the appendicular anatomy of the elegant crested …the appendicular anatomy of the elegant crested...

The Appendicular Anatomy of the Elegant Crested Tinamou (Eudromia elegans) 1

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Bull. Kitakyushu Mus. Nat. Hist. Hum. Hist., Ser. A, 12: 1–48, March 31, 2014

The Appendicular Anatomy of the Elegant Crested Tinamou (Eudromia elegans)

Daisuke Suzuki1, kentaro Chiba

2, Collin S. Vanburen3 & Tomoyuki OhaShi

4

1Department of Anatomy, Sapporo Medical University, School of Medicine, Sapporo 060-8556, Japan2Department of Ecology and Evolutionary Biology, University of Toronto, Toronto M5S 3B2, Canada

3Department of Earth Sciences, University of Cambridge, Cambridge CB2 3EQ, United Kingdom.4Kitakyushu Museum of Natural History & Human History, Kitakyushu 805-0071, Japan

(Received December 28, 2012; accepted February 4, 2014)

ABSTRACT — Tinamids are small cursorial birds with limited flight ability. They are phylogenetically nested within a clade composed mostly of large, flightless birds (ratites). Their ability to fly and the evolution of flightlessness in the clade are currently not well understood, and this is largely due to a paucity of literature on the osteological and muscular anatomy of these birds. Two Eudromia elegans (Palaeognathae: Tinamidae) were dissected and four skeletons were examined. The skeletons of Eudromia are characterized by a thin sternum, short and stout humeri, and developed lower limbs. Eudromia maintains some ancestral characters in the postcranial skeleton, such as elongated lateral trabeculae of the sternum, an absent rostral external spine of the sternum, and lack of fusion between the distal ilium and ischium. The lost of the hallux suggests cursorial adaptation occured not only in Strutioformes (Struthio has only two digits) but also even in tinamids. Accordingly, the muscles inserting on the hallux are lost or shifted to other digits. However, the body plan of Eudromia is quite similar to other modern volant birds, like Gallus. Our specimens showed differences in musclular morphology from previous descriptions of tinamou anatomy, particularly, the absence of M. iliofemoralis internus and the femoral head of M. tibialis cranialis. We also compared Eudromia with other ratites, such as Struthio, Rhea, Apteryx, and Dromaius. In the shoulder girdle, Eudromia has a large M. pectoralis thoracica and M. supracoracoideus, which are used for the downstroke and upstroke, respectively, but these muscles do not have such antagonistic actions in other ratites due to differing origins and insertions. The morphological changes in the pelvic girdle are minor compared with those in shoulder and forelimb regions. Ratite have enlarged Mm. femorotibiales, and M. iliotorochantericus medius and M. ischiofemoralis are diminished in size, except in Apteryx. Eudromia has a thin M. caudofemoralis pars pelvica, while other ratites have lost M. caudofemoralis pars caudalis (in Dromaius and Rhea) or it is considerably diminished (in Struthio). The differences between Eudromia and other ratites we find are attributed to the retention of flight ability in Eudromia.

KEY WORDS: Tinamou, Osteology, Myology, Comparative anatomy

INTRODUCTION

Tinamous (Palaeognathae: Tinamidae) are a monophyletic group of small, primarily cursorial birds capable of short bursts of flight when necessary. Because tinamous are nested within the clade Paleognathae which is composed of all flightless birds except for tinamous, there is a debate about whether flight in this family is due to retention of the ancestral condition, or if they re-evolved the ability to fly (e.g., HarShman et al., 2008; PhillipS et al., 2010). This debate is in part due to the ambiguity surrounding their phylogenetic relationships to other palaeognaths, with some analyses considering them the outgroup

to all other palaeognaths (e.g., CraCrafT, 1974; CaSperS et al., 1994; CraCrafT & Clarke, 2001) and others recovering the ostrich (Struthio) as the outgroup to all other palaeognaths (HarShman et al., 2008; PhillipS et al., 2010; JOhnSTOn, 2011; HaDDraTh & Baker, 2012). Some authors have been suggested the flight ability was lost multiple times in Palaeognathae, which is used to explain the clade’s global distribution (HarShman et al., 2008; PhillipS et al., 2010). However, parsimony-based character analysis suspended this conclusion because there was lack of evidence to suggest homology in the pectoral characters (LiVezey & ZuSi, 2007).

Daisuke Suzuki, Kentaro Chiba, Collin S. VanBuren & Tomoyuki OhaShi2

Despite numerous morphological phylogenies of palaeognaths, little work has been done to document the morphology of tinamous. HuDSOn et al. (1972) described the myology of 22 specimens of 13 species of tinamous, but they did not describe osteological morphology. Many morphological phylogenies use a limited character matrix of <100 characters (CraCrafT, 1974; JOhnSTOn, 2011) and are the only phylogenies which are able to incorporate fossil taxa that may aid in testing hypotheses of multiple losses of flight. The goal of the present study is therefore to describe the myology and osteology of the Elegant Crested Tinamou (Eudromia elegans) as a tool for future work on the phylogeny of extinct and extant palaeognaths. By comparing the anatomy of E. elegans to other extant archosaurs (both crocodylians and birds), we also highlight similarities and differences in the anatomy that might help future studies begin to explore the question of multiple losses of flight or a single gain of flight in palaeognaths from an anatomical perspective.

Institutional Abbreviation – KMNH: Kitakyushu Museum of Natural History and Human History, Fukuoka, Japan; YIO: Yamashina Institute of Ornithology, Chiba, Japan.

MATERIALS AND METHODS

Two elegant crested tinamous (Eudromia elegans) (KMNH VR 700,000 and YIO 2006-0047) were used. These specimens are stored in the Kitakyushu Museum of Natural History and Human History, Kitakyushu City, and Yamashina Institute of Ornithology, Abiko, Japan. KMNH VR specimen was three years and one month old at the time of death, 45 cm in total length (from the nib to the tip of the rectrix), and 695 g in weight. The cause of death was systemic amyloidosis. YIO specimen was one year old at the time of death, total length could not measured (cranial part was removed, but the size was almost same as KMNH VR specimen), and it was 620 g in weight. These specimens did not have any evident morphological abnormarities, and were frozen and stored at ˗20 °C. KMNH VR 700,000 was then thawed before being fixed in 10 % neutral formalin. YIO 2006-0047 was not fixed after being thawed. The visceral organs of KMNH VR 700,000 had been removed during autopsy. Significant damage to the left shoulder girdle occurred during the autopsy at the zoo prior to our dissection. In addition, we observed five osteological specimens, stored at the National Museum of Nature and Science, and Yamashina Institute of Ornithology (Table 1). The muscles are identified with comparison to HuDSOn et al. (1972) and then described based our specimen. The lines of muscle action are estimated from the direction of muscle fibers, tendon and origin an insertion, and confirmed using passive action in postmortem specimens. Osteological and myological terminology followed Baumel (1993).

DESCRIPTION

Osteology

1. Scapula (Figures 1, 4)

The scapula consists of thick proximal portion composed of the glenoid and acromion processes and an elongated scapular blade. The coracoid tubercle, where the coracoid articulates with the scapula, is located between the glenoid and the acromion. The clavicular facet, which is the articular facet for the furcula, is located distal to the acromion. The glenoid process of the scapula contributes to the glenoid fossa along with the glenoid process of the coracoid, which articulates with the humerus. The scapulo-coracoid joint of Eudromia is not as large as in crocodiles and non-avian dinosaurs, whose joints are tightly connected or sometimes fused. The dorsoventral width of the scapular blade is relatively consistent along the proximodistal length of the scapula, and the mediolateral thickness reduces distally. The dorsal margin is occupied by the insertion of M. rhomboideus superficialis laterally and M. rhomboideus profundus medially. The lateral surface of the scapular blade is smooth and lacks rugose osteological correlates. Two tendinous origins of M. scapulotriceps attach proximally on the scapular blade. The muscular origins of M. subscapularis caput laterale and M. scapulohumeralis caudalis cover almost the entire lateral surface of the distal scapular blade. The medial surface of the scapula is proximally occupied by the origin of M. subscapularis caput mediale. M. serratus superficialis cranialis inserts near the proximal end and the insertion is oblique relative to the long axis of the scapular blade, extending cranially from the ventral margin to the dorsal margin. The insertions of both M. serratus superficialis caudalis and M. serratus profundus are located on the distal portion. Because the insertions of Mm. serratus are fleshy, there is no obvious osteological correlate for these muscle insertions.

2. Coracoid (Figures 2, 4)

The coracoid is generally a major component of the shoulder girdle in birds and reptiles. The coracoid is articulated

Table 1. Examined specimen (skeletons). Institute No. Genus Specis

NMNS A343 Eudromia elegans NMNS A344 Eudromia elegans YIO 00321 Eudromia elegans YIO 00325 Eudromia elegans YIO 60631 Nothoprocta cinerascens


with the furcula and scapula distally and the sternum proximally. The coracoid has roughly an hourglass shape with a wider proximal end. The proximal and distal ends are orthogonal to one another, and the coracoid is distally enlarged dorsoventrally and enlarged proximally mediolaterally. The articular surface for the scapula is reduced and shifted caudally compared to the condition in other sauropsids (ViCkaryOuS & Hall, 2006). The coracoid consists of the glenoid process that, along with the glenoid process of the scapula (see above), forms the glenoid fossa, which articulates with the humerus. The glenoid fossa is directed more caudally than in crocodiles, as stated by Bakker (1971). The cranial-most portion of the distal end is occupied by the acrocoracoid process (the facet for articulation with the furcula), which comprises the distal border of the triosseal canal. The distal end of the acrocoracoidal process provides the small fibrous attachment of the furcula and the site of origination for both Mm. deltoideus minor and major; however their origins

also extend onto the glenohumeral joint capsule so that the actual size of the origin of these muscles extends beyond the bony surfaces. The articular surface for the furcula is medial to the acrocoracoid process, but its surface is small and difficult to distinguish. There is no supracoracoidal foramen as found in non-avian dinosaurs and crocodiles. The ventral side of the glenoid has a common tendinous origin for Mm. biceps brachii and coracobrachialis cranialis. The lateral process provides the origin for M. coracobrachialis caudalis cranially and the insertion for M. sternocoracoideus caudally.

3. Furcula (Figures 2, 4)

The avian furcula is homologous to fused clavicles in other reptiles. In many reptiles, the clavicles are reduced, but a robust furcula is maintained in most birds, as it plays a critical role in avian flight. The fusion of the clavicles occurred in basal theropod dinosaurs (NOrell et al., 1997), and CarranO et al.

Fig. 1. The left scaoula of Eudromia elegans with muscle attachment sites. (A) Lateral view. (B) Medial view.


Fig. 2. The left coracoid and furcula of E. elegans with muscle attachment sites. (A) Coracoid, posterior view. The dotted part of M. subcoracoideus is not for attachment of the coracoid, but the muscle is pass through there. (B) Coracoid, anterior view. (C) Coracoid, dorsal view. (D) Furcula. Ventral and dorsal view


(2005) suggested the Jurassic coelosauroid Segisaurus had a furcula, which had previously been regarded as the clavicle. The furcula of Eudromia is more U-shaped than V-shaped, and is very thin. The furcula articulates with the coracoid at

the clavicular facet, and is connected to the medial side of the coracoid and the sternum via membrana sternocoracoclavicularis. The cranial margin of the furcula provides the insertion for M. pectoralis thoracica. M. deltoideus minor and M. deltoideus pars

Fig. 3. The sternum of E. elegans with muscle attachment sites. (A) Lateral view. (B) Dorsal and ventral view.


propatagialis insert on the dorsal cranial surface of the furcula near the dorsal apex, and M. rhomboideus superficialis inserts on the dorsal caudal surface.

4. Sternum (Figures 3, 4)

In many reptiles, the sternum is highly reduced, and is still unossified in Archaeopteryx (WellnhOfer & TiSChlinger, 2004). However, modern birds have huge sterna and a sternal carina (keel) protruding from the midline of the sternal body (Baumel et al., 1993). This projection is expanded to increase the origin area for M. pectoralis thoracica and M. supracoracoideus. Flightless paleognaths, such as rheas and ostriches, therefore, do not develop the sternal carina at all. On the other hand, tinamids have a developed sternal carina because they have limited flight capabilities and fairly large pectoralis musculature. The body of the sternum is mediolaterally thin. The craniolateral trabecula extends laterally from the base of the sternal body. The intermediate tubercula branches from the sternal body cranially and extends caudally parallel to the sternal body. The sternal notch membrane spans the area between the body of the sternum and intermediate tubercula. There are costal facets for the articulation of the ribs with the sternum on the dorsoproximal intermediate trabecula. The rostrum sterni extendeds cranially from the sternal body and is bifurcated. The articular surface for the coracoid, the coracoidal

facet, lies between the rostrum sterni and the craniolateral tubercle. The origin of M. supracoracoideus extends from the sternal carina to the base of the sternal body. The bony origin of M. pectoralis is limited to the distal sternal carina. M. pectoralis continues a fleshy origination along the surface of M. supracoracoideus and the sternal notch membrane. M. coracobrachialis caudalis originates on the ventral surface of the craniolateral trabecula. M. subcoracoideus originates on the dorsal cranial surface of the rostrum sterni. M. sternocoracoideus and M. sternocostalis originate on the cranial and caudal portions of the dorsal craniolateral trabecula, respectively.

5. Humerus (Figure 5)

The humerus is the proximal-most forelimb bone and is expanded at its proximal and distal epiphyses. The deltopectoral crest is developed along the dorsal margin of the proximal humerus and is directed cranially, while the dorsal tubercle is developed on the caudal surface of the proximal humerus. The humeral head is oval in proximal view, articulating with the glenoid fossa, which is composed of the scapula and coracoid. Distally, the humerus has two condyles that articulate with the radius and ulna, termed the dorsal (lateral) condyle and

Fig. 4. The skeleton of the sternal region of E. elegans. (A) Lateral view. Left coracoid and scapula was removed. (B) Ventral view. (C) Medial view.


Fig. 5. The left humerus of E. elegans with muscle attachment sites. (A) Anterior view. (B) Dorsal view. (C) Ventral view. (D) Posterior view.


the ventral (medial) condyle, respectively. The lateral surface of the dorsal condyle is termed the dorsal epicondyle, and the medial surface of the ventral condyle is termed the ventral epicondyle. Many important flight muscles that cause movement at the glenohumeral joint insert onto the proximal humerus.

Proximally, M. deltoideus minor, the developed tendon of M. supracoracoideus, and two slips of M. deltoideus major insert along to the dorsal caudal side of the humerus, in proximodistal order. The insertion of the scapulohumeral ligament is on the dorsal tubercle, just distal to the humeral head on the caudal surface of the humerus. The common tendon of M. subscapularis

Fig. 6. The left ulna and radius of E. elegans with muscle attachment sites. (A) Dorsal view of ulna and radius. (B) Ventral view.


and M. subcoracoideus and the tendon of M. scapulohumeralis caudalis insert onto the ventrocaudal surface of the humerus, forming the ventral tubercle. M. scapulohumeralis cranialis inserts proximal to the origin of M. humerotriceps. The deltopectoral crest, which is 1/5 the total length of the humerus distal from the proximal end, is strongly developed. It provides the insertion of the large M. pectoralis thoracis on its ventral surface, and the insertion of M. coracobrachialis cranialis lies ventrodistal to the insertion of M. pectoralis thoracica. The origin of M. humerotriceps spans nearly all of the caudal diaphysis. The caudal surface of the diaphysis has a narrow ridge (caudal margin) and it provides the insertion for M. latissimus dorsi cranialis. M. brachialis originates on the cranial side of the distal diaphysis proximal to the ventral condyle. The distal end of the humerus is dorsoventrally expanded. The forearm extensor muscle group originates on the dorsal (lateral) epicondyle. The forearm extensor muscle origins

are nearly indistinguishable arranged proximolaterally as M. supinator, M. extensor metacarpi radialis, M. extensor digitorum communis, and M. ectoepiconylo-ulnaris. On the ventral (medial) epicondyle are the origins of the forearm flexor muscles. These muscle origins are arranged proximodistally as M. pronator superficialis, M. pronator profundus, M. epicondyloulnaris, and M. flexor carpi ulnaris. The origin of M. flexor carpi ulnaris is separated distally from the other flexor origins, but the origins of other forearm flexors are nearly indistinguishable from one another. In both flexor and extensor muscle groups, therefore, it is impossible to identify the individual originations based on osteological correlates alone.

