The role of mechanical forces on the patterning of the avian feather-bearing skin: A biomechanical analysis of the integumentary musculature in birds

The integumentary musculature of birds consists of three distinct components. The smooth musculature comprises feather and apterial muscles, which form a continuous musculo-elastic layer within the dermis. The feather muscles, which consistently include at least erectors and depressors, interconnect contour feathers within pterylae (i.e., feather tracts) along gridlines that are oriented diagonally to the longitudinal and transverse axes of the body. The apterial muscles interconnect pterylae by attaching to the contour feathers along their peripheries. The striated musculature is composed of individual subcutaneous muscles, most of which attach to contour feathers along the caudal periphery of pterylae A new integrative functional analysis of the integumentary musculature proposes how apterial muscles stabilize the pterylae and modulate the tension of the musculo-elastic layer, and how subcutaneous muscles provide the initial stimulus for erector muscles being able to ruffle the contour feathers within pterylae. It also shows how the arrangement of the contour feathers and integumentary muscles reflects the stresses and strains that act on the avian skin. These mechanical forces are in effect not only in the adult, especially during flight, but may also be active during feather morphogenesis. The avian integument with its complex structural organization may, therefore, represent an excellent model for analyzing the nature of interactions between the environment and genetic material. The predictions of our model are testable, and our study demonstrates the relevance of integrated analyses of complex organs as mechanically coherent systems for evolutionary and developmental biology.     

Size scaling and stiffness of avian primary feathers: implications for the flight of Mesozoic birds

The primary feathers of birds are subject to cyclical forces in flight causing their shafts (rachises) to bend. The amount the feathers deflect during flight is dependent upon the flexural stiffness of the rachises. By quantifying scaling relationships between body mass and feather linear dimensions in a large data set of living birds, we show that both feather length and feather diameter scale much closer to predictions for geometric similarity than they do to elastic similarity. Scaling allometry also indicates that the primary feathers of larger birds are relatively shorter and their rachises relatively narrower, compared to those of smaller birds. Two-point bending tests indicated that larger birds have more flexible feathers than smaller species. Discriminant functional analyses (DFA) showed that body mass, primary feather length and rachis diameter can be used to differentiate between different magnitudes of feather bending stiffness, with primary feather length explaining 63% of variance in rachis stiffness. Adding fossil measurement data to our DFA showed that Archaeopteryx and Confuciusornis do not overlap with extant birds. This strongly suggests that the bending stiffness of their primary feathers was different to extant birds and provides further evidence for distinctive flight styles and likely limited flight ability in Archaeopteryx and Confuciusornis.     

Variations in the morphology,distribution, and arrangement of feathers in domesticated birds

Domesticated birds exhibit a greater diversity in the morphology of their integument and its appendages than their wild ancestors. Many of these variations affect the appearance of a bird significantly and have been bred selectively by poultry and pigeon fanciers and aviculturists for the sake of visual appeal. Variations in feather distribution (e.g., feathering of legs and feet, featherless areas in normally feather-bearing skin) are widespread in chickens and pigeons. Variations in the number of feathers (e.g., increased number of tail feathers, lack of tail feathers) occur in certain pigeon and poultry breeds. Variations in feather length can affect certain body regions or the entire plumage. Variations in feather structure (e.g., silkiness, frilled feathering) can be found in exhibition poultry as well as in pet birds. Variations in feather arrangement (e.g., feather crests and vortices) occur in many domesticated bird species as a results of mutation and intense selective breeding. The causes of variations in the structure, distribution, length and arrangement of feathers is often unknown and opens a wide field for scientific research under various points of view (e.g., morphogenesis, pathogenesis, ethology, etc.). To that extent, variations in the morphology, distribution and arrangement of feathers in domesticated birds require also a concern for animal welfare because certain alleles responsible for integumentary variations in domesticated birds have pleiotropic effects, which often affect normal behaviour and viability.     

