Crocodylian forelimb musculature and its relevance to Archosauria

Authors

  • Mason B. Meers

    Corresponding author
    1. Department of Cell Biology and Anatomy, Johns Hopkins University School of Medicine, Baltimore, Maryland
    • Department of Biology, University of Tampa, 401 W. Kennedy Blvd., Tampa, FL 33606-1490
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Abstract

The musculoskeletal anatomy of the crocodylian forelimb is documented to facilitate functional morphological studies of extant and extinct archosaurs. Comparative descriptions of muscles of the forelimb of several crocodylian species are presented, including attachment sites, innervation, and anatomical functions. The muscular anatomy of the crocodylian forelimb is highly conservative among the different species; however, interspecific differences do occur. Interspecific anatomical variation is interpreted functionally, and discussed in the context of the terrestrial locomotion of crocodylians as it applies to the forelimb. In addition, muscular apomorphies are identified among a phylogenetically diverse sample of extant crocodylians, providing insight into the evolution of forelimb anatomy in a clade of archosaurs possessing highly variable terrestrial locomotor behaviors. Anat Rec Part A 274A:891–916, 2003. © 2003 Wiley-Liss, Inc.

The archosaurian forelimb is perhaps one of the most functionally diverse structures of the tetrapod body, although its morphology has remained surprisingly consistent. Over the 220 million year history of the clade, the forelimb has evolved to facilitate cursorial locomotion in a variety of taxa (e.g., Sebecus, Terrestrisuchus, various Ornithopod dinosaurs, and others). It acts as a flipper in aquatic crocodyliforms (Metriorhynchus, Teleosaurus, and their relatives), as a pillar in graviportal locomotion among sauropod dinosaurs, and even as a propulsive organ in powered flight in two clades (pterosaurs and birds). Consequently, a thorough knowledge of the anatomy of the forelimb in extant archosaurs (crocodylians and birds) has the potential to impact our understanding of major morphological transformations in locomotor anatomy. Moreover, given the phylogenetically important position of Crocodylia within Archosauria, delineating the anatomy of the crocodylian forelimb is critical to establishing the primitive condition for members of this clade. Various works on extant crocodylian locomotion have demonstrated variability among these taxa (Cott, 1961; Bustard and Singh, 1977; Webb and Gans, 1982), which suggests that intrinsic interest in the crocodylian forelimb is equally justified (see Meers, 1999, 2002). In this light, it is surprising that the muscular anatomy of the forelimb has not been thoroughly documented previously. Indeed, this deficit represents one of the most surprising omissions in the anatomical sciences today, particularly given the numerous studies published regarding the forelimb in several avian taxa.

The study of the anatomy of crocodylians has one of the longest histories of any taxon, beginning in 440 B.C. when Herodotus made the first observation of crocodylian anatomy by incorrectly observing that the crocodile's “upper jaw” (rather than its lower) is hinged (Komroff, 1936)—clearly an erroneous observation of basking Nile crocodiles (Crocodylus niloticus). In slightly more modern times, Goüye (1688) offered the first published dissection of a crocodylian (C. niloticus); however, that work was temporally preceded by Duverney, whose study was published posthumously in 1734 (Duverney, 1734; Ahrenfeldt, 1953). Most of the 17-century works on crocodylians were of a similarly elementary nature, simply noting the presence or absence of major features (e.g., scutes). It was not until the 19th century that the musculoskeletal anatomy of crocodylians commanded the attention of the great comparative anatomists of the time (e.g., Buttman, 1826; Meckel, 1828; Dumeril, 1835; Pfeiffer, 1854; Stannius, 1856; Haughton, 1866; Rolleston, 1868; Rüdinger, 1868; Fürbringer, 1876; Ribbing, 1907).

Fürbringer (1876) was the first to provide a description of the crocodylian shoulder and brachium in a juvenile Crocodylus acutus, which he figured in some detail. His report was limited to the shoulder and brachium, undoubtedly due to the very small size of specimens available to him at the time. Of historical interest, Fürbringer's system for muscle nomenclature was developed in part through that work, and subsequently has been applied broadly to reptiles, despite its tendency to obscure homology in anatomical work (Davis, 1936). It was not until Ribbing's (1907) work on Alligator mississippiensis, Caiman crocodilus, and Crocodylus acutus that the antebrachium received any attention in the literature. Haines (1939) later clarified Ribbing's work on the extensor musculature of the antebrachium in A. mississippiensis, although this excellent work appears to have gone largely unnoticed in subsequent years. More recently, Jenkins (1993) presented some details of shoulder anatomy in A. mississippienisis, although this clearly was not the focus of his work, while Meers et al. (1993) used the pilot work for the present study in the reconstruction of forelimb musculature in dinosaurs. As a consequence of the limited treatment of the crocodylian forelimb among the classic comparative anatomical works, the manus and portions of the antebrachium have gone entirely undescribed, and the remainder of the forelimb has only been briefly treated.

The crocodylian forelimb is unique among extant tetrapods in the range of variations in limb posture it may adopt (Meers, 1999, 2002), some of which place differing mechanical demands on anatomical components (Haines, 1946; Holmes, 1980; Landsmeer, 1984). Consequently, the study of crocodylians provides a unique opportunity to examine the relationships between anatomy and function in a clade that is derived from more dedicated terrestrial taxa (possibly specialized cursors) (Reilly and Elias, 1998; Meers, 1999), and that now exhibits a wide range of locomotor behavior. Further, it is a thorough understanding of the soft tissues of extant phylogenetically relevant taxa that enables us to understand the form and inference of function in extinct taxa (Bryant and Russell, 1992; Witmer, 1995). It follows, then, that elucidating the locomotor transformations from early crocodyliforms (sensu Clark, 1994) to the varied locomotor behaviors of extant taxa first requires a full understanding of the anatomy of the locomotor apparatus in the extant species. Thus, this research extends our knowledge of the soft-tissue anatomy of crocodylians both taxonomically and regionally.

MATERIALS AND METHODS

The specimens used in this research were acquired through a variety of sources to minimize the impact of dissection on preserved specimens in museum collections. Since Gans (1952) found a high degree of variation in his study of the snake genus Dasypeltis, he argued that morphological studies (such as the present study) should incorporate as large a sample as possible. However, Raikow et al. (1990) found very limited individual variation in avian muscular anatomy, and suggested that the problem is at best ambiguous. Perhaps more importantly, the current political and ecological situations surrounding most species of crocodylian clearly inhibit the ability of museums to replace valuable specimens sacrificed to dissection. Consequently, most specimens in this research originated from private captive breeding facilities. In no case was any animal killed for this research. All of the specimens died from natural causes or via the normal operating procedures of the institutions housing them during life.

The sample available for dissection included representatives of the major subclades of Crocodylia, as well as the outgroup to all other taxa, G. gangeticus (see Table 1). In addition to phylogenetic diversity in the sample, ecological diversity was ensured by the inclusion of G. gangeticus, the most aquatic living crocodylian, and A. mississippiensis, a well-studied generalized species. Unfortunately, none of the more terrestrially active crocodylians (Crocodylus rhombifer, C. novaeguineae, etc.) were available for this study.

Table 1. Dissection specimens
TaxaNumber (adults/juveniles)Source of specimens
Alligator mississippiensis4 (2/2)D. Weishampel, L. Witmer, St. Augustine Alligator Farm (SAAF)
Crocodylus siamensis1 (0/1)SAAF
Crocodylus acutus2 (1/1)P. Moler, Florida Wildlife Research
Osteolaemus tetraspis2 (0/2)SAAF
Gavialis gangeticus1 (0/1)American Museum of Natural History, AMNH 81802

The use of captive animals in anatomical research has been controversial at best. While captive and wild animals clearly differ in their osteological morphology and biomechanical properties (Hollister, 1917; Hilzheimer, 1937; Björk, 1950; Kingdon, 1984; Meers, 1999, 2002), soft-tissue anatomical details have not been shown to differ in any significant way other than muscle mass, which is not a component of this research. This justifies the use of captive specimens in the present study. Where qualitative assessments of muscular development have been made, all efforts have been made to restrict comments to wild-killed individuals.

The specimens that were dissected for this research were either preserved by submersion in 10% neutral buffered formalin solution, with subsequent preservation in 95% ethyl alcohol (to reduce noxious gasses released from formalin-fixed specimens), or dissected without preservation after being temporarily frozen. Standard dissection techniques were utilized to determine muscle origin, insertion, relationships, and innervation. The architecture was noted by visual inspection of the muscle bellies. In some very small specimens, dissection was aided by the use of a Nikon dissecting microscope. Dissection was documented through the use of photographs, illustrations, and direct application of insoluble ink to the periosteum for purposes of defining muscle attachment sites.

Discussions of muscle function are usually problematic in anatomical research unless the function is explicitly defined (Walker, 1973). Consequently, descriptions of muscle actions are inferred from morphological (geometrical) relationships to bones and articular surfaces of relevant elements. In other words, functions are described from an anatomical, rather than physiological or kinematic, perspective. Consequently, it should be understood that speculation about the in vivo functions of a muscle may be made based on qualitative assessments of relative size, mechanical advantages, etc. It is indeed possible, for example, that muscles described herein as abductors of a joint may act solely as a stabilizer of that joint during life. Nonetheless, purely anatomical descriptions of muscle function are a legitimate means of documenting anatomical function (Walker, 1973). Moreover, the utility of these descriptions is enhanced, as homologous muscles in other taxa may be best studied with reference to anatomical, rather than kinematic, function. When available, unpreserved specimens were utilized in this research for determination of function through postmortem manipulation of limbs via muscle tendons.

Descriptions of anatomy necessarily require the use of relative anatomical terms, such as cranial, caudal, medial, lateral, etc. The use of these terms in this work was based on the sprawling, or “low walk” (sensu Reilly and Elias, 1998), posture of the crocodylian forelimb (Fig. 1). Consequently, the scapulocoracoid presents relatively flat medial and lateral surfaces, while cranially and caudally it is represented by edges. Because of its nearly horizontal resting position, the humerus has both dorsal and ventral surfaces, and a nearly horizontal long axis. The long axis runs both mediolaterally and craniocaudally; therefore, the surfaces of the humerus perpendicular to the dorsal surface can be described as either cranial/lateral or medial/caudal, respectively. The antebrachium possesses a nearly vertical posture, yielding cranial and caudal surfaces in addition to medial and lateral surfaces. Finally, the manus presents a dorsal, or extensor, surface as well as a palmar, or flexor, surface. The axial midline of the manus is defined here to run through the middle of the third digit; however, this may not represent the functional axis of the manus during locomotion.

Figure 1.

Crocodylian forelimb posture and anatomical position. The right forelimb skeleton in anatomical position is shown here from a craniolateral view. Note that the scapula is nearly vertical in orientation, while the coracoid adopts a more horizontal posture. The humerus adopts a near horizontal posture, creating dorsal and ventral surfaces (extensor and flexor surfaces, respectively). The resulting medial and lateral surfaces of the humerus roughly equate to the surfaces visible in a walking crocodylian. The subvertical orientation of the antebrachium results in cranial, caudal, medial, and lateral surfaces for the radius and ulna, while the manus retains a traditional orientation.

Since the osteology of the crocodylian forelimb was described previously (Mook, 1921; Knüsel, 1944; Romer, 1944), these descriptions are referred to in the present work. However, in order to clarify explanations of origins and insertions, osteological elements are figured below.

Terminology has long been a problem with reptilian musculature due to confusion regarding muscular homologies (Davis, 1936). Consequently, muscle names applied in this research reflect hypothesized homologies to other tetrapod groups—primarily Aves, the sister taxon of Crocodylia—as determined in the literature (e.g., Getty, 1975; McGowan, 1986; Baumel et al., 1993) and ongoing research (Meers et al., 1993; unpublished results). Where homologous nomenclature obscures muscle function or attachment sites, the conventions of the Nomina Anatomica Veterinaria (Habel et al., 1983) are followed.

