Primary feather lengths may not be important for inferring the flight styles of Mesozoic birds

Chan, N.R., Dyke, G.J. & Benton, M.J. 2013: Primary feather lengths may not be important for inferring the flight styles of Mesozoic birds. Lethaia, Vol. 46, pp. 146–152. Although many Mesozoic fossil birds have been found with primary feathers preserved, these structures have rarely been included in morphometric analyses. This is surprising because the flight feathers of modern birds can contribute approximately 50% of the total wing length, and so it would be assumed that their inclusion or exclusion would modify functional interpretations. Here we show, contrary to earlier work, that this may not be the case. Using forelimb measurements and primary feather lengths from Mesozoic birds, we constructed morphospaces for different clades, which we then compared with morphospaces constructed for extant taxa classified according to flight mode. Consistent with older work, our results indicate that among extant birds some functional flight groups can be distinguished on the basis of their body sizes and that variation in the relative proportions of the wing elements is conservative. Mesozoic birds, on the other hand, show variable proportions of wing bones, with primary feather length contribution to the wing reduced in the earlier diverging groups. We show that the diverse Mesozoic avian clade Enantiornithes overlaps substantially with extant taxa in both size and limb element proportions, confirming previous morphometric results based on skeletal elements alone. However, these measurements cannot be used to distinguish flight modes in extant birds, and so cannot be used to infer flight mode in fossil forms. Our analyses suggest that more data from fossil birds, combined with accurate functional determination of the flight styles of living forms is required if we are to be able to predict the flight modes of extinct birds. □Birds, flight, morphospace, Mesozoic, wing.     

Avian furcula morphology may indicate relationships of flight requirements among birds

This study examined furcula (wishbone) shape relative to flight requirements. The furculae from 53 museum specimens in eight orders were measured: 1) three-dimensional shape (SR) as indicated by the ratio of the direct distance between the synostosis interclavicularis and the ligamentous attachment of one of its clavicles to the actual length of the clavicle between those same two points, and 2) curvature within the primary plane (LR) as indicated by the ratio of the length of the clavicle to the sum of the orthogonal distances between the same points using a projected image. Canonical discriminant analysis of these ratios placed the individuals into a) one of four general flight categories and b) one of eight taxonomic orders. The four flight categories were defined as: i) soaring with no flapping, ii) flapping with no soaring, iii) subaqueous (i.e., all wingbeats taking place under water), and iv) partial subaqueous (i.e., wingbeats used for both aerial and submerged flapping). The error rate for placement of the specimens in flight categories was only 26.4%, about half of the error rate for placement in taxonomic orders (51.3%). Subaqueous fliers (penguins, great auks) have furculae that are the most V-shaped. Partial subaqueous fliers (alcids, storm petrels) have furculae that are more U-shaped than the subaqueous fliers but more V-shaped than the aerial flapping fliers. The partial subaqueous fliers have furculae that are also the most anteriorly curved, possibly increasing protraction capability by changing the angle of applied force and increasing attachment area for the origin of the sternobrachialis pectoralis. The increased protraction capability can counteract profile drag, which is greater in water than in air due to the greater density of water. Soaring birds have furculae that are more U-shaped or circular than those of flapping birds and have the smallest range of variation. These results indicate that the shape of the furcula is functionally related to general differences in flight requirements and may be used to infer relationships of these requirements among birds.     

Barb geometry of asymmetrical feathers reveals a transitional morphology in the evolution of avian flight

The geometry of feather barbs (barb length and barb angle) determines feather vane asymmetry and vane rigidity, which are both critical to a feather''s aerodynamic performance. Here, we describe the relationship between barb geometry and aerodynamic function across the evolutionary history of asymmetrical flight feathers, from Mesozoic taxa outside of modern avian diversity (Microraptor, Archaeopteryx, Sapeornis, Confuciusornis and the enantiornithine Eopengornis) to an extensive sample of modern birds. Contrary to previous assumptions, we find that barb angle is not related to vane-width asymmetry; instead barb angle varies with vane function, whereas barb length variation determines vane asymmetry. We demonstrate that barb geometry significantly differs among functionally distinct portions of flight feather vanes, and that cutting-edge leading vanes occupy a distinct region of morphospace characterized by small barb angles. This cutting-edge vane morphology is ubiquitous across a phylogenetically and functionally diverse sample of modern birds and Mesozoic stem birds, revealing a fundamental aerodynamic adaptation that has persisted from the Late Jurassic. However, in Mesozoic taxa stemward of Ornithurae and Enantiornithes, trailing vane barb geometry is distinctly different from that of modern birds. In both modern birds and enantiornithines, trailing vanes have larger barb angles than in comparatively stemward taxa like Archaeopteryx, which exhibit small trailing vane barb angles. This discovery reveals a previously unrecognized evolutionary transition in flight feather morphology, which has important implications for the flight capacity of early feathered theropods such as Archaeopteryx and Microraptor. Our findings suggest that the fully modern avian flight feather, and possibly a modern capacity for powered flight, evolved crownward of Confuciusornis, long after the origin of asymmetrical flight feathers, and much later than previously recognized.     