Horse hooves and bird feathers: Two model systems for studying the structure and development of highly adapted integumentary accessory organs--the role of the dermo-epidermal interface for the micro-architecture of complex epidermal structures

Accessory organs of the integument are locally modified parts of the potentially feather-bearing skin in birds (e.g., the rhamphotheca, claws, or scales), and of the potentially hairy skin in mammals (e.g., the rhinarium, nails, claws, or hooves). These special parts of the integument are characterised by a modified structure of their epidermal, dermal and subcutaneous layers. The developmental processes of these various integumentary structures in birds and mammals show both similarities and differences. For example, the development of the specialised epidermal structures of both feathers and the hoof capsule is influenced by the local three-dimensional configuration of the dermis. However, in feathers, in contrast to hooves, the arrangement of the corneous cells is only partially a direct result of the particular arrangement and shape of the dermal surface of the papillary body. Whereas the diameter of the feather papilla, as well as the number, length, and width of dermal ridges on the surface of the feather papilla influence the three-dimensional architecture of the feather rami, there is no apparent direct correlation between the dermo-epidermal interface and the development of the highly ordered architecture of the radii and hamuli in the feather vane. In order to elucidate this morphogenic problem and the problem of locally different processes of keratinisation and cornification, the structure and development of feathers in birds are compared to those of the hoof capsule in horses. The equine hoof is the most complex mammalian integumentary structure, which is determined directly by the dermal surface of the papillary body. Perspectives for further research on the development of modified integumentary structures, such as the role of the dermal microangioarchitecture and the selective adhesion and various differentiation pathways of epidermal cells, are discussed.     

The scaling of the size and stiffness of primary flight feathers

Birds encompass a large range of body sizes, yet the importance of body size on feather morphology and mechanical properties has not been characterized. In this study, I examined the scaling relationships of primary flight feathers within a phylogenetically diverse sample of avian species varying in body size by nearly three orders of magnitude. I measured the scaling relationships between body mass and feather linear dimensions as well as feather flexural stiffness. The resnlts of an independent contrasts analysis to test the effects of phylogenetic history on the characters measured had no effect on the scaling relationships observed. There was slight, but not significant, positive allometry in the scaling of shaft diameter with respect to feather length across a range of body masses. The scaling of feather length and diameter against body mass was not significantly different from isometry. Flexural stiffness, however, exhibited strong negative allometry. Therefore, larger birds have relatively more flexible feathers than smaller birds. The more flexible primary feathers of large birds may reduce stresses on the wing skeleton during take-off and landing and also make these feathers less susceptible to mechanical failure. Conversely, the greater flexibility of these feathers may also reduce their capacity to generate aerodynamic lift.     

The Integumentary Morphology of Modern Birds--An Overview

Avian integument is thin, elastic, and loosely attached to thebody, giving birds the freedom of movement needed for flight.Its epidermis is both keratinized and lipogenic, and the skinas a whole acts as a sebaceous secretory organ. The skin iscovered by feathers over most of the body, but many birds showcolored bare skin or integumentary outgrowths on the head andneck. Heavily cornified epidermis covers the beak, claws, spurs,and the scales on the legs and feet. These structures (exceptthe back of the leg and underside of the foot) contain beta-keratinlike that in reptilian scales. Most birds have sebaceous secretoryglands at the base of the tail and in the ear canals. Feathersare the most numerous, elaborate, and diverse of avian integumentaryderivatives. Their diversity is due to the possibilities inherentin their basic plan of a shaft with two orders of branches andthe use of modified beta-keratin as a strong, light, and plasticbuilding material. The evolution of feathers in birds has beenaccompanied by the development of complex systems for producingcolors and patterns, the innovations of feather arrangementand follicles with their musculature and innervation, and theprocess and control of molting.     

Quantifying structural variation in contour feathers to address functional variation and life history trade‐offs

Body feathers are important to many interactions birds have with their physical and social environments, such as streamlining the body for flight, thermoregulation, and social signaling. Birds differ dramatically in the texture of their body plumage depending on species and age class, likely reflecting different functional demands and age‐related trade‐offs in feather production. Despite the important insights potentially offered by studying variation in the structure of body feathers, there is no clear system for quantifying this variation. We present methods for quantifying age and species differences in the structure of body feathers. Most variation in our measures is due to species and age‐class differences, with little variance attributable to individual birds or to differences among feathers sampled from the same bird. We use our measures to test the hypothesis that the loosely‐textured plumage characteristic of many juvenile passerines reflects a trade‐off between investment in feather quality and rapid body growth that promotes early fledging. The structure of juvenile feathers was negatively correlated with duration of the nestling period among ten species of New World warblers (Parulidae), suggesting a trade‐off between investment in feathers and investment in rapid somatic development promoting fledging. Systematic studies of variation in the structure of body feathers will likely offer numerous other insights into avian biology.     