6. Ulna (Figure 6)

The forearm consists of the radius and ulna. The ulna is longer and thicker than the radius. A slight olecranon process

Fig. 7. The left manus of E. elegans with muscle attachment sites. (A) Dorsal view. (B) Ventral view.


Fig. 8. The pelvis of E. elegans with muscle attachment sites. (A) Lateral view. (B) Medial view. (C) Dorsal view.


is developed on the proximal ulna and provides the common insertion site for M. scapulotriceps and M. humerotriceps. The ulnar head articulates with the entire ventral condyle and a part of the dorsal condyle of the humerus. The boundary of the articulation of the two condyles is separated by the intercondylar crest on the ulnar head. Distally the ulna articulates with the ulnare. The origin of M. extensor digitorum communis lies on the proximodorsal surface. The proximodorsal ulna is the insertion area for many of the extensor muscles. M. ectoepicondylo-ulnaris inserts onto the caudal part of the diaphysis and the papillae of the remiges, which are traces of the flight feathers along the caudal margin. The cranial part of the proximal ulnar diaphysis has the origin of M. extensor pollicis longus. The origin of M. ulnometacarpalis dorsalis lies on the distal dorsal surface of the ulna near the epiphysis. The flexor muscles attach to the ventral surface of the ulnar diaphysis. M. brachialis and M. entepicondyloulnaris insert onto a ridge that extends distally from the intercondylar crest. M.

flexor digitorum profundus originates distally to M. brachialis and M. entepicondyloulnaris along the majority of the diaphysis. M. ulnometacarpalis ventralis originates on the distal diaphysis near the epiphysis.

7. Radius (Figure 6)

The radius is a rod-like bone that is not expanded at either epiphysis, instead maintaining a relatively consistent width along its length. The radial head articulates with a portion of the dorsal condyle of the humerus proximally and with the ulnar head caudally, making the radioulnar joint. Distally the radius articulates with the radiale of the carpus. M. biceps brachialis inserts onto the ventral surface of joint capsule of the radioulnar joint and the proximoventral surfaces of the radius and ulna, leaving obvious scars on these bones. M. supinator inserts onto the proximodorsal radial diaphysis. M. extensor pollicis longus originates on the dorsal midshaft of the radius, and M. extensor indicis longus originates on the

Fig. 9. The pelvic girdle of E. elegans. (A) Dorsal view. (B) Ventral view.


posterodistal diaphysis. The ventral diaphysis serves as the insertion site for M. pronator profundus proximally and M. pronator superficialis distally.

8. Proximal carpus (Figure 7)

The proximal carpus of Eudromia consists of the ulnare and radiale. The radiale is wedge-shaped and firmly articulated with the radius. There is no mobility at the radius-radiale-carpometacarpus joints. This articulation artificially elongates the radius to make it longer than the ulna. As a result, the wrist is naturally in an ulnarly flexed position. The ulnare is not located directly between the ulna and carpometacarpus, and is instead located on the ventral surface of the carpometacarpus. The bone limits palmar flexion and overall range of motion at the wrist joint. The tendon of M. flexor carpi ulnaris and M. flexor digitorum superficialis insert on the ventral surface of the ulnare.

9. Carpometacarpus (Figure 7)

It has been debated whether the avian wing contains digits II-III-IV with a reduced digit I and V (Burke & FeDuCCia, 1997; Xu et al., 2009) or digits I-II-III with digits IV and V reduced (PaDian & Chiappe, 1998; VargaS & FallOn, 2005). This paper followed the latter according to Tamura et al. (2011). The carpometacarpus is composed of the fused metacarpals (I-III) and distal carpals. The pisiform process, which is a remnant of the pisiform, is projected ventrally from the ventral surface of the proximal carpometacarpus. The alular process is the remnant of metacarpal I, which is very short and slightly protrudes to make the articular surface of the first phalanx of the first digit (I1), the metacarpophalangeal joint. The second metacarpal is the most robust and longest in the carpometacarpus. The ventral surface of the diaphysis of metacarpal II has a fleshy insertion point for M. adductor indicis. The third metacarpal is thin, but almost as long as the metacarpal II. The diaphysis is strongly bowed, creating a space between metacarpals II and III. The edge of this space is the insertion area for M. interosseous ventralis ventrally and M. interosseus dorsalis dorsally.

10. Manual Phalanges (Figure 7)

The digits generally have limited capacity for flexion and extension at the metacarpophalangeal (MP) and interphalangeal (IP) joints. Each phalanx is flat and thin, and the articular surface is expanded craniocaudally to allow adduction and abduction. The proximal phalanx of the first digit (I1) is the largest and longest of all the phalanges. It forms the alula, which is important for maintaining lift during landing (AlVarez

et al., 2001). The carpometacarpus-phalanx I1 joint, therefore, is the only MP joint have a large range of motion not only with adduction/abduction, but also with flexion/extension and internal/external rotation. It also provides the area of insertion for muscles that control these movements. The second digit has two phalanges—the proximal phalanx (II1) and distal phalanx (II2). Both phalanges have the flanges on their lateral surfaces. The third digit has one small phalanx (III1).

11. Ilium (Figures 8, 9)

The avian pubis, ischium, and ilium are fused firmly each other and have obliterated sutures. The dorsal portion of the acetabulum, which articulates with the head of the femur, is derived from the ilium, the cranial ventral portion is formed by pubis, and the caudal ventral portion is formed by ischium. When articulated, the acetabulum completely covers the femoral head with the developed acetabular roof (the dorsal rim of the acetabulum); there are no thick menisci as in crocodiles (Suzuki et al., 2011). Caudal to the acetabulum is the developed antitrochanter, which receives the femoral facies articularis antitrochanterica. Another unique character of the avian pelvis is the lack of an articulation between the left and right ischia and pubes; the pelvic floor is supported solely by trunk muscles. The iliac blade is elongate craniocaudally and separated by the relative placement of the acetabulum. The cranial expansion is the preacetabular process, and the caudal expansion is the postacetabular process. M. iliotibialis cranialis originates cranially on the preacetabular process, and M. iliotibialis lateralis originates on the caudal preacetabular process. The lateral surface of the preacetabular process is concave, and it is largely occupied by the origin of M. iliotrochantericus caudalis. The ventral margin is occupied by the origins of Mm. iliotrochantericus cranialis and medialis. M. iliofemoralis externus originates dorsal to the acetabulum, around the undefined barrier of the pre- and post-acetabular processes. The lateral surface of the postacetabular process provides the origin of M. iliofibularis and the ventral margin provides the origin of M. caudofemoralis pars pelvica. The dorsal surface of the postacetabular process is expanded, but no muscles attach here.

12. Pubis (Figures 8, 9)

In birds, the pubis is very small compared to other pelvic elements. The pubis comprises the anteroventral portion of the pelvis in most reptiles, but the pubis of birds is rotated caudally, and is parallel to the ischium. The pubis has a small cranial projection, called the prepubic process. M. ambiens originates on the prepubic process. The area ventral to the acetabulum at the boundary of the pubis and ischium is the origination site of M. obturatorius


lateralis. The puboischiadic membrane spans both the pubis and ischium, and the membrane provides the origin area for Mm. puboischiofemoralis pars medialis (anteroventral) and lateralis (posteroventral) and M. flexor cruris medialis (dorsal).

13. Ischium (Figures 8, 9)

The ischium constitutes the caudal portion of the pelvis. It is more robust than the pubis. Two membranes attach to the ischium, connecting it to the other elements of the pelvis. The ilioischiadic membrane spans the caudal distance between the ilium and ischium, and the puboischiadic membrane spans the space between the ischium and pubis. The cranial edge of the proximal ischium projects the obturator process, which creates the obturator notch with the caudal margin of the pubis. Obturator nerves, arteries, and veins pass through the obturator foramen, innervating and circulating the “adductor” region. The medial surface of the ischium has a large origination

site for M. obturatorius medialis. This insertion continues onto the ilioischiadic and puboischiadic membranes. The lateral surface of the ischium is almost completely occupied by the origin of M. ischiofemoralis.

14. Femur (Figure 10)

The femur is the proximal-most long bone of the hind limb. The femoral head, which articulates with the acetabulum, is spherical (unlike the condition seen in other reptiles) and clearly distinguished from the shaft by the femoral neck. The trochanteric crest is expanded farther cranially and dorsally and is higher than the femoral head, whereas other palaeognaths have a reduced femoral trochanter. The cranial margin of the femoral trochanter extends distally to the middle of diaphysis to create the trochanteric crest. The diaphysis is almost straight with a slightly caudal curve distally. The distal epiphysis is comprised of the medial and lateral epiphyses, with the lateral epiphysis being slight larger. The

Fig. 10. The left femur of E. elegans with muscle attachment sites. (A) Medial view. (B) Anterior view. (C) Lateral view. D. Posterior view.


lateral surface of the lateral condyle has an indentation, which is the articular surface for the fibular head. The intercondylar fossa separates the two condyles and allows the cranial and caudal cruciate ligaments to pass between them. A number of muscles attach to the femur, some of which have tendinous insertions and cause discernable muscle scarring. The proximal trochanteric crest is the insertion site of M. iliotrochantericus caudalis, and Mm. iliotrochantericus cranialis and medius insert ventrally (distally) to M. iliotrochantericus caudalis. The lateral surface of the femoral trochanter has the strong tendinous insertion of M. obturatorius medialis and weak fleshy insertion of M. obturatorius lateralis. Ventral to the insertions of Mm. obturatorius, there are tendinous insertions of M. iliofemoralis externus and M. ischiofemoralis. These two insertions are almost the same size, and both create impressive scarring. The diaphysis is mostly covered by the origins of Mm. femorotibiales. The cranial surface of the diaphysis contains the linea intermuscularis cranialis that extends along the diaphysis from the trochanteric crest to the medial epicondyle,

dividing the origin of M. femorotibialis lateralis and M. femorotibialis intermedius. The caudal surface contains the linea intermuscularis caudalis that extends along the diaphysis to the medial epicondyle along the boundary between the origins of Mm. femorotibialis medialis and externus. All insertions are fleshy, excluding the caudal margin of M. femorotibialis medialis, which has an aponeurotic origin along linea intermuscularis caudalis, so there are few obvious traces of muscle insertion. The caudal surface of the distal diaphysis contains many muscle insertions. M. flexor cruris lateralis pars accessorius inserts along the ridge that extends from the medial condyle. Lateral to this ridge, there are the fleshy insertion of M. puboischiofemoralis and the fleshy origin of the intermediate head of M. gastrocnemius. Near the intercondylar fossa, there is a common origin of the medial head of M. flexor perforans digiti (FP) IV, FP III, FP II, M. flexor hallucis longus (FHL), and M. flexor digitorum longus (FDL) from proximal to distal. This area on the femur has a rugose surface, but it is not possible to distinguish individual muscle insertions.

Fig. 11. The left crus of E. elegans with muscle attachment sites. (A) Anterior view. (B) Medial view. (C) Posterior view. (D) Lateral view. E. Anterolateral view of juvenil E. elegans. The cranial cnemial crest and the patella or neomorph are unfused.


The lateral epicondyle provides the origins of the lateral head of M. gastrocnemius, M. flexor perforans et perforatus digiti (FPP) II, FPP III and the lateral head of FP IV from proximal to distolateral. Ansa iliofibularis attaches proximal to these muscles. In addition, the lateral collateral ligament (LCL) attaches on the lateral epicondyle, cranial to FPP III; the lateral epicondyle has rough surface overall. The medial epicondyle has only the insertion of the medial collateral ligament (MCL). This attachment site is slightly concave, but the epicondyle is mostly smooth.

15. Tibiotarsus (Figure 11)

The tibiotarsus is longer than the femur, and the diaphysis is almost straight. The proximal epiphysis is the strongly expanded tibiotarsal plateau, the articular surface for the condyles of the femur via thick menisci (Herzmark, 1938), and the large cnemial crests. The plateau is divided into the medial and lateral facet and between the facets, there is a slightly uplifted intercondylar eminence for the insertion of the anterior cruciate ligament (ACL). The distal epiphysis of the tibiotarsus forms a trochlea, differing from the reptilian tibia, which forms

Fig. 12. The left pes of E. elegans with muscle attachment sites. (A) Dorsal view. (B) Plantar view. The inset shows the terminology of each bone of the pes.


an astragular facet. The tibiotarsus of birds is the bone composed of the fused tibia, astragalus, and calcaneum (e.g., MCGOwan, 1984, 1985), shown by the incomplete fusion of these elements in closely related alverezsaurid theropods (Chiappe et al., 2002). The tibiotarsal trochlear surface articulates with the tarsometatarsus, forming hinge joint. In birds, the most prominent features on the proximal tibiotarsus are the enlarged cranial and lateral cnemial crests, located cranial and somewhat medial to the tibiotarsal plateau. The cranial cnemial crest is considered to correspond to a neomorphic tibial tuberosity (Fig. 11E; BarneTT & LewiS, 1958; ViCkaryOuS & OlSOn, 2007; HuTChinSOn pers. comm.) while dinosaurs have only one cnemial crest, corresponding to the lateral cnemial crest of birds (HuTChinSOn, 2002). The dorsal surface of the cranial cnemial crest contains the common insertion of Mm. iliotibialis cranialis and lateralis and Mm. femorotibialis medialis and lateralis. The lateral surface contains the origin of M. fibularis (peroneus) longus, and the medial surface contains the origin of the medial head of M. gastrocnemius. M. fibularis longus and the medial head of M. gastrocnemius are developed significantly in birds. The origin of M. tibialis cranialis extends over the lateral cnemial crest and proximal fibula. The medial proximal surface of the tibiotarsuscontains the insertion of the MCL and a weak insertion of M. flexor cruris lateralis directly caudal to the MCL. M. popliteus and M. plantaris insert ventral to the caudal margin of the medial facet. Between the medial and lateral facet, there is a shallow fossa, which is the insertion of M. flexor cruris lateralis pars pelvica. The tibiotarsal diaphysis is straight and has a consistent diameter over most of its length. M. flexor digitorum longus originates on the cranial surface of the diaphysis. The medial head of M. gastrocnemius originates on the medial diaphysis, and M. extensor digitorum longus originates on the caudal diaphysis. The lateral proximal surface of the tibiotarsus develops the fibular crest, which articulates with the proximal diaphysis of the fibula. The distal-most diaphysis has two tendon canals, formed by the ossification of the pons supratendinous, which separates the paths of the EDL tendon. There is almost no muscle attachment on the distal tibiotarsus.