The fossil record and limb disparity of enantiornithines, the dominant flying birds of the Cretaceous

Morphometric and stratigraphic analyses that encompass the known fossil record of enantiornithine birds (Enantiornithes) are presented. These predominantly flighted taxa were the dominant birds of the second half of the Mesozoic; the enantiornithine lineage is known to have lasted for at least 60 million years (Ma), up until the end of the Cretaceous. Analyses of fossil record dynamics show that enantiornithine 'collectorship' since the 1980s approaches an exponential distribution, indicating that an asymptote in proportion of specimens has yet to be achieved. Data demonstrate that the fossil record of enantiornithines is complete enough for the extraction of biological patterns. Comparison of the available fossil specimens with a large data set of modern bird (Neornithes) limb proportions also illustrates that the known forelimb proportions of enantiornithines fall within the range of extant taxa; thus these birds likely encompassed the range of flight styles of extant birds. In contrast, most enantiornithines had hindlimb proportions that differ from any extant taxa. To explore this, ternary diagrams are used to graph enantiornithine limb variation and to identify some morphological oddities ( Otogornis , Gobipteryx ); taxa not directly comparable to modern birds. These exceptions are interesting – although anatomically uniform, and similar to extant avians in their wing proportions, some fossil enantiornithines likely had flight styles not seen among their living counterparts.     

Avian wing proportions and flight styles: first step towards predicting the flight modes of mesozoic birds

We investigated the relationship between wing element proportions and flight mode in a dataset of living avian species to provide a framework for making basic estimates of the range of flight styles evolved by Mesozoic birds. Our results show that feather length (f(prim)) and total arm length (ta) (sum of the humerus, ulna and manus length) ratios differ significantly between four flight style groups defined and widely used for living birds and as a result are predictive for fossils. This was confirmed using multivariate ordination analyses, with four wing elements (humerus, ulna/radius, manus, primary feathers), that discriminate the four broad flight styles within living birds. Among the variables tested, manus length is closely correlated with wing size, yet is the poorest predictor for flight style, suggesting that the shape of the bones in the hand wing is most important in determining flight style. Wing bone thickness (shape) must vary with wing beat strength, with weaker forces requiring less bone. Finally, we show that by incorporating data from Mesozoic birds, multivariate ordination analyses can be used to predict the flight styles of fossils.     

PHYLOGENY AND FORELIMB DISPARITY IN WATERBIRDS

Previous work has shown that the relative proportions of wing components (i.e., humerus, ulna, carpometacarpus) in birds are related to function and ecology, but these have rarely been investigated in a phylogenetic context. Waterbirds including “Pelecaniformes,” Ciconiiformes, Procellariiformes, Sphenisciformes, and Gaviiformes form a highly supported clade and developed a great diversity of wing forms and foraging ecologies. In this study, forelimb disparity in the waterbird clade was assessed in a phylogenetic context. Phylogenetic signal was assessed via Pagel's lambda, Blomberg's K, and permutation tests. We find that different waterbird clades are clearly separated based on forelimb component proportions, which are significantly correlated with phylogeny but not with flight style. Most of the traditional contents of “Pelecaniformes” (e.g., pelicans, cormorants, and boobies) cluster with Ciconiiformes (herons and storks) and occupy a reduced morphospace. These taxa are closely related phylogenetically but exhibit a wide range of ecologies and flight styles. Procellariiformes (e.g., petrels, albatross, and shearwaters) occupy a wide range of morphospace, characterized primarily by variation in the relative length of carpometacarpus and ulna. Gaviiformes (loons) surprisingly occupy a wing morphospace closest to diving petrels and penguins. Whether this result may reflect wing proportions plesiomorphic for the waterbird clade or a functional signal is unclear. A Bayesian approach detecting significant rate shifts across phylogeny recovered two such shifts. At the base of the two sister clades Sphenisciformes + Procellariiformes, a shift to an increase evolutionary rate of change is inferred for the ulna and carpometacarpus. Thus, changes in wing shape begin prior to the loss of flight in the wing‐propelled diving clade. Several shifts to slower rate of change are recovered within stem penguins.     