Feather function and the evolution of birds

The ability of feathers to perform many functions either simultaneously or at different times throughout the year or life of a bird is integral to the evolutionary history of birds. Many studies focus on single functions of feathers, but any given feather performs many functions over its lifetime. These functions necessarily interact with each other throughout the evolution and development of birds, so our knowledge of avian evolution is incomplete without understanding the multifunctionality of feathers, and how different functions may act synergistically or antagonistically during natural selection. Here, we review how feather functions interact with avian evolution, with a focus on recent technological and discovery-based advances. By synthesising research into feather functions over hierarchical scales (pattern, arrangement, macrostructure, microstructure, nanostructure, molecules), we aim to provide a broad context for how the adaptability and multifunctionality of feathers have allowed birds to diversify into an astounding array of environments and life-history strategies. We suggest that future research into avian evolution involving feather function should consider multiple aspects of a feather, including multiple functions, seasonal wear and renewal, and ecological or mechanical interactions. With this more holistic view, processes such as the evolution of avian coloration and flight can be understood in a broader and more nuanced context.     

Phenotypic flexibility of a southern African duck Alopochen aegyptiaca during moult: do northern hemisphere paradigms apply?

Phenotypic flexibility during moult has never been explored in austral nomadic ducks. We investigated whether the body condition, organ (pectoral muscle, gizzard, liver and heart) mass and flight‐feather growth Egyptian geese Alopochen aegyptiaca in southern Africa show phenotypic flexibility over their 53‐day period of flightless moult. Changes in body mass and condition were examined in Egyptian geese caught at Barberspan and Strandfontein in South Africa. Mean daily change in primary feather length was calculated for moulting geese and birds were dissected for pectoral muscle and internal organ assessment. Mean body mass and condition varied significantly during moult. Body mass and condition started to decrease soon after flight feathers were dropped and continued to do so until the new feathers were at least two‐thirds grown, after which birds started to regain body mass and condition. Non‐moulting geese had large pectoral muscles, accounting for at least 26% of total body mass. Once moult started, pectoral muscle mass decreased and continued to do so until the flight feathers were at least one‐third grown, after which pectoral muscle mass started to increase. The regeneration of pectoral muscles during moult started before birds started to gain overall body mass. Gizzard mass started to increase soon after the onset of moult, reaching a maximum when the flight feathers were two‐thirds grown, after which gizzard mass again decreased. Liver mass increased significantly as moult progressed, but heart mass remained constant throughout moult. Flight feather growth was initially rapid, but slowed towards the completion of moult. Our results show that Egyptian geese exhibit a significant level of phenotypic flexibility when they moult. We interpret the phenotypic changes that we observed as an adaptive strategy to minimize the duration of the flightless period. Moulting Egyptian geese in South Africa undergo more substantial phenotypic changes than those reported for ducks in the northern hemisphere.     

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.     

Coevolution of caudal skeleton and tail feathers in birds

Birds are capable of a wide range of aerial locomotor behaviors in part because of the derived structure and function of the avian tail. The tail apparatus consists of a several mobile (free) caudal vertebrae, a terminal skeletal element (the pygostyle), and an articulated fan of tail feathers that may be spread or folded, as well as muscular and fibroadipose structures that facilitate tail movements. Morphological variation in both the tail fan and the caudal skeleton that supports it are well documented. The structure of the tail feathers and the pygostyle each evolve in response to functional demands of differing locomotor behaviors. Here, I test whether the integument and skeleton coevolve in this important locomotor module. I quantified feather and skeletal morphology in a diverse sample of waterbirds and shorebirds using a combination of linear and geometric morphometrics. Covariation between tail fan shape and skeletal morphology was then tested using phylogenetic comparative methods. Pygostyle shape is found to be a good predictor of tail fan shape (e.g., forked, graduated), supporting the hypothesis that the tail fan and the tail skeleton have coevolved. This statistical relationship is used to reconstruct feather morphology in an exemplar fossil waterbird, Limnofregata azygosternon. Based on pygostyle morphology, this taxon is likely to have exhibited a forked tail fan similar to that of its extant sister clade Fregata, despite differing in inferred ecology and other aspects of skeletal anatomy. These methods may be useful in reconstructing rectricial morphology in other extinct birds and thus assist in characterizing the evolution of flight control surfaces in birds. J. Morphol. 275:1431–1440, 2014. © 2014 Wiley Periodicals, Inc.     