RESULTS

Organization of the Crocodylian Forelimb

The organization of the crocodylian forelimb is similar to that of most tetrapods. Organizationally, extrinsic forelimb musculature attaches the pectoral girdle to the axial skeleton, although a bony attachment is present between the coracoid and the interclavicle (Romer, 1956). The brachium is divisible into an extensor compartment and a flexor compartment. However, the nerve supplies to each compartment are not as clearly defined as in other tetrapods (e.g., mammals (Harris, 1939)). The antebrachium is also divisible into flexor and extensor compartments, and presents an organization consistent with that of squamates, chelonians, and birds (e.g., Howell, 1936; Walker, 1973; Baumel et al., 1993). The manus presents a relatively primitive organization as well, with a large number of intrinsic extensor muscles that are common in “reptilian” grade tetrapods (e.g., Haines, 1939; Walker, 1973). Muscles are innervated by the ventral rami of spinal nerves (SN) VII–XI, which together constitute the brachial plexus and present an innervation pattern largely consistent with that of other tetrapods (Harris, 1939; personal observation).

Brachial Plexus

The crocodylian brachial plexus is formed by SN VII–XI (Giffin, 1990), with XI occasionally omitted (Fig. 2). Each SN root gives rise to “trunks,” which in turn give rise to dorsal and ventral divisions. The union of the various divisions results in the formation of dorsal and ventral cords, as noted by Henle in the 19th century (Henle, 1871). These cords then give rise to terminal branches (such as the radial n., axillary n., etc.) that supply the muscles themselves. The resulting distribution of nerves is more or less consistent across Tetrapoda, and is thus a useful tool for discerning homology (e.g., Henle, 1871; Fürbringer, 1888; Cunningham, 1891; Haines, 1935; Harris, 1939).

Figure 2.

Brachial plexus (Alligator mississippiensis). Structurally, the brachial plexus of Alligator mississippiensis is nearly identical to that of other species examined. SN roots from VII–XI may contribute to the brachial plexus. Terminal branches of the dorsal and ventral cords are consistent with those of other tetrapods. Note that the nerve to m. humeroradialis (a powerful flexor of the antebrachium) is a branch of the axillary nerve, indicating its developmental origin from dorsal musculature.

The morphology of the brachial plexus is highly conservative among the species examined here, with interspecific differences consistent with the intraspecific variation found in A. mississippiensis, the most widely sampled species represented in this study. Previously, Fürbringer (1876) figured the brachial plexus of C. acutus, and Harris (1939) figured the brachial plexi of three crocodylian species (Caiman crocodilus, Crocodylus acutus, and Crocodylus niloticus). The variations in anatomical detail shown in these earlier works likely reflects small sample sizes, poor preservation quality, and primitive dissection techniques rather than true apomorphic characters for these species. Nevertheless, the small sample size of the present study warrants the qualification that discrepancies exist within Crocodylia, as described in previous works as well as in the present study.

Morphology

Proximal to the formation of the dorsal and ventral cords, a few muscular branches arise from the brachial plexus (Fig. 2), a situation that is common among tetrapods (e.g., Harris, 1939). Muscular branches from SN trunks or divisions typically innervate the musculature with a close axial affinity and limited involvement with the forelimb distal to the pectoral girdle.

The ventral cord is derived from the union of ventral divisions from SNs VIII, IX, and X, with variable contributions from SNs VII and XI. The ventral cord itself supplies developmentally-ventral musculature. For example, the muscles of the flexor compartment of the brachium (e.g., m. biceps brachii) are innervated by branches from the ventral cord, with one notable exception: m. humeroradialis. Similarly, the short dorsal cord is derived by dorsal divisions of SNs VIII, IX, and X, with possible contributions from SNs VII and XI. Again, the dorsal cord supplies developmentally dorsal musculature, such as the triceps brachii muscle complex, supplied by the radial n., a branch of the dorsal cord.

The ventral cord gives rise to a large number of muscular branches, including the supracoracoideus n., medianoulnar n., and ventral brachial cutaneous nerve. Subsequent muscular branches are derived from these nerves and supply the flexor, or ventral, musculature of the brachium and antebrachium (see also Harris, 1939).

The dorsal cord divides into its terminal branches, axillary n. and radial n., shortly after the the cord is formed from the dorsal divisions of the SNs. The cord itself thus gives rise to but a few muscular nerves (Harris, 1939; personal observation). Consequently, the radial and axillary nn. supply most of the remaining extensor musculature.

The species examined for this research showed little variation beyond what might reasonably be attributed to dissection error and the influence of variable muscle development. In some cases (one specimen each of A. mississippiensis, C. acutus, C. siamensis, and O. tetraspis), a contribution to the brachial plexus from SN VII could not be verified. The contribution found in remaining specimens was typically miniscule; therefore, no definitive differences were established. Similarly, the sole specimen of C. siamensis, one specimen of A. mississippiensis, and both O. tetraspis specimens lacked a contribution from SN XI to the brachial plexus. Again, the small size of these contributions found in other species means that the significance of the failure to find them in a few species is inconclusive. Unfortunately, the gharial (Gavialis gangeticus) specimen used in this research was not available for an in-depth dissection of the brachial plexus.

Extrinsic Musculature—Dorsal Group

The dorsal extrinsic forelimb musculature described here includes all muscles attaching to the dorsal axial skeleton and the pectoral limb or girdle.

M. trapezius.

M. trapezius is a thin but extensive sheet-like, fan-shaped, superficial muscle of the dorsal trunk, innervated by a branch from SN VII (Fürbringer, 1876). Overlying the craniodorsal portion of m. deltoideus scapularis and all of m. levator scapulae, it originates from the thoracodorsal fascia ventrolateral to the median row of dorsal scutes along the surface of the back. The origin may, in fact, appear nearly continuous with that of m. latissimus dorsi caudally, although it is always separable from it. M. trapezius then inserts either fleshily (C. acutus) or via a somewhat aponeurotic sheet (other species) along the cranial edge of the scapula, dorsal to the acromion (Fig. 3), covering some portions of the adjacent m. deltoideus clavicularis. Another portion of the insertion may occasionally pass caudodorsally over m. deltoideus scapularis (with some intermingling of fibers) to attach to the dorsal region of the lateral aspect of the scapula, between the origins of mm. deltoideus scapularis and teres major, in some variations seen in A. mississippiensis. In C. acutus, the insertion may extend dorsally to the suprascapular cartilage.

Figure 3.

Muscle map of the scapulocoracoid. Origins (red) and insertions (blue) are shown on the lateral surface of the crocodylian scapulocoracoid.

M. trapezius rotates the scapulocoracoid cranially, assisting in protraction of the forelimb. Cranial scapular rotation has been observed in living crocodylians during manual manipulation (personal observation, all species in this sample) and the “high walk” (personal observation, Crocodylus rhombifer). Protraction of the scapula likely occurs as an accessory stride-lengthening movement, increasing locomotor efficiency by a mechanism similar to that in chameleons (Peterson, 1984).

M. latissimus dorsi.

M. latissimus dorsi lies superficial to all other musculature of the dorsal trunk, overlying m. serratus ventralis thoracis and the caudal fibers of m. trapezius. Taking its origin from the thoracodorsal fascia cranially near the spinous process of the first dorsal vertebra, the origin continues linearly to approximately the level of the sixth dorsal rib. The sub-parallel fibers converge and give rise to a large, flat tendon that passes between m. triceps longus lateralis and the belly of m. scapulohumeralis brevis to insert onto the craniodorsal surface of the humerus in common with m. teres major. This insertion is characterized by a large scar at approximately one-quarter the shaft length from the head of the humerus (Figs. 4 and 5). This scar may take the form of a large tubercle or pit, and is found even in hatchling specimens. Occasionally, some fibers may leave the belly of this muscle to intermingle with those of the underlying mm. serratus ventralis thoracis and obliquus externus thoracis. This muscle is anatomically conservative, and presented no additional variation in the specimens utilized in this research.

Figure 4.

Muscle map of the crocodylian humerus. Origins (red) and insertions (blue) are shown on the lateral and dorsal views.

Figure 5.

Muscle map of the crocodylian humerus. Origins (red) and insertions (blue) are shown on the medial and ventral views.

M. latissimus dorsi is innervated by a branch from the axillary nerve, and acts as a strong extensor of the humerus, lifting the humerus dorsally. In addition, it may simultaneously rotate and retract the humerus to some degree.

M. levator scapulae.

M. levator scapulae is entirely overlaid by m. trapezius. The thick, broad, fan-shaped m. levator scapulae in turn overlies m. serratus ventralis cervicis. M. levator scapulae is parallel-fibered, but is substantially broader along its ventral margin, where it may reach three to four times the thickness of the muscle along its dorsal margin (Figs. 6 and 7). As is typical of this muscle across Tetrapoda, it originates from cranial cervical ribs, and inserts via a fleshy attachment to the cranial margin of the scapula for most of its length (Figs. 3, 6, and 7). Variation in the insertion was limited, with Crocodylus species exhibiting an insertion that extended onto the cranial margin of the coracoid.

Figure 6.

Dissection of lateral shoulder and brachial regions. To allow viewing of deep muscle structures, most muscles have been sectioned. Several overlying muscles have been removed (mm. pectoralis, trapezius, latissimus dorsi, and costocoracoideus). Note the unusual trochlea surrounding the tendon of m. humeroradialis.

Figure 7.

Dissection of the medial aspect of the shoulder and brachium of a crocodylian, illustrating the relationships of the muscles of these regions. Note the unusual tendon of origin for m. triceps longus caudalis.

Given its orientation, m. levator scapulae is a cranial rotator of the scapula. The difference in muscle cross-sectional area ventrally is likely a consequence of the relatively limited mobility of the ventral scapula, or mechanical advantage provided by a more lateral attachment. It thus seems likely that scapular rotation is an important part of crocodylian locomotion. Variation in coracosternal joint morphology is in fact significant among taxa; however, no functional hypothesis has been expressed to date. It is possible that variable mobility at this joint would be reflected by variation in the development of the m. levator scapulae. Note also that m. levator scapulae is an effective abductor of the neck, and hence the head, which is an important factor in some crocodylian feeding behaviors (personal observation).

M. levator scapulae is innervated by branches arising from SN VII. In the present study, this could not be verified in all specimens because of the preservation methods used and the small size of the specimens. This finding is in agreement with those of Fürbringer (1876); however, Harris (1939) was unable to confirm this contribution in the species he dissected.

Extrinsic Musculature—Ventral Group

M. pectoralis.

M. pectoralis is the most prominent muscle of the ventral surface of the crocodylian pectoral girdle (Fig. 8). It relates to m. levator scapulae craniomedially and is partly overlaid by this muscle; m. supracoracoideus longus lies craniolaterally to m. pectoralis (Fig. 8). This extensive, thick, parallel-fibered muscle completely overlies mm. costocoracoideus, sternocostalis, coracobrachialis brevis ventralis, and a portion of the tendon of m. biceps humerii. It also overlies m. obliquus externus thoracis, albeit not completely. M. pectoralis originates along the midline from the episternum, the ventral aspect of the sternum, the mesosternum, and the sternal portions of the thoracic ribs. However, this simple description of its origin obscures some of the complexity of this muscle. The crocodylian m. pectoralis is variably divided into two (cranial and caudal) or three (cranial, caudal, and deep) heads by the tendon of origin from m. levator scapulae. The cranial head takes its origin lateral to midline, with some fibers lying deep to the caudal head of m. pectoralis. The caudal head takes its origin primarily from the mesosternum, and most commonly from sternal portions of the first eight thoracic ribs. In one of the C. acutus specimens, the origin extended caudally to the first three gastralia. The irregular deep head arises deep to the caudal head from the ventrolateral surface of the mesosternum. All portions of m. pectoralis converge to insert fleshily onto the apex of the deltopectoral crest of the humerus, overlapping the insertion of m. deltoideus clavicularis.