16. Fibula (Figure 11)

The fibula is very thin, tapering distally until becoming a connective tissue that fuses to the diaphysis of the tibiotarsus. However, the fibular head is relatively large and articulates with the lateral condyle of the femur. The proximal fibula contains the origin of M. tibialis cranialis cranially and the LCL laterally. The caudal surface contains the origin of FP II and the insertion of M. popliteus. M. iliofiburalis inserts laterally, and FP IV originates on the anteromedial mid-diaphysis.

17. Tarsometatarsus (Figure 12)

The tarsometatarsus is rod-like and approximately two-thirds the length of the tibiotarsus. It is comprised of fused metatarsals II-IV. The first metatarsal of most tinamids is not fused to metatarsals II-IV, and instead attaches to the midshaft of the tarsometatarsus. However, the first metatarsal is lost in Eudromia. The distal end is tri-radiate, forming the articular surfaces for the proximal phalanges. The avian embryo also develops separated metatarsals that fuse ontogenetically. There are proximally two cotyles that articulate with the distal trochlear surface of the tibiotarsus, which are separated by a central eminence. The proximodorsal eminence is reduced for the origin of M. extensor proprius digiti III. M. tibialis cranialis inserts distal to the origin of M. extensor proprius digiti III, leaving two oval scars. On the proximal ventral surface, there is a bony tuberosity called the hypotarsus that covers the tibial cartilage. The hypotarsus is the insertion for each tendon of M. plantalis and M. gastrocnemius (Achilles tendon). The hypotarsus has grooves through which tendons of FHL, FPP II, FP II, III and IV, and FDL pass, thus stabilizing the tendons. Different from the condition seen in Gallus, all tendon pathways are grooved, but do not become canals. The diaphysis is fairly straight. M. abductor digiti II, M. extensor brevis digiti III, and M. extensor brevis digiti IV originate dorsally on the tarsometatarsus in mediolateral order. The ventral surface contains the sulcus tendinis to direct the flexor tendons. M. abductor digit IV also originates laterally on the ventral surface, and M. adductor digiti II arise distally on the ventral surface.

18. Pedal phalanges (Figure 12)

Eudromia has three pedal digits (II-IV). The digits II, III, and IV have three, four and five phalanges, respectively (digital formula = x:3:4:5:x). The proximal phalanx is the longest. Although all the phalanges are similar in morphology, the phalanges of the second and third digits are relatively large, but small in digit IV. The distal phalanx of each digit forms a claw.

Myology

Muscles in the Forelimb

1. Muscles from the trunk and shoulder girdle, Dorsal group

M. rhomboideus (Figure 13) M. rhomboideus is divided into M. rhomboideus superficialis and M. rhomboideus profundus. These are well developed and are deep to M. latissimus dorsi cranialis. These muscles adduct the scapula.


M. rhomboideus superficialis M. rhomboideus superficialis originates from the spinal processes of the first to fifth thoracic vertebrae aponeurotically. The muscle runs anterolaterally and has a fleshy insertion onto the dorsal margin of the scapula.

M. rhomboideus profundus M. rhomboideus profundus also has a fleshy origin on the spinal processes of the first to fifth thoracic vertebra. This muscle runs posterolaterally, and the direction is almost orthogonal to M. rhomboideus superficialis. This muscle is thicker and larger than M. rhomboideus superficialis. The aponeurotic insertion of M. rhomboideus profundus is on the medial surface of the dorsal margin of the scapular blade.

M. serratus (Figure 13) M. serratus extends from the ribs to the scapula and stabilizes the scapula on the trunk. It is usually divided into M. serratus superficialis and M. serratus profundus, and the former is further divided to Mm. serratus superficialis cranialis, caudalis, and metapatagialis in most birds, including Eudromia. Unlike Mm. rhomboideus, Mm. serratus superficialis and profundus do not overlap each other, and the insertions are well separated.

M. serratus superficialis cranialis M. serratus superficialis cranialis has a fleshy origin on the uncinate process of the first and second thoracic ribs. HuDSOn et al. (1972) described the origin on the last two cervical ribs. The muscle belly is thin and narrow, running anterodorsally, inserting

Fig. 13. The Dorsal and shoulder musculature of E. elegans. (A) Dorsal superficial musculature. (B) Superficial musculature of the lateral aspect of the scapula. (C) Musculatures of the medial aspect of the scapula.


onto the proximal medial surface of the scapular blade.

M. serratus superficialis caudalis M. serratus superficialis caudalis originates on the uncinate processes of the first to forth thoracic ribs. The muscle belly is larger than that of M. serratus superficialis cranialis. The muscle runs posterodorsally and inserts onto the medial surface of distal-most scapular blade.

M. serratus superficialis metapatagialis M. serratus superficialis metapatagialis has a fleshy origin on the third thoracic rib and is a long, narrow muscle. The distal part was damaged in our specimen, and we cannot confirm the insertion. HuDSOn et al. (1972) described it as running anterodorsally, inserting near the caudal end of the humeral tract, i.e. near the axilla.

M. serratus profundus M. serratus profundus originates on the transverse processes of the three posterior-most cervical vertebrae. Each of

the three muscle slips runs posterodorsally, deep to M. serratus superficialis cranialis. The muscle slips merge into one slip and have a fleshy insertion on the medial surface of the dorsal margin of the scapular blade.

2. Muscle from trunk to the shoulder girdle, Ventral group

M. sternocoracoideus M. sternocoracoideus has a fleshy origin on the cranial dorsal margin of the sternum, on the craniolateral trabecula. It is a short, but powerful muscle and makes up the cranial wall of thorax. The fleshy insertion is on the posterolateral surface of the proximal coracoid.

3. Muscles from shoulder girdle/trunk to humerus, Dorsal group

M. latissimus dorsi (Figure 13) M. latissimus dorsi is divided into three parts, Mm.

Fig. 14. Musculature of the pectoral region of E. elegans. (A) Ventral view. All muscles are removed on the right side. (B) Lateral view of left pectoral region. M. pectoralis pars thoracica and muscles in scapular region are removed. (C) Ventral view. Superficial musuluture of the pectoral region.


latissimus dorsi cranialis, caudalis, and metapatagialis. These muscles comprise the most superficial layer of the dorsal region, as in other reptiles, but this muscle is not as divided in most other reptiles. This group forms the caudal part of the axillary wall and inserts onto the humerus and axilla. This muscle retracts the humerus at the glenohumeral joint.

M. latissimus dorsi cranialis M. latissimus dorsi cranialis originates on the spinal processes of thoracic vertebrae II-VI. It runs anterolaterally superficial to Mm. rhomboideus. It is wide near its origin but becomes thinner towards the insertion, which is on the caudal (dorsal) crest of the middle of the humerus.

M. latissimus dorsi caudalis This muscle was damaged in this specimen, and we could not confirm the origin and insertion. The following description complements HuDSOn et al. (1972) with respect to the damaged area. The origin of M. latissimus dorsi caudalis covers a large dorsal area and can be divided into two parts. One part originates on the spinal processes of the posterior thoracic vertebrae and has a sheet-like, aponeurotic origin. The other portion has a fleshy origin on thoracic ribs II-V and the cranial margin of the ilium. These muscular bundles run anterolaterally. It is deep to

M. serratus superficialis caudalis and superficial to M. serratus superficialis metapatagialis. The muscle is tapered suddenly near insertion and becomes aponeurotic. It inserts onto the skin and the fascia of M. latissimus dorsi cranialis, M. deltoideus major, and M. scapulotriceps.

M. latissimus dorsi metapatagialis This muscle was also damaged, so the morphology and origin could not be clearly confirmed. It originates on the spinal processes of the posterior thoracic vertebrae and is very thin and string-like. The insertion of M. latissimus dorsi metapatagialis is on the caudal portion of M. serratus superficialis metapatagialis (HuDSOn et al., 1972).

M. supracoracoideus (Figure 14) M. supracoracoideus has a fleshy origin on the sternal carina, sternal body, sternal notch membrane, and the cranial (ventral) surface of the coracoid. It is a large, thick muscle, deep to M. pectoralis thoracica and in contact with M. coracobrachialis caudalis laterally. The muscle belly becomes a thick tendon as it passes through the triosseal foramen, which consists of the furcula, scapula, and coracoid. It finally inserts on the dorsal tubercle, which is on the dorsal surface of the proximal humerus. Although the origin is similar to the superficial M. pectoralis thoracica, the actions of these muscles are completely different.

Fig. 15. Musculature of the brachial region of E. elegans. (A) Superficial musculature of the humerus, anterior view. (B) Deep musculature of the humerus, anterior view. M. pectoralis pars thoracica and M. biceps brachii are removed. (C) Superficial musculature of the humerus, posterior view. (D) Deep musculature of the humerus, posterior view. M. scapulotriceps is removed.


M. supracoracoideus generally powers the upstroke of the wings. M. supracoracoideus elevates and externally rotates the humerus in European starlings and pigeons (POOre et al. 1997). This muscle also might perform similar action in Eudromia based on its insertion point on humerus and line of action. This muscle is complimented by M. pectoralis thoracica, which powers the downstroke assisted by the acrocoraohumeral ligament (Baier, 2007).

M. scapulohumeralis cranialis The scapulohumeralis cranialis is small and thin, and has a fleshy origin on the anterodorsal margin of the scapula. The muscle runs dorsal to the scapula, and has a fleshy insertion onto the proximal humerus. It contacts M. scapulohumeralis caudalis caudally. The action of this muscle is adduction and extension at the glenohumeral joint, but the force might be weak because the muscle belly is very thin.

M. scapulohumeralis caudalis (Figure 13) M. scapulohumeralis caudalis is relatively large, and has a fleshy origin that nearly covers the entire lateral surface of the scapula. The muscle runs anterolaterally, deep to M. latissimus dorsi cranialis. Its cranial margin contacts M. scapulohumeralis cranialis, and the caudal margin contacts M. latissimus dorsi caudalis. It inserts onto the ventral tubercle of the humerus with strong tendon, distal to the insertion of M. scapulohumeralis cranialis. The action of this muscle is adduction and extension of the humerus at the glenohumeral joint, retracting the humerus posteromedially.

M. subscapularis (Figure 13) M. subscapularis is divided into medial and laterale heads and have fleshy origins on the medial and lateral side of the proximal scapula, respectively. These heads are fused just below the ventral margin of the scapula; both heads are, therefore, very short. The muscle belly immediately forms a common tendon with M. subcoracoideus, which inserts onto the ventral tubercle of the humerus.

M. subcoracoideus (Figure 13) The fleshy origin of M. subcoracoideus is on the lateral surface of the rostrum sterni and the medial surface of the sternocoracoclavicle membrane. This powerful muscle runs medially and dorsally to the coracoid, but does not attach to the coracoid. The muscle becomes a common tendon with M. subscapularis and inserts onto the ventral tubercle of the humerus. It is deep to M. biceps brachii near its insertion. M. subscapularis and M. subcoracoideus adduct/retract the humerus at the glenohumeral joint.

Mm. deltoideus (Figure 15) M. deltoideus extends from the scapula and furcula to

the humerus. In birds, it consists of Mm. deltoideus major (the powerful, long, superficial muscle) and minor (the small, short, deep muscle. Both abducted and flex (protract) the humerus at the glenohumeral joint. The M. deltoideus propatagialis lies superficial to Mm. deltoideus major and minor but does not insert onto the humerus. Instead, it becomes the propatagialis.

M. deltoideus major M. deltoideus major has a fleshy origin on the acrocoracoid process of the coracoid. The origin is deep to pars propatagialis and superficial to M. deltoideus minor. Its fleshy insertion is on the dorsal surface of the proximal humerus.

M. deltoideus minor M. deltoideus minor has a fleshy origin on the dorsal apex of the furcula and the acrocoracoid process. It covers the articular capsule of the glenohumeral joint, and inserts on the dorsal surface of the humerus, proximal to the insertion of M. deltoideus pars major. SulliVan (1962) proposed that this muscle should be termed M. coracobrachialis cranialis, because it develops from the ventral mass embryologically. However, SulliVan (1962) was referring to a different muscle than M. deltoideus pars minor, which is M. coracobrachialis cranialis.

M. deltoideus propatagialis M. deltoideus propatagialis has a fleshy origin on the dorsal apex of the furcula. This thin muscle is superficial to M. deltoideus major and extends the propatagialis. The tendon of propatagialis is a long, elastic connective tissue with muscles spanning between the shoulder and the radiale. In addition, birds also have a similar structure, the metapatagialis spanning between trunk and elbow. Birds obtain lift during flying by expanding the propatagialis on the leading edge and the metapatagialis on the trailing edge of the wings (RaikOw, 1985). Embryological evidence suggests this muscle might be related to other deltoideus muscles (SulliVan, 1962), but it functions very differently. The muscles inserting onto the propatagialis tendon are M. cucullaris capitis, M. pectoralis, M. biceps brachii and Mm. deltoideus major and minor (Baumel et al., 1993). These slips, including M. deltoideus, tauten the propatagialis tendon.

Acrocoracohumeral ligament (Figure 15) The acrocoracohumeral ligament is a mediolateally broad, but relatively thin ligament running from the acrocoracoid process of the coracoid and the cranial side of the proximal humerus. Recently the role of this ligament has been reassessed. This ligament remains taut through downstroke and most of upstroke, while becoming slack during the transition from downstroke to upstroke (Baier, 2012). When M. pectoralis thoracica contracts to produce the downstroke, this force is


counterbalanced by the acrocoracohumeral ligament, which prevents the shoulder from dislocating (Baier et al., 2007).

4. Muscles from shoulder girdle/trunk to humerus, Ventral group

Mm. coracobrachiales (Figures 14, 15) The avian Mm. coracobrachiales is divided into two parts, Mm. coracobrachialis cranialis and caudalis. These muscles run between the coracoid and the humerus to adduct and flex humerus at the glenohumeral joint. Generally these muscles are large and divided into two or three slips in reptiles, including birds and other archosaurs, while that of mammals is reduced and composed of a single slip. This difference might be related to the reduction of the coracoid in mammals relative to the condition in reptiles. It is innervated by the medianoulnar nerve (N. medianoulnaris).

M. coracobrachialis cranialis M. coracobrachialis cranialis has a tendinous origin on the dorsolateral process of the coracoid. The origin is located near

that of M. biceps brachialis. It has a fleshy insertion on a large area of the cranial humeral diaphysis distal to the insertions of M. biceps brachialis and M. pectoralis thoracica.

M. coracobrachialis caudalis M. coracobrachialis caudalis is large muscle with a fleshy origin on the ventral craniolateral trabecula of the sternum that extends to the lateral surface of the coracoid and the fascia of M. supracoracoideus. It inserts tendinously onto the ventral tubercle of the humerus.