Bone histological correlates of high-frequency flapping flight and body mass in the furculae of birds: a phylogenetic approach

A parsimony optimization of the presence of high-frequency flapping flight onto a phylogeny of 29 species of birds shows that this is a derived character state that has been acquired at least four independent times: by the last common ancestor of Alcidae, that of Podicipedidae, that of Anatidae, and that of Rallidae. Cineradiographic analysis has shown that the furculae of birds underwent extraordinary deformations during the wingbeat cycle. Cyclical deformations are known to produce microfractures in the bone tissue, which may be a stimulus for Haversian remodelling, a mechanism of resorption and reconstruction of bone tissue that may repair bone microdamage. In the present study, we performed a comparative analysis in a phylogenetic context to test the effect of the frequency of cyclical deformations and body mass on the rate of Haversian remodelling in the furculae of birds. A variation partitioning analysis showed that the type of flight (high-frequency flapping flight vs. other kinds of flight of lower wing beat frequency) and body mass explained a significant portion of Haversian bone density (the outcome of Haversian remodelling) and that the phylogeny also explained a significant part of this variation. This phylogenetic signal on Haversian bone density variation may be the outcome of phylogenetic signal on the proximate causes producing Haversian remodelling.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 729–738.     

The quality of the fossil record of Mesozoic birds

The Mesozoic fossil record has proved critical for understanding the early evolution and subsequent radiation of birds. Little is known, however, about its relative completeness: just how 'good' is the fossil record of birds from the Mesozoic? This question has come to prominence recently in the debate over differences in estimated dates of origin of major clades of birds from molecular and palaeontological data. Using a dataset comprising all known fossil taxa, we present analyses that go some way towards answering this question. Whereas avian diversity remains poorly represented in the Mesozoic, many relatively complete bird specimens have been discovered. New taxa have been added to the phylogenetic tree of basal birds, but its overall shape remains constant, suggesting that the broad outlines of early avian evolution are consistently represented: no stage in the Mesozoic is characterized by an overabundance of scrappy fossils compared with more complete specimens. Examples of Neornithes (modern orders) are known from later stages in the Cretaceous, but their fossils are rarer and scrappier than those of basal bird groups, which we suggest is a biological, rather than a geological, signal.     

Pedal Claw Curvature in Birds,Lizards and Mesozoic Dinosaurs – Complicated Categories and Compensating for Mass-Specific and Phylogenetic Control

Pedal claw geometry can be used to predict behaviour in extant tetrapods and has frequently been used as an indicator of lifestyle and ecology in Mesozoic birds and other fossil reptiles, sometimes without acknowledgement of the caveat that data from other aspects of morphology and proportions also need to be considered. Variation in styles of measurement (both inner and outer claw curvature angles) has made it difficult to compare results across studies, as have over-simplified ecological categories. We sought to increase sample size in a new analysis devised to test claw geometry against ecological niche. We found that taxa from different behavioural categories overlapped extensively in claw geometry. Whilst most taxa plotted as predicted, some fossil taxa were recovered in unexpected positions. Inner and outer claw curvatures were statistically correlated, and both correlated with relative claw robusticity (mid-point claw height). We corrected for mass and phylogeny, as both likely influence claw morphology. We conclude that there is no strong mass-specific effect on claw curvature; furthermore, correlations between claw geometry and behaviour are consistent across disparate clades. By using independent contrasts to correct for phylogeny, we found little significant relationship between claw geometry and behaviour. ‘Ground-dweller’ claws are less curved and relatively dorsoventrally deep relative to those of other behavioural categories; beyond this it is difficult to assign an explicit category to a claw based purely on geometry.     

The patterns and modes of the evolution of disparity in Mesozoic birds

The origin of birds from non-avian theropod dinosaurs is one of the greatest transitions in evolution. Shortly after diverging from other theropods in the Late Jurassic, Mesozoic birds diversified into two major clades—the Enantiornithes and Ornithuromorpha—acquiring many features previously considered unique to the crown group along the way. Here, we present a comparative phylogenetic study of the patterns and modes of Mesozoic bird skeletal morphology and limb proportions. Our results show that the major Mesozoic avian groups are distinctive in discrete character space, but constrained in a morphospace defined by limb proportions. The Enantiornithines, despite being the most speciose group of Mesozoic birds, are much less morphologically disparate than their sister clade, the Ornithuromorpha—the clade that gave rise to living birds, showing disparity and diversity were decoupled in avian history. This relatively low disparity suggests that diversification of enantiornithines was characterized in exhausting fine morphologies, whereas ornithuromorphs continuously explored a broader array of morphologies and ecological opportunities. We suggest this clade-specific evolutionary versatility contributed to their sole survival of the end-Cretaceous mass extinction.     

