri (Aves: Enantiornithes) from China. Can. J. Earth Sci. 42: 13311338.
  • Zinoviev, V. 2009. An attempt to reconstruct the lifestyle of confuciusornithids (Aves, Confuciusornithiformes). Paleontol. J. 4: 8391.

Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

Data S1 Primary feather lengths of early birds with respect to avian wing shape evolution.

As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer-reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.

FilenameFormatSizeDescription
JEB_2253_sm_DataS1.doc164KSupporting info item

Please note: Wiley Blackwell is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.