M. pectoralis thoracica (Figure 14) M. pectoralis thoracica is the largest muscle in volant birds and is the most superficial muscle in the ventral region of the trunk. It has a fleshy origin that extends onto the sternal carina, intermediate tubercula, sternal notch membrane, and ventrolateral surface of the furcula. This muscle has not clear boundary as known as the membrana intramuscularis between superficial pers sternobrachialis and deep pers thoracobrachialis in Eudromia, differing from the condition of other birds (SimiC & AnDrejeViC, 1963; Dial et al., 1988). However, the boundary

Fig. 16. Musculature of the forearm region of E. elegans, dorsal (extensor) view. (A) Musculature of superficial layer. (B) Musculature of the forearm. M. extensor digitorum communis (EDC) was removed. (C) Musculature of the second layer of the forearm. M. ectoepicondylo-ulnaris, M. extensor metacarpi radialis (EMR) and M. extensor carpi ulnaris (ECU) were removed. (D) Musculature of the deepest layer of the forearm. M. extensor pollicis longus (EPL) was removed. Other Abbreviations in this figure: ECU, extensor carpi ulnaris; EDC, extensor digitorum communis; EPL, extensor pollicis longus; FCU, flexor carpi ulnaris.


becomes clear at the distal narrow part of M. pectoralis. The insertion, partly tendinous medially and fleshy laterally, is on the deltopectoral crest of the humerus probably corrsesponding pers sternobrachialis and thoracobrachialis, respectively. The action of this muscle is flexion of the humerus at the glenohumeral joint, which causes the strong downstroke (Dial et al., 1988). It is innervated by the lateral and medial thoracic nerve.

M. pectoralis propatagialis M. pectoralis propatagialis is also referred to as M. tensor propatagialis longus in veterinary anatomy. This muscle originates from the belly of M. pectoralis thoracica, and inserts onto the anteroventral margin of the propatagialis tendon. The

propatagialis attaches to the lateral surface of the radiale, as noted above.

M. pectoralis abdominalis This muscle is probably one of the cutaneous muscles. We could not find a distinct origin and insertion for this muscle in our specimen.

5. Brachial muscles, Extensors

M. triceps brachii (Figure 15) M. triceps brachii is a highly developed extensor muscle and is generally divided into three heads in mammals, five in

Fig. 17. Musculature of the forearm region of E. elegans, ventral (flexor) view. (A) Musculature of superficial layer of the forearm. (B) Musculature of the forearm, M. pronator superficialis was removed. (C) Musculature of the forearm, M. flexor digitorum superficialis (FDS) was draw forward. (D) Musculature of the forearm, M. pronator profundus was removed. (E) Musculature of the deepest layer of the forearm. M. flexor carpi ulnaris (FCU) and extensor muscles were removed. Other Abbreviations in this figure: EMR, extensor metacarpi radialis; FCU, flexor carpi ulnaris; FDP, flexor digitorum profundus; FDS, flexor digitorum superficialis.


Crocodylia (MeerS, 2003), and two in Aves (RaikOw, 1985). This muscle in Eudromia is also divided into two heads. One is biarticular, M. scapulotriceps, and the other, M. humerotriceps, is monoarticular. The radial nerve innervates them both. M. scapulotriceps extents the ulna at the elbow joint, and M. humerotriceps extends the humerus at the glenohumeral joint.

M. scapulotriceps The origin of M. scapulotriceps is divided into two tendinous slips on the lateral surface of the scapula. One attaches distal to the glenoid fossa, and the other is proximal to the origin of M. scapulohumeralis cranialis. These two tendons are confluent, becoming one belly running parallel to the humeral shaft. The belly of M. scapulohumeralis fuses with that of M. humerotriceps and inserts onto the olecranon.

M. humerotriceps M. humerotriceps originates on the diaphysis of the humerus. The origin is mostly fleshy, but partially aponeurotic.

The muscle belly is deep to M. scapulohumeralis caudalis, notched by the pneumatic foramen and the tendon of M. scapulohumeralis caudalis. The dorsal margin of the belly contacts M. latissimus dorsi cranialis near its origin. M. humerotriceps is divided into a central, large belly and smaller slips dorsally (medially) and ventrally (laterally). The ventral and central bellies distally converge onto a common, broad tendon occupying the profundus layer of the tendinous insertion onto the olecranon. The dorsal belly has a fleshy insertion onto the tendon.

6. Brachial muscles, Flexors

M. biceps brachii (Figure 15) M. biceps brachii is the largest forelimb flexor muscle. The origin is broad and aponeurotic, extending from the anterolateral distal coracoid to the bicipital crest of the humerus, and deep to M. pectoralis thoracica. As in most reptiles, it consists of one head, which is broad proximally and narrow distally. It is in

Fig. 18. Musculature in the manus region of E. elegans, dorsal view. (A) Musculature and tendons, anterodorsal view. (B, C) Muscle attachment of the pollicis (thumb). (D) Muscle attachment of the indicis (index finger). Other Abbreviations in this figure: EMR, extensor metacarpi radialis; EPL: extensor pollicis longus; EDC, extensor digitorum communis.


contact with M. coracobrachialis cranially and M. humerotriceps laterally. There are no muscles in contact with M. biceps brachii medially. The insertion attachment is a strong tendon and attaches to both the proximal radius and proximal ulna. The biceps slip, which is a branched small muscle and inserts to the propatagium is absent as described HuDSOn et al. (1972). M. biceps brachii flexes and pronates the forearm at the elbow joint, and it is innervated by the medianoulnar nerve.

M. expansor secundarium M. expansor secundarium is very thin, and was damaged when our specimen was skinned. According to HuDSOn et al. (1972), the muscle has a tendinous origin on the distal end of M. latissimus dors caudalis, ventral edge of M. scapulohumeralis caudalis and the posterolateral edge of M. subcoracoideus. The muscle belly is very small and runs along the caudal aspect of M. humerotriceps, and divides into three slips near the olecranon process. It inserts on the proximal three quills of the secondary flight feathers.

M. brachialis (Figure 17)

M. brachialis has a fleshy origin on the distal ventral epiphysis of the humerus. The belly of this muscle is short, but powerful. The fleshy insertion is on the brachial fossa on the ventral proximal ulna.

7. Antebrachial muscles, Flexors

M. pronator superficialis (Figure 17) M. pronator superficialis has a short tendinous origin on the ventral epicondyle of the humerus. It lies superficial to the forearm extensors, and the belly lies over M. pronator profundus. The muscle runs along the radius and inserts onto the distal two fifths of the radial shaft. HuDSOn et al. (1972) referred this muscle to M. pronator sublimes.

M. pronator profundus (Figure 17) M. pronator profundus has a short tendinous origin on the medial epicondyle of the humerus distal to the origin of M. pronator superficialis. It runs obliquely across the forearm. The muscle belly fused with M. entepicondylo-ulnaris. The muscle inserts onto the mid-diaphysis of the radius.

Fig. 19. Musculature in the manus region of E. elegans, palmar view. (A) Musculature and tendons, posteroplantar view. (B) Musculature and tendons of the wrist, posteroplantar view. (C) Muscle attachment of the indicis (index finger). (D) Muscle attachment of the palmar. Other Abbreviations in this figure: FCU, flexor carpi ulnaris; FDP, flexor digitorum profundus; FDS, flexor digitorum superficialis.


M. entepicondylo-ulnaris (Figure 17) M. entepicondylo-ulnaris has two origins; one is a short tendinous origin proximal to the tendinous origin of M. flexor digitorum superficialis on the ventral epicondyle of the humerus. The tendon of M. entepicondylo-ulnaris is deep to the tendon of M. pronator profundus. The two tendons are partially fused each other, and therefore could be regarded as a common tendon. The other origin is on the ventral surface of the ulna. The muscle belly is deep to M. flexor carpi ulnaris and M. flexor digitorum superficialis. The muscle has a fleshy insertion on the ventral aspect of the proximal ulnar shaft.

M. flexor digitorum superficialis (FDS) (Figure 17) M. flexor digitorum superficialis has a thin tendinous origin distal to the tendinous origin of M. pronator profundus on the ventral epicondyle of the humerus. The muscle belly is thin and deep to M. flexor carpi ulnaris. It is superficial to M. flexor digitorum profundus. The muscle becomes tendonous near the wrist joint and partially inserts onto the ulnare. This insertion is via thick, dense connective tissue, and there is no scarring on the ulnare. Another branch of the tendon runs along the second digit until it finally inserts onto the ventral surface of the distal phalanx of digit II (II2). HuDSOn et al. (1972) referred this muscle to M. flexor digitorum sublimes.

M. flexor carpi ulnaris (FCU) (Figure 17) The origin of M. flexor carpi ulnaris is on the distal ventral epicondyle of the humerus and is the largest of the muscles that originate on the ventral epicondyle. It is tendinous near the origin and wraps around the ulnar trochlea. It becomes a fleshy belly running along the ulnar shaft. This muscle is superficial to M. flexor digitorum superficialis, M. flexor digitorum profundus, and M. entepicondylo-ulnaris. The caudal margin of the fascia of M. FCU is firmly connected to the base of the secondary feathers (Remiges secundariae). It has a tendinous insertion on the ulnare.

M. flexor digitorum profundus (FDP) (Figure 17) The fleshy origin of M. flexor digitorum profundus lies along the ventral ulnar diaphysis and is part of the deepest layer of forelimb muscles. The proximal portion of M. FDP is deep to the belly of M. pronator profundus and the insertion of M. entepicondylo-ulnaris. The muscle is relatively large, running along the cranial margin of the ulna, and becomes superficial near the middle ulna diaphysis. The muscle is in contact with M. pronator superficialis and M. pronator profundus cranially (radially) and M. FDS caudally (ulnarly). It contacts M. extensor indicis longus, the deepest extensor muscle, via the interosseous membrane. M. FDP runs between the radius and ulna, and becomes tendinous near the wrist joint.

The distal tendon of M. FDP passes through the cranial groove of the pisiform process, and then divides into two parts. One slip inserts the phalanx of digit I (I1), while the other extends to digit II where it fuses with the tendon of M. FDS near the proximal phalanx (II2) and inserts onto the ventral surface of the distal phalanx.

M. ulnometacarpalis ventralis (Figure 19) M. ulnometacarpalis ventralis has a fleshy origin on the ventral aspect of the distal diaphysis of the ulna. It is short and lies in deep layer of ventral forearm muscles deep to M. FDP. M. ulnometacarpalis ventralis becomes tendonous near wrist joint and inserts onto the cranial proximal carpometacarpus.

8. Antebrachial muscles, Extensors

M. extensor metacarpi radialis (EMR) (Figure 16) M. extensor metacarpi radialis has a tendinous origin on the dorsal epicondyle of the humerus. The muscle belly is large and superficial to other forearm extensor muscles. It contacts M. extensor digitorum communis caudally and M. extensor pollicis longus (EPL) distally. The tendon of this muscle runs parallel to the tendon of M. EPL and inserts onto the cranial region of the proximal metacarpus I along with M. EPL. The forearm extensor muscles do not extend the elbow, but flex the elbow joint due to their lines of action (RaikOw, 1985). The dorsal epicondyle, which is termed the ectepicondyle or lateral epicondyle in other animals, faces dorsally, and the insertions of extensors also face dorsally. The extensors, therefore, do not pass through the caudal to the elbow joint. M. supinator (Figure 16) M. supinator originates as a short tendon on the dorsal epicondyle of the humerus. The muscle is deep to and completely covered by the tendon of M. EMR and M. EDC, and it inserts on the proximal middle of the radial shaft.

M. extensor digitorum communis (EDC) (Figure 16) The tendinous origin of M. extensor digitorum communis is composed of a thick tendon that originates on the dorsal epicondyle of the humerus and a narrow tendon that originates on the proximal end of the ulna. The origin on the dorsal epicondyle is located distal to the origin of M. EMR and M. supinator. The muscle belly is large near the proximal forearm and tapers distally near the mid-diaphyses of the radius and ulna, becoming tendinous near the distal 20 % of the forearm. The tendon passes through the extensor retinaculum with the tendon of M. ECU, and divides into thick branches that insert onto the dorsal aspect of the caudal metacarpal I. The primary M. EDC tendon passes along a shallow groove on the dorsal carpometacarpus and inserts onto the distal phalanx of the digit II.


M. ectepicondylo-ulnaris (Figure 16) It forms a common tendon with M. extensor carpi ulnaris at its origin on the dorsal epicondyle. The belly extends to the forearm and inserts onto the anterodorsal surface of the proximal ulnar shaft. M. ectepicondylo-ulnaris is innervated by the radial nerve. HuDSOn et al. (1972) referred this muscle to M. anconeus. This muscle is strongly suggested to be homologous to the extensor ulnaris in crocodiles (MeerS, 2003) because of its morphology, relationship to other muscles, and innervation.

M. extensor carpi ulnaris (ECU) (Figure 16) M. extensor carpi ulnaris has a fleshy origin on the fascia of M. ectoepicondylo-ulnaris near the middle of the muscle’s belly. M. ECU is very thin. It contacts M. EDC cranially and partially covers M. ectoepicondylo-ulnaris. The muscle belly becomes a tendon near the wrist joint, and the tendon passes through the extensor retinaculum with the tendon of M. EDC, finally inserting onto the dorsal aspects of the caudal carpometacarpus.

M. extensor pollicis longus (EPL) (Figure 16) M. extensor pollicis longus has a fleshy origin that extends from the proximal ulna to the diaphysis of the radius across the interosseus membrane ventrally. It is a fairly large muscle deep to M. supinator, M. EDC, and M. ectoepicondylo-ulnaris proximally. M. EPL can be seen near the distal forearm as M. EDC reduces in size. Near this region, the muscle lies superficial to M. extensor indicis longus. It becomes tendinous near the wrist joint, and the tendon inserts onto the cranial surface of metacarpal I ventral to the insertion of M. EMR.

M. extensor indicis longus (Figure 16) The fleshy origin M. extensor indicis longus lies on the distal third of the caudal radial diaphysis. The posterior interosseous nerve, a deep branch of the radial nerve, runs along the surface of this muscle. It becomes tendinous near the distal radius, runs obliquely across the distal articular surface of the ulna, and inserts onto the proximal phalanx of the digit II.

M. ulnometacarpalis dorsalis (Figure 19) The tendinous origin of M. ulnometacarpalis dorsalis lies on the cranial margin of the distal ulna. It becomes fleshy as it runs across the caudal dorsal carpometacarpus and then inserts onto the dorsal surface of metacarpal III.

9. Muscles of Manus

M. abductor pollicis (Figure 19) The fleshy origin of M. abductor pollicis is near the insertion of M. EMR on metacarpal I. The muscle belly is relatively large compared to other dorsal intrinsic muscles. It has a fleshy insertion on the lateral surface of the digit I phalanx.

M. flexor pollicis (Figure 19) M. flexor pollicis has a fleshy origin proximally on the ventral surface of the carpometacarpus. The muscle runs between metacarpal I and the pisiform process. It is small and lies between M. abductor pollicis and the tendon of M. FDP. It has a fleshy insertion on the caudal margin of the ventral surface of the digit I phalanx.

M. adductor pollicis (Figure 19) The fleshy origin of M. adductor pollicis is on the cranial margin of the ventral surface of metacarpal II. This muscle runs cranially and inserts onto the first phalanx of digit I and the two quills attached to the allula.

M. extensor pollicis brevis (EPB) (Figure 18) The origin of M. extensor pollicis brevis lies on the cranial surface of the proximal metacarpal I. The muscle is short, but relatively large. It runs parallel to the tendons of M. extensor pollicis longus (EPL) and M. extensor metacarpi radialis (EMR). It has a fleshy insertion on the dorsal surface of the first phalanx of digit I (I1) distal to the insertions of M. EPL and M. EMR. However, the insertion of M. EPB is highly variable (HuDSOn et al., 1972). HuDSOn et al. (1972) described M. EPB originating from the common tendon of the M. EMR and M. EPL with an absent or sometimes slight connection with the carpometacarpus. It inserts on antereior surface of digit I (I1).