Figure 8.

Ventral pectoral and brachial regions. Several muscles have been removed on each side to facilitate viewing deeper structures. On the left side, mm. brachialis and humeroradialis have been removed to show the origin of m. triceps brevis intermedius. On the right, mm. deltoideus clavicularis, pectoralis, and the supracoracoideus complex have been removed to show deeper structures.

The consequent “fan shape” of the muscle is unmistakable. M. pectoralis is a powerful adductor of the humerus, which aids in humeral retraction. Therefore, it is very likely that m. pectoralis plays a substantial role in the maintenance of limb posture in crocodylians, particularly during the high walk and gallop. This large muscle is innervated by a prominent branch from the ventral cord of the brachial plexus.

Mm. costocoracoideus.

The mm. costocoracoideus complex is composed of thick, parallel-fibered muscles that are clearly divisible into two bellies traversing the region from the coracoid to the lower thoracic ribs deep to m. pectoralis (Fig. 8). Collectively they serve to pull the coracoid caudally relative to the sternum. Because the caudal margin of the sternal articular surface of the coracoid ultimately acts as a pivot-point during this action, mm. costocoracoideus may be described as a caudal rotator of the pectoral girdle. The mobility of the coracosternal articulation was confirmed using several unpreserved specimens. This joint was always found to be somewhat mobile; however, this mobility varied among the examined taxa. The common innervation of these muscles is via branches from the ventral division of SN IX and the trunks of SNs X and XI.

M. costocoracoideus pars superficialis.

The superficial division of this muscle complex maintains an extensive, fleshy origin along the cranial edges of the first sternal rib and, to a lesser degree, on the second. The insertion is broadly along the caudal edge and adjacent dorsal region of the coracoid from the sternocoracoidal junction nearly to the glenoid rim, with occasional fibers also inserting directly on the sternum (Fig. 3). As noted above, the superficial head of the costocoracoideus complex serves to retract the coracoid, although the few fibers found to insert onto the sternum itself could act in retraction of the entire shoulder girdle. However, given the rarity of this occurrence and the small number of muscle fibers, movement or stabilization of the sternum is not believed to be a significant function of this musculature. In a few specimens of Alligator mississippiensis, the fibers of m. obliquus (hypaxial trunk musculature, outside of the scope of this study) clearly arose from within the belly of m. costocoracoideus pars superficialis. This arrangement was not observed in other taxa.

M. costocoracoideus pars profundus.

The much smaller deep costocoracoideus muscle originates more caudally, from the cranial surfaces of free ribs, and inserts deep to the craniolateral edge of the sternal plate as well as to the ventral surface of the proximocaudal coracoid (Fig. 3). Its action is expected to be similar to the overlying superficial musculature.

Pectoral Girdle Musculature—Dorsal Group

M. deltoideus scapularis.

M. deltoideus scapularis presents a bipinnate architecture in all of the species examined, indicating that this muscle possesses relatively great strength due to its increased physiological cross-sectional area. This prominent muscle of the craniodorsal surface of the scapula is bounded cranially by m. levator scapulae and the insertion of m. trapezius, and caudally by the belly of m. teres major (Fig. 6). The belly of m. deltoideus scapularis lies deep to m. trapezius cranially and m. deltoideus clavicularis cranioventrally, while its tendon of insertion overlaps the origins of both mm. triceps longus lateralis and triceps brevis cranialis, passing between m. deltoideus clavicularis and m. triceps longus lateralis.

M. deltoideus scapularis takes its fleshy origin from the lateral surface of the scapula and adjacent suprascapular cartilage, extending ventrally along the scapula slightly further than m. teres major (see below). M. deltoideus scapularis inserts via a strong, flat tendon along the caudolateral edge of the humeral head proximal to that of m. teres major and immediately adjacent to the origin of m. triceps brevis cranialis, and proximal to the prominent insertion of m. deltoideus clavicularis, while it lies deep to the belly of mm. deltoideus clavicularis and superficial to that of m. triceps lateralis. This is not to be confused with the insertion of mm. teres major and latissimus dorsi.

Given its large physiological cross-sectional area, and relatively poor mechanical advantage on the humerus, m. deltoideus scapularis likely is an important stabilizer of the shoulder joint. However, its use as a humeral abductor may also be important—primarily in fast, powerful movements of the humerus. Its innervation is via a branch of the dorsal cord, which it shares with m. latissimus dorsi.

M. teres major.

This prominent, superficial, strap-like muscle is found ventral to mm. latissimus dorsi and trapezius. M. deltoideus scapularis is cranial to m. teres major, and the former may be slightly overlaid by the latter. M. teres major originates on the caudodorsal aspect of the lateral surface of the scapular blade and slightly from the adjacent suprascapular cartilage directly caudal to the origin of m. deltoideus scapularis and cranial to the insertion of m. serratus ventralis thoracis (Fig. 6). The sub-parallel fibers of m. teres major insert via a strong, flat tendon in common with m. latissimus dorsi onto the proximal craniodorsal humerus directly opposite the apex of the deltopectoral crest. A qualitative variation in size was noted only in the presence of poorly developed m. teres major in C. acutus; other species exhibited similarly developed musculature. Some fibers of m. teres major were found to intermingle with those of m. latissimus dorsi in Alligator mississippiensis prior to the formation of its tendon. The conjoined insertion of these two muscles produces a prominent muscle scar on humeri in all crocodylian species, regardless of size or maturity.

Together with m. latissimus dorsi, m. teres major elevates the humerus and flexes the glenohumeral joint. It is innervated by branches from both the radial and axial nn (e.g., Fürbring, 1876; Harris, 1939).

M. deltoideus clavicularis.

This superficial, parallel-fibered muscle of the brachium lies immediately ventral to the tendinous insertion of m. trapezius, and overlies the ventral portion and insertion of mm. deltoideus scapularis and teres major (Fig. 6). M. deltoideus clavicularis relates to mm. supracoracoideus along its cranioventral margin, and entirely overlies m. coracobrachialis brevis dorsalis (Figs. 3, 4, and 6). The fleshy origin of m. deltoideus clavicularis is from the acromion process along the cranial margin of the scapula, primarily ventral to the process itself (some fibers may originate from the tendinous insertion of m. trapezius). Distally, it inserts onto the cranial aspect of the deltopectoral crest in a polygonal area terminating at a prominent muscle scar that lies between the distal end of this insertion and the proximal end of the origin of m. humeroradialis (Fig. 4). A distal slip of the muscle, found only in A. mississippiensis, attaches to a strong, intermuscular septum (lying between mm. humeroradialis and biceps brachii) that in turn runs the length of the humerus to the ligamentous sheath surrounding the tendon of m. humeroradialis. Consequently, this distal slip may be accurately described as inserting on the radius via the ligamentous trochlea associated with m. humeroradialis (see below). M. scapulohumeralis cranialis, a small, deep differentiation of m. deltoideus clavicularis, is absent in all of the species examined in this study, as also noted by Romer for Alligator mississippiensis (1944).

M. deltoideus clavicularis is a powerful protractor of the humerus and assuredly also supports the shoulder joint, particularly during the high walk. The auxilliary insertion of m. deltoideus clavicularis onto the proximal radius most likely acts as the primary protractor of the forelimb, and may also serve to promote antebrachial flexion during the swing phase of the forelimb. Its nerve supply is via a muscular branch of the axillary nerve.

M. subscapularis.

M. subscapularis is the long, thick, parallel-fibered, fleshy muscle that dominates the medial surface of the scapula, closely applied to m. scapulohumeralis caudalis (Fig. 7). M. subscapularis takes its origin from the medial surface of the scapula ventral to the insertion of m. serratus ventralis cervicis and cranial to the insertion of m. serratus ventralis thoracis, continuing as far ventrally as the constriction of the scapula (Fig. 3). Distally, it descends ventrally and slightly caudally between the body of the scapula and the complex tendon system of the m. triceps longus caudalis to converge abruptly and insert on the medial protruberance of the humerus via the joint capsule. Given its poor mechanical advantage for movement of the humerus, m. subscapularis likely serves as a stabilizer of the shoulder. However, humeral retraction and adduction cannot be ruled out as secondary functions on the basis of its geometry. M. subscapularis is innervated via the axillary nerve via a muscular branch it shares with m. scapulohumeralis caudalis (subscapular nerve).

M. scapulohumeralis caudalis.

M. scapulohumeralis caudalis is deep to mm. teres major, triceps longus lateralis, and latissimus dorsi (Fig. 6). It is completely overlaid by m. teres major and directly overlies the shoulder joint capsule. At this point it is closely applied to m. subscapularis, to the point where it is difficult to separate the two in dissection. This small, fleshy muscle originates from the lower portion of the caudal region of the dorsolateral surface of the scapula, just dorsal to the glenoid rim (Fig. 3). Its insertion is by converging fleshy muscle fibers onto the dorsum of the proximal humerus in a relatively broad, triangular area, bounded cranially by m. triceps brevis intermedius and caudally by m. triceps brevis caudalis (Fig. 4). Innervation is via two distinct branches of the axillary nerve, one in common with m. subscapularis (n. subscapular).

M. scapulohumeralis caudalis may elevate the humerus and assist in its protraction; however, given its diminutive size, it is more likely a stabilizer of the glenohumeral joint.

Pectoral Girdle Musculature—Ventral Group

Mm. supracoracoideus.

The mm. supracoracoideus complex comprises the primary protractors of the humerus in crocodylians. Their short, thick bellies cover the bulk of the body of the coracoid cranial to the glenoid (Figs. 3 and 6). The nerve to m. supracoracoideus is shared by all divisions and arises as a branch of SN VIII, although it may also incorporate fibers from SN VII.

M. supracoracoideus longus.

This muscle complex is dominated by m. supracoracoideus longus, a fan-shaped muscle of the shoulder. This muscle takes its extensive fleshy origin from the cranial half of the medial surface of the scapula and adjacent coracoid opposite the glenoid (Fig. 3). A slip of fibers are occasionally found originating along the cranial edge of the external surface of the coracoid shaft, but these are largely insignificant in mass. The muscle then inserts via a narrow fleshy attachment onto the cranial edge of the humerus at the apex of the deltopectoral crest (Figs. 4 and 5). It is important to note that this insertion lies ventral to the distal insertion of m. coracobrachialis brevis dorsalis, which in turn is ventral to that of m. deltoideus clavicularis, and slightly dorsal to the insertion of m. supracoracoideus brevis. In this position, m. supracoracoideus longus is a powerful protractor of the humerus and may also serve in adduction of this element. From a practical standpoint, this long head is often difficult to separate clearly from the other heads of the supracoracoideus complex, owing to intermingling of muscle fibers, and thus is the least likely to be distinguished in dissection.

M. supracoracoideus intermedius.

M. supracoracoideus intermedius is a relatively short, thick muscle compared to the long head in this complex. It inserts in common with the long head; however, its origin on the scapulocoracoid is restricted by the origins of the larger long and short heads of this muscle (Fig. 3).