Linking the molecular evolution of avian beta (β) keratins to the evolution of feathers

Feathers of today's birds are constructed of beta (β)-keratins, structural proteins of the epidermis that are found solely in reptiles and birds. Discoveries of "feathered dinosaurs" continue to stimulate interest in the evolutionary origin of feathers, but few studies have attempted to link the molecular evolution of their major structural proteins (β-keratins) to the appearance of feathers in the fossil record. Using molecular dating methods, we show that before the appearance of Anchiornis (～155 Million years ago (Ma)) the basal β-keratins of birds began diverging from their archosaurian ancestor ～216?Ma. However, the subfamily of feather β-keratins, as found in living birds, did not begin diverging until ～143?Ma. Thus, the pennaceous feathers on Anchiornis, while being constructed of avian β-keratins, most likely did not contain the feather β-keratins found in the feathers of modern birds. Our results demonstrate that the evolutionary origin of feathers does not coincide with the molecular evolution of the feather β-keratins found in modern birds. More likely, during the Late Jurassic, the epidermal structures that appeared on organisms in the lineage leading to birds, including early forms of feathers, were constructed of avian β-keratins other than those found in the feathers of modern birds. Recent biophysical studies of the β-keratins in feathers support the view that the appearance of the subfamily of feather β-keratins altered the biophysical nature of the feather establishing its role in powered flight.     

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.     

Adaptation to the sky: Defining the feather with integument fossils from mesozoic China and experimental evidence from molecular laboratories

In this special issue on the Evo-Devo of amniote integuments, Alibardi has discussed the adaptation of the integument to the land. Here we will discuss the adaptation to the sky. We first review a series of fossil discoveries representing intermediate forms of feathers or feather-like appendages from dinosaurs and Mesozoic birds from the Jehol Biota of China. We then discuss the molecular and developmental biological experiments using chicken integuments as the model. Feather forms can be modulated using retrovirus mediated gene mis-expression that mimics those found in nature today and in the evolutionary past. The molecular conversions among different types of integument appendages (feather, scale, tooth) are discussed. From this evidence, we recognize that not all organisms with feathers are birds, and that not all skin appendages with hierarchical branches are feathers. We develop a set of criteria for true avian feathers: 1) possessing actively proliferating cells in the proximal follicle for proximo-distal growth mode; 2) forming hierarchical branches of rachis, barbs, and barbules, with barbs formed by differential cell death and bilaterally or radially symmetric; 3) having a follicle structure, with mesenchyme core during development; 4) when mature, consisting of epithelia without mesenchyme core and with two sides of the vane facing the previous basal and supra-basal layers, respectively; and 5) having stem cells and dermal papilla in the follicle and hence the ability to molt and regenerate. A model of feather evolution from feather bud --> barbs --> barbules --> rachis is presented, which is opposite to the old view of scale plate --> rachis --> barbs --> barbules (Regal, '75; Q Rev Biol 50:35).     

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 skin development and the evolutionary origin of feathers

The discovery of several dinosaurs with filamentous integumentary appendages of different morphologies has stimulated models for the evolutionary origin of feathers. In order to understand these models, knowledge of the development of the avian integument must be put into an evolutionary context. Thus, we present a review of avian scale and feather development, which summarizes the morphogenetic events involved, as well as the expression of the beta (beta) keratin multigene family that characterizes the epidermal appendages of reptiles and birds. First we review information on the evolution of the ectodermal epidermis and its beta (beta) keratins. Then we examine the morphogenesis of scutate scales and feathers including studies in which the extraembryonic ectoderm of the chorion is used to examine dermal induction. We also present studies on the scaleless (sc) mutant, and, because of the recent discovery of "four-winged" dinosaurs, we review earlier studies of a chicken strain, Silkie, that expresses ptilopody (pti), "feathered feet." We conclude that the ability of the ectodermal epidermis to generate discrete cell populations capable of forming functional structural elements consisting of specific members of the beta keratin multigene family was a plesiomorphic feature of the archosaurian ancestor of crocodilians and birds. Evidence suggests that the discrete epidermal lineages that make up the embryonic feather filament of extant birds are homologous with similar embryonic lineages of the developing scutate scales of birds and the scales of alligators. We believe that the early expression of conserved signaling modules in the embryonic skin of the avian ancestor led to the early morphogenesis of the embryonic feather filament, with its periderm, sheath, and barb ridge lineages forming the first protofeather. Invagination of the epidermis of the protofeather led to formation of the follicle providing for feather renewal and diversification. The observations that scale formation in birds involves an inhibition of feather formation coupled with observations on the feathered feet of the scaleless (High-line) and Silkie strains support the view that the ancestor of modern birds may have had feathered hind limbs similar to those recently discovered in nonavian dromaeosaurids. And finally, our recent observation on the bristles of the wild turkey beard raises the possibility that similar integumentary appendages may have adorned nonavian dinosaurs, and thus all filamentous integumentary appendages may not be homologous to modern feathers.     