Multiphase morphospace saturation in cyrtocrinid crinoids

The study of the relationship between disparity (occupied morphospace) and diversity (number of taxa) through geological time represents a powerful tool in the macroevolutionary study of groups. In this contribution, this approach is applied for the first time to the cyrtocrinid crinoids, a major clade of mostly Mesozoic articulate crinoids also represented by rare Cenozoic forms (two extant taxa). The analysis of disparity identified two separate evolutionary radiations for cyrtocrinids with maximum morphospace exploration, one at the beginning of the evolutionary history of the group in the Pliensbachian and a second one between the Late Jurassic and Early Cretaceous. On the methodological level, the disparity measured both as total variance and as sum of ranges shows compatible results, with trends well coupled to the diversity curve indicating that, in cyrtocrinid crinoids, an increase or decrease in the number of taxa in the history of the clade corresponds a proportional increase and decrease also in the occupied morphospace. The curves obtained were interpreted in the light of the clade's phylogeny, major oceanographic events, newly available ecological niches and relative key innovations, which would be able to increase the fitness of the group. The group diversity was already in decline starting from the Aptian, and the mass extinction at the K‐PG boundary had no effect on the history of the clade. The results show once again the importance and potential of diversity/disparity studies when put into the light of palaeotectonic, palaeoecological and palaeoenvironmental factors.     

The primary feather lengths of early birds with respect to avian wing shape evolution

We examine the relationships between primary feather length (f(prim)) 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 f(prim) (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 f(prim) (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 f(prim)/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 f(prim)/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.     

Multivariate analysis of neognath skeletal measurements: implications for body mass estimation in Mesozoic birds

The abundant fossils of avian stem taxa unearthed during the last years make it necessary to review and improve the models for estimating body mass used in palaeoecological studies. In this article, single and multiple regression functions based on osteological measurements were obtained from a large data set of extant flying birds for estimating the body mass of 42 Mesozoic specimens from stem taxa Archaeopterygidae, Jeholornithidae, Sapeornithidae, Confuciusornithidae, and Enantiornithes, and basal members of Ornithuromorpha. Traditionally, body mass has been estimated in fossil vertebrates using univariate scaling functions. In contrast, multiple regression functions have been used less frequently. Both predictive methods can be affected by different sources of error from statistics, phylogenetic relationships, ecological adaptations, and bone preservation; however, although some studies have addressed these biases, few have tested them within the context of a single data set. In our data set, we find that the models with greater predictive strength and applicability for new specimens, especially for stem taxa, are those derived from multiple regression analyses. For this reason, we suggest that multiple regression analyses may provide improved predictive strength for stem group specimens. Moreover, the methodology used for selecting variables allowed us to obtain specific sets of predictors for each fossil stem group that presumably minimized the variation resulting from historical contingency (i.e. differences in skeletal morphology arising from phylogeny), locomotor adaptations, and diagenetic compaction. The loss of generalizability in the multiple regression models resulting from collinearity effects was negligible on the body mass estimates derived from our data set. Therefore, the body mass values obtained for Mesozoic specimens are accurate and can be used in future studies in a number of palaeobiological and evolutionary aspects of extinct birds, particularly the first stages of avian flight. © 2015 The Linnean Society of London     

A morphospace‐based test for competitive exclusion among flying vertebrates: did birds,bats and pterosaurs get in each other's space?

Three vertebrate groups – birds, bats and pterosaurs – have evolved flapping flight over the past 200 million years. This innovation allowed each clade access to new ecological opportunities, but did the diversification of one of these groups inhibit the evolutionary radiation of any of the others? A related question is whether having the wing attached to the hindlimbs in bats and pterosaurs constrained their morphological diversity relative to birds. Fore‐ and hindlimb measurements from 894 specimens were used to construct a morphospace to assess morphological overlap and range, a possible indicator of competition, among the three clades. Neither birds nor bats entered pterosaur morphospace across the Cretaceous–Paleogene (Tertiary) extinction. Bats plot in a separate area from birds, and have a significantly smaller morphological range than either birds or pterosaurs. On the basis of these results, competitive exclusion among the three groups is not supported.     