M. supracoracoideus brevis.

M. supracoracoideus brevis is a relatively thin muscle that originates on the lower portion of the lateral surface of the acromion, and frequently on the adjacent coracoid (Fig. 3). Muscle fibers converge toward its short, wide, tendinous insertion on the deltopectoral crest of the humerus, just distal to the insertion of m. supracoracoideus longus and immediately ventral to the insertion of m. deltoideus clavicularis. M. supracoracoideus brevis protracts and adducts the humerus in concert with other portions of this complex. Similarly, it is closely related to other limb adductors and protractors—most notably m. pectoralis, with which it may extensively intermingle.

M. coracobrachialis brevis ventralis.

This extremely broad, fan-shaped muscle takes its extensive, fleshy origin (Figs. 6 and 7) from most of the ventral surface of the coracoid caudal and deep to the origin of m. biceps brachii, and cranial to the insertion of m. costocoracoideus superficialis (Fig. 3). The line of origin extends from very close to the sternum to immediately ventral to the coracoid foramen. In addition, the origin extends onto the scapula immediately cranial to the glenoid in C. acutus. The muscle fibers present an extensive, thick, fleshy insertion along the caudoventral surface of the deltopectoral crest in a broad triangular area that extends somewhat distally on the humeral shaft (Fig. 5). The insertion is bounded ventrally by the insertion of mm. supracoracoideus and pectoralis. It is bounded caudally by the origin of m. triceps brevis caudalis, and distally by m. triceps brevis intermedius.

The broad distribution of this muscle across the coracoid provides a range of functions for this muscle, as a result of the many lines of action it may adopt. These include flexion at the shoulder joint, as well as retraction, and adduction of the humerus. The innervation of m. coracobrachialis brevis ventralis is via the common coracobrachial nerve arising from the ventral cord at approximately the level of the pectoral nerve.

M. coracobrachialis brevis dorsalis.

This dorsal counterpart to m. coracobrachialis brevis ventralis is a decidedly much more gracile, fan-shaped muscle (Fig. 6). Its fleshy origin is from the dorsolateral cranial portion of the scapula, directly ventral to the acromion and caudal to the origin of m. supracoracoideus brevis, and caudoventral to m. deltoideus clavicularis (Fig. 3). The fibers converge abruptly to insert tendinously onto the cranioventral aspect of the joint capsule and adjacent deltopectoral crest just distal to the head of the humerus (Fig. 4). In this location, m. coracobrachialis brevis dorsalis probably acts primarily as a stabilizer of the head of the humerus in the glenoid, though it may assist in protraction and flexion of the forelimb. M. coracobrachialis brevis dorsalis takes its nerve supply from the ventral cord of the brachial plexus in common with that for m. coracobrachialis brevis ventralis.

Brachial Musculature—Extensor Compartment

Mm. triceps brachii.

The mm. triceps brachii of crocodylians consists of a large, complex mass of not three, but five muscle heads (Figs. 6 and 7). The two long heads (mm. triceps longus lateralis et caudalis) serve to flex the brachium on the shoulder, while all heads extend the antebrachium on the brachium, thereby supporting the body off the ground against gravity in a variety of postures. All heads derive their nerve supplies from the radial nerve, a branch of the dorsal cord.

Because of the complexity of the five heads, each one is discussed separately:

M. triceps longus lateralis.

M. triceps longus lateralis is a very long, superficial muscle on the cranial aspect of the dorsal brachium (Fig. 6). It originates by a broad, thick tendon from the lower portion of the lateral surface of the scapula immediately dorsal to the glenoid rim. This tendon typically leaves a prominent scar in all but the smallest hatchlings (Fig. 3). Dorsally, the origin is bordered by the origin of m. scapulohumeralis caudalis and caudally by the ventral portion of the insertion of m. serratus ventralis thoracis, and is largely overlaid by m. deltoideus scapularis. The parallel fibers of this muscle insert along the superficial triceps tendon to attach along the lateral aspect of the olecranon process of the ulna (Fig. 6).

Near its origin, the belly of m. triceps longus lateralis passes between the tendons of insertion of mm. teres major and deltoideus scapularis, while distally it relates to portions of m. triceps brevis cranialis and overlies m. triceps brevis intermedius (Fig. 6). Along its length it may occasionally be joined by fibers of m. triceps longus caudalis halfway down the length of the humerus.

M. triceps longus caudalis.

M. triceps longus caudalis is a long, broad, multipinnate, superficial muscle occupying the caudodorsal brachium (Fig. 7). The belly of m. triceps longus caudalis partially overlies the intermediate and caudal heads of mm. triceps brevis. In G. gangeticus the dominance of this belly is pronounced. The most striking feature of this muscle is its unusual tendon of origin, via a tendinous arc that attaches to both the scapula and the coracoid, immediately overlying the tendon of insertion of m. subscapularis. The tendinous arc is present in all species; however, different portions (pars coracoideus and pars scapularis) were dominant in different specimens, with no species-specific pattern.

The pars scapularis, which may be the dominant tendon of origin (based on thickness) in most individuals, attaches to the caudal edge of the scapula, dorsal to the glenoid rim. However, this tendon is joined by the tendon from the coracoid, displacing the line of action of the muscle ventrally. Some specimens of A. mississippiensis appear to exhibit a dominance of the pars coracoideus, which would indicate a dorsal displacement of the line of action in this unique muscle. Rarely, an occasional short accessory tendon may arise from the caudal aspect of the humeral head and attach near the center of this tendinous arc. This condition was observed in a single specimen each of A. mississippiensis and C. acutus. M. triceps longus caudalis inserts somewhat obliquely on the superficial triceps tendon, distal to the insertion of m. triceps longus lateralis (Fig. 7), and so functions in concert with the other heads of this complex.

M. triceps brevis cranialis.

M. triceps brevis cranialis lies immediately dorsal to the belly of m. humeroradialis, with the caudal border of m. triceps brevis cranialis lying along the distal half of m. triceps brevis intermedius (Fig. 6). Its origin is roughly linear, partially fleshy and partially aponeurotic, along the proximal craniodorsal humerus. This origin is bounded cranially by the tendon of insertion of mm. deltoideus scapularis, deltoideus clavicularis, and humeroradialis, and caudally by the tendon of insertion of mm. teres major and latissimus dorsi, and the origin of m. triceps brevis intermedius (Fig. 4). M. humeroradialis partially overlies the muscle belly of the short cranial head of mm. triceps brachii for most of its length, and may occasionally partially fuse to it. M. triceps brevis intermedius relates closely to the belly of m. triceps brevis cranialis caudally, while m. humeroradialis primarily relates to it distally. The majority of the muscle mass of this head is concentrated proximally. M. triceps brevis cranialis attaches to the common triceps tendon in a bimodal fashion, partially fleshy along the cranial and ventral surface of the superficial triceps tendon, and partially tendinous to the deep triceps tendon over the lateral epicondyle of the humerus.

M. triceps brevis intermedius.

M. triceps brevis intermedius relates to m. triceps brevis cranialis cranially, and to mm. humeroradialis and triceps brevis caudalis caudally (Figs. 6 and 7), with the radial nerve passing between it and m. humeroradialis. The most prominent muscle of the deep surface of the humerus, m. triceps brevis intermedius takes its fleshy origin from virtually the entire dorsal surface of the humeral shaft, wrapping around the shaft both cranially and caudally with each side nearly contacting the other beneath at approximately the mid-point of the humerus (Figs. 4 and 5). Cranially, the origin is bounded by that of m. triceps brevis cranialis and the insertion of m. scapulohumeralis caudalis, and is overlaid by the tendon of m. teres major. M. triceps brevis intermedius is distinct from the other heads of triceps; it inserts into the deep triceps tendon and is joined there by fibers of m. triceps brevis caudalis (Fig. 6).

M. triceps brevis caudalis.

M. triceps brevis caudalis takes its fleshy origin from the caudoventral surface of the caudal process of the humerus, just medial and distal to the humeral head (Fig. 5). This muscle is bounded proximally by the insertion of m. subscapularis, cranially by the insertion of m. scapulohumeralis caudalis (Fig. 4), and caudally by the origin of m. triceps brevis intermedius (Fig. 5). As a result of its origin from the variably developed caudal process of the humeral head, triceps brevis caudalis is variably displaced medially from the other short heads. The development of the caudal process may, in fact, serve primarily to alter the line of action of this muscle—hence the differences among species. The belly of this muscle is deep to m. triceps longus caudalis, and relates to this muscle dorsally and to m. biceps brachii ventrally (Fig. 7). This smallest division of the triceps system inserts onto the caudal surface of the deep triceps tendon.

Brachial Musculature—Flexor Compartment

M. biceps brachii.

The long, thin, superficial m. biceps brachii takes its origin via a very wide, long tendon from the cranial edge of the coracoid shaft near its base and immediately superficial to m. coracobrachialis brevis ventralis (Fig. 3) in all species except G. gangeticus. In this species, the origin is somewhat displaced onto the shaft of the coracoid. A large, prominent scar running parallel to the shaft of the coracoid is typically present in all species. The tendon of origin runs across the surface of m. coracobrachialis brevis ventralis (Fig. 8) and is overlaid by m. pectoralis and partially covered by m. supracoracoideus longus, while the belly begins distal to the head of the humerus (Fig. 6). The parallel-fibered m. biceps brachii inserts by way of a short tendon on the caudal aspect of the proximal radius just below the head, caudal to the prominent “radial” tuberosity (more properly termed the humeroradialis tubercle; see below). Occasionally, a poorly developed short head may originate slightly more proximally from the joint capsule in A. mississippiensis. As is typical of m. biceps brachii, the muscle flexes the antebrachium and simultaneously extends the humerus at the shoulder joint. The innervation of m. biceps brachii is via the medianoulnar nerve, the direct continuation of the ventral cord.

M. humeroradialis.

M. humeroradialis is a parallel-fibered, thick, robust, superficial muscle unique to archosaurs. Its large, fleshy origin from the craniodorsal surface of the proximal humerus, just distal to the deltopectoral crest, is highly scarred in all species of crocodylian and can be easily distinguished in most archosaurs (Fig. 4). The site of origin is separated from the insertion of m. deltoideus clavicularis proximally by a large, rugose muscle scar at all stages of development in crocodylians (even in hatchlings). The origin and belly of m. humeroradialis is bounded ventrally by the origin of m. brachialis, and dorsomedially by that of m. triceps brevis cranialis. The muscle scar of m. humeroradialis muscle may extend onto the ventral surface of the humerus in a linear extension of the epimysial sheath of this muscle. M. humeroradialis was surprisingly well developed in the G. gangeticus specimen examined, and was notably larger than a similar-sized A. mississippiensis.

The insertion of m. humeroradialis requires a detailed examination. A long, round tendon passes through a well-developed ligamentous trochlea attached to the proximal radius (Fig. 6). From this point, the tendon inserts onto the prominent humeroradialis tubercle (Figs. 9 and 10). The tubercle is so well developed in all species (including Gavialis gangeticus) that it is easily seen even in hatchlings. The insertion is slightly distal to that of mm. biceps brachii and brachialis inferior, and is bounded by the origin of m. supinator and the insertion of m. pronator teres.

Figure 9.

Muscle maps of the extensor surfaces of the radius and ulna, and the cranial surface of the radius. Muscle origins are shown in red and insertions are shown in blue.

Figure 10.

Muscle maps of the flexor surfaces of the radius and ulna, and the caudal surface of the ulna. Muscle origins are shown in red and insertions are shown in blue.

The robust nature of m. humeroradialis, and its stout tendon, make this muscle a strong flexor of the antebrachium. The presence of the ligamentous trochlea has the effect of altering the line of action of the muscle, locating the effective origin near the brachio-antebrachial joint, and so increases the speed of flexion of the antebrachium. Given the robusticity of the muscle belly and tendon, and the effect the trochlea has on the speed of antebrachial flexion, m. humeroradialis is likely an important muscle for fast flexion of the antebrachium during locomotion.