Do feathered dinosaurs exist? Testing the hypothesis on neontological and paleontological evidence

The origin of birds and avian flight from within the archosaurian radiation has been among the most contentious issues in paleobiology. Although there is general agreement that birds are related to theropod dinosaurs at some level, debate centers on whether birds are derived directly from highly derived theropods, the current dogma, or from an earlier common ancestor lacking suites of derived anatomical characters. Recent discoveries from the Early Cretaceous of China have highlighted the debate, with claims of the discovery of all stages of feather evolution and ancestral birds (theropod dinosaurs), although the deposits are at least 25 million years younger than those containing the earliest known bird Archaeopteryx. In the first part of the study we examine the fossil evidence relating to alleged feather progenitors, commonly referred to as protofeathers, in these putative ancestors of birds. Our findings show no evidence for the existence of protofeathers and consequently no evidence in support of the follicular theory of the morphogenesis of the feather. Rather, based on histological studies of the integument of modern reptiles, which show complex patterns of the collagen fibers of the dermis, we conclude that "protofeathers" are probably the remains of collagenous fiber "meshworks" that reinforced the dinosaur integument. These "meshworks" of the skin frequently formed aberrant patterns resembling feathers as a consequence of decomposition. Our findings also draw support from new paleontological evidence. We describe integumental structures, very similar to "protofeathers," preserved within the rib area of a Psittacosaurus specimen from Nanjing, China, an ornithopod dinosaur unconnected with the ancestry of birds. These integumental structures show a strong resemblance to the collagenous fiber systems in the dermis of many animals. We also report the presence of scales in the forearm of the theropod ornithomimid (bird mimic) dinosaur, Pelecanimimus, from Spain. In the second part of the study we examine evidence relating to the most critical character thought to link birds to derived theropods, a tridactyl hand composed of digits 1-2-3. We maintain the evidence supports interpretation of bird wing digit identity as 2,3,4, which appears different from that in theropod dinosaurs. The phylogenetic significance of Chinese microraptors is also discussed, with respect to bird origins and flight origins. We suggest that a possible solution to the disparate data is that Aves plus bird-like maniraptoran theropods (e.g., microraptors and others) may be a separate clade, distinctive from the main lineage of Theropoda, a remnant of the early avian radiation, exhibiting all stages of flight and flightlessness.     

Feather holes and flight performance in the barn swallow Hirundo rustica

Feather holes are small (0.5–1?mm in diameter) deformities that appear on the vanes of flight feathers. Such deformities were found in many bird species, including galliforms and passerines. Holey flight feathers may be more permeable to air, which could have a negative effect on their ability to generate aerodynamic forces. However, to date the effects of feather holes on flight performance in birds remained unclear. In this study we investigated the relationship between the number of feather holes occurring in the wing or tail feathers and short term flight performance traits – aerial manoeuvrability, maximum velocity and maximum acceleration – in barns swallows, which are long distance migrating aerial foragers. We measured short-term flight performance of barn swallows in a standardized manner in flight tunnels. We found that acceleration and velocity were significantly negatively associated with the number of holes in the wing flight feathers, but not with those in the tail feathers. In the case of acceleration the negative relationship was sex specific – while acceleration significantly decreased with the number of feather holes in females, there was no such significant association in males. Manoeuvrability was not significantly associated with the number of feather holes. These results are consistent with the hypothesis that feather holes are costly in terms of impaired flight. We discuss alternative scenarios that could explain the observed relationships. We also suggest directions for future studies that could investigate the exact mechanism behind the negative association between the number of feather holes and flight characteristics.