The evolution of cranial form and function in theropod dinosaurs: insights from geometric morphometrics

Theropod dinosaurs, an iconic clade of fossil species including Tyrannosaurus and Velociraptor, developed a great diversity of body size, skull form and feeding habits over their 160+ million year evolutionary history. Here, we utilize geometric morphometrics to study broad patterns in theropod skull shape variation and compare the distribution of taxa in cranial morphospace (form) to both phylogeny and quantitative metrics of biting behaviour (function). We find that theropod skulls primarily differ in relative anteroposterior length and snout depth and to a lesser extent in orbit size and depth of the cheek region, and oviraptorosaurs deviate most strongly from the "typical" and ancestral theropod morphologies. Noncarnivorous taxa generally fall out in distinct regions of morphospace and exhibit greater overall disparity than carnivorous taxa, whereas large-bodied carnivores independently converge on the same region of morphospace. The distribution of taxa in morphospace is strongly correlated with phylogeny but only weakly correlated with functional biting behaviour. These results imply that phylogeny, not biting function, was the major determinant of theropod skull shape.     

Comparable disparity in the appendicular skeleton across the fish–tetrapod transition,and the morphological gap between fish and tetrapod postcrania

Appendicular skeletal traits are used to quantify changes in morphological disparity and morphospace occupation across the fish–tetrapod transition and to explore the informativeness of different data partitions in phylogeny reconstruction. Anterior appendicular data yield trees that differ little from those built from the full character set, whilst posterior appendicular data result in considerable loss of phylogenetic resolution and tree branch rearrangements. Overall, there is a significant incongruence in the signals associated with pectoral and pelvic data. The appendicular skeletons of fish and tetrapods attain similar levels of morphological disparity (at least when data are rarefied at the maximum sample size for fish in our study) and occupy similarly sized regions of morphospace. However, fish appear more dispersed in morphospace than tetrapods do. All taxa show a heterogeneous distribution in morphospace, and there is a clear separation between fish and tetrapods despite the presence of several evolutionarily intermediate taxa.     

Development of the clavicles in birds and mammals

Clavicles (collar bones) are variably present in mammals. Furculae (wishbones)--which may or may not be homologous with clavicles--are variably present and/or fused in birds and present in theropod dinosaurs. In this overview the development of clavicles and furculae is discussed with special attention to modes of skeletogenesis (whether intramembranous or endochondral), numbers of centres of ossification (one in chick furculae; two in murine clavicles), presence of cartilage (primary in clavicles, secondary in furculae), evidence from experimental analysis and from mutations for dependence of both clavicular and furcular growth on mechanical stimulation, and syndromes and mutations affecting clavicular development leading to both under and over development. J. Exp. Zool. 289:153-161, 2001.     

Gravity-defying Behaviors: Identifying Models for Protoaves

Most current phylogenetic hypotheses based upon cladistic methodologyassert that birds are the direct descendants of derived maniraptorantheropod dinosaurs, and that the origin of avian flight necessarilydeveloped within a terrestrial context (i.e., from the "groundup"). Most theoretical aerodynamic and energetic models or chronologicallyappropriate fossil data do not support these hypotheses forthe evolution of powered flight. The more traditional modelfor the origin of flight derives birds from among small arborealearly Mesozoic archosaurs ("thecodonts"). According to thismodel, protoavian ancestors developed flight in the trees viaa series of intermediate stages, such as leaping, parachuting,gliding, and flapping. This model benefits from the assemblageof living and extinct arboreal vertebrates that engage in analogousnon-powered aerial activities using elevation as a source ofgravitational energy. Recent reports of "feathered theropods"notwithstanding, the evolution of birds from any known groupof maniraptoran theropods remains equivocal.     

中国中生代的鸟类:介绍及综述

最近十来年 ,中国辽宁发现的早白垩世的鸟类化石超过了世界上其它任何一个地区。中国的中生代鸟类化石代表了始祖鸟化石之后鸟类历史上第一次显著的分异。它们不仅包括了带有明显恐龙祖先特征的长尾的鸟类 ,而且还包括了许多进步或特化的种类 ,如早白垩世最大的鸟类 ,最原始的反鸟类 ,以及保存最好的、飞行结构和现生鸟类几乎一样的今鸟类。这些早期鸟类在诸如飞行、大小和食性等所反映的演化、形态和生态学特征等方面出现了重大的分异。具有长尾骨骼的原始基干鸟类热河鸟和驰龙类具有的相似性 ,进一步支持了鸟类起源于恐龙的学说。中国发现的早白垩世的鸟类以及树栖的恐龙化石还为鸟类飞行的树栖起源假说提供了十分重要的证据。“恐龙下树”的假说结合了鸟类起源于恐龙的学说和鸟类飞行的树栖起源学说 ,因此也得到了化石证据的支持。由于多种恐龙带有羽毛 ,因此羽毛不一定代表了恒温。恒温的鸟类可能到了早白垩世的进步鸟类中才开始出现