M. humeroradialis is an unusual flexor of the antebrachium, considering that it is innervated by the axillary nerve. Innervation from the dorsal cord of the brachial plexus indicates derivation of the muscle from the developmentally dorsal, or extensor, musculature (e.g., Fürbringer, 1888; Harris, 1939). Consequently, its function as a flexor of the antebrachium must be viewed as apomorphic. Further, the lack of evidence of the muscle in clades other than Archosauria (m. humeroradialis is homologous to m. tensor propatagialis in Aves (Meers et al., 1993)), leads to additional questions regarding the evolutionary origins of this unusual muscle.

M. brachialis.

M. brachialis inferior is a strap-like, parallel-fibered muscle that occupies the craniomedial surface of the brachium, compressed between the bellies of mm. biceps brachii and humeroradialis (Figs. 5–8). Taking a long, narrow origin from the cranioventral edge of the humerus along the deltopectoral crest distal to its peak (Figs. 4 and 5), it inserts onto the caudal surface of the caudal end of the radius in conjunction with the m. biceps tendon. As such, m. brachialis inferior serves as a flexor of the antebrachium on the brachium. Its innervation is via the medianoulnar nerve distal to the branch for m. biceps brachii.

Antebrachial Musculature—Extensor Compartment

M. supinator.

M. supinator is a large, well-developed, superficial muscle of the antebrachium that is innervated by a branch of the radial nerve. M. supinator is a prominent landmark of the antebrachium, relating to m. extensor carpi radialis longus laterally (Fig. 11) and m. pronator teres caudally (Fig. 12). Its belly overlies a portion of m. abductor radialis and is partially overlaid by m. extensor carpi ulnaris longus at its distal insertion (see below). Taking its origin from the proximal surface of the cranial epicondyle of the humerus (Fig. 4), with occasional attachments to the flexor surface of the humerus via the humeroradialis trochlea in some specimens, it inserts onto the cranial border of the radius in a linear fashion for most of its length, distal to the humeroradialis tubercle (Fig. 9). This muscle functions as a supinator of the antebrachium, and also assists in flexion of the antebrachium on the brachium.

Figure 11.

Dissection of the extensor region of the antebrachium. Superficial muscles were sectioned to allow access to deeper structures.

Figure 12.

Dissection of the flexor region of the antebrachium. Superficial muscles were sectioned to allow access to deeper structures.

M. extensor carpi radialis longus.

The parallel-fibered m. extensor carpi radialis longus lies between m. supinator cranially and m. flexor ulnaris caudally (Fig. 11). It is overlaid by m. abductor radialis and the radial head of m. extensor carpi radialis brevis. Its thin, fusiform, superficial muscle belly originates from a long, flat tendon anchored to the cranial epicondyle of the humerus just lateral to the origin of m. supinator and medial to the insertion of m. flexor ulnaris, with which it may fuse slightly in some individuals. Inserting via a well-defined tendon onto the dorsal edge of the proximal surface of the radiale, m. extensor carpi radialis longus extends the wrist, abducts the manus, and may provide some flexion and stabilization of the humeroradial joint. Its innervation is derived from the radial nerve, in common with m. supinator.

M. extensor carpi ulnaris longus.

M. extensor carpi ulnaris longus is a long, strap-like muscle lying along the cranial aspect of the antebrachium. This important extensor of the wrist overlies the head of m. extensor carpi radialis brevis pars ulnaris and m. abductor radialis (Fig. 11). The m. extensor carpi ulnaris longus originates tendinously from the cranial epicondyle of the humerus, immediately distal to the origin of m. extensor carpi radialis longus and proximal to that of m. extensor ulnaris (Fig. 4). In most taxa, the insertion is by a well-defined tendon to the base of metacarpal II; however, there may be some fusion with the tendon of m. abductor radialis in some specimens. In C. acutus, the tendon fans out superficially to attach to the extensor fascia overlying digit I. (Since both of the C. acutus specimens were dissected prior to preservation, it is possible that this delicate attachment was missed in other species examined.) Crossing the wrist joint and the carpo-metacarpo joint of the second digit, m. extensor carpi ulnaris longus extends the wrist and metacarpal II, while providing moderate flexion and stability of the elbow. The slight medial displacement of the insertion indicates that m. extensor carpi ulnaris longus may serve as a partial adductor of the manus. However, the diminutive nature of the lateral digits indicates a medially-displaced functional central axis in the manus, likely centering on digit II. Consequently, the insertion of m. extensor carpi ulnaris longus lies directly along the functional central axis of the manus. Innervation is via the radial nerve.

M. flexor ulnaris.

M. flexor ulnaris is a long, superficial muscle of the craniolateral surface of the antebrachium, with fibers diverging toward its sweeping insertion (Fig. 11). Its origin is from the epitrochlea, or cranial epicondyle, of the humerus (Fig. 4), with some fibers in common with those of m. extensor carpi radialis longus. M. flexor ulnaris inserts onto the craniolateral surface of most of the ulna, partially extending to the fascial septum between it and m. extensor carpi radialis brevis pars ulnaris (Fig. 9). This long, linear insertion differs from that in other vertebrates (e.g., Haines, 1950), possibly indicating a greater variation in the line of action associated with the maintenance of limb-posture in crocodylians. M. flexor ulnaris serves to flex the antebrachium. Its innervation via the radial nerve, however, betrays its evolutionary origin as an extensor.

M. abductor radialis.

The parallel-fibered m. abductor radialis lies deep to mm. supinator and extensor carpi radialis longus (Fig. 11), and takes its tendinous origin along the cranial epicondyle of the humerus, cranial to that of m. extensor carpi radialis longus (Fig. 4). Its fleshy insertion is to the proximal half of the cranial surface of the radius, adjacent to and continuous with the more distal origin of m. extensor carpi radialis brevis (Fig. 9). A slight septum separates the former from the latter. M. abductor radialis is an abductor of the antebrachium. However, its relatively poor lever-arm advantage implies a physiological function aimed more toward stabilizing the radius at its humeral articulation. Innervation is via the radial nerve.

M. extensor carpi radialis brevis.

In crocodylians, m. extensor carpi radialis brevis consists of two discrete heads: a pars radialis and a pars ulnaris. Together, these heads extend the wrist and adduct the manus. Both heads are innervated by muscular branches of the radial nerve.

M. extensor carpi radialis brevis pars radialis.

This small radial head, which lies deep to mm. supinator and extensor carpi radialis longus (Fig. 11), takes its fleshy, linear origin from the distal half of the craniomedial surface of the radius (Fig. 9), and inserts by a small diffuse tendon conjointly with that of insertion of the ulnar head of m. extensor carpi radialis brevis onto the dorsal edge of the proximal surface of the radiale (Fig. 11). This head also relates to the more distal fibers of the ulnar head caudally.

M. extensor carpi radialis brevis pars ulnaris.

The ulnar head of m. extensor carpi radialis brevis relates to the radial head cranially, and to m. abductor radialis caudally, while being overlaid by mm. flexor ulnaris and extensor carpi radialis longus (Fig. 11). In contrast to the radial head, the ulnar head is a large muscle that dominates the deep extensor region of the antebrachium. It takes its fleshy origin along the entire medial border from the radioulnar ligament to the distal expansion of the ulna (Fig. 9). Distally, its fibers converge to span the proximal wrist joint, and end in a short, broad tendon that is continuous with that of the radial head of m. extensor carpi radialis brevis. The tendon overlaps the belly of m. extensor digiti III in some specimens of Alligator mississippiensis, and inserts onto the axial/medial edge of the dorsal aspect of the proximal surface of the radiale in all species.

Antebrachial Musculature—Flexor Compartment

M. pronator teres.

The very large m. pronator teres can be found relating to the humeral head of m. flexor digitorum longus caudally and m. supinator craniolaterally (Fig. 12). Proximally, it overlies the insertion of m. biceps brachii, where it takes a tendinous origin on the caudal (flexor) epicondyle of the humerus proximal to the origin of the humeral head of m. flexor digitorum longus (Fig. 5). Some additional fibers may take their origin from a small ligament arising from the head of the ulna. Distally, m. pronator teres inserts over the distal three-quarters of the most medial surface of the radius, and less so onto the interosseous membrane (Fig. 10). Serving as the primary pronator of the antebrachium, m. pronator teres may also flex the radiohumeral joint to some degree, and thus likely assists in the maintenance of limb posture. The innervation of m. pronator teres is via a complex set of muscular branches derived from the medianoulnar nerve just distal to the elbow joint.

M. flexor carpi ulnaris.

M. flexor carpi ulnaris is a large, fusiform, bipinnate muscle lateral to the humeral head of m. flexor digitorum longus. It overlies the majority of m. pronator quadratus and the ulnar head of m. flexor digitorum longus (Fig. 12). This muscle takes its origin by means of a long, thick tendon attached to the caudal epicondyle of the humerus, just distal to the humeral head of m. flexor digitorum longus (Fig. 5). Distally, the muscle flares over the lateral portion of the cranial surface of the antebrachium, inserting onto the prominence of the pisiform (Fig. 12). M. flexor carpi ulnaris serves many functions in the crocodylian forelimb, including flexion and abduction of the carpus, stabilization of the elbow joint, and some adduction of the antebrachium. M. flexor carpi ulnaris is innervated by a muscular branch of the medianoulnar n.

M. flexor digitorum longus.

M. flexor digitorum longus is a complex system of muscle heads that take their origin from the caudal epicondyle of the humerus (humeral head), the caudal surface of the ulna (ulnar head), and the ulnar aspect of the carpus (carpal head). All heads join to form a common central flexor tendon at approximately the level of the distal carpal joint, where the tendon is stabilized by means of the cartilaginous hammate process of the radiale. From this point, it divides into three distal digital tendons that extend onto digits I–III. These tendons bifurcate halfway along each metacarpal (allowing the insertion tendons of m. flexor digitorum brevis superficialis to pass through), as is typical in tetrapods (e.g., Wake, 1979). Terminally, these tendons insert onto the flexor aspect of the penultimate phalanx of digits I–III. Together these muscle bellies serve to flex the wrist, carpometacarpal joints, metacarpophalangeal joints, and all but the most distal interphalangeal joints. Proximally, the muscle provides a small degree of flexion and stabilization at the brachioantebrachial joint. All heads of this muscle complex are supplied by muscular branches from the medianoulnar nerve.

M. flexor digitorum longus pars humeri.

The humeral head of m. flexor digitorum longus originates by means of a thin tendon on the caudal epicondyle of the humerus lateral to the origin of m. pronator teres and medial to that of m. flexor carpi ulnaris (Fig. 5), also taking some origin from a thick septum separating it from m. pronator teres for about two-thirds the length of the antebrachium. Distally, the humeral head inserts on the axial edge of the central tendon of m. flexor digitorum longus, ending in a long, thin tendon that passes beneath the flexor retinaculum. Cranially, m. pronator teres is closely related to the humeral head of m. flexor digitorum longus, while m. flexor carpi ulnaris is a close caudal relation (Fig. 12).

M. flexor digitorum longus pars ulnaris.

The ulnar head originates broadly on the caudal surface of the ulna, occupying the entire width of the shaft distally (Fig. 10), and converges distally to form a thick tendon that passes beneath the flexor retinaculum and then crosses the proximal carpal joint to join the central flexor tendon. The bulk of this belly lies deep to m. flexor carpi ulnaris (Fig. 12).

M. flexor digitorum longus pars carpalis.

The carpal head of m. flexor digitorum longus is included in this discussion of extensor musculature for purely functional reasons. The muscle itself is clearly a primitive flexor of the manus (e.g., Wake, 1979), although in crocodylians its specialized nature has altered its function. The muscle takes its origin from the deep ulnar surface of the distal carpals and overlying ligaments, and extends to the dorsal surface of the ulnare. Distally, its mixed tendinous and fleshy insertion attaches to the deep surface of the tendon of insertion of m. flexor digitorum longus pars ulnaris. Its resulting line of action then allows m. flexor digitorum pars carpalis to function as either a flexor or an extensor of the digits of the manus.

M. pronator quadratus.

The attachment of m. pronator quadratus to the ulna is fleshy and broad, extending onto the proximal expansion of the ulna, while the attachment to the radius is by a well defined tendon that runs the length of the radius (Figs. 9 and 10). In some species (C. acutus and C. siamensis), its radial attachment may be predominantly fleshy, rather than tendinous. This muscle lies deep to all other musculature of the flexor aspect of the antebrachium, except for m. flexor digitorum ulnaris, which is adjacent to it and lies between the lateral edge of the radius and the craniomedial surface of the ulna (Figs. 11 and 12). As is the case in all tetrapods (e.g., Haines, 1950 (and references therein); Wake, 1979), m. pronator quadratus pronates the antebrachium and stabilizes the radius and ulna. M. pronator quadratus is innervated by the anterior interosseus nerve, a branch of the medianoulnar nerve.

Intrinsic Musculature of the Manus—Extensor Musculature

The manual extensor musculature is all supplied by branches from the radial nerve. In the manus itself, intrinsic musculature is supplied by a series of branches beginning near the wrist and following the digits.

Mm. extensor digitorum superficialis.

The mm. extensor digitorum superficialis muscle complex can be clearly divided into various heads serving digits I–V (Fig. 13). Because the details of their anatomy differ significantly, even though each head serves to extend the metacarpophalangeal joints and all interphalangeal joints, they are treated separately here to emphasize their detailed differences among the crocodylians under consideration.

Figure 13.

Superficial extensor musculature of the manus. The superficial extensors of the manus are largely intrinsic. Each digit possesses its own extensor, while digits I and II also may be extended by m. extensor pollicis superficialis et indicus proprius.

M. extensor digiti I superficialis.

M. extensor digiti I superficialis lies lateral to the belly of m. extensor pollicis superficialis et indicus proprius, and is the largest superficial extensor muscle of the manus (Fig. 13). It takes its fleshy origin from the proximal surface of the radiale and overlying ligaments, and is followed by a short gap before it continues its origin from the dorsal surface of the proximal half of metacarpal I. Some intermingling of fibers with m. extensor metacarpi I may occur near this origin. The muscle inserts via tendon to the extensor process of the ungual phalanx, and thus serves to extend the metacarpophalangeal joint and the interphalangeal joint of digit I. Its slightly lateral displacement may allow the muscle to partially adduct digit I as well.

M. extensor digiti II superficialis.

M. extensor digiti II superficialis lies immediately medial to m. extensor digiti I superficialis and takes its origin from the proximomedial surface of the radiale, just distal to (and thus somewhat deep to) that of m. extensor pollicis superficialis et indicus proprius (Fig. 13). Its insertion is tendinous, attaching to the tendon of m. extensor digiti II profundus over the middle of metacarpal II to insert in common with the latter onto the extensor process of the ungual phalanx. Nerve fibers can be seen entering the muscle belly near the base of metacarpal II, the likely motor point of this muscle.

M. extensor digiti III superficialis.

M. extensor digiti III superficialis is found between the more lateral radial head of m. extensor digiti IV superficialis and the more medial m. extensor pollicis superficialis et indicus proprius (Fig. 13). This small extensor takes its fleshy origin from the axial portion of the radiale, proximal to midshaft, and inserts onto the proximal surface of the ungual phalanx (P4), but may send small slips of tendon to the proximal extensor attachments of P1–P3. Primarily tendinous, the insertion arises at the level of the middle of metacarpal III in most specimens; however, some variability was found with tendons arising either more proximally or distally among all species.

M. extensor digiti IV superficialis.

M. extensor digiti IV superficialis can usually be divided into two units: a pars radiale and a pars ulnare. The ulnare head appears to be the most prominent. It gives rise to its tendon of insertion at about midshaft of metacarpal IV, while the radiale head gives rise to its tendon just distal to the carpometacarpal joint of digit IV (Fig. 13). The two tendons of insertion fuse immediately proximal to the metacarpophalangeal joint of digit IV, and insert in common to the extensor process of the ungual phalanx of digit IV. The origin of the pars radiale is fleshy and arises from the proximal surface of the radiale, closely applied to the extensor digiti III superficialis, while the origin of the pars ulnare is tendinous and arises from the distal ulna and dorsum of the ulnare. In G. gangeticus, only a single head was found, which took its origin across the entire span (principally from the ulnare).

M. extensor digiti V superficialis.

M. extensor digiti V takes its origin with m. extensor metacarpi IV on the lateral portion of the distal ulna and proximal ulnare (Fig. 13). It remains distinct from the other superficial digital extensors of the manus by inserting via fascia along the entire length of digit V to the level of the dorsal extensor process of the ungual phalanx. Its distal margin is clearly more tendinous than its proximal margin, although usually a clear tendon of insertion cannot be distinguished. However, the function of m. extensor digiti V superficialis appears to be identical to that of the other superficial digital extensors, which is the extension of the digit at the metacarpophalangeal joint and all interphalangeal joints.

M. extensor metacarpi I.

This large muscle of the manus takes its fleshy origin from the proximal half of the dorsolateral surface of the radiale deep to that of m. extensor digiti I superficialis (Figs. 13 and 14). M. extensor metacarpi I is clearly distinguished from m. extensor digiti I superficialis by its insertion to the first metacarpal, while m. extensor digiti I superficialis continues distally to insert on the ungual phalanx, as noted above. Consequently, m. extensor metacarpi I serves to extend the metacarpophalangeal joint of digit I.

Figure 14.

Deep extensor musculature of the manus. The deep extensors of the manus are similar in organization to the superficial extensors.

M. extensor metacarpi IV.

M. extensor metacarpi IV lies deep to mm. extensor digiti V superficialis and extensor digiti IV superficialis, and takes its origin from the proximodorsal ulnare (Fig. 14). The insertion of this small muscle is via fleshy fibers onto the dorsolateral surface of metacarpal IV for approximately the proximal third of its length. The muscle functions in simple extension of metacarpal IV.

M. extensor pollicis superficialis et indicus proprius.

M. extensor pollicis superficialis et indicus proprius is an unusual, small fusiform muscle that serves two digits of the manus. Originating via a fleshy attachment to the dorsomedial surface of the proximal end of the radiale, it gives rise to a long tendon of insertion at approximately the level of the carpometacarpal joint. The tendon subsequently splits approximately at half its length to insert medially at the base of P1 of digit I and laterally at the base of P1 of digit II (Fig. 13). Consequently, m. extensor pollicis superficialis et indicus proprius extends the metacarpophalangeal joints and interphalangeal joints of digits I and II.

Mm. extensor digitorum profundi.

The mm. extensor digitorum profundi complex comprises the deep digital extensors of the manus, and usually underlies the superficial digital extensors described above (Fig. 14).

M. extensor digiti I profundus.

M. extensor digiti I profundus arises via fleshy fibers from the dorsolateral surface of metacarpal I. It subsequently gives rise to tendon near the distal end of that metacarpal and inserts on the extensor process of the ungual phalanx (Fig. 14). This deep digital extensor consequently extends the metacarpophalangeal joint and interphalangeal joint of digit I.

M. extensor digiti II profundus.

M. extensor digiti II profundus takes its fleshy origin from the lateral half of the proximal region of metacarpal I adjacent to the radiale, as well as from the adjacent carpal ligaments in a partially tendinous manner. It then inserts via a long, broad tendon onto the extensor process of P1 and continues distally to insert on the extensor process of the ungual phalanx (Fig. 14). Consequently, m. extensor digiti II profundus extends the entire second digit of the crocodylian manus.

M. extensor digiti III profundus.

The deep digital extensor of digit III can be divided into two and occasionally three discrete heads (a pars brevis, and a pars longus which may have discrete ulnare or radiale heads), with a common insertion onto the extensor processes of the phalanges of digit III (Fig. 14). Both heads work in conjunction as extensors of the carpometacarpal joint, the metacarpophalngeal joint, and all interphalangeal joints of digit III.

M. extensor digiti III profundus pars longus.

The long head of m. extensor digiti III superficialis is remarkably small, and is sometimes restricted to as little as one or two muscle buncles. It joins the short head as a tendon at the midshaft of metacarpal III in most specimens (random variability was noted among species), and lies deep to the tendon of m. extensor digiti III superficialis (Fig. 14). This long head originates via fascia from either the dorsolateral surface of the radial distal carpal element and radiale, or the ulnare, paralleling the insertion tendon of m. extensor digiti III superficialis.

M. extensor digiti III profundus pars brevis.

This much more substantial short head originates from the cartilaginous distal radial carpal element and the proximomedial surface of metacarpal II. As noted above, its tendon fuses with that of the long head at approximately midshaft of metacarpal III (Fig. 14).

M. extensor digiti IV profundus.

The deep digital extensor of digit IV arises fleshily from the dorsoproximal surface of metacarpal III and inserts in common with m. extensor digiti IV superficialis as an irregular, tendinous insertion to the base of P1, digit IV (Fig. 14). Consequently, m. extensor digiti IV profundus extends the metacarpophalangeal joint of digit IV.

M. extensor digiti V profundus.

The m. extensor digiti V profundus is possibly the smallest muscle of the entire manus, consisting of only a few muscle fibers. Nonetheless, its discrete character warrants inclusion here. Taking its origin from the dorsal surface of the distal carpal element, it inserts via fleshy fibers to the base of metacarpal V (Fig. 14). M. extensor digiti V profundus may well extend the metacarpal of this diminutive digit, but given its size, it is likely of little functional consequence.

Intrinsic Musculature of the Manus—Flexor Musculature

All of the palmar flexor musculature is innervated by terminal muscular branches of the medianoulnar nerve. Digital branches are typically referred to by the number of their corresponding digit (e.g., flexor nerve to digit I). Otherwise, muscle names apply to branches of the medianoulnar nerve in the manus.

M. transversus palmaris.

M. transversus palmaris is the most superficial muscle of the flexor surface of the manus. Its strap-like, robust appearance is obvious; however, occasionally it is divided into two distinct heads, as seen in A. mississippiensis. The muscle takes its origin via a broad tendon from the caudomedial aspect of the distal surface of the radius, although it remains tightly fused to the ligaments of the wrist. Distally, it inserts by means of a tendon onto the ventrodistal surface of metacarpal V, continuing to P2 or P3 of digit V along their lateral surfaces (Fig. 15). M. transversus palmaris serves to adduct metacarpal V, and thus digit V, and also flexes the carpometacarpal joint and interphalangeal joints, which it crosses variably. Its geometry indicates that it is important for maintaining manual integrity under heavy or irregular loading.

Figure 15.

Superficial flexor musculature of the manus. The prominent m. transversus palmaris is an important landmark of the manus, and may serve to stabilize the manus during terrestrial locomotion. Flexor tendons of the superficial muscles divide to allow the passage of tendons from m. flexor digitorum longus.

M. flexor digiti quinti pars superficialis et profundus.

The flexors of the fifth digit, m. flexor digiti quinti pars superficialis et profundus, usually consist of a very small, thin pair of triangular muscles that insert in common but retain distinct bellies adjacent to m. transversus palmaris. Proximally, they originate by means of a deep tendinous sheet anchored on the axial surface of the radiale. Their common insertion is from a long tendon that attaches to the palmar surface of P3 of digit V (Fig. 15), as well as on the axial side of the distal end of metacarpal V in some specimens, with no species-specific pattern. Consequently, m. flexor digiti quinti serves to flex digit V via the carpometacarpal joint and the metacarpophalangeal joint.

M. abductor metacarpi I.

The short, thick m. abductor metacarpi I is closely related to the internal surface of the ulnar head of m. flexor digitorum longus, as well as mm. flexor digiti quinti and transversus palmaris. Its fleshy origin is from the ventrolateral surface of the radiale, and it inserts by a stout tendon onto the proximolateral surface of the base of metacarpal I (Fig. 15). As such, m. abductor metacarpi I serves to abduct digit I.

M. abductor metacarpi V.

The small m. abductor metacarpi V occupies the superficial lateral surface of the proximal manus. Originating by fleshy attachment to the distal surface of the pisiform (Fig. 15), just distal to the insertion of m. flexor carpi ulnaris, it inserts tendinously along the length of the lateral surface of metacarpal V. Given its orientation, m. abductor digiti quinti clearly serves in abducting digit V.

Mm. flexor digitorum brevis superficialis I–IV.

Mm. flexor digitorum brevis superficialis represents a complex of small, bipinnate, fusiform muscles found distal and somewhat deep to the other musculature of each digit (Fig. 15). They originate from the distal row of carpals and tendinously from the overlying m. flexor digitorum longus, extending to the pisiform. Each belly inserts by means of a strong, discrete tendon onto the sides of one or more phalanges. Tendons arise at approximately midshaft of the metacarpals and split to allow passage of the tendons from m. flexor digitorum longus. In all cases, mm. flexor digitorum brevis superficiali serve to flex metacarpophalangeal joints and some interphalangeal joints of their respective digits. Digit V appeared to lack such a muscle in the observed specimens.

M. flexor digitorum brevis superficialis digiti I.

M. flexor digitorum brevis superficialis digiti I is typical of the muscles of this series (Fig. 15). The tendon of insertion bifurcates at approximately the level of one-half the length of the metacarpal to insert on the flexor processes of P1, digit I. Consequently, it functions in flexion of the metacarpophalangeal joint.

M. flexor digitorum brevis superficialis digiti II.

M. flexor digitorum brevis superficialis digiti II bifurcates proximal to the metacarpophalangeal joint to accommodate the passage of the tendon of m. flexor digitorum longus, and continues beneath the distal flexor retinaculum to insert at the base of P2 (Fig. 15).

M. flexor digitorum brevis superficialis digiti III.

M. flexor digitorum brevis superficialis digiti III is similar to m. flexor digitorum brevis superficialis digiti II (Fig. 15). However, in one specimen of Alligator mississippiensis, this muscle gave off a lateral tendinous slip that attached to both sides of the distal head of metacarpal III on one manus and on P1 on the contralateral manus.

M. flexor digitorum brevis superficialis digiti IV.

M. flexor digitorum brevis superficialis digiti IV is similar to that of digit II; however, a single specimen of Alligator mississippiensis exhibited an unbifurcated tendon that inserted onto the base of P1 (Fig. 15).

M. flexor digitorum intermedius digiti IV et V.

M. flexor digitorum intermedius digiti VI et V is an inconsistent muscle of the manus between the superficial and deep palmar musculatures. Taking its origin from the distal margin of the ulnare, it overlies the deep musculature of the manus in the plane of the lumbricals. Distally, it inserts most commonly on the distal end of P1 of digit IV (Fig. 16). However, this muscle frequently bears an accessory tendon of insertion to the distal metacarpal of digit V. It clearly functions in flexion of digit IV, although flexion and abduction of digit V may occur when the accessory tendon is present.

Figure 16.

Lumbricals. Lumbricals arise from the tendon of m. flexor digitorum longus. Note also the intermediate flexors of the manus.

M. flexor digitorum intermedius digiti V.

M. flexor digitorum intermedius digiti V directly overlies m. flexor digitorum profundus digiti V. Its origin from the distal carpal proximal to digit V is immediately proximal and lateral to that of m. flexor digitorum profundus digiti V. Distally, this muscle inserts onto the ventral surface of the base of P1 of digit V, overlying the insertion of m. flexor digitorum profundus digiti V (Fig. 16). In this study, M. flexor digitorum intermedius digiti V was commonly (but not always) found in Alligator mississippiensis, but was not found in any other species. Consequently, it may simply be a rare anomalous differentiation of m. flexor digitorum profundus digiti V.

M. flexor digitorum profundus digiti I.

The deep digital flexor of digit I originates from the ventral surface of the distal carpal row, extending slightly onto the base of metacarpal I. From here, it gives rise to a flat, broad tendon that inserts onto the flexor process at the base of P1 (Fig. 17). The tendon of insertion may be irregularly divided into two separate tendons in some specimens of Alligator mississippiensis. The short span of m. flexor digitorum profundus digiti I restricts its action to flexion of the metacarpophalangeal joint and to some flexion, as permitted by ligamentous anatomy, of the carpometacarpal joint.

Figure 17.

Deep flexor musculature of the manus. Each digit possesses a single deep flexor; however, digit II possessed two in all specimens examined.

M. flexor digitorum profundus digiti II.

M. flexor digitorum profundus digiti II was distinctly divided into two heads in all of the species examined (Fig. 17). Consequently each head is described separately. Presumably, each head can act independently; however, function would be nearly identical and restricted to flexion of the metacarpophalangeal joint.

M. flexor digitorum profundus digiti II pars medialis.

The pars medialis of this muscle takes its origin from the ventromedial surface of the base of metacarpal II, and inserts onto the ventromedial surface of the flexor expansion at the base of P1 of digit II (Fig. 17).

M. flexor digitorum profundus digiti II pars lateralis.

The pars lateralis, in obvious contrast, takes its origin from the ventrolateral surface of the base of metacarpal II, while inserting onto the ventrolateral surface of the flexor process at the base of P1 of digit II. In short, it is a mirror image of the pars medialis, although it is slightly more laterally displaced from the central axis of metacarpal II (Fig. 17).

M. flexor digitorum profundus digiti III.

M. flexor digitorum profundus digiti III takes its origin slightly from the unnamed distal carpal element proximal to metacarpal III, but primarily extending from the ventral surface of metacarpal III for about half its length (proximal to distal). Distally, it inserts onto the ventral base of P1 of digit III, slightly displaced laterally toward the ulnar side (Fig. 17). Consequently, m. flexor digitorum profundus digiti III flexes the metacarpophalangeal joint and slightly flexes the carpometacarpal joint. Given its slight lateral displacement, it may also cause slight abduction of digit III toward the ulnar side of the hand.

M. flexor digitorum profundus digiti IV.

The deep flexor muscle of the fourth digit appears to be irregularly split into two heads in at least two species (Alligator mississippiensis and Crocodylus acutus), though more commonly it is represented as a single muscle belly. It takes its extensive origin from the ventral surface of metacarpal IV, extending from the unnamed distal carpal proximal to metacarpal IV onto the ventral surface of metacarpal IV for three-quarters of its length. Distally, it inserts onto the ventral base of P1 of digit IV and thus serves to flex the metacarpophalangeal joint (Fig. 17). As with m. flexor digitorum profundus digiti I, it may also flex the carpometacarpal joint; however, it likely serves a greater physiological function in the stabilization of the manus during locomotion.

M. flexor digitorum profundus digiti V.

The deep digital flexor of digit V takes its origin from the ventral surface of metacarpal V for the proximal two-thirds of its length and inserts onto the ventral surface of the base of P1, just deep to that of m. flexor digiti V intermedius, which immediately overlies this muscle (Fig. 17). Consequently, m. flexor digitorum profundus digiti V flexes the metacarpophalangeal joint of digit V.

Mm. lumbricales.

Crocodylian lumbricales appear to be very similar in overall morphology to the lumbricales of other tetrapods (e.g., Haines, 1950). These small muscle bellies originate from the digital extensions of the common flexor digitorum longus tendon and insert on the extensor aspect of the metacarpophalangeal joints (Fig. 16). Consequently, they flex the carpometacarpal joint and simultaneously extend the metacarpophalangeal joints of digits II–IV. They also serve to slightly adduct these digits, and thus assist mm. interossei. Each lumbrical is described below in order to provide a more detailed account of their occurrence in crocodylians. Innervation was indeterminate, but is presumed to be via muscular branches of the medianoulnar nerve, in common with other manual flexor musculature.

M. lumbrical 1.

The first lumbrical extends from the dorsal surface of the long flexor tendon leading to digit II, with some fibers from the tendon to digit I, to the metacarpophalangeal joint capsule of digit II (Fig. 16).

M. lumbrical 2.

Lumbrical 2 extends from the dorsomedial surface of the long flexor tendon leading to digit II to the medial side of the metacarpophalangeal joint capsule of digit II (Fig. 16).

M. lumbrical 3.

The third lumbrical extends from the dorsal surface of the long flexor tendon leading to digit III to the metacarpophalangeal joint capsule of digit III along the same side as its origin (Fig. 16).

M. lumbrical 4.

Likewise, the fourth lumbrical extends from the dorsal surface of the long flexor tendon leading to digit III to the metacarpophalangeal joint capsule of digit III along its same side (Fig. 16).

M. lumbrical 5.

The fifth and last lumbrical extends from the lateral surface of the long flexor tendon leading to digit IV to the medial side of the metacarpophalangeal joint of the same digit (Fig. 16).

Mm. interossei dorsalae.

Dorsal interossei muscles are traditionally distinguished from their ventral counterparts by homology of function as much as by their anatomical relationships (e.g., Haines, 1950). For the sake of maintaining clear homology in the current work, this convention is followed. All interossei consistently maintain bipinnate architecture; therefore, this is not noted below (Fig. 18). Innervation is common to all mm. interossei, which are muscular branches of the medianoulnar nerve.

Figure 18.

Interosseus musculature of the manus. A full complement of dorsal and palmar interosseus muscles allow a full range of motion for all digits of the manus.

M. interosseus dorsalis digiti II.

M. interosseus dorsalis digiti II overlies m. interosseus palmaris digiti I near its origin and takes its own origin from the dorsomedial surface of metacarpal I, just distal to and somewhat between the origins of the deep extensors of digits I and II. From there it inserts onto the lateral surface of the metacarpophalangeal joint of digit II and to a lesser extent, attaches to the lateral side of the distal one-third of metacarpal II (Fig. 18). Given its origin from metacarpal I, m. interosseus dorsalis digiti II functions in the abduction of digit II from the midline of the hand, assuming that m. abductor metacarpi I exerts antagonistic force to stabilize the origin of this lumbrical. In the absence of this antagonist, m. interosseus dorsalis digiti II serves as an adductor of metacarpal I, assuming antagonistic action from m. interosseus palmaris digiti II. M. interosseus dorsalis digiti II also may serve to slightly extend metacarpal II.

M. interosseus dorsalis digiti III radialis.

The radial head of m. interosseus dorsalis digiti III originates from the dorsal aspect of the base of metacarpal II, just distal to the origin of m. extensor digiti III profundus and inserts onto the dorsoradiolateral surface of the metacarpophalangeal joint of digit III (Fig. 18). Consequently, this muscle, which overlies m. interossei palmaris digiti II at its origin, abducts and slightly extends digit III toward midline.

M. interosseus dorsalis digiti III ulnaris.

M. interosseus dorsalis digiti III ulnaris takes its origin from the lateral or ventrolateral surface of the base of metacarpal IV and inserts onto the ulnolateral surface of the distal head of metacarpal III via the joint capsule (Fig. 18). As a result, this dorsal interosseus muscle abducts digit III laterally away from midline and may slightly flex the digit at the metacarpophalangeal joint.

M. interosseus dorsalis digiti IV.

M. interosseus dorsalis digiti IV originates from the medial surface of the proximal base of metacarpal V. Distally, it inserts onto the lateral surface of the metacarpophalangeal joint capsule of digit IV and onto the lateral surface of metacarpal IV for about its distal half (Fig. 18). Consequently, it abducts digit IV from the midline of the manus.

Mm. interossei ventralis (palmaris).

The ventral interossei function in adduction of the digits of the manus toward manual midline, as is the case with all tetrapods (e.g., Haines, 1950). As noted above, all crocodylian interossei maintain a bipinnate architecture and consistent innervation (Fig. 18). Consequently, these small but strong muscles are well suited to exert relatively great force in maintaining manual posture.

M. interosseus ventralis digiti I.

M. interosseus palmaris digiti I is overlaid by m. interossei dorsalis digiti II and originates from the dorsolateral surface of the proximal end of metacarpal II, immediately distal to and nearly surrounded by the origin of m. extensor digitorum II profundus. Distally, this muscle inserts onto the distolateral surface of metacarpal I, as well as the metacarpophalangeal joint of digit I (Fig. 18). M. interosseus palmaris digiti I adducts digit I toward the manual midline.

M. interosseus ventralis digiti II.

M. interosseus palmaris digiti II is overlaid at its origin by the proximal end of m. interossei dorsalis digiti III radialis, and thus is difficult to identify in dissection. It takes its origin from the lateral surface of the base (proximal head) of metacarpal III ventral to the proximal end of m. interossei dorsalis digiti III radialis. Distally, it inserts onto the lateral surface of metacarpal II beginning about the distal third of the metacarpal and continuing distally to the joint capsule (Fig. 18). This muscle adducts digit II toward the manual midline.

M. interosseus ventralis digiti IV.

This third palmar interosseus muscle originates from the lateral base of metacarpal III and inserts onto the dorsolateral surface of the head of metacarpal IV (Fig. 18). Consequently, it adducts digit IV toward the manual midline (given a stable metacarpal III). Alternatively, m. interosseus palmaris digiti IV may function weakly in abduction of digit III.

M. interosseus ventralis digiti V.

M. interosseus palmaris digiti V is somewhat overlaid by m. interosseus dorsalis digiti IV at its origin. The origin of this final interosseus muscle is from the dorsomedial surface of metacarpal V, lateral to the origin of m. interossei dorsalis digiti IV. Distally, it inserts onto the medial surface of the base of P1 of digit V (Fig. 18). M. interosseus palmaris digiti V functions in adduction of digit V via its metacarpal, as in the above interosseus muscles.

DISCUSSION

The forelimb anatomy of crocodylians is quite conservative in overall morphology, with differences being confined largely to subtle alterations in origins and insertions. As a consequence, the behaviorally and ecologically moderate American alligator (Alligator mississippiensis) appears to be representative of crocodylians regardless of locomotor behavioral differences, as Walker (1973) found for Pseudemys among chelonians possessing similarly varied locomotor behaviors.

Interspecific variation, which might be expected to reflect either locomotor adaptation to specific environments (degree of terrestriality) or the influence of phylogeny (e.g., Harvey and Pagel, 1991), was primarily found among muscles of the shoulder girdle, and included details of attachment points (e.g., m. pectoralis, m. trapezius, and many others above) and the methods of attachment (e.g., fleshy or tendinous; see m. trapezius and others above).

The hypothesis that anatomical variation correlates with locomotor behavior is supported, in part, by anatomical and inferred functional differences between relatively aquatic and amphibious taxa (see below). Likewise, the hypothesis that anatomical variation may reflect the phylogeny of Crocodylia is also supported in part by the identification of phylogenetically parsimonious distributions of anatomical characters (see below).

M. triceps longus caudalis, an unusual extensor of the antebrachium that takes its origin from both the scapula and the coracoid, was qualitatively much larger in the aquatic reference, G. gangeticus, than in other species. G. gangeticus is known to exhibit highly restricted movements on land, and consequently makes little use of terrestrial habitats (Bustard and Singh, 1977; Whitaker, 1978; Whitaker and Andrews, 1988). Further, this species exhibits a locomotor pattern that is apparently unique among crocodylians (Bustard and Singh, 1977). This “forward push” involves the placement of all four limbs cranially, followed by simultaneous retraction of all four limbs (Bustard and Singh, 1977). Since the long heads of m. triceps brachii affect the extension of both the antebrachium and the brachium, the species-specific difference in G. gangeticus arguably may relate to extension of the shoulder joint as well as the antebrachium, which is an important aspect of unusual locomotion in this species.

G. gangeticus also presents a more ventromedially displaced origin for m. biceps brachii. In all other species, the origin of this muscle (indicated by a distinct muscle scar (Fig. 3)) is relatively high on the body of the coracoid. However, the origin in G. gangeticus is clearly displaced ventromedially. This displacement has the effect of increasing the mechanical advantage to m. biceps brachii, providing relatively strong flexion of the brachium and antebrachium. Similarly, the relative size of m. humeroradialis, a flexor of the antebrachium, seems somewhat enlarged in G. gangeticus. These two observations imply particularly strong flexion of the antebrachium. Since flexion of the antebrachium occurs during the recovery stroke in terrestrial locomotion (personal observation), little resistance to flexion of the antebrachium is encountered. However, the “forward push” of the gharial (G. gangeticus) may place the manus into contact with the substrate during recovery. As a consequence, strong flexion of the antebrachium may be required to minimize this type of incidental contact. Kinematic work on this unusual form of locomotion would undoubtedly provide insight into these peculiarities.

In the current research, the inclusion of G. gangeticus, the outgroup to all other crocodylians, was also informative as regards the pattern of muscular evolution within Crocodylia. However, the lack of a second outgroup prohibits any certain determination of character polarity. Still, in some instances, it is likely that G. gangeticus represents the primitive condition. For example, m. extensor digiti IV superficialis exhibited a single head in G. gangeticus, whereas other species exhibited two heads (a pars radiale and a pars ulnare). The differentiation of single muscles into multiple heads through time is a well-known evolutionary phenomenon (such as the differentiation of the long manual flexors among tetrapods over time (e.g., Howell, 1936; Haines, 1939; Harris, 1939)). Consequently, the presence of a single head in G. gangeticus, combined with this species' phylogenetic position as an outgroup to the remaining crocodylians (e.g., Brochu, 1997), implies that this is the primitive morphology for this muscle. The taxonomic sampling in the present study indicates that the muscle divided into two heads as part of the evolution of all crocodylians after the divergence of Gavialis. Given the reduced nature of the fourth digit in extant crocodylians, it seems unlikely that this muscle is of great functional consequence today. However, if the early history of Crocodylia included a significant number of terrestrial habitats with irregular surfaces, the muscle could have benefited early crocodylians by refining manual dexterity during locomotion.

Intraspecific variation was assessed in the American alligator (Alligator mississippiensis) because that was the largest group of specimens available. Generally, intraspecific variations are restricted to details regarding attachment sites and anatomical relationships. The functional implications of most intraspecific variations were consistent with the functions of more regularly occurring structures. As evolutionary neutral variants, these intraspecific differences may reflect random variation or an evolutionary history that includes unknown selection pressures on the anatomy of the forelimb.

M. trapezius exhibits a variable insertion, with an accessory aponeurosis inserting in an unusual location on the scapula (see above) in some A. mississippiensis specimens. The limited extent of the extra insertion suggests that it is functionally unimportant. However, the migration of the insertion of m. trapezius to more caudal portions of the scapula may increase scapular rotation in some individuals.

M. pectoralis also exhibits some intraspecific variation in A. mississippiensis, with an irregular deep head being observed in a few specimens. No mentions of similar phenomena were found in the literature, and the development of the muscle was also quite poor. Consequently, it is viewed here as an unimportant anomaly.

M. deltoideus clavicularis presents an interesting variant in A. mississippiensis, causing this muscle to occasionally cross the brachio-antebrachial joint. In two specimens, this muscle incorporated a distal slip that attached to a strong, intermuscular septum between mm. humeroradialis and biceps brachii. The septum extended the length of the humerus, ultimately attaching to the ligamentous sheath surrounding the humeroradialis trochlea. Consequently, m. deltoideus clavicularis ultimately inserted on the radius in these specimens. Anatomically, this variant is clearly not the deep differentiation of m. deltoideus clavicularis that Romer (1944) noted was absent in Alligator mississippiensis; rather, it appears to pass along a fascial plane.

The variation seen in the tendinous arc serving as the origin of m. triceps longus caudalis is also not species-specific. The dominance of part of the tendinous arc is variable among and within species. Consequently, little functional interpretation can be made. This structure prompts interesting questions regarding the migration of attachment sites in vertebrate muscles, and is worthy of additional inquiry in future studies. Specifically, assessing the phylogenetic distribution of homologous muscle scars among other archosaurs and their ancestors could provide insights into the selection pressures that result in a muscle requiring such divergently set points of origin.

Intraspecific variation in the antebrachium and manus of crocodylians primarily involves anatomical relationships (see above). In A. mississippiensis, for example, m. extensor carpi radialis brevis overlaps the belly of m. extensor digiti III in some specimens, while in others it overlaps the tendon of insertion. These minor differences appear to have little functional or phylogenetic importance. The musculature of the manus is primitive in its musculoskeletal anatomy with respect to Diapsida, and the variability seen here may be reflective of the retention of primitive degrees of variability.

This work documents the anatomy of the forelimb in a phylogenetically and behaviorally diverse group of crocodylians. Interspecific variation may be reflective of phylogenetically constrained morphology and/or functional specialization within Crocodylia. For example, m. extensor digiti IV superficialis appeared to possess two distinct heads in all species examined, with the exception of G. gangeticus. Similarly, the dominance of various muscles of the brachium in G. gangeticus, relative to other species, was apparently distinct from other species. Consequently, the hypothesis that phylogenetically constrained soft-tissue characters of the forelimb distinguish members of Crocodylia is supported at least in part by the current findings. The examination of additional crocodylian species will undoubtedly improve the resolution of this character, and ultimately enable a more complete assessment of its evolution within Crocodylia.

Other interspecific variations appear to relate more directly to function than to phylogeny. For example, relative muscle development appears to vary among species in patterns that may be associated with limb kinematics. The unusual locomotion of G. gangeticus may, in fact, be the causal factor behind many of the anatomical differences described above. Since crocodylian locomotion has been shown to differ fundamentally from the sprawling gait of squamates (likely due to different primitive conditions (Reilly and Elias, 1998)), it follows that the unique gait of G. gangeticus (Bustard and Singh, 1977) has unforeseen biomechanical consequences. Specifically, rotation of the humerus and strong flexion of the antebrachium may be required to facilitate the recovery stroke of the forelimb. Thus, forelimb kinematic studies and anatomical comparisons to noncrocodylian species that exhibit similar gaits (such as the sea turtles Chelonia mydas and Dermochelys coriacea (e.g., Hendrickson, 1958; Bustard, 1972)) would facilitate the testing of these hypotheses.

The anatomy of the crocodylian forelimb reflects compromises between functional specializations and the common restrictions placed on an amphibious mode of life. The variations in locomotor postures alone may account for much of the variability in forelimb anatomy discerned through this research; however, it is clear that some variations are reflective of phylogeny as well. Because functional interpretations of morphological differences were founded in the sciences of anatomy, physics, and geometry, their validity is supported by the anatomy itself. In the present work, such interpretations have been extrapolated to limb dynamics; however, as noted by Landsmeer (1984), these postulates should be clearly understood as such. For example, it is not possible to accurately identify muscles that act as stabilizers of joints from the geometry of attachment sites.

Finally, by sampling within Crocodylia, it was possible to make phylogenetic interpretations