M. abductor indicis (Figure 18) The fleshy origin of M. abductor indicis is located along the dorsal surface of metacarpal II, extending from the pisiform process to the distal edge of metacarpal II. The muscle belly has a shallow groove, through which passes the tendon of M. FDP. M. abductor indicis becomes tendinous near the wrist (metacarpophalangeal) joint and inserts onto the proximal dorsal surface of phalanx II1.

M. interosseus dorsalis (Figure 18) M. interosseus dorsalis originates on from the caudal margin of metacarpal II to the dorsal caudal margin of metacarpal III (the edges of the gap produced by the fused metacarpals). This muscle is pinnate-form and fills the dorsal interosseus space. It is thinner than M. interosseus ventralis. It becomes tendinous distally and inserts onto the caudal surface of phalanx III1.

M. interosseus ventralis (Figure 19) The origin of M. interosseus ventralis is located on the ventral cranial margin of metacarpal II and the dorsal cranial margin of metacarpal III. It is a pinnate-form muscle and fills the ventral interosseus space between metacarpals II and III. It becomes tendinous near the carpometacarpus-phalanx II1 joint


Fig. 20. Musculature in the pelvic and thigh region of E. elegans, lateral view. (A) Musculature of the superficial layer of the thigh. (B) Musculature of the second layer of the thigh. M. iliotibialis lateralis was removed. (C) Musculature of the third layer of the thigh. M. iliofibularis was removed. (D) Musculature of the fourth layer of the thigh. M. flexor cruris lateralis was removed. (E) Musculature of the anterior part of the thigh. M. iliotibialis cranialis and iliofemoralis cranialis were removed. (F) Musculature of the deepest layer of the thigh. Mm. caudofemorales and M. flexor cruris medialis were removed.


and then divides into cranial and caudal tendons. These tendons insert onto the proximal cranial surfaces of phalanges II1 and II2 respectively. HuDSOn et al. (1972) referred this muscle to M. interosseus volaris, claimed that the caudal tendon was stouter than the cranial tendon. However, these tendons in our specimen were similar in size, with the cranial tendon being slightly larger. HuDSOn et al. (1972) also described an attachment to several primary quill follicles, but we could not confirm this attachment. M. flexor digiti III (Figure 19) M. flexor digiti III originates on the ventral surface of metacarpal III. The muscle is small near its origin, but becomes enlarged near its middle. It becomes tendinous near the carpometacarpus-phalanx III1 joint and inserts near the caudal edge of phalanx III1. Baumel et al. (1993) refer to this muscle as M. flexor digiti minoris.

Muscles in Hindlimb

10. Thigh muscles, Extensors

Mm. iliotibiales (Figure 20) Mm. iliotibiales are superficial muscles covering the cranial surface of the femur. The innervation and location of Mm. iliotibiales are very similar to Mm. iliotibiales of non-avian reptiles, but these muscles occupy a larger area in the thigh in birds than those in reptiles. It is generally divided into three slips in crocodiles and two or three slips in birds. Mm. iliotibiales are separated into two slips in Eudromia—the smaller M. iliotibialis cranialis and larger M. iliotibialis lateralis. This muscle group is mostly innervated by the femoral nerve but also partially by the ischiadic nerve. Mm. iliotibiales variably flex or extend the hip joint, and extend and abduct the knee joint.

M. iliotibialis cranialis M. iliotibialis cranialis has a fleshy origin on the anterodorsal margin of the iliac crest. This muscle covers most cranial and superficial part of the thigh. The belly is longer and thicker than M. iliotibialis lateralis. M. iliotibialis cranialis is superficial to and covers M. femorotibialis medialis. It inserts tendinously onto the cranial cnemial crest of the tibia. M. iliotibialis cranialis was refered to as M. sartorius by HuDSOn et al. (1972).

M. iliotibialis lateralis M. iliotibialis lateralis originates on almost the entire surface of the iliac crest. It is further divided into two sections. The cranial one-third is referred to as M. iliotibialis lateralis pars preacetabularis, which is innervated by the femoral nerve, and the caudal two-thirds is referred to as M. iliotibialis lateralis pars postacetabularis, which is innervated by the ischiadic nerve. However, the boundary between these muscles is not

clear. The belly of M. iliotibialis lateralis is thin mediolaterally and fan-shaped. It is fused with M. femorotibialis lateralis and intermedius aponeurotically at the anterolateral area of the middle of the thigh and inserts onto the lateral cnemial crest of the tibia. This muscle cranially contacts the caudal margin of M. iliotibialis cranialis. The middle portion of M. iliotibialis lateralis is located superficial to M. iliofemoralis externus and Mm. femorotibiales. The caudal portion is superficial to the cranial part of M. iliofibularis. The pars postacetabularis extends the hip joint differently from the pars preacetabularis because it is positioned caudal to the hip joint. However the pars postacetabularis assists during hindlimb flexion by active lengthening (eccentric contraction) to stabilize knee joint (Carr et al., 2011a, b).

Mm. iliotrochanterici (Figure 20) Mm. iliotrochanterici is a large muscle group that occupies the cranial iliac fossa and is divided into three portions; M. iliotrochantericus cranialis, medius, and caudalis, as in other birds (Berger, 1952; Klemm, 1969; RaikOw, 1970). These muscles produce the internal rotation of the femur, and less protraction due to a short lever arm from the center of the hip joint (RaikOw, 1985). The muscles also play a role in joint stabilization (RaikOw, 1970). Mm. iliotrochanterici medius and cranialis are fused in Tinamus and Crypturellus, while these muscles are not fused in the other tinamous including Eudromia (HuDSOn et al., 1972), as seen in our specimen. ROwe (1986) showed that Mm. iliotrochanterici were developed from two different anlargens. M. iliotrochantericus caudal i s develops f rom a common anlagen wi th M. iliofemoralis externus. The former study also reported that Mm. iliotrochanterici cranialis and medialis develop from same anlagen with M. iliofemoralis internus. In addition, he concluded that Mm. iliotrochanterici pars cranialis and medius are homologous to Mm. puboischiofemoralis internus (PIFI) in crocodiles because of developmental similarities, although Mm. iliotorchanterici originate from the lateral surface of the preacetabular process in birds, and PIFI in crocodiles and M. psoas major in mammals originate on the posterior dorsal and lumbar vertebrae, respectively.

M. iliotrochantericus medius M. iliotrochantericus medius has a fleshy origin along the the ventrolateral margin of the ilium, cranial to the acetabulum and caudal to M. iliotrochantericus cranialis. The parallelogram-shaped belly is the smallest in this group, and it is deep to M. iliofemoralis cranialis. The muscle runs caudally with M. iliotrochantericus cranialis. This muscle has a tendinous insertion on the anteroventral surface of the femoral trochanter of the femur, ventral to M. iliotrochantericus cranialis and deep to M. iliofemoralis cranialis.


M. iliotrochantericus cranialis M. iliotrochantericus medius has a fleshy origin along the ventrolateral margin of the illium, cranial to the acetabulum. The origin is located cranial to M. iliotrochantericus medius. The muscle belly is triangular and larger than M. iliotrochantericus medius, and it is also deep to M. iliofemoralis cranialis. This muscle inserts tendinously on the anteroventral surface of the femoral trochanter of the femur.

M. iliotrochantericus caudalis The iliotrochantericus caudalis is referred to as M. iliofemoralis cranialis (ROwe, 1986) or M. iliotrocantericus

posterior (HuDSOn et al., 1972). This muscle orginates on the cranial iliac fossa. This muscle is deep to M. iliotibialis cranialis cranially and M. iliotibialis lateralis proximally. It is the largest M. iliofemoralis. The belly is distally divided into a superficial and deep layer. The deep layer has a strong, tendinous insertion along the cranial margin of the trochanteric crest, and the superficial layer inserts on this tendinous insertion of the deep layer. M. iliotrochantericus caudalis is innervated by the lumber nerve.

Mm. iliofemorales (Figure 20) Mm. iliofemorales run between the ilium and femur.

Fig. 21. Musculature in the pelvic and thigh region of E. elegans. (A) Musculature of the superficial layer of the thigh, medial view. (B) Musculature of the second layer of the thigh, medial view. The detached the right lower leg from pelvis. M. ambiens was removed. (C) Musculature of the deepest layer of the thigh, anteromedial view. M. femorotibialis lateralis and intermedius were detached. (D) Musculature of the pelvis, medial view. (E) Musculature of the deepest layer of the thigh, lateral view.


Baumel et al. (1993) divided this muscle into Mm. iliofemoralis externus and internus. The external M. iliofemoralis externus is wide but is not very long. The M. iliofemoralis internus is on the medial side of pelvis; it is small, weak muscle. There are many synonyms of M. iliofemoralis interenus, such as M. iliacus (HuDSOn et al., 1972) and M. cuppedicus (ROwe, 1986).

M. iliofemoralis externus M. iliofemoralis externus has a fleshy origin on the caudal margin of the iliac crest. This muscle is deep to M. iliotibialis cranially and M. iliofibularis caudally. The shape of the belly is trianglular. This muscle has tendinous insertion on the trochanteric shelf, which is located on the proximolateral surface of the femur. The insertion area is deep to M. femorotibialis medialis. M. iliofemoralis externus is innervated by the ishchiadic nerve. HuDSOn et al. (1972) regarded this muscle as M. glutaeus medius et minimus.

M. iliofemoralis internus M. iliofemoralis internus is referred to as M. cuppedicus by ROwe (1986), and M. iliacus by HuDSOn et al. (1972). According to these authors, this muscle has a fleshy origin on the ventral margin of the ilium and has a fleshy insertion on the posteromedial surface of the proximal shaft, located medially to both Mm. iliotrochanterici cranialis and medialis. However, this muscle was absent in two specimens of E. elegans.

Mm. femorotibiales (Figures 20, 21) The Mm. femorotibiales group, innervated by the femoral nerve, is a large group of muscles that originate from the cranial, lateral, and medial surfaces of the femoral diaphysis and insert on to the cranial cnemial crest of the tibia. Baumel et al. (1993) divided this muscle into three parts from lateral to medial side in birds: Mm. femorotibiales lateralis, intermedius, and medialis. M. femorotibialis lateralis and intermedius are separated proximally and are fused distally, while M. femoralis medialis is the thinnest and only independent slip of Mm. femorotibiales, located deep and medially.

M. femorotibialis lateralis M. femorotibialis lateralis has a fleshy origin that covers the entire lateral surface of the femoral diaphysis. It is deep to M. iliotibialis medialis and contact with M. femorotibialis intermedius cranially. M. femorotibialis lateralis becomes the short femorotibial tendon with the intermedius inserting onto the cranial cnemial crest of the tibia. HuDSOn et al. (1972) noted that this muscle part was uniquely long in Eudromia compared to other tinamids.

M. femorotibialis intermedius M. femorotibialis intermedius has a fleshy origin that covers the cranial surface of the femoral diaphysis, but this

muscle expands laterally to contact with M. femorotibialis lateralis, and cover M. femorotibialis medialis partially. This muscle is covered with M. iliotibialis and M. ambiens. The muscle belly is fused with M. femorotibialis lateralis near the distal femur, while the insertion tendon of M. iliofemoralis cranialis runs between M. femorotibialis intermedius and M. femorotibialis medialis at the point. Distal to the point of fusion, the lateralis and intermedius form a strong tendon that inserts on the lateral cnemial crest of the tibia.

M. femorotibialis medialis M. femorotibialis medialis is an independent muscle and has a fleshy origination that spans from the proximolateral portion of the femoral shaft to the preacetabular process. This muscle is deep to M. femorotibialis intermedius and M. ambiens cranially. It has a tendinous insertion on the cranial cnemial crest of the tibia.

M. ambiens (Figure 21) M. ambiens has a fleshy origin on the pectineal process of the pubis. It is a superficial muscle on the medial side of the thigh. It is a relatively thin muscle. It runs between M. femorotibialis intermedius and M. femorotibialis medialis, becomes a thin tendon, and passes deep to the patellar tendon. It inserts onto the tendinous origin of the lateral head of M. flexor perforatus digiti II. M. ambiens is innervated by the femoral nerve.

11. Thigh muscles, Flexors

M. iliofibularis (Figure 20) The cranial half of M. iliofibularis originates on the superficial fascia and tendon of M. iliofemoralis externus and the caudal half originates from the tubercle of the caudal iliac crest. Its cranial margin contacts M. femorotibialis lateralis. The caudal margin is strongly united with the superficial fascia of M. flexor cruris lateralis. The ischiadic nerve and femoral artery and vein pass along the cranial deep layer of M. iliofibularis, and the ischiadic nerve then innervates the muscle. The belly is large and tapers distally. It becomes tendinous at the distal thigh and passes under the ligamentous ansa m. iliofibularis near the proximal end of the fibula. The common fibular nerve, which is a branch of the ischiadic nerve, also passes under the ansa m. iliofibularis. M. iliofibularis inserts on the proximal fibular shaft. This muscle is a major hip extensor and knee flexor. HuDSOn et al. (1972) used the inappropriate (mammalian) name M. biceps femoris for M. iliofibularis.

M. flexor cruris lateralis (Figure 20) M. flexor cruris lateralis is a large muscle that is divided into two parts: Mm. flexor cruris lateralis pars pelvica and pars accessoria. It is deep to M. iliotibialis. M. flexor cruris lateralis


was called M. semimembranosus and M. semitendinosus by HuDSOn et al. (1972).

M. flexor cruris lateralis pars pelvica M. flexor cruris lateralis pars pelvica originates on the caudal part of the ilium and lateral side of the first to forth caudal vertebrae. The belly is thick and wide proximally, but becomes thinner and narrower distally. M. flexor cruris lateralis pars pelvica fuses with M. flexor cruris lateralis pars accessoria near the distal femur and forms a large belly that then divides into three slips. One slip fuses with the fascia of the intermedial head of M. gastrocnemius and with M. flexor cruris medialis. Another slip extends to the caudal side of the tibiotarsus where it has a fleshy insertion on the flexor fossa, and the final slip partially becomes a thin aponeurosis, inserting on the proximal tibiotarsus caudal to the insertion of the medial collateral ligament. This muscle is innervated by the ischiadic nerve.

M. flexor cruris lateralis pars accessoria M. flexor cruris lateralis pars accessoria has a broad fleshy origin on the caudal side of the distal femoral shaft. The belly is thin but broad. The insertion is the muscle belly of the M. flexor cruris lateralis pars pelvica, forming aponeurotic raphe, near the distal femur.

M. flexor cruris medialis (Figure 20) M. flexor cruris medialis has a fleshy origin on the caudal end of the pubis and the puboischiadic membrane. The proximal part of the muscle is deep to M. caudofemoralis and is distally deep to M. flexor cruris lateralis. The width and thickness of the muscle is constant along the length. It fuses with M. flexor cruris lateralis at the distal thigh and inserts onto the intermedial head of M. gastrocnemius. The muscle is innervated by the ischiadic nerve.

M. caudoiliofemoralis (Figure 20) M. caudoiliofemoralis is small and thin muscles in birds because the caudal vertebrae in birds are highly reduced. This muscle is divided into M. caudofemoralis and M. iliofemoralis (Baumel et al., 1993). However, we used “M. caudofemoralis pars caudalis/pelvic” here, to avoid the confusion of this M. iliofemoralis with other thigh muscle, such as M. iliofemoralis internus/externus. It was suggested that M. caudofemoralis pars caudalis and pars pelvica have a common anlagen based on studies of chicken embryology (ROmer, 1927; VanDen-Berge, 1982). HuDSOn et al. (1972) referred to this muscle as M. piriformis and to as pars caudofemoralis and iliofemoralis. The pars pelvica seems to attain an origin on the ischia secondarily. The above two parts make a common tendon and inserts on the lateral side of the proximal femur.

M. caudofemoralis pars caudalis

HuDSOn et al. (1972) conclude that M. caudofemoralis pars caudalis (M. piriformis Pars caudifemoralis) is absent in Eudromia, but this muscle is present in our specimen. The muscle originates on the last two or three free caudal vertebrae and the uropygium. The origin does not extend onto the pygostyle. The proximal portion is deep to M. flexor cruris lateralis. The thin belly runs along the ventral margin of the pelvis. This muscle forms a thin common tendon with M. caudofemoralis pars pelvica and inserts on caudal surface of the proximal femur. M. caudofemoralis pars caudalis likely flexes the uropygium rather than retracts the femur because if its small size, but this speculation has not been tested experimentally.

M. caudofemoralis pars pelvica M. caudofemoralis pars pelvica has a fleshy origin on the dorsal surface of the caudal iliac crest, ventrocaudal to the origin of M. iliofibularis. The parallelogram-shaped belly of M. caudofemoralis pars pelvica is thinner than that of M. caudofemoralis pars caudalis. The ischiadic nerve and ischiadic artery emerge onto the superficial surface of the muscle through the ilio-ischiadic fenestra that is located in the middle of the belly. The proximal and distal portions are deep to M. flexor cruris lateralis and M. iliofibularis, respectively. This muscle has a common fleshy insertion on the caudal surface of the proximal femur with M. caudofemoralis pars caudalis. HuDSOn et al. (1972) noted that this muscle is developed in Tinamidae, but it is very thin in our specimen.

M. ischiofemoralis (Figure 20) M. ischiofemoralis has a fleshy origin on the ischium, the pubis, and the ilioischiadic membrane. This muscle is deep to M. caudofemoralis pars caudalis around its origin on the ischium and M. caudofemoralis pars pelvica at the middle of the belly. It is a very large muscle that runs craniocaudally. The muscle belly becomes a strong tendon anterodistally and inserts onto the lateral surface of the proximal femur. The tendinous insertion of M. iliofemoralis externus is superficial to the tendinous insertion of M. ischiofemoralis. This muscle is innervated by the ischiadic nerve, which extends from the caudal surface of the femur.

Mm. obturatorius (Figure 21) Mm. obturatorius is a muscle group that passes through the obturator foramen, which is composed of the proximal pubis and ischium. This muscle group is divided into the larger M. obturatorius medialis and smaller M. obturatorius lateralis. This muscle group is innervated by the obturator nerve.

M. obturatorius medialis M. obturatorius medialis has a fleshy origin on the medial surface of the ilium, ischium, and pubis, as well as the ilioischiadic and ischiopubic membrane. It is the only large muscle that originates on the medial surface of the pelvis. The


muscle runs cranially, tapering from its origin to its insertion. After this muscle passes through the obturator foramen, M. obturatorius lateralis attaches to M. obturatorius medialis. The muscle becomes a strong tendon distally and inserts onto the proximolateral surface of the femur.

M. obturatorius lateralis M. obturatorius lateralis is a very small muscle that originates on the lateral surface of the pubis, cranial to the obturator foramen. It runs deep to the tendon of M. obturatorius medialis. A proximal part of this muscle inserts onto the tendon of the internus, and a distal part has a fleshy insertion on the lateral surface of the proximal femur, caudal to the insertion of M. obturatorius medialis. M. obturatorius lateralis is innervated by the obturator nerve.

M. pubo-ischio-femoralis (Figures 20, 21) M. pubo-ischio-femoralis has a fleshy origin that extends from the pubic to the ischium along the puboischiadic membrane. It is composed of lateral (M. pubo-ischio-femoralis

pars lateralis) and medial (M. pubo-ischo-femoralis pars medialis) heads (Baumel et al., 1993), but these heads are difficult to differentiate in tinamids. In Eudromia, there appears to be only a single head of this muscle, which is trapezoidal in shape. It inserts onto the caudal surface of the distal femur. The proximal half of this insertion is fleshy, and the distal half is tendinous. It is innervated by the obturator nerve. HuDSOn et al. (1972) referred to this muscle as M. adductor longus.

12. Crural muscles, Extensors

M. tibialis cranialis (Figure 22) The origin of M. tibialis cranialis is generally divided into a femoral head and a tibial head in birds, in which the femoral head has a tendinous origin on the cranial surface of the lateral condyle of the femur, and the tibial head originates on the proximal tibiotarsus (CraCrafT, 1971; MCgOwan, 1979). HuDSOn et al. (1972) also described the presence of two heads in timanids, but the femoral head of M. tibialis cranialis is absent in our specimens.

Fig. 22. Musculature in the crural region of E. elegans, anterior view. (A) Musculature of the superficial layer of the crus. (B) Musculature of the second layer of the crus, anteromedial view. The medial head of M. gastrocnemius was removed. (C) Musculature of the second layer of the distal crus. (D) Musculature of the deepest layer of the crus, anterior view. M. fibularis longus and tibialis cranialis were removed


The tibial head of the M. tibialis cranialis is divided into a medial and a lateral slip. Both slips have fleshy origin on the lateral surface of the lateral cnemial crest and the fascia of M. EDL, respectively. Because the origin of the lateral slip

spans across fascia, the bony muscle scar does not reflect the true shape and size of the muscle’s origin. The medial slip is roughly twice as thick as the lateral slip and develops a strong fascia proximally. Both slips are immediately fused and deep

Fig. 23. Musculature in the crural region of E. elegans, posterior view. (A) Musculature of the superficial layer of the crus, posteromedial view. (B) Musculature of the second layer of the crus, posteromedial view. The medial head of gastrocnemius was removed. (C) Musculature of the second layer of the crus, posteromedial view. The lateral head of M. gastrocnemius was removed. (D) Musculature of the superficial layer of crus, posterolateral view. The lateral head of M. gastrocnemius was removed. (E) Musculature of the superficial layer of the crus, posterolateral view. M. fibularis longus was removed. (F) Musculature of the superficial layer of the crus, showing the structure of FP IV and III. M. FPPII and III are removed. (G) The musculature of the second layer of the crus. FPII, III, and IV were removed. (H) The deep musculature of the popliteal region. M. FHL and FDP were removed. Other Abbreviations in this figure: FDP, flexor digitorum profundus; FHL, flexor hallucis longus; FP, flexor perforates; FPP, flexor perforans et perforatus


to M. fibularis longus. It becomes tendinous around the distal 3/4 of the tibiotarsus, running deep to M. extensor retinaculum. The distal tendon becomes thick and divides into two parts and inserted on the proximal 1/5 of the tarsometatarsus. This muscle is innervated by the deep fibular nerve.

M. extensor digitorum longus (Figure 22) M. extensor digitorum longus (EDL) originates on the lateral surface of the cranial cnemial crest. The belly is large, but not as thick as M. tibialis cranialis. This muscle is largely covered by M. tibialis cranialis. It becomes tendinous near

the distal 1/5 of the tibiotarsus, and it runs along the lateral side of the tendon of M. tibialis cranialis, deep to M. extensor retinaculum, and through the foramen for M. EDL, which is located on the distal tibiotarsus. The tendon of this muscle splits into tendons that extend to digits II (tendon TII), III (TIII), and IV (TIV). The TII additionally is divided further into two tendons, and these tendons insert onto the extensor hood (a sheath-like covering) of phalanges II2 and II3. TIII also divided into two tendons that insert on the extensor hood of phalanges III3 and III4. TIV inserts on the extensor hood of phalanges IV4 and IV5. This muscle is innervated by the deep fibular nerve. The origin of

Fig. 24. Musculature in the pes region of E. elegans. (A) M. fibularis brevis. The inset shows the tendon and insertion of M. fibularis brevis. (B) Musculature of superficial layer of the pes. The tendon of M. extensor digitorum longus was shifted to show the deeper layer. (C) Musculature of the deepest layer of the pes, dorsal view. The tendon of M. extensor digitorum longus was removed. The inset shows the lateral view of the pes. M. abductor digiti II was shown. (D) The plantar view of pes. The tendon of FP II was penetrated by the tendon of FPP II. And the FPP II was penetrated by the tendon of FDP (not shown). The Achilles tendon was removed. (E) The plantar view of pes. The tendon of FP III was penetrated by the tendon of FPP III. And the FPP III was penetrated by the tendon of FDP. (F) Musculature of the deepest layer of the pes. The common tendon of M.FDP and FHL were removed.


M. EDL in birds is different from its origin in crocodiles, which arise from the cranial surface of the distal femur (HuTChinSOn, 2002).

Mm. fibulares (Figures 22, 24) Mm. fibularis (or Mm. peroneus) is divided into Mm. fibularis longus and brevis. A lateral branch of M. EDL branches is referred to as M. fibularis tertius in some mammals, but it is absent in birds. M. fibularis longus is distinctly larger than M. fibularis brevis in crocodiles and birds, but this difference is more exaggerated in birds. These muscles are innervated by the superficial fibular nerve.

M. fibularis longus This muscle has a fleshy origin that extends along the cranial surface of the fibula, the medial crest of the tibiotarsus and the fascia of M. tibialis cranialis M. fibularis longus in birds is much more developed than in other animals, extending along the lateral and cranial surfaces of the crus. The belly is wide, but relatively thin. The belly drastically narrows, becoming tendinous near the distal crus. The tendon is divided into two slips. One slip inserts onto the posterolateral surface of the tibial cartilage and the other merges with the tendon of M. FP III.

M. fibularis brevis M. fibularis brevis in our specimen is exteremely small. This muscle has a fleshy origin on the lateral surface of the fibular shafts, slightly proximal to the midshaft. The belly is short and becomes tendinous distally. The tendon passes through the peroneal retinaculum, wraps around the lateral malleolus, and inserts on the posterolateral edge of the proximal tarsometatarsus.

13. Crural muscles, Flexors

M. gastrocnemius (Figure 23) The origin of M. gastrocnemius is divided into the pars lateralis, intermedia and medialis. This muscle is the largest muscle in the crus, covering nearly the entire circumference of the crus, excluding cranial surfaces. The pars lateralis and medialis do not fuse as a muscle belly, but as a tendon. The tendon of M. gastrocnemius inserts onto the tibial cartilage (Cartilago tibialis), which is attached to the caudal (plantar) surface of the proximal tarsometatarsus. M. gastrocnemius is innervated by the tibial nerve.

Pars lateralis The origin of the pars lateralis is divided into a superficial and deep layer. The superficial layer has fleshy origin on the lateral epicondyle of the femur, and the deep layer has thick tendinous origin on the lateral epicondyle. The tendon of the deep layer is fused with ansa iliofibularis. The muscle belly

contacts FPP III laterally, and is deep to FPP II. The pars lateralis of M. gastrocnemius becomes tendinous at the distal 1/4 of the tibiotarsus, and then fuses with the distal tendon of the medial head. The lateral head of M. gastrocnemius flexes the knee joint and plantar flexes the ankle joint.

Pars medialis The pars medialis has a fleshy fleshy origin on the fascia of M. femorotibialis medialis and the medial surface of the cranial cnemial crest of the tibiotarsus. In addition, there is a separate origin on the medial diaphysis of the tibiotarsus that is posterodistally long and craniocaudally thin. It has a very large belly that covers the posteromedial and cranial sides of the crus. The medial head contacts M. fibularis longus on the cranial side of the crus and becomes tendinous at the distal 1/4 of the tibiotarsus. The medial head fuses with the intermedial head at the midshaft of the tibiotarsus, proximal to the fusion of the medial and lateral heads. The medial head of M. gastrocnemius causes plantar flexion of the ankle joint.

Pars intermedia The pars intermedia has a fleshy origin on the proximal lateral epicondyle of the femur. It is much smaller than the other two heads. It becomes tendinous at the proximal 1/3 of the tibiotarsal shaft and fuses the belly of the medial head, thereby following a similar path to the insertion on the caudal tarsometatarsus. The intermedial head of M. gastrocnemius flexes the knee joint and plantar flexes the ankle joint.

Ansa iliofibularis (Figure 23) Ansa iliofibularis is a connective tissue that wraps around the tendinous insertion of M. iliofibularis mediolaterally. It originates from the proximal to the lateral epicondyle of the femur and inserts on the lateral fascia of the lateral head of M. gastrocnemius.

M flexores perforans et perforatus digiti II (FPP II) (Figure 23) M. flexores perforans et perforatus digiti II (FPP II) has a fleshy origin on the lateral epicondyle of the femur, the proximal fascia of the lateral head of M. gastrocnemius, and the patellar tendon. The belly is deep to the lateral head of M. gastrocnemius, and it partially covers M. FPP III. This muscle contacts M. iliofibularis and M. FP IV medially. The muscle belly is thin and short. The belly becomes tendinous near the distal 1/4 of the tibiotarsal shaft. The tendon runs slightly obliquely to the long axis of the tibiotarsus and passes along the medial side of the tibial cartilage with M. FDL. The tendon dives deeper to the tendon of M. FP II at the middle of the tarsometatarsus. The tendon passes through the two slips of the tendon of M. FP II, and then divides into a medial and lateral tendon, through which M. FDL passes. The medial tendon fuses with M. FP II and inserts on the ventral surface of phalanx II2. The smaller lateral


tendon inserts on the proximoventral phalanx II3.

M. flexores perforans et perforatus digiti III (FPP III) (Figure 23) M. flexores perforans et perforatus digiti III has a fleshy and tendinous origin. The fleshy origin arises from the lateral epicondyle of the femur, just distal to the origin of M. FPP II. The tendinous origin arises from the lateral cnemial crest of the tibiotarsus. The muscle slip with the tendinous origin is deep to the lateral head of M. gastrocnemius and M. FPP II. This muscle contacts M. FPP II, the tendon of M. iliofibularis, and M. FP IV. The muscle belly, which is covered with a thick aponeurosis, is longer and broader than that of M. FPP II. The muscle becomes tendinous at the middle of the tibiotarsal shaft and then penetrates the tibial cartilage along with M. FDL. The tendon passes deep to M. FP III at the middle of the tarsometatarsus. The tendon penetrates the tendon of M. FP III, and then diverges into a medial and lateral tendon, through which the tendons of M. FDL pass. The medial tendon fuses with M. FP II and inserts on the ventral aspect of the phalanx III3 and the smaller lateral tendon inserts on the ventral surface of the proximal surface of phalanx III4.

M. flexores perforatus digiti II (FP II) (Figure 23) M. flexor perforatus digiti II has a medial and lateral head. The large medial head has a common fleshy origin on the caudal surface of the femoral epiphysis with M. FHL and the medial head of M. FP IV. The lateral head has a tendinous origin on the caudal surface of the fibular head. The tendon of the lateral head serves as the insertion site for M. ambiens. The medial head has larger attachment area than that of the lateral head. The muscle belly of M. FP II is thin, deep to M. FP digiti III and superficial to M. FHP. It becomes tendinous and runs along the tarsometatarsus with the tendon of M. FDL. The tendon divides near the distal tarsometatarsus and is penetrated by M. FPP II and M. FDL. The medial tendon merges with the tendon of M. FPP III and inserts onto the ventral surface of phalanx II1 and the lateral tendon inserts onto the ventral surface of the proximal phalanx II2.

M. flexor perforatus digiti III (FP III) (Figure 23) M. flexor perforatus digiti III has a medial and a lateral head. The large medial head has a fleshy origin on the caudal surface of the femoral epiphysis, cranial to M. FP IV, and it surrounds the caudal tibial artery and fibular artery. The lateral head has a fleshy origin on the deep fascia of M. FP IV. The medial head is fusiform and relatively large, and it is larger than the belly of M. FP IV. The belly of the medial head becomes a tendinous at the cranial 2/3 of the tibiotarsal shaft. The muscle belly of the lateral head is very thin. The lateral head fuses with the medial head after the medial head becomes tendinous. The tendon of M. FP III passes through a tendon sheath at the ankle with M. FP IV and then penetrates the middle of the tibial

cartilage. The tendon of M. FP II is then divided into a lateral and medial tendon, through which the tendons of M. FPP III and M. FDP pass near the distal tarsometatarsus. The lateral tendon inserts onto the ventral surface of phalanx III2 and the medial tendon inserts on the ventral surface of phalanx III3. M. FP II is innervated by the tibial nerve.

M. flexor perforatus digiti IV (FP IV) (Figure 23) M. flexor perforatus digiti IV has a medial and lateral head. The medial head has a fleshy origin on the caudal surface of the femoral epiphysis, just proximal to the origins of M. FP II, M. FHL, and M. FDL. The lateral head has an aponeurotic origin on the caudal surface of the fibular shaft. This muscle has a thin but broad belly because both heads merge very close to their origination. The muscle belly is partially deep to M. FPP III, M. iliofibularis, and ansa iliofibularis. The belly becomes tendinous at the cranial 3/4 of the tibiotarsal shaft and descends parallel to the tendon of M. FP III. The tendon divides into lateral and medial slips near the distal tarsometatarsus and is penetrated by the tendon of M. FDL. Both tendons are further divided, becoming four tendons at digit IV. The lateral-most and medial-most tendons insert onto the ventral surface of phalanx IV1. The other tendons insert on the ventral surface of phalanx IV2. This muscle is innervated by the tibial nerve.

M. plantaris (Figure 23) M. plantaris has a fleshy origin on the caudal surface of the medial proximal tibiotarsus. The muscle belly is very short and becomes tendinous as it reaches the proximal 1/3 of the tibiotarsal shaft. It descends with the Achilles tendon, passs through the thick tibial cartilage (similar to M. gastrocnemius), and inserts on the caudal surface of the proximal tarsometatarsus. The tibial nerve innervates M. plantaris.

M. flexor hallucis longus (FHL) (Figure 23) M. flexor hallucis longus has a tendinous origin on the caudal surface of the medial femoral epiphysis that it shares with M. FP II and M. FDL. The short proximal tendinous portion of the muscle passes between the lateral and medial condyles of the tibiotarsus and becomes fleshy at the tibiotarsal midshaft. It becomes tendinous again distally as it approaches the distal 1/3 of the tibiotarsal shaft. The tendon runs deep to the Achilles tendon, changes direction at the medial malleolus, and makes a thick plantar fascia with the tendon of M. flexor digitorum longus. The plantar fascia divides into three branches at the distal tarsometatarsus. Each branch penetrates the tendons of Mm. FP and Mm. FPP on digits II and III, and the tendons of M. FP IV on digit IV. Finally, each branch inserts on the ventral surface of each distal phalanx. M. FHL does not insert on the hallux because this structure is lost in Eudromia.

M. flexor digitorum longus (FDL) (Figure 23)


M. flexor digitorum longus has a fleshy origin that extends over the caudal surface of the distal epiphysis of the femur, the proximal fibular shaft and a large area of the caudal tibiotarsal shaft. Its origin on the distal femur is shared with M. FP II and M. FHL. This muscle lies in the deepest layer. The thin but broad belly is covered by a thick aponeurosis. It contacts M. flexor hallucis longus caudally. The belly becomes tendinous near the distal 1/6 of the tibiotarsal shaft. The tendon then passes along the medial side of the tibial cartilage, changes the direction at medial malleolus, and fuses with the tendon of M. FHL to produce the plantar fascia. M. popliteus (Figure 23) M. popliteus has a fleshy, but superficially aponeurotic origin on the caudal surface of the fibular head. The small and short muscle belly runs obliquely to the long axis of the fibula and inserts on the caudal surface of the proximomedial tibiotarsal shaft. It lies in the deepest layer of crural muscles along with M. flexor digitorum longus. This muscle is innervated by the tibial nerve.

14. Muscles of Pes

M. lumbricalis M. lumbricales has a fleshy origin on the dorsal (deep) surface of the plantar fascia, which is composed of the tendons of M. FHL and M. FDL. Baumel et al. (1993) described the muscle bellies of Mm. lumbricales on each digit bilaterally; the lateral belly is larger than the medial one. In our specimens, the origins of the multiple bellies M. lumbricales were confirmed.

M. abductor digiti II (Figure 24) M. abductor digiti II has a fleshy origin on the lateral dorsal tarsometatarsus proximal to digit II. The muscle is short but has a thick belly. It has a tendinous insertion on the proximal ventral surface of phalanx II1.

M. adductor digiti II (Figure 24) M. adductor digiti II has a fleshy origin on the ventral medial surface of the distal tarsometatarsus proximal to digit III. The muscle belly is narrow but become broader distally. It has a tendinous insertion on the lateral margin of the proximal phalanx II1.

M. extensor proprius digiti III (EP III) (Figure 24) M. extensor proprius digiti III has a short tendinous origin on the dorsoproximal metatarsus and on the joint capsule of the ankle tendon. The origin is located proximal to the insertion of M. tibialis cranialis, and the proximal tendinous portion of M. EP III passes through the bifurcated tendon of M. tibialis cranialis. This muscle is thin, and passes along a groove that runs from the proximal to midshaft of the dorsal surface of the tarsometatarsus.

The muscle runs lateral to the tendon of M. extensor digitorum longus and inserts on the dorsal surface of the phalanx III4.

M. extensor brevis digiti III (EB III) (Figure 24) M. extensor brevis digiti III has a fleshy origin on the medial dorsal surface of the distal tarsometatarsus. The muscle contacts M. abductor digiti II laterally and M. extensor brevis digiti IV medially. The muscle has a tendinous insertion on the dorsal surface of the phalanx III1.

M. extensor brevis digiti IV (EB IV) (Figure 24) M. extensor brevis digiti IV has a fleshy origin along the dorsolateral shaft of the tarsometatarsus. This muscle contacts M. extensor proprius digiti II medially and becomes tendinous near the distal tarsometatarsus. The tendon passes along a bony canal between metatarsals III and IV of the tarsometatarsus. The muscle finally inserts on the proximal medial phalanx IV1.

M. abductor digiti IV (Figure 24) M. abductor digiti IV has a fleshy origin laterally on the ventral surface of the tarsometatarsus. It has a tendinous insertion proximally on the lateral surface of phalanx IV1.

M. flexor hallucis brevis, M. extensor hallucis longus These muscles are absent in Eudromia due to the loss of the hallux.

DISCUSSION

General Features of Appendicular Muscular System of Eudromia elegans

Unlike other paleognaths, tinamids have flight abilities. The morphological characteristics of tinamids that reflect this difference include a developed sternal carina to support the large attachment site of M. pectoralis thoracica and winged forelimb capable of flight. Tinamids, therefore, look similar to volant neognath birds, such as quails or domestic fowl. However, they also maintain some ancestral characters in their skeleton (BerTelli & Chiappe, 2005), such as elongated lateral trabeculae of the sternum (BleDSOe, 1988), an absent rostral external spine of the sternum (Parker, 1866), a proximodorsal foramen in the coracoid (Parker, 1866), the absence of dorsodistal foramina (BerTelli, 2002), a humerus with a shallow transverse ligamental groove (the attachment of acrocoracohumeral ligament; Lee et al., 1997), a ventral condyle longer than the dorsal condyle in the humerus (Clarke & Chiappe, 2001), lack of fusion between the distal ilium and ischium (CraCrafT, 1974), and a strong, rounded depression between the tibiotarsal condyles (BerTelli & Chiappe, 2005). In general, the muscular anatomy of tinamids is similar to chickens, as mentioned by HuDSOn et al. (1972). Our results

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in R

hea

is m

orph

olog

ical

ly

diff

eren

t. br

achi

alis

O

O

O

O

O

O

A

nteb

rach

ial m

uscl

es

pron

ator

su

perf

icia

lis

O

O

O

O

O

O

pron

ator

pr

ofun

dus

O

X

X

X

X

O

1/9

in E

mu

ente

pico

ndyl

o-ul

naris

O

X

O

O

X

O

2/9

in E

mu

flexo

r dig

itoru

m

supe

rfic

ialis

O

X

X

X

X

O

fle

xor d

igito

rum

pr

ofun

dus

O

O

X

X

O

O

flexo

r car

pi u

lnar

is

O

O

O

O

O

O

FC

U h

as tw

o he

ads a

nd tw

o in

serti

ons i

n Rh

ea

ulno

met

acar

palis

ve

ntra

lis

O

O

O 2

par

ts

X

O

O


ble

2. C

ontin

ued.

Eu

drom

ia

Stru

thio

Rh

ea

Dro

mai

us

Apte

ryx

Gal

lus

Syno

nym

C

omm

ents

Aut

hors

M

uscl

es

Our

ob

serv

atio

n +

HU

DSO

N e

t al.

(197

2)

Our

ob

serv

atio

nO

ur

obse

rvat

ion

MA

XW

ELL

(200

7)

MC

GO

WA

N

(198

2)

Our

ob

serv

atio

n +

YA

SUD

A

(200

2)

Ant

ebra

chia

l mus

cles

ecto

epic

ondy

lo-u

lnar

is

O

O

O

O

O

O

an

cone

us

the

mus

cle

belly

of

EEC

U a

nd

ECU

are

fuse

d in

O

stric

h.

exte

nsor

met

acar

pi ra

dial

is

O

O

O

O

O

O

EMR

of O

stric

h do

not

reac

h m

etac

arpa

ls.

supi

nato

r

O

O

O

O

O

O

exte

nsor

dig

itoru

m

O

O

O

X

X

O

orig

inat

e fr

om

ulna

in O

stric

h

exte

nsor

car

pi u

lnar

is

O

O

X

X

X

O

ex

tens

or m

etac

arpi

ul

naris

the

mus

cle

belly

of

EEC

U a

nd

ECU

are

fuse

d in

O

stric

h.

exte

nsor

pol

licis

lo

ngus

O

O

O

O

O

O

ex

tens

or lo

ngus

alu

lae

the

mus

cle

belly

of

EPL

and

EIL

ar

e fu

sed

in

Ost

rich

exte

nsor

indi

cis

long

us

O

O

X

X

O

O

the

mus

cle

belly

of

EPL

and

EIL

ar

e fu

sed

in

Ost

rich

ulno

met

acar

palis

do

rsal

is

O

O

O

O

O

O

Tabl

e 2.

Con

tinue

d.

Eudr

omia

St

ruth

io

Rhea

D

rom

aius

Ap

tery

x G

allu

s Sy

nony

m

Com

men

ts

Aut

hors

M

uscl

es

Our

ob

serv

atio

n +

HU

DSO

N e

t al.

(197

2)

Our

ob

serv

atio

nO

ur

obse

rvat

ion

MA

XW

ELL

(200

7)

MC

GO

WA

N

(198

2)

Our

ob

serv

atio

n +

YA

SUD

A

(200

2)

Man

ual m

uscl

es

abdu

ctor

pol

licis

O

O

O

X

X

O

fle

xor p

ollic

is

O

O

O

X

X

O

addu

ctor

pol

licis

O

O

O

X

X

O

ex

tens

or p

ollic

is

brev

is

O

O

O

X

X

O

abdu

ctor

indi

cis

O

O

O

X

X

O

inte

ross

eous

do

rsal

is

O

? O

X

X

O

in

tero

sseo

us

vent

ralis

O

O

O

X

X

O

fle

xor d

igiti

III

O

O

O

X

X

O

exte

nsor

indi

cis

br

evis

X

O

?

X

X

O


from the dissection of Eudromia elegans are consistent with those of HuDSOn et al. (1972) in almost all respects. However we did find some differences, such as the cranial and caudal tendon of M. interosseous ventralis were similar in size, rather than the cranial tendon being slightly larger, M. iliofemoralis internus is absent, the presence of M. caudofemoralis pars pelvica, a thin M. caudofemoralis pars caudalis, and the lack of a femoral head of M. tibialis cranialis. These differences could be attributed to individual variation, but we suggest the absence of M. iliofemoralis internus might be real because both sides of the two specimens (the same number as in HuDSOn et al., 1972) lacked this muscle. Similarly, we consider the absence of the femoral head of M. tibialis cranialis to be real, as well. Eudromia inhabit open grasslands (DaVieS, 2002), and they are therefore primarily adapted for cursorial locomotion. The hip extensor (Mm. femorotibiales and Mm. iliotibiales) and hip extensor/knee flexor (M. flexor cruris lateralis and M. iliofibularis) muscles of the hindlimb are highly developed in Eudromia. As in most birds, mobility in the trunk of E. elegans is limited due to the fused synsacrum, which contains the last thoracic, lumbar, sacral, and the proximal caudal vertebrae. The preacetabular process is highly developed, providing enlarged attachment sites for hindlimb flexor muscles.

The Myological Comparison with other ratites

The absence and presence of muscles in Eudromia, Struthio, Rhea, Dromius, Apteryx and Gallus are summarized in Tables 2 and 3.

Muscles from trunk and shoulder girdle

Many ratites have lost the ability to fly, and this change in locomotion is reflected strongly their forelimb and wing myology. In relation to reduction of wings and forelimbs, the muscles of the shoulder girdle and trunk are also reduced. For example, M. rhomboideus and M. serratus are reduced to some degree in all ratites. M. rhomboideus superficialis is absent in Struthio and profundus is absent in Apteryx (MCGOwan, 1982). M. serratus superficial metapatagialis is absent in Struthio, Rhea and Apteryx. M. pectoralis thoracica and M. supracoracoideus have been severely reduced in volume. However, M. supracoracoideus remains a relatively strong muscle compared to M. pectoralis thoracica. The positional relationship of these muscles has been considerably changed, and the function of these muscles is different from their antagonist functions during down-stroke and up-stroke, as seen in volant birds. M. deltoideus minor is absent in all examined ratites, and M. scapulohumeralis cranialis is absent in all examined ratites except for Struthio. Eudromia possesses all muscles found in the trunk and the shoulder girdles of Gallus and basal members of Neognathane.

Brachial muscles

Ratites lost the series of muscles related to the pro- and meta-patagium, including the biceps slip, Mm. deltoideus minor, and M. scapulohumeralis cranialis (Maxwell & LarSSOn, 2007). M. expansor secundarium is rather developed in Struthio, but other ratites lack this muscle and the biceps slip was absent in Eudromia, as well. Almost all brachial muscles in ratites are thin and reduced in volume comparing volant birds, including Eudromia. Eudromia has all antebrachial muscles seen in Gallus.

Antebrachial muscles

Struthio has relatively developed antebrachial muscles compared to other ratites, but it has lost three flexor muscles, i.e. M. entepicondyle, M. pronator profundus and M. flexor digitorum profundus. Rhea, Dromaius, and Apteryx have lost many flexor and extensor antebrachial muscles. Although the antebrachial muscles in ratite are considerably reduced and many muscles are absent, Struthio maintains many of the antebrachial muscles found in other birds. It is known that Struthio frequently use their wings for running away from the predators, mating displays, and to shade chicks (Sauer, 1972). Eudromia maintains all antebrachial muscles seen in Gallus.

Manual muscles

The manual muscles of Apteryx and Dromaius are considerably reduced or lost in relation to the reduction of manual bones. All manual muscles shown in Table 2 are absent. However, Struthio and Rhea retain almost all of these muscles, and the muscles relating to the pollex are well developed. The polluces of these species do not function like the alula in volant birds, but they have an increased range of motion, based on the morphology of their first matacarpophalangeal joint. Eudromia retains all manual muscles seen in Gallus except for M. extensor indices brevis, and the muscles related to the pollex are more similar to those of Gallus than Struthio and Rhea.

Thigh muscles

Compared to the forelimb, the muscles of hindlimb are quite developed in ratites. An example is seen in Mm. femorotibiales, which has is very large and branches into more than three parts in all ratites. There is a problem with the terminology M. femorotibialis lateralis (= externus) and intermedius (= rmedius) (Gangl et al., 2004); the intermedius slip is quite expanded and completely covers the original externus part in many ratites. Some authors, therefore, regarded this slip as M. femorotibialis lateralis proximal part (MCGOwan, 1979; PaTak & BalDwin, 1998; PiCaSSO, 2010). ZinOVieV (2006) claimed the intermedius shouled be attributed to M.


ble

3. H

indl

imb

mus

cles

of r

atite

s Gal

lus a

nd E

udro

mia

.

Eu

drom

ia

Stru

thio

Rh

ea

Dro

mai

us

Apte

ryx

Gal

lus

Syno

nym

C

omm

ents

Aut

hors

M

uscl

es

Our

ob

serv

atio

n +

HU

DSO

N

et a

l. (1

972)

Our

ob

serv

atio

n +

GA

NG

LE

et a

l. (2

004)

Our

ob

serv

atio

n +

PIC

ASS

O

(201

0)

P ATA

K &

B

ALD

WIN

(1

998)

MC

GO

WA

N

(197

9)

Our

ob

serv

atio

n +

YA

SUD

A

(200

2)

Thig

h m

uscl

es

iliot

ibia

lis

cran

ialis

O

O

O

O

O

O

sa

rtoriu

s

iliot

ibia

lis

late

ralis

O

2 p

arts

O

3 p

arts

O

2 p

arts

O

2 p

arts

O

1 p

arts

O

2 p

arts

te

nsor

fasc

ia la

tae

&

bice

ps fe

mor

is

ambi

ens

O

O

O

O

O

O

rect

us fe

mor

is

iliof

ibul

aris

O

O

O

O

O

O

bi

ceps

fem

oris

/ se

mite

ndin

osus

flexo

r cru

ris la

tera

lis

(pel

vica

) O

O

O

O

O

O

se

mim

embr

anos

us/

sem

itend

inos

us

flexo

r cru

ris la

tera

lis

(acc

esso

ria)

O

O

O

O

O

O

fle

xor c

ruris

med

ialis

O

O

O

O

O

O

grac

ilis

caud

ofem

oral

is

pars

cau

dalis

O

O

X

X

O

O

pi

rifor

mis

par

s ili

ofem

oral

is

caud

ofem

oral

is

pars

pel

vica

O

O

O

O

O

?

pirif

orm

is p

ars

caud

ofem

oral

is

abse

nt in

Eu

drom

ia

(HU

DSO

N e

t al.,

19

72)

isch

iofe

mor

alis

O

O

O

O

O

O

qu

adra

tus f

emor

is

iliot

roch

ante

ricus

cr

ania

lis

O

O

O

O

O

O

glut

eus m

ediu

s

ili

otro

chan

teric

us

med

ius

O

X

O

O

O

O

glut

eus p

rofu

ndus

iliot

roch

ante

ricus

ca

udal

is

O

O

O

O

O

O

iliof

emor

alis

cau

dalis

iliof

emor

alis

in

tern

us

X

O

O

O

O

O

iliac

us, c

uppe

dicu

s

pres

ent i

n Eu

drom

ia

(HU

DSO

N e

t al.,

19

72)

iliof

emor

alis

ex

tern

us

O

O

O

O

O

O

glut

eus s

uper

ficia

lis

pect

ineu

s

X

O

X

X

X

X

se

nsu

MEL

LET

(199

4)

obtu

rato

rius

med

ialis

O

O

O

O

O

O

in

tern

us

obtu

rato

rius

late

ralis

O

O

O

O

O

O

ex

tern

us

pubo

isch

iofe

mor

alis

O

O

O

O

2 p

art

O

O

addu

ctor

long

us

med

ialis

and

la

tera

lis

The Appendicular Anatomy of the Elegant Crested Tinamou (Eudromia elegans) 43Ta

ble

3. C

ontin

ued.

Eu

drom

ia

Stru

thio

Rh

ea

Dro

mai

us

Apte

ryx

Gal

lus

Syno

nym

C

omm

ents

Aut

hors

M

uscl

es

Our

ob

serv

atio

n +

HU

DSO

N e

t al

. (19

72)

Our

ob

serv

atio

n +

GA

NG

LE e

t al

. (20

04)

Our

ob

serv

atio

n +

PIC

ASS

O

(201

0)

P ATA

K &

B

ALD

WIN

(1

998)

MC

GO

WA

N

(197

9)

Our

ob

serv

atio

n +

YA

SUD

A

(200

2)

Thig

h m

uscl

es

fem

orot

ibia

lis

late

ralis

O

O

O

O

O

O

ex

tern

us/v

astu

s la

tera

lis

fem

orot

ibia

lis

acce

ssor

ius

X

O

O

O

O

X

se

nsu

MEL

LET

(199

4)

fem

orot

ibia

lis

inte

rmed

ius

O

O

O

O

O

O

med

ius/

late

ralis

fem

orot

ibia

lis

med

ialis

O

O

O

O

O

O

in

tern

us

Cru

ral m

uscl

es

tibia

lis

cran

ialis

O

O

O

O

O

O

ex

tens

or d

igito

rum

lo

ngus

O

O

O

O

O

O

fib

ular

is

long

us

O

O

O

O

O

O

fibul

aris

br

evis

O

smal

l O

smal

l X

X

O

O

ga

stro

cnem

ius

late

ral h

ead

O

O

O

O

O

O

gast

rocn

emiu

s m

edia

l hea

d O

O

O

O

O

O

gast

rocn

emiu

s su

pram

edia

lis

X

O

O

O

X

X

desc

ribed

as

inte

rmed

ia c

auda

lis in

D

rom

aius

gast

rocn

emiu

s in

term

edia

l he

ad

O

O

O

O

O

O

FPP

II

O

X

O

O

O

O

FPP

III

O

O

O

O

O

O

FP II

O

X

O

O

O

O

FP

III

O

X

O

O

O

O

FP IV

O

O

O

O

O

O

pl

anta

ris

O

X

O

O

O

O

flexo

r hal

luci

s lo

ngus

O

O

O

O

X

O

fle

xor d

igito

rum

lo

ngus

O

O

O

O

O

O

po

plite

us

O

O

O

O

? O

Daisuke Suzuki, Kentaro Chiba, Collin S. VanBuren & Tomoyuki OhaShi44Ta

ble

3. C

ontin

ued.

Eu

drom

ia

Stru

thio

Rh

ea

Dro

mai

us

Apte

ryx

Gal

lus

Syno

nym

C

omm

ents

Aut

hors

M

uscl

es

Our

ob

serv

atio

n +

HU

DSO

N e

t al.

(197

2)

Our

ob

serv

atio

n +

GA

NG

LE e

t al.

(200

4)

Our

ob

serv

atio

n +

PIC

ASS

O

(201

0)

P ATA

K &

B

ALD

WIN

(1

998)

MC

GO

WA

N

(197

9)

Our

ob

serv

atio

n +

YA

SUD

A

(200

2)

Peda

l mus

cles

lu

mbr

ical

is

O v

estig

al

O

O v

estig

ial

O

O

O v

estig

ial

abdu

ctor

dig

iti II

O

X

O

O

O

O

ad

duct

or d

igiti

II

O

X

O

O

? O

ex

tens

or d

igiti

III

prop

rius

O

O

O

O

O

O

ex

tens

or d

igiti

III

brev

is

O

O

O

O

O

O

exte

nsor

dig

iti IV

br

evis

O

O

O

X

O

O

ab

duct

or d

igiti

IV

O

O

O

O

O

O

addu

ctor

dig

iti IV

X

X

X

O

X

X

ex

tens

or d

igiti

IV

flexo

r hal

luci

s

brev

is

X

X

X

X

X

O

exte

nsor

hal

luci

s lo

ngus

X

X

X

X

O

O

femorotibialis externus pars proximalis in Struthio based on other avian anatomy and previous studies. Also he claimed pars accessorius (sensu Gangl et al., 2004) might be appropriately attributed to the “distal part of M. femorotibialis intermedius.” These ideas of ZinOVieV (2006) are reasonable, but there are no evidences based on anatomical structure or development patterns. It is need to investigation of the pelvic and femoral muscle of ratites. In Eudromia, there is no confusion in terminology of Mm. femorotibiales because the intermedius part is not as large as that of other ratites. M. femorotibialis intermedius is located “medially,” between M. femorotibialis medialis and externus (see Fig. 21C). M. iliotibialis lateralis in other ratites is broader than that of Eudromia and Gallus and has a clear border between pars pre- and post-acetabularis. Another characteristic of many ratites is a reduced M. iliotrochantericus caudalis, espetially in Strutio and Dromaius. However, Rhea and Apteryx have relatively large M. iliotrochantericus caudalis. While ZinOVieV (2006) challenged the Gangl et al. (2004)’s muscular identification; he suggested M. iliotrochantericus caudalis was fused M. iliofemoralis externus and Gangl et al. (2004)’s M. iliotrochantericus caudalis should be M. iliotrochantericus medius. Since M. iliofemoralis externus of Struthio has two insertional tendons, and it was odd character not seen in other aves. If this interpretation is confirmed, the M. iliotrochantericus medialis was not lost in Struthio and the muscle has rather developped. That problem is not applicable to Dromaius because M. iliofemoralis has only one insertional tendon. In either case, the reduction of M. iliotrochantericus caudalis in Struthio and Dromaius might be real comparing to that of Eudromia and Gallus (see description). The ratites tend to have diminished or absent M. caudofemoralis pars caudalis, but a developed pars pelvica. In addition, M. ischiofemoralis is considerably diminished, except in Apteryx. In Eudromia, M. caudofemoralis pars pelvica is also thinner or absent (HuDSOn et al., 1972) and is more strongly developed than M. ischiofemoralis. M flexor cruris medialis in Struthio is smaller and has a shorter belly with a long tendon, compared with its morphology in Eudromia and Gallus; however this muscle in other ratites, such as Dromaius, Apteryx, and Rhea, is rather similar to that of Eudromia. The hip extensor/knee flexor muscles are also considerably larger due to enlargement of the postacetabular area of the ilium. Although the number of the thigh muscles is reduced in some ratites due to the missing M. caudofemoralis pars caudalis, the volume of the muscles is larger than those of volant birds. Eudromia and Gallus also possess well-developed thigh muscles, but the proportional volume is smaller than those of other ratites.


Crural muscles

Among the crural muscles, the number of the parts and proportional size of M. gastrocnemius is highly variable among the ratites. The terminology is also variable. Struthio, Rhea and Dromaius have four heads of this muscle (Gangl et al., 2004; PaTak & BalDwin, 1998; ZinOVieV, 2006; PiCCaSO, 2010) and Apteryx has three (MCGOwan, 1979). The general avian M. gastrocnemius is divided into three heads, pars medialis, pars lateralis and pars intermedius (Baumel, 1993). The fourth head, pars supramedialis (sensu Gangl et al., 2004) branches from pars medialis. PaTak & BalDwin (1998) named this fourth slip as intermedia pars caudalis in Dromaius. In Rhea, PiCaSSO (2010) used simply “fourth part”, which corresponds to pars supramedialis. ZinOVieV (2006) was claimed this pars supramedialis should be attributed M. plantaris because the morphology is similar to M. plantaris of other birds, except for fusing M. gastrocnemius pars medialis. The largest slip of M. gastrocnemius in ratites is generally the pars medialis. The pars medialis in Apteryx is 50 % larger than pars lateralis (MCGOwan, 1979) and a similar condition is seen in Rhea (PiCaSSO, 2010, Fig. 12b). M. gastrocnemius pars medialis in Dromaius is slightly larger than pars lateralis (PaTak & BalDwin, 1998, Fig. 6), while pars medialis in Struthio is roughly the same size as pars lateralis (Gangl et al., 2004, our observation). M. gastrocnemius pars medialis does not function as a knee flexor because it originates from the proximal tibia. These size differences might affect the gait and running. The pars medialis of Eudromia is quite larger than pars lateralis. In addition, many ratites have a reduced hallux, except for Apteryx, and the related muscles are missing. Eudromia has also lost the hallux and some related muscles, such as M. flexor hallucis brevis and M. extensor hallucis longus.

Phylogenetic Position of Tinamiidae and Future Impication for Evolution of Flight

The monophyly of palaeognaths is well supported by both morphological and molecular data (CraCrafT, 1974; CaSperS et al., 1994; SlaCk et al., 2007). However, the relationships of Tinamidae with other members of Palaeognathae are still debated. Traditionally, Tinamidae was considered the outgroup of ratites (ostriches, kiwis, rheas, emus, and cassowaries) because of their similarity to volant neornithine birds (CraCrafT & Clarke, 2001; LiVezey & ZuSi, 2007). Understanding these relationships is important for reconstructing the vicariant events that led to the current distribution of flightless palaeognathes, given their inability to cross large geographical barriers, such as the oceans that often separate closely related genera. Currently, the divergence dating for Palaeognathae predates the separation of continents on which many flightless species live. Some have therefore doubted the monophyly of the flightless

ratites (DaVieS, 2002; BriggS, 2003), which has been supported by recent molecular phylogenies (SlaCk, 2007; HarShman et al., 2008, PhilipS et al., 2010; SmiTh et al., 2012) and earlier morphological phylogenies (e.g., ElzanOwSki, 1995). In some of these analyses, Struthio (the ostrich) is recovered as the outgroup to all other palaeognathes, and tinamids are the sister group to the now-extinct moas of New Zealand (e.g., SmiTh et al., 2012). This topology suggests that flightlessness may have evolved multiple times in palaeognathes, although this hypothesis is less parsimonious than a single reversal in tinamids to the ancestral volant state. If tinamous did experience a reversal and are secondarily volant, they may be a model system for studying the evolution of flight in vertebrates. In order for a parsimonious hypothesis for character evolution to be rejected, contrary evidence of character acquisition is required. In this example, it needs to be shown that all flightless palaeognathes differ in either their mechanisms that cause the reduced development of their flight features and/or the anatomy of features ancestrally related to flight (e.g., wings) to falsify this hypothesis. We hope that our anatomical description has allowed for further investigation into the anatomy of one member of Palaeognathae to inspire future research to examine the interesting anatomy of this important clade.

ACKNOWLEDGEMENTS

We wish to thank Dr. Akinori AzumanO (Zoorasia Yokohama Zoological Gardens), Drs. Kyoko Iwami and Takeshi YamaSaki (Yamashina Institute of Ornithology), Drs. Makoto Manabe and Isao NiShiumi (National Museum of Nature and Science), Ryoko MaTSumOTO (Kanagawa Prefectural Museum of Natural History) for providing the Eudromia specimens. We also thank John HuTChinSOn and an anonymous reviewer for helpful feedback on earlier versions of this manuscript.

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