Flight feather attachment in rock pigeons (Columba livia): covert feathers and smooth muscle coordinate a morphing wing

Abstract

Mechanisms for passively coordinating forelimb movements and flight feather abduction and adduction have been described separately from both in vivo and ex vivo studies. Skeletal coordination has been identified as a way for birds to simplify the neuromotor task of controlling flight stroke, but an understanding of the relationship between skeletal coordination and the coordination of the aerodynamic control surface (the flight feathers) has been slow to materialize. This break between the biomechanical and aerodynamic approaches – between skeletal kinematics and airfoil shape – has hindered the study of dynamic flight behaviors. Here I use dissection and histology to identify previously overlooked interconnections between musculoskeletal elements and flight feathers. Many of these structures are well‐placed to directly link elements of the passive musculoskeletal coordination system with flight feather movements. Small bundles of smooth muscle form prominent connections between upper forearm coverts (deck feathers) and the ulna, as well as the majority of interconnections between major flight feathers of the hand. Abundant smooth muscle may play a role in efficient maintenance of folded wing posture, and may also provide an autonomically regulated means of tuning wing shape and aeroelastic behavior in flight. The pattern of muscular and ligamentous linkages of flight feathers to underlying muscle and bone may provide predictable passive guidance for the shape of the airfoil during flight stroke. The structures described here provide an anatomical touchstone for in vivo experimental tests of wing surface coordination in an extensively researched avian model species.

Introduction

Avian wing mechanics

Bird wings are flexible airfoils capable of creating efficient aerodynamic force across a wide range of flight speeds, kinematics, and postures. The superficial similarities between bird wings and human‐designed fixed‐wing airfoils have been instrumental in uncovering the biomechanics of bird flight. However, as this understanding has developed into increasingly complex and sensitive models (Parslew, 2015) dynamic wing shape change in flight has emerged as an important consideration (Crandell & Tobalske, 2011). In contrast to the relatively invariant kinematics of downstroke (Dial et al. 2008), pronounced changes in wing shape occur during the recovery phase or upstroke in flapping flight, where the shape of the wing at mid‐upstroke often shows a strong relationship to flight speed (Fig. 1A‐C) (Tobalske & Dial, 1996; Tobalske, 2007; Crandell & Tobalske, 2015). The kinematic and taxonomic variability of wing shape at mid‐upstroke offers the chance to test macroevolutionary hypotheses regarding flight performance that can be anchored on all sides with data from extant taxa.

Figure 1.

Skeletal anatomy and wing shape in rock pigeons. (A–C) Silhouettes in dorsal aspect showing wing outlines and approximate skeletal positions during upstroke in (A) slow flight (tip‐reversal upstroke), (B) transitional (feathered upstroke), and (C) fast flight (swept‐wing upstroke). Flight speed ranges after Tobalske & Dial (1996). (D) Position and anatomy of the distal limb elements in Columba livia. (E,F) mechanisms of passive coordinated flexion (E) and extension (F), showing the lines of action for salient muscular and ligamentous structures, after Vazquez (1994). Abbreviations as in text and Appendix 1. (G) Hypotheses of ligamentous limits on flight feather motion, as summarized by Pelissier (1923) and Raikow (1985).

The anatomy and neuromotor control of the shoulder joint (the major determinant of overall wing position in flight stroke) are both well‐characterized (Hedrick et al. 2003; Tobalske & Biewener, 2008; Baier, 2012; Baier et al. 2013). In contrast, the anatomical structures that govern wing shape past the elbow joint are poorly known. The musculoskeletal elements of the distal wing currently form a functional ‘black box’ that sits between the two most heavily studied aspects of avian flight biomechanics: modulation of the contractile forces of the major flight muscles, and the aerodynamic forces generated by the moving wing. Integrating the mechanics of wing shape change into existing models of flight will require a detailed understanding of the linkages that transmit forces between the humerus and the feathers that make up the wing surface.

Several mechanisms may contribute to wing shape control. Neuromuscular control of joint angles undoubtedly plays a major role, as with other tetrapods. Birds also show a suite of unique mechanisms for coordinating wing shape (Fig. 1E‐G). Flight feather shafts bend passively under aerodynamic load, storing strain energy that contributes to limb deceleration at the end of downstroke (Corning & Biewener, 1998). Small masses of both smooth and skeletal muscle insert on the shafts of flight feathers, conceivably influencing feather position during flight (Berger, 1956; Lucas & Stettenheim, 1972; Stegmann, 1978). Most notably, passive mechanical linkages that couple flexion and extension of the elbow have been shown to be major contributors to wing kinematics, allowing for normal level flight even in the absence of neuromotor control over the wrist and hand in pigeons (Dial, 1992). Characterizing the structures that tie flight feather follicles to the distal forelimb skeleton provides a basis for comparing the effects of each of these potential inputs.

Coupled joints in the pigeon forelimb

Mechanisms of coupled flexion and extension of the elbow and wrist in avian forelimbs have a long history of investigation (Bergmann, 1839; Alix, 1874; Garrod, 1875; Pelissier, 1923; Sy, 1936; Fisher, 1957). More recent anatomical work has documented the role the propatagial ligament and forelimb musculature in coordinating wing kinematics, as well as the contributions of individual muscles to joint motion in vitro (Vazquez, 1994, 1995; Brown et al. 1995). Although these mechanisms account for the position of the musculoskeletal component of the wing, up to 85% of the area of a fully extended wing is composed of feathers (Pennycuick, 2008). Understanding dynamic wing shape change requires an additional element that accounts for the relationship between musculoskeletal coordination and coordination of the positions of flight feathers in the wing.

Attachment of flight feathers

Flight feathers (primary and secondary remiges, along with coverts or deck feathers) attach to each other and the rest of the wing through several small ligaments and muscles. These attachments have been shown to coordinate furling (i.e. secondary and distal primary adduction, proximal primary abduction) and unfurling in adjacent feathers during wing flexion and extension ex vivo (Pelissier, 1923; Stettenheim, 1959). This system has received sporadic attention, beginning with descriptions of feather position and the attachment of the secondaries to remigial papillae (quill knobs) on the ulna (Prechtl, 1846). Later work provided insight into the connection of flight feathers to major forelimb muscles, and the presence of elastic tissue in many of the ligaments (Alix, 1874; Robin & Chabry, 1884; Edington & Miller, 1941). The most comprehensive studies have considered the role of feather attachment anatomy in relation to flight stroke, leading to a current synthesis in which the follicles of the secondary and proximal primary remiges abduct and adduct as the wings flex and extend during flight stroke, but are fixed against elevation and rotation (Fig. 1G), whereas the follicles of the distal primaries are firmly fixed to the phalanges of the major and minor digits (Pelissier, 1923; Sy, 1936; Brown, 1953; Raikow, 1985).

Smooth muscle in avian skin

The smooth muscle fibers in bird skin are easily overlooked (Nitzsch & Burmeister, 1840; pp. 203–204). They occur most often within elastic ligaments (Petry, 1951; Ostmann et al. 1963) and, indeed, both tissues appear to be derived from a common pool of dermal myoblasts during development (Drenckhahn & Jeikowski, 1978). The earliest investigations of feather muscle physiology played a prominent role in defining the concept of the autonomic nervous system (Langley, 1903), and the mm. pennarum (or mm. pennati) have continued to be an important pharmacological model for the study of adrenergic neurotransmission mechanisms (Bennett et al. 1970; Levinger et al. 1985; Lot, 1987; Dehpour et al. 1994). These studies have uniformly concluded that the mm. pennarum are innervated by adrenergic terminals of the sympathetic nervous system (Golenhofen & Petry, 1968; Jeikowski & Drenckhahn, 1981).

With few exceptions (Berger, 1956; Lucas & Stettenheim, 1972; Hikida & Peterson, 1983), morphological studies of feather musculature have focused on feather tracts on the neck and trunk. The musculature of contour feathers has been proposed to function in streamlining and drag reduction (Homberger & de Silva, 2003), such that their action is responsible for the ‘body drag anomaly’, a marked difference in parasitic drag measured from living and dead (frozen) birds (Pennycuick et al. 1996). Smooth muscle bundles associated with wing feathers may likewise be involved in modulating flow attachment and aeroelastic behaviors, with concomitant effects on the induced drag and profile drag of the wings themselves. Any differences here are likely to have a pronounced effect on the power requirements of low‐speed or maneuvering flight (Shyy et al. 2013).

The aim of this study is to expand our understanding of the anatomical underpinnings of wing shape coordination in rock pigeons (Columba livia Gmelin 1789), one of the most commonly used model species for experimental studies of avian flight biomechanics. The technical capability to track representative feather positions (e.g. Crandell & Tobalske, 2015) and model the aerodynamic effects of subtle wing surface changes (Song et al. 2014) provides the basis to test mechanisms of flight control in unsteady flight (take‐off, maneuvering, landing). The degree to which these mechanisms are under active neuromotor control or are the result of passive mechanical constraints, is a distinction that will fundamentally affect the way we approach research on the function and evolution of avian flight control. To this end, this study aims to identify anatomical structures that may contribute to wing feather coordination, to provide an updated basis for experimental studies of wing shape in flight.

Materials and methods

Specimens

The pigeons used in this study were purchased as formalin‐fixed cadavers from a biological supply house (Bio Corporation, Alexandria, MN, USA). Specimens were examined by standard dissection (n = 3), micro‐computed tomography (microCT; n = 7), and histological sectioning (n = 5).

Cross‐sectional anatomy and histology

Serial semithin sections were used to visualize millimeter‐ to micron‐scale structures in situ. Samples for histology were taken from the proximal ulna [including secondaries 9–12 (S9–S12)], distal ulna (S1–S8), carpometacarpus [carpal remex (C) and primaries 1–6 (P1–P6)], and major and minor digits (P6–P10). Aside from cutting to isolate the samples, all soft tissues were left intact, including the calami of the remiges and coverts. Samples were plastic‐embedded following a standard protocol (Sterchi & Eurell, 1989). Embedded blocks were sectioned at ≈ 1‐mm intervals using a diamond wafering saw (Isomet 1000, Buehler). Separate specimens were sectioned in transverse, parasagittal, and horizontal planes to provide a more thorough overview of microanatomical relationships. Serial sections were mounted on plastic slides with cyanoacrylate adhesive and ground to ≈ 100 μm using a laboratory grinding and polishing lap (Ecomet 4, Beuhler).

Prepared sections were examined in transmitted unpolarized, linear cross‐polarized, and circular cross‐polarized light using a compound microscope (Eclipse 50i, Nikon). Collagen (and hence bone, ligament, and tendon), feather keratin, and muscle are all highly birefringent, thus polarized light microscopy allows an assessment of the distribution and orientation of these tissues. At higher magnifications, the striations of muscle sarcomeres are plainly visible in semithin sections, allowing the discrimination of smooth and skeletal muscle (Fig. 2). Elastic tissues are poorly birefringent – comparison between unpolarized and circularly‐polarized images allows discrimination of this tissue on unstained specimens. In addition to standard micrographs, fast and unstitched whole‐specimen images in circularly polarized light were obtained by placing slides on a black felt cropping mask between ‘crossed’ (inverted) sheets of left‐handed circular polarizing filter film (Edmund Optics, Barrington, NJ) on a copy‐stand light table, and using a DSLR camera equipped with a macro lens.

Figure 2.

Tissue discrimination in unpolarized and circularly polarized micrographs. (A,B) Example of musculotendinous junction between skeletal muscle and collagenous tendon. Striations are clearly visible in skeletal muscle, and the both actin and collagen are birefringent and thus visible under crossed circular polarizers (B). (C,D) Example of musculotendinous junction between smooth muscle and elastic tendon, characteristic of the mm. pennarum of avian skin and their derivatives. Actin renders the smooth muscle visible under crossed circular polarizers (D), but elastin is poorly birefringent and can only be seen un unpolarized light (C). Scale bars: 50 μm.

microCT

Micro‐computed tomography (microCT) was used as a means to visualize the relationship between delicate connective tissue structures, feathers, and bones. In addition to scanning embedded blocks before sectioning, radiocontrast stains were used on a subset of four unembedded specimens. Minor and marginal coverts, along with contour feathers, were plucked from isolated wings. The remaining flight feathers were trimmed at the calamus and left in place. Specimens were stained with either potassium iodide (IKI) or phosphotungstic acid (PTA), following protocols from Metscher (2009). Stained specimens were scanned in water or 70% ethanol. Both embedded and stained specimens were scanned with a VivaCT 75 scanner (Scanco Medical, Brüttisellen, Switzerland) at 70 kVp.

Results

The more prominent musculoskeletal components of pigeon forelimbs have been described in detail elsewhere (Berger, 1956; Stegmann, 1978; Baumel & Raikow, 1993; Baumel & Witmer, 1993; Vanden Berge & Zweers, 1993; Vazquez, 1994, 1995; Brown et al. 1995). Figures 3 and 4 provide a general overview of features relevant to the attachment and coordination of flight feathers and coverts. Nomenclature for previously described structures follows Nomina Anatomica Avium (Baumel, 1993). A list of terms and abbreviations is included in Appendix 1. Note that abbreviations for smooth muscle bundles are given the prefix ‘mn’ (muscularis nonstriatus) to distinguish them from skeletal muscle.

Figure 3.

Schematic arrangement of mm. pennarum. Each first‐row upper minor covert is connected to two feathers in the second row by (i) a caudolateral erector muscle (mnEPcl) that runs from the ventral surface of the second‐row follicle to the medial side of the first‐row follicle in the next adjacent column, (ii) paired belt‐like caudomedial erector muscles (mnEPcm) that run both medial and lateral sides of the first‐row follicle to the next second‐row follicle in the same column, and (iii) a caudomedial depressor muscle (mnDP) that runs from the medial surface of the second‐row follicle to the lateral surface of the next first‐row follicle in the same column. A rotator muscle (mnRP) connects adjacent feathers in the same row.

Figure 4.

Overview of the forelimb skeleton (A) and musculature (B) in Columba livia. Right limb, dorsal view. Abbreviations as in Appendix 1.

Overview of feather tract musculature

The muscles and ligaments that interconnect the secondary feathers, their coverts, and the musculoskeletal elements of the forelimb (Figs 5 and 6) are generally congruent with the basic arrangement of non‐striated interfollicular erector and depressor muscles and tendons in avian skin (mm. pennarum, Fig. 3). The basic repeating elements consist of paired caudomedial erectors (mnEPcm), a caudolateral erector (mnEPcl), a caudomedial depressor (mnDP), and a medial rotator (mnRP). In the standard numbering system for feathers of the alar tracts, numbered columns of feathers follow an arc that begins at a secondary feather and ends at the marginal coverts of the leading edge of the wing. From the upper median coverts cranially, the next feathers in the same numbered column are attached to the first by mnEPcm and mnDP. The series of mnEPcm and mnDP arc from craniolateral to cranial as they continue along the numbered column. Feathers in the same row in adjacent columns are connected by rotators (mnRP). To complete the series, each feather receives a caudolateral erector (mnEPcl) from a feather one column medial and one row cranial from itself, and passes its own caudolateral erector to a feather in the next column lateral and one row caudal to itself.

Figure 5.

Overview of under coverts, remiges, and their attachments. (A) Under major coverts and ventral ligaments of the primary and secondary remiges. Under coverts are shown in red. (B) Secondary remiges, primary remiges, and the carpal remex. Primary and secondary remiges are shown in orange. Abbreviations as in Appendix 1.

Figure 6.

Overview of upper coverts and dorsal aponeurosis. (A) Upper major coverts, shown in yellow, and their muscular and ligamentous attachments. (B) Upper median coverts, shown in green, and the dorsal aponeuroses of the forearm and hand. Abbreviations as in Appendix 1.

Overview of secondary flight feathers and coverts

Upper minor and median secondary coverts

The upper minor and median secondary coverts (TSDmin and TSDmed) are attached to adjacent coverts by smooth muscle [mm. pennarum and median dorsal covert depressor (mnDTDmed), Figs 6B and 7]. On both the upper minor and median secondary coverts, bundles of smooth muscle run from the caudolateral aspect of the follicle sheaths. In more distal secondary feather columns (S3–S8), these bundles insert on adjacent caudal remigial papillae (PRC) one column lateral to their position (PRC2–PRV7) as dorsal ulnotectricial muscles (mnUTDmed, mnUTDmin, Figs 7, 8, 9). Similar bundles in proximal secondary feather rows (S9–S15) insert on the medial aspects of adjacent ventral remigial papillae (PRV) one column lateral to their position (PRV8–PRV14).

Figure 7.

Schematic showing interconnection of musculature and ligaments linking the marginal coverts with the upper coverts and secondary remiges. The region depicted in (A) is outlined on the forelimb skeleton in inset (B), and the position of the third secondary remex (S3) is highlighted in the wing silhouette shown in (C). Abbreviations as in Appendix 1.

Figure 8.

Oblique views of a single secondary remex attachment with adjacent coverts. (A) Wing silhouette showing the position of the third secondary remex; (B) caudolateral view; (C) caudomedial view.

Figure 9.

Cross‐sections of secondary remex and covert attachments. (A) Coronal section through S10–S11 calami, tip of S12 follicle. Note the prominent dorsal ulnotectricial muscles (mnUTDmaj12 and mnUTDmed12). Dashed line indicates fracture in ulna. (B) Coronal section through diastema (asterisk) and S6–S7 calami. The separate fiber tracts of an ulnoremigial ligament (LUR7) and a remigiotectricial aponeurosis/ventral ulnotectricial ligament (ARTV7) are apparent. Note also the distinct muscle fiber orientation of the remigial part of m. flexor carpi ulnaris, which is interposed between the major and median under coverts. (C,D) Adjacent coronal sections caudal to the ulnocarpal joint. These two sections show the attachment of ulnotectricial and ulnoremigial smooth muscle bundles (mnUTDmin3, mnUTDmed3, mnUR2) as well as a remigiotectricial aponeurosis (ARTV2) to the caudal remigial papilla (PRC2). (E–G) Schematics showing the position of sections (A–D). Scale bars: (A–D) 500 μm. Abbreviations as in Appendix 1.

Upper major secondary coverts and secondary remiges

Whereas the majority of follicles in the alar pterylae retain the rhombic spacing characteristic of other feather tracts, the upper major secondary coverts (TSDmaj) are displaced medially from the line of their column (Figs 6A–8). Upper major secondary coverts retain the erector and caudomedial depressor elements of mm. pennarum, but lack rotators or caudolateral depressors. In distal secondary feather rows (S2–S8), both the upper major secondary coverts and the secondary remiges bear ventromedially directed fibrous ligaments derived from their follicle sheaths that insert on the lateral aspect of the caudal ulnar papilla that corresponds to their column (Figs 6A and 7, 8, 9). The distal extent of each upper major covert follicle sheath is attached to its associated secondary remex follicle sheath by a fibrous caudal secondary remigiotectricial ligament (LRTSca) on the medial side and a non‐striated secondary remigiotectricial muscle (mnRTS) on the lateral side (Figs 6A, 8, and 10B).

Figure 10.

Cross‐sectional views of the dorsal aponeurosis of the forearm and minor interremigial ligament. (A) Coronal section showing position of ADA relative to upper minor and marginal coverts. (B) Coronal section through S3–S4, showing proximodistal differences in the junction of ARTV and LIRmin. ARTV4 shows the proximal, ventrolaterally‐oriented ARTV, S3 shows the reflection to ventro‐medial orientation caudal to LIRmin. (C) Schematic showing the position of sections (A,B).

Dorsal aponeurosis of the forearm and cubital limiting ligament

The dorsal aponeurosis of the forearm (ADA) extends from digitations that arise from the cranial tips of secondary remex follicles, across the surface of ulnar extensor musculature, running between these muscles and the upper coverts (Figs 6B and 10A). At its proximal cranial edge, the ADA terminates in loose connective tissue at the caudal margin of m. brachialis (mB). At a more distal position, roughly in line with S11, the ADA becomes confluent with the cubital limiting ligament (LLC). At the distal end of m. supinator, the ADA inserts directly on the exposed dorsal surface of the radius for a short distance, then continues with a termination in loose connective tissue along the caudal margin of m. extensor longus alulae (mELA, Fig. 4B). As the ADA crosses the distal end of the radius, it passes over the tendon of mELA and inserts on the cranial side of sulcus tendinosus on the radius. From this insertion, the ADA continues distally as the dorsal aponeurosis of the hand (ADC).

The sheet‐like aponeurosis of the cubital limiting ligament begins primarily at m. tensor propatagialis pars caudalis (mTPca), with a thin sheet extending to m. tensor propatagialis pars cranialis (mTPcr). Caudally, the LLC fuses with ADA and cannot be distinguished at a histological level.

Secondary remiges, under major secondary coverts, and underlying skeletal muscle

Secondary remiges attach to their respective under major coverts (TSVmaj) by a broad ventral remigiotectricial aponeurosis (ARTV) that forms a pouch along the lateral side of the secondary follicle (Figs 4A, 8, and 9). In most secondary remiges (S2–S12), a remigial fat body (CARs) fills this pouch and other parts of their follicle sheath, and a smaller fat body surrounds the cranial tip of the associated under major covert. The cranial tips of under major covert follicles lie close to the ventral remigial papillae for most positions, and a continuation of the ventral remigiotectricial aponeurosis forms a ventral ulnotectricial ligament (LUTv) which attaches to the ventral remigial papillae. The distance between ventral ulnotectricial ligament attachment and ulnoremigial ligament attachment at each secondary remex position decreases from proximal to distal, running in line with the dorsal margin of m. ulnometacarpalis ventralis (mUV, Fig. 8).

Digitations from the dorsal limb of the humerocarpal septum (SH, Figs 4 and 7), an aponeurosis that extends dorsocaudally from m. flexor digitorum superficialis (mFDS), blend into the ventral ulnotectricial ligaments and ventral remigiotectricial aponeuroses (SHDR, Figs 8 and 9). The distal extent of each ventral remigiotectricial aponeurosis continues to attach to a distinct remigial part of m. flexor carpi ulnaris (mFCUr) along the insertion tendon of the pennate muscle belly (LIRmin, Figs 8 and 10). The thickened edge of the mFCUr insertion tendon bears the NAA name l. elasticum interremigale minor (Baumel & Raikow, 1993). Histological examination of this structure shows that, in pigeons, it is primarily composed of collagen fiber bundles, with only isolated regions of elastic tissue (Fig. 10B). The distal extents of the secondary remex follicles are interconnected by slips of the major elastic interremigial ligament (LIRmaj, Fig. 5B), which is visible in non‐polarized light but lacks the birefringent contrast characteristic of collagenous or muscular structures under polarized light.

Regional differences in secondary remex attachment

1st secondary remex

The first secondary remex (S1) is attached to the marginal coverts of the forearm through the first upper major and median secondary coverts (Fig. 6). S1 sits directly on the proximal ends of m. ulnometacarpalis dorsalis (mUD, Fig. 5B). The mUD splits into three heads – dorsal (mUDd), ventral (mUDv), and caudal (mUDca). An accessory ligament of mUDca (LmUD) runs from the minor metacarpus to sulcus tendineus of the ulna. The follicle sheath of S1 attaches in part to this accessory ligament. Where the follicle sheath of S1 crosses over the split between mUDd and mUDv, it attaches to the ulnare by a short ligament that runs between the two muscle heads (Fig. 9C). A thin slip of ligament from the S1 follicle sheath continues to the septum humerocarpale and the ventral remigiotectricial aponeurosis of S2. The distal extent of the S1 follicle sheath is attached to the carpal remex (C) by a continuation of the major elastic interremigial ligament.

2nd–8th secondary remiges

In the distal secondary remiges aside from S1, the ulnotectricial muscles of the upper median and minor coverts mUTmin and mUTmed pass ventrolaterally to insert on the caudal remigial papillae associated with the next most distal secondary feather (Figs 7, 8, 9C,D). In addition to these muscles, a robust ulnoremigial ligament (LUR) from the secondary remex and a dorsal ulnotectricial ligament (LUTd) from the upper major covert pass medially and ventromedially, respectively, to attach on the lateral side of the caudal remigial papilla associated with that secondary position (Figs 8 and 9B). Small bundles of smooth muscle (mnUR) arise from the ventral surfaces of the secondary follicles and insert on the caudal ventral papillae adjacent to the insertions of LUR (Fig. 9B). The attachments of the ventral remigiotectricial aponeuroses of S1–S4 to the remigial part of m. flexor carpi ulnaris are initially inclined ventrodistally, pointing towards the ulnare. As the attachment continues caudally to the distal end of the under major covert follicle, the collagenous insertion tendon of mFCUr gives way to an elastic region, and the ventral remigiotectricial aponeurosis attachment takes on a ventromedial orientation, pointing towards the elbow joint (Fig. 10B).

Diastema

The fifth secondary remex is absent in pigeons (diastaxy). The spacing of upper major and under major coverts 4–6 remains consistent (Figs 5A, 6B, and 9B). The fifth upper major and under major coverts are connected by a pattern of smooth muscle typical of the mm. pennarum‐derived remigiotectricial ligament of the upper major covert. The fifth upper major covert has a small dorsal ulnotectricial ligament (LUTd5) that attaches to a faint caudal remigial papilla (PRC5).

9th–15th secondary remiges

More proximal secondary positions show a gradient from reduction in the diameter of ulnoremigial and dorsal ulnotectricial ligaments to the apparent absence of these ligaments proximal to S10. With the absence of ulnoremigial ligaments, the closest skeletal attachment for proximal secondaries is through ventral remigiotectricial aponeuroses to ventral remigial papillae (Fig. 9A). The insertion sites of the ulnotectricial muscles of the upper median and minor coverts (mnUTDmed, mnUTDmin) also shift, from caudal remigial papillae in the distal secondaries, to ventral remigial papillae in the proximal secondaries.

The digitations of the ADA to secondary remiges become more indistinct medial to the axis of the cubital limiting ligament, and are not discernible for secondaries S11–S15. The remigiotectricial muscles of the upper major coverts (mnRTS) decline from a directly ventral orientation in the distal secondaries to ventromedial in the proximal secondaries. While the proximodistal position of these muscles remains similar across the row of secondaries, a proximad reduction in secondary remex follicle length brings the major elastic interremigial ligament position from distal to approximately even with the upper major covert remigiotectricial muscles (Fig. 6A). A separate belly of smooth muscle, the m. expansor secondariorum (mnES, Fig. 4B), arises from the tendon of m. coracotriceps to insert on the follicle sheaths of S12–S15.

Primary flight feathers and coverts

The connective tissues that sheath the carpal remex and the primaries show several interconnections (Figs 11C and 12A). This set of features defies easy separation by individual feathers or skeletal elements, and in places the distinction between ligament, tendon, and dermis is ambiguous. The names proposed here are based on major patterns of connection between and among the carpometacarpus, phalanges, primary remiges, and their associated dorsal and ventral tectrices.

Figure 11.

Overview of under coverts and proximal primaries on the carpometacarpus. The area depicted in (A) and (C) is outlined on the forelimb skeleton in (B), and the proximal primaries are highlighted on the wing silhoutte in (D).

Figure 12.

Upper coverts (A) and dorsal aponeurosis (B) on the carpometacarpus.

In contrast to the extensive pterylae of the forearm that possess several rows of marginal coverts, the dorsal pterylae of the hand are relatively sparse, consisting of an upper major and an incomplete upper median covert series immediately joined to a patch of marginal coverts that covers the leading edge of the hand‐wing. Both the classical numbering scheme and the orientation of the feather arcade are reversed from the forearm – the upper major primary coverts are displaced laterally from their associated primaries, and the upper median coverts, when present, lie directly dorsal to the follicles of the primary feathers. The upper major primary coverts are interconnected by a cranial intertectricial muscle (mnITDcr) at their cranial extent, and a caudal intertectricial muscle (mnITDca) in line with the minor metacarpus, both composed of smooth muscle fibers (Fig. 12A). A dorsal aponeurosis of the hand (ADC) continues from the ADA. In contrast to ADA, the ADC rides over the top of the upper major coverts and extends caudally along their follicle sheaths to the same extent as the caudal margin of the carpometacarpus and digits (Figs 6B and 13D).

Figure 13.

Cross‐sections of proximal primary attachments. (A) Coronal section through P1–P2 calami, tip of P3 follicle. Note the prominent cranial metacarporemigial ligaments (LMRcr), as well as the tendon sheath surrounding the tendon of m. extensor longus digiti majoris (tmELDM). (B) Coronal section through the calami of P1–P4, at the level of the minor metacarpus (MCIII). Note the position of the dorsal carpal aponeurosis (ADC) with respect to the upper major coverts (TPDmaj), the prominent caudal metacarporemigial ligaments (LMRca), and the robust ulnocarporemigial aponeurosis (AUR). (C) Coronal section through P1–P3 calami, at the level of the caudal head of m. ulnometacarpalis dorsalis. Remigial slips of the same muscle insert on the ventral surfaces of primary follicle sheaths (mUDcap). (D) Coronal section through P1–P3 calami just caudal to mUDca. Two slips from each segment of the ulnocarporemigial retinaculum are visible: one that extends caudally along the ventral surface of each remex, and another that wraps dorsolaterally around the associated upper major covert. (E–G) Schematics showing the position of sections (A–D). Scale bars: (A–D) 1 mm.

Attachments of the alular feathers are not well‐represented in the histological series, but from available material it can be seen that they interconnect and attach to the alula by prominent bands of smooth muscle.

Carpal remex

The carpal remex (C) receives a continuation of the cranial intertectricial muscle from the first upper major covert. The follicle sheath of the carpal remex attaches to the accessory ligament of m. ulnometacarpalis dorsalis pars caudalis (Fig. 11). The orientation of the upper major carpal covert is more consistent with that of the adjacent upper major secondary coverts than the remaining upper major primary coverts (Fig. 12B).

Overview of proximal primary remiges

The five most proximal primary remiges are attached entirely to the carpometacarpus and its associated musculature (Fig. 11B). An expansion and thickening of the follicle sheaths (LMRca) attaches these feathers to the accessory ligament of mUDca (P1–P2) or the minor metacarpus (P3–P5, Fig. 13B).

The ventral aspect of the hand is covered by the prominent ulnocarporemigial aponeurosis (AUR), which is continuous with the distal end of the humerocarpal septum in the forearm, and shares an attachment on crus longum of the ulnare (Fig. 13A–C). The cranial portions of lower major primary covert follicles 1–6 (TPVmaj 1–6) are attached to the ulnocarporemigial aponeurosis by short digitations that split ventrally from the aponeurosis on the proximal side of each follicle and attach to that follicle's ventral surface (Fig. 13C). Longer digitations from the ulnocarporemigial aponeurosis continue onto the ventral surfaces of the P1–P5 as ulnocarporemigial retinacula (RUR, Fig. 13D) and continue around the lateral surface of these follicles to insert on upper major primary coverts 1–5 (TPDmaj1–5). Slips of skeletal muscle from the caudal margin of mUDca attach directly to P1–P5 follicle sheaths with the RUR (mUDcap, Fig. 13C). P1–P5 follicles are interconnected distally by two bands of smooth muscle. The more proximal of these, the dorsal carpal interremigial muscles (mnIRCd), also attach to the ventral surfaces of the upper major primary covert follicle sheaths. The ventral surfaces of P1–P5 are interconnected further distally by straight ventral carpal interremigial muscles (mnIRCv).

Dorsal aponeurosis of the hand

The dorsal aponeurosis of the hand has a prominent attachment complex to the major metacarpus that ranges from an area just distal to the supratrochlear fossa to the intermetacarpal process. This complex serves as a sheath for the tendon of m. extensor longus digit majoris (tmELDM, Fig. 13A) and provides a short vinculum for the tendon of m. extensor metacarpi ulnaris (tmEMU, Fig. 11A). Distally, a thin attachment of the cranial edge of the ADC to the dorsal surface of the major metacarpus continues to wrap cranially around head of the major metacarpus, forming a sheath for the tendon of m. extensor digitorum communis (tmEDC), and inserting on the proximal phalanx of the major digit. A thickened cord of the ADC (RDDM) continues across the dorsal surface of the metacarpophalangeal joint and onto the craniodorsal surface (pila cranialis) of the proximal phalanx of the major digit (Fig. 14A).

Figure 14.

Under coverts, ventral ligaments, and distal primaries on the major and minor digits. The area depicted in (A) and (C) is outlined on the forelimb skeleton in (B), and the distal primaries are highlighted on the wing silhouette in (D).

1st–3rd primary remiges

The follicle sheaths of P1–P3 project across the dorsal surface of the major metacarpus. These three primary remiges share a prominent attachment in the ADC at the position of the tendon sheath of mELDM (LMRcr, Figs 11C and 13A). Each remex bears a fat pad (CARp) positioned laterally between the remex follicle and major metacarpus. Carpal interremigial ligaments (LIC) arise from the ventral surfaces of the fat pads of P1–P2 and pass cranially to the dorsal surfaces of P2–P3 (Fig. 13A). Upper median coverts are absent for these remex positions.

4th–5th primary remiges

P4–P5 are connected to TPDmaj 3 and TPDmaj4, respectively, by belts of ligament that surround each remex–covert pair (LRTPcr, Fig. 12A). A prominent fat pad in P4 extends laterally between TPDmaj4 and the major metacarpus. TPDmed 4 and 5 attach to TPDmaj 3–5 with the standard complement of mm. pennarum.

Overview of distal primary remiges

The follicles of P6–P10 have their most prominent skeletal attachments to digits II and III. All show prominent caudal phalangoremigial ligaments (LPRca) that extend in a helix from ventral to medial to dorsal around the follicle (Fig. 14B). The associated upper major coverts have similar and more robust caudal phalangotectricial ligaments (LPTca). P6–P10 also bear ventral phalangoremigial ligaments (LPRv) that extend from their skeletal attachments in a manner similar to ulnoremigial retinacula of P1–P5 (Fig. 14A). Like P4–P5, P6–P10 are attached to the next most medial TPDmaj by a belt‐like LRTPcr (Fig. 15A). Distally on the follicles of P6–P10, near the tapered end of the caudal phalangoremigial ligament, a short band of smooth muscle attaches TPDmaj6–TPDmaj10 to their respective primaries (mnRTD, Fig. 15B). The positions of mnRTD are similar to the medial halves of mnIRCd on P1–P5. The remaining units of smooth muscle form oblique interremigial muscles (mnIRo) from the dorsal surfaces of P6–P9, across the ventral surfaces of TPDmaj6–TPDmaj9, then down to the dorsal surfaces of TPVmaj7–TPVmaj10 and the ventral surfaces of P7–P10 (Fig. 14B).

Figure 15.

Upper coverts (A) and dorsal aponeurosis (B) on the major and minor digits.

Dorsal cord of the dorsal aponeurosis

The ADC continues from the carpometacarpus with a thickened dorsal cord (RDDM) across pila cranialis of the major digit proximal phalanx (Figs 14A and 16A,B). The thinner aponeurosis continues as well, extending cranially from RDDM across a fat pad to attach to tmELDM as a vinculum, and from there to insert on tendon sheaths of m. flexor digitorum superficialis (mFDS) and m. flexor digitorum profundus (mFDP). The aponeurosis also extends caudally from RDDM over the tendon sheath of m. interosseus dorsalis (mID), and across the dorsal surfaces of TPDmaj7–10 (Fig. 16B–E). The RDDM itself inserts in the dorsal aspect of the distal phalanx of the major digit, in between the insertions of tmELDM cranially and tmID caudally.

Figure 16.

Cross‐sections of distal primary attachments. (A–F) ≈ Parasagittal sections through the major and minor digits (II‐1, II‐2, III). Interconnections of the dorsal cord of the dorsal carpal aponeurosis are visible in (A–E). Positions of dorsal and ventral interossei tendons relative to adjacent follicles are visible in (A–F). (G,H) Schematics showing the position of sections (A–F). Scale bars: (A–F) 500 μm.

Ventral interosseous muscle

The tendon of m. interosseus ventralis (tmIV) passes along the caudal aspect of the proximal phalanx of the major digit, encased in a tendon sheath that forms a prominent attachment site for the cranial phalangoremigial and ventral phalangotectricial ligaments (LPRcr and LPTv, Figs 14B, 15A, and 17). Despite its close proximity to feather attachments, the tendon itself does not share fibers with any of the phalangoremigial or phalangotectricial ligaments until its insertion on II‐2, at most passing over a fold in the caudal phalangotectricial ligament of TPDmaj10 that forms a guide for the tendon between the proximal and distal phalanges of the major digit (Fig. 17D,E).

Figure 17.

Characteristic arrangements of ligamentous sheets around distal primary remiges and tectrices. These include the belt‐like cranial primary remigiotectricial ligaments (LRTPcr, A), strap‐like ventral intertectricial ligaments (LITv, B), and oblique interremigial smooth muscles (mnIRO, C). Scale bars: 500 μm.

6th–7th primary remiges

The caudal and ventral phalangoremigial ligaments of P6–P7 arise from the ventral surface of digit III (Figs 14A and 16B). The proximal end of the follicle sheath of P6 sits on the surfaces of mID and mIV. The proximal follicle sheath of P7 sits across the metacarpophalangeal joint. Where the cranial end of the P7 follicle abuts skeletal elements, it is surrounded by a fat body (CARp7, Fig. 16A). Just distal on P7 to the belt‐like LRTPcr with TPDmaj6, an open sling of ligament runs from TPDmaj6, under P7, up to the ventral surface of TPDmaj7 as a ventral intertectricial ligament (LITv, Fig. 15A). Distal to LIT, P7 bears a cranial phalangoremigial ligament formed from expansion of the follicle sheath, similar to the metacarporemigial ligaments of P1–P5, that attaches to the caudomedial edge of the major digit of the proximal phalanx.

8th–9th primary remiges

The cranial ends of P8–P9 sit within fat pads that fill the dorsal fossae (FRP, FRD) of the major digit (Figs 14A and 18A,B). P8 and P9 follicles each bear a cranial phalangoremigial ligament that attaches to the tendon sheath of mIV as it crosses the caudal edge of the major digit proximal phalanx. TPDmaj8 and TPDmaj9 each bear both belt‐like LRTPcr (Fig. 18A) and sling‐like LITv (Fig. 18B). Just distal to these ligaments, TPDmaj8 and TPDmaj9 each bear a continuous sheet of cranial phalangotectricial ligament (LPTcr) on their ventral surfaces. For both tectrices, the sheet runs obliquely beneath the follicle from craniomedial, to directly ventral, to caudolateral (Fig. 14A). The caudal and ventral phalangoremigial ligaments of P8 (Fig. 18B), along with the caudal phalangotectricial ligament of TPDmaj8, arise from the caudal surface of the proximal phalanx of the major digit at the caudal extent of pila obliqua (the ridge between the dorsal fossae). The caudal phalangoremigial ligament of P9 arises from the tendon sheath of mIV on the internal index process of the major digit. The ventral phalangoremigial ligament of P9, and the caudal phalangotectricial ligament of TPDmaj9, arise from a common attachment on the ventral surface of the internal index process (Fig. 17C).

Figure 18.

Course of the ventral interosseous muscle tendon. (A–E) The position of the tmIV relative to the caudal margin of II‐1 (A, B), the internal index process (IIP, C), and the caudal phalangoremigial ligament of the 10th primary (asterisk).

10th primary remex

Unlike P6–P9, P10 bears a very thin fat pad, along with thin axial sheets of ligament that run from the distal phalanx of the major digit to the circumference of the follicle, in parallel with axes of supination and pronation (Fig. 16F). The caudal phalangoremigial ligament of P10 runs craniomedial to caudolateral beneath the tendon of mIV before arcing dorsally to insert on the dorsal surface of the remex. P10 also bears a very prominent interphalangoremigial ligament (LIPR) that arises from both the proximal and distal phalanges at the caudal edge of the interphalangeal joint surface. The ventral distal phalangoremigial ligament of P10 is confluent with fibers at the insertion of tmIV. P10 is attached to TPDmaj9 by a belt‐like LRTPcr, but does not bear a sling‐like intertectricial ligament to TPDmaj10.

Discussion

Smooth muscle function in bird wings

The extensive distribution of smooth muscle in pigeon flight feather attachments is surprising but not without precedent in other avian taxa (Lucas & Stettenheim, 1972). The seemingly antagonistic arrangements of fiber bundles attached to flight feathers raises the question of whether smooth muscle contractions provide active control of wing shape during flight. Smooth muscle fibers typically show long latency between stimulation and force generation, and shortening velocities an order of magnitude slower than skeletal muscle (Murphy et al. 1997). The smooth muscle of m. expansor secondariorum shows a relatively rapid response to stimulation (Golenhofen & Petry, 1968), but even this rapid response is not within the ~ 8‐Hz range necessary to match pigeon wingbeat frequency (Dial, 1992). Given these conditions, it would not seem plausible for positive work produced by the ulnotectricial or interremigial muscles to contribute to phasic changes in wing shape synchronized to flight stroke. It is more likely that the smooth muscles observed here are involved in tonically maintaining wing postures (e.g. folded‐wing posture at rest). This does not rule out the possibility that they may also produce net positive work over several wingbeat cycles in flight to tune the stiffness of musculoelastic linkages, thus influencing wing shape.

Available evidence suggests that the innervation of mm. pennarum is entirely adrenergic (Jeikowski & Drenckhahn, 1981). This leads to the intriguing possibility that a graded progression between the smooth muscle contributions to two extremes of flight feather posture (e.g. at rest vs. fully extended) could be accomplished by varying the expression of α₁ (excitatory) and β₂ (inhibitory) adrenergic receptors between antagonistic groups of smooth muscle. Such a system could be likened to setting the positions of slats and flaps on an airplane wing with a single control input, in this case sympathetic tone, with ‘trim’ available over a longer time period by altering receptor expression patterns.

Remex–covert interconnections

Prior assessments of flight feather attachment have focused on the remiges, at most illustrating the position of upper and lower major coverts (Robin & Chabry, 1884). The unique attachments of upper median and minor secondary coverts to the remigial papillae of the ulna, the dense interconnections between primary remiges and upper major primary coverts, and the independent attachments of upper major primary coverts to the major digit, all suggest that covert feathers play a more important role in forming a coordinated wing surface than previously appreciated. This echoes the findings of a recent morphometric investigation of wing shape variability across extant birds (Wang & Clarke, 2015). The morphometric analysis found that after controlling for phylogeny, a common trend in the extent of dorsal and ventral primary coverts was the greatest source of shape variability in extended wings. The functional significance of covert feathers in extant birds has received only scant interest (Petrides, 1943), leaving a fairly open field for experimental studies of the aerodynamic significance of covert structure.

Flight feather arthrology and wing folding

Relative motions of musculoskeletal components during the passive coordination of flexion and extension have been well characterized (Vazquez, 1994, 1995; Brown et al. 1995). The expected motions of flight feathers in this system can be mapped out by considering the movements of their points of attachment during extension (Table 1). These are speculative relationships, and should be regarded as working hypotheses.

Table 1.

Attachment points of remiges in Columba and their expected response to coordinated forelimb extension

Remex	Cranial attachment	Pivot	Caudal attachment	Expected action on elbow extension
S9–S15	Coverts via mm. pennarum	Caudal ulnar papillae	Flexor carpi ulnaris, expansor secondariorum	Initial: abduction, elevation; Final: abduction, depression
S2–S8	Dorsal aponeurosis, cubital limiting ligament	Caudal ulnar papillae	mFCUR	Abduction
P1–P5	Dorsal aponeurosis	Accessory ligament of mUDca, minor metacarpal	Caudal edge of mUDca	Adduction
P6	mID perimysium	mIV perimysium	Flexor process digit III	–
P7	Fat pad in metacarpophalangeal joint	Tendon sheath of mIV	Ventral surface, tip of digit III	–
P8–P9	Fat pads in dorsal fossae	Tendon sheath of mIV	Caudal and ventral surface, proximal phalanx digit II	–
P10	Fixed to distal phalanx digit II	None	Caudal and ventral surface, distal phalanx digit II	–

As the radius retracts relative to the ulna in limb extension, the cranial edge of the ADA retracts with it. The LLC contributes craniomedial tension during the same motion. This action is expected to pull the tips of the secondaries medially or craniomedially, depending on whether the pivot point is around the dorsal ulnar papilla (with lengthening of the ulnotectricial muscles) or within the sling formed by the ulnotectricial muscles and the ulnoremigial ligament (isometry of ulnotectricial muscles). The ventral remigiotectricial aponeuroses and ulnotectricial ligaments, in their attachment to the ulna, are expected to constrain the joint axis to a plane of abduction and adduction (Fig. 19).

Figure 19.

Schematic view of the relationship of secondary abduction (A) and adduction (B) with ulnar extension and flexion.

As the highly elastic propatagium lengthens during forelimb extension, the rhomboid network of feather muscles that connect the marginal coverts will be stretched mediolaterally, applying medially directed tension to the upper coverts of the distal secondary remiges. This same motion is expected to contribute to a craniocaudal shortening of the network near the proximal secondaries, potentially applying cranially directed tension to the secondary coverts in this region. As the proximal coverts have poorly developed or absent ulnoremigial ligaments and dorsal ulnar papillae, this tension is expected to result in an abduction and/or elevation moment of the proximal secondaries, which, as above, are restrained by the ulnotectricial and ventral ulnoremigial ligaments.

Although reversal of these mechanisms is expected to occur passively with flexion at the elbow joint, the smooth muscle tissue of m. expansor secondariorum and the ulnotectricial muscles of the upper median and minor secondary coverts may also play a role in tonic adduction of the secondary remiges at rest. Shortening of m. expansor secondariorum is expected to adduct S15–S12. Shortening of the ulnotectricial muscles associated with the proximal secondary rows (S9–S15) is expected to pull and hold the cranial ends of the secondaries and their upper major coverts ventrolaterally. Shortening of the ulnotectricial muscles associated with the distal secondary rows (S2–S8) is expected to pull and hold the cranial ends of the secondaries and their upper major coverts laterally. Although both of these actions are synergistic with the general sense of passive adduction, they may also provide an energetically efficient means for maintenance of a folded‐wing posture, in concert with postural mechanisms that have been proposed for the shoulder joint (Meyers 1992).

Extension of the elbow joint is passively coupled with extension of the ulnocarpal and carpo‐carpometacarpal joints. This extension pulls the insertion tendon of m. flexor carpi ulnaris distally. Because the insertion tendon lies on the external surface of this pinnate muscle, the associated attachments of the major under coverts and secondary remiges are pulled distally as well. Combined with medial or craniomedial movement of the tip of the secondary remiges, this initial extension is expected to result in abduction of the secondaries, independent of their interconnection through the major interremigial ligament. The finding that ex vivo limb extension abducts the secondaries, even after the major interremigial ligament has been severed (Stettenheim, 1959), is congruent with this mechanism.

Continued extension of the limb tenses the mFCU and, as noted by Sy (1936), the mFCU bowstrings ventrally when the limb is fully extended, aligning the mFCUr to pull the proximal secondaries ventrally. Depression of the proximal secondaries would result in root‐to‐tip washout in the airfoil, similar to that seen in propeller blades, where the wing's ‘angle of attack’ (in reference to purely morphological axes, not necessarily with respect to airflow) decreases from proximal to distal. Washout is especially relevant to low‐speed flapping flight, where the wing root and wingtip are required to maintain attached flow at very different airspeeds. The ability to alter washout may be part of the extraordinary ability of birds to maintain attached flow across a range of flight speeds (Shyy et al. 2013).

The humerocarpal septum, an aponeurotic extension from mFDS, inserts on the ulnare (Baumel & Raikow, 1993) along with mFCU and the ulnocarporemigial aponeurosis. As with mFCU, extension of the ulnocarpal joint pulls the humerocarpal septum distally. This action is expected to apply a ventrodistally oriented tension to the ventral ulnoremigial and ulnotectricial ligaments, and may stabilize or modify the axis of secondary abduction/adduction.

Extension of the ulnocarpal joint lengthens mUDca. Because the fibers of this muscle do not uniformly terminate on an insertion tendon, but instead extend to the follicles of the proximal primary remiges, the expected effect on the remiges is medially directed tension that is most pronounced in the shortest, proximal fibers, and least pronounced in the longest, distal fibers. Lengthening of the mUDca is also expected to medially retract the accessory ligament that carries the caudal metacarporemigial ligament of the first primary. Considering the extent and position of the fat pads of P1–P4, the cranial metacarporemigial ligaments may allow more mobility than the caudal metacarporemigial ligaments, setting pivot points for the proximal primaries near the caudal edge of the minor metacarpal. The net effect of extension on the proximal primaries is expected to be a graded adduction, most pronounced on P1 and resulting in minimal movement of P5 (Fig. 20).

Figure 20.

Schematic view of the relationship of proximal primary abduction (A) and adduction (B) with carpometacarpal extension and flexion.

The metacarpophalangeal and interphalangeal joints are not considered to be passively linked to elbow joint extension (Vazquez, 1994). Abduction and adduction of the distal primary remiges is, in this sense at least, mechanically uncoupled from flexion and extension of the forelimb. The range of flexion and extension of the major digit phalanges is limited – the proximal phalanx can flex over an ~ 30° range, the distal phalanx over ~ 35° (Vazquez, 1995). Because the entire length of the phalanx of the minor digit is closely attached to the proximal phalanx of the major digit, it is assumed that its range of motion does not exceed that of its neighbor. When taken over the multiple elements to which the distal primaries attach, this range can still account for the graded abduction necessary to completely fan P6–P10 relative to P5 (~ 60°) with only slight motion of each remex on its skeletal attachments (Fig. 21). Flexion and extension of the digits may thus directly control folding and unfolding of the wingtip without the need for input from more proximal flight feathers. In addition, bundles of smooth muscle at the proximal and distal extent of each primary remex follicle may contribute to distal primary abduction/adduction, either in concert with the skeletal muscles or by themselves.

Figure 21.

Schematic view of the relationship of distal primary abduction (A) and adduction (C) with extension and flexion. Also shown are arrangements of ligament and muscle that may contribute to rotational stability during abduction (B) and the ability to passively supinate during adduction (D).

Flight feather arthrology and flight stroke

Prior considerations of wing folding and unfolding have ascribed varying degrees of importance to the major elastic interremigial ligament, either as a major determinant or an important accessory to flight feather coordination (Pelissier, 1923; Raikow, 1985). The major elastic interremigial ligament has often been interpreted to be composed of elastic tissue along its entire length, including the primaries (Pelissier, 1923), which limits its action to passive redistribution of tension along the entire row of flight feathers as they are abducted by the distal primaries, and elastic return to a fully folded position. The finding that the band of tissue joining the primary feathers at the distal extent of the follicle is composed of smooth muscle in pigeons (as observed in Gallus and Meleagris; Lucas & Stettenheim, 1972), together with the uncoupling of P6–P10 from forelimb extension, provides much more scope for active control of wingtip shape.

The differences in wingtip shape that accompany different flight speeds (Tobalske & Dial, 1996; Tobalske et al. 2003; Tobalske, 2007) could conceivably arise from somatic neuromotor control of the digital flexors and extensors, autonomic control of the oblique interremigial muscles that link P6–P10, or some combination of these two. Pigeons are able to maintain kinematically normal level flight at 7–8 ms⁻¹ after the radial and medioulnar nerves have been severed, blocking all somatic (and presumably autonomic) motor control past the elbow joint, but they lose the ability to take off without assistance and perform coordinated landings (Dial, 1992), maneuvers that would normally be accomplished with an inverted‐tip upstroke.

Some avian taxa use a flexed‐wing or feathered upstroke pattern across all recorded flight speeds, most notably passeriform taxa (Tobalske et al. 2003; Tobalske, 2007). Wing aspect ratio has been singled out as a potential correlate to this kinematic pattern, as the taxa that maintain a prominent flexed‐wing upstroke across their flight speed range also have short, rounded wingtips, whereas taxa that vary upstroke kinematics and wingtip shape tend to have long, pointed wingtips. Galliform birds (e.g. Meleagris) are an exception to this pattern (Tobalske & Dial, 2000). The tissue composition of interremigial ligaments in passeriform and birds has yet to be investigated, but the presence and complexity of smooth muscle bundles between the primary remiges noted in Meleagris by Lucas & Stettenheim (1972) raises the possibility that the ability to generate lift across a range of upstroke kinematics is facilitated by the ability to change the length of smooth muscle bundles, and hence the length/tension properties of the musculoelastic links that govern abduction and torsion in the distal primaries. The pattern of varying upstroke kinematics across living birds may be the result of evolutionary developmental constraint on the architecture of distal primary feather musculature.

Conclusions

The skeletal and soft tissue structures that link the flight feathers to the forelimb in rock pigeons provide an anatomical basis for coordination of flight feather position, both at rest and during flight, that is tied into previously described musculoskeletal mechanical linkages in the forelimb. The pattern of ligaments and muscles that attach the secondary flight feathers to the ulna can be readily reconciled with the primitive pattern of mm. pennarum in feathered skin. An unexpected concentration of smooth muscle tissue around the flight feathers suggests tonic autonomically regulated control of wing shape. Whether this control occurs during rest, in flight or both remains to be seen, but this finding opens an entirely new line of inquiry for the study of avian flight control. The structures described here provide targets for in vivo kinematic and strain studies of wing coordination, providing a new meeting point for anatomical and experimental studies of flight.

Appendix 1. Anatomical terms and abbreviations. Unless otherwise noted, terminology follows Nomina Anatomica Avium (Baumel, 1993)

Anatomical term	Abbreviation
Aponeurosis dorsalis antebrachii	ADA
Aponeurosis dorsalis carpalis a	ADC
Aponeurosis remigiotectralis ventralis a	ARTV
Aponeurosis ulnocarpo‐remigialis	AUR
Aponeurosis ventralis antebrachii	AVA
Corpus adiposum remigale primarii a	CARp
Corpus adiposum remigale secondarii a	CARs
Fossa remigalis distalis a	FRD
Fossa remigalis proximalis a	FRP
Ligamentum (L.) collaterale ventrale	LCV
L. elasticum interremigale major	LIRmaj
L. Interphalangoremigalis	LIPR
L. interremigale carpalis caudalis a	LICca
L. interremigale carpalis cranialis a	LICcr
L. interremigale minor	LIRmin
L. intertectricale dorsale	LITd
L. intertectricale ventrale	LITv
L. limitans cubiti	LLC
L. metacarporemigialis caudalis a	LMRca
L. metacarporemigialis cranialis a	LMRcr
L. musculus ulnometacarpalis dorsalis	LmUD
L. phalangoremigalis caudalis a	LPRca
L. phalangoremigalis cranialis a	LPRcr
L. phalangoremigalis ventralis a	LPRv
L. phalangotectricalis pars caudalis a	LPTca
L. phalangotectricalis pars cranialis a	LPTcr
L. phalangotectricalis pars ventralis a	LPTv
L. propatagiale	LP
L. remigiotectricalis carpalis cranialis a	LRTCcr
L. remigiotectricalis primarius a	LRTPcr
L. remigiotectricalis secundarius caudalis a	LRTSca
L. remigiotectricalis secundarius cranialis a	LRTScr
L. ulnoremigialis a	LUR
L. ulnotectricalis dorsalis majoris a	LUTd
L. ulnotectricalis ventralis	LUTv
Muscularis (M.) adductor alulae	mAA
M. adductor digiti majoris	mADM
M. anconeus	mA
M. biceps brachii, pars propatagialis	mBBp
M. brachialis	mB
M. deltoideus major	mDM
M. depressor tectricalis secundarius dorsalis medius	mDTDmed
M. extensor brevis alulae	mEBA
M. extensor brevis alulae, pars caudalis	mEBAca
M. extensor brevis alulae, pars cranialis	mEBAcr
M. extensor carpi radialis	mECR
M. extensor carpi radialis, caput dorsalis	mECRD
M. extensor carpi radialis, caput ventralis	mECRV
M. extensor digitorum communis	mEDC
M. extensor longus alulae	mELA
M. extensor longus digiti majoris	mELDM
M. extensor longus digiti majoris, pars brevis	mELDMb
M. extensor metacarpi ulnaris	mEMU
M. flexor carpi ulnaris	mFCU
M. flexor carpi ulnaris, pars remigialis	mFCUr
M. flexor digit minimi	mFDM
M. flexor digitorum profundus	mFDP
M. flexor digitorum superficialis	mFDS
M. humerotriceps	mHT
M. interosseus dorsalis	mID
M. interosseus ventralis	mIV
M. nonstriatus (n). depressor pennae	mnDP
M. n. erector pennae lateralis	mnEPcl
M. n. erector pennae medialis	mnEPcm
M. n. expansor secondariorum	mnES
M. n. interremigale carpalis, pars dorsalis a	mnIRCd
M. n. interremigale carpalis, pars ventralis a	mnIRCv
M. n. interremigale obliquusa	mnIRO
M. n. intertectricale dorsale caudale	mnITDca
M. n. intertectricale dorsale craniale	mnITDcr
M. n. remigiotectricalis primarius a	mnRTP
M. n. remigiotectricalis secondarius caudalis a	mnRTSca
M. n. rotator pennae	mnRP
M. n. ulnoremigalis a	mnUR
M. n. ulnotectricalis dorsalis majoris a	mnUTDmaj
M. n. ulnotectricalis dorsalis medii a	mnUTDmed
M. n. ulnotectricalis dorsalis minoris a	mnUTDmin
M. pronator profundus	mPrp
M. pronator superficialis	mPrs
M. scapulotriceps	mST
M. supinator	mS
M. tensor propatagialis, pars cranialis	mTPcr
M. tensor propatagialis, pas caudalis	mTPca
M. ulnometacarpalis dorsalis	mUD
M. ulnometacarpalis dorsalis, pars caudalis	mUDca
M. ulnometacarpalis dorsalis, pars caudalis, digitationes primarii a	mUDcap
M. ulnometacarpalis dorsalis, pars dorsalis	mUDd
M. ulnometacarpalis dorsalis, pars ventralis	mUDv
M. ulnometacarpalis ventralis	mUV
Metacarpus major	MCII
Metacarpus minor	MCIII
Os carpi ulnare crus breve	OCUcb
Os carpi ulnare crus longum	OCUcl
Os carpi ulnare proc. muscularis	OCUpm
Papilla remigalis caudalis	PRC
Papilla remigalis ventralis	PRV
Phalanx digiti minimi	III‐1
Phalanx distalis digiti majoris	II‐2
Phalanx proximalis digiti majoris	II‐1
Phlanx digit alulae	I‐1
Pila cranialis phalangis	PC
Pila obliqua fossae b	PO
Remex carpalis	C
Remex primarius	P
Remex secondarius	S
Retinacula ulnocarpo‐remigialia	RUR
Retinaculum dorsalis digiti majoris a	RDDM
Septum humerocarpale	SH
Septum humerocarpale, digitationes remigales	SHDR
Tectrix carpalis dorsalis major	TCDmaj
Tectrix carpalis ventralis major	TCVmaj
Tectrix primaria dorsalis major	TPDmaj
Tectrix primaria dorsalis medius	TPDmed
Tectrix primaria ventralis major	TPVmaj
Tectrix primaria ventralis minor	TPVmin
Tectrix secundaria dorsalis major	TSDmaj
Tectrix secundaria dorsalis medius	TSDmed
Tectrix secundaria dorsalis minor	TSDmin
Tectrix secundaria ventralis major	TSVmaj
Tendo m. extensor digitorum communis	tmEDC
Tendo m. extensor longus digiti majoris	tmELDM
Tendo m. extensor metacarpi ulnaris	tmEMU
Tendo m. interosseus ventralis	tmIV
Tendo m. iInterosseus dorsalis	tmID

^aNew term.

^bLivezey & Zusi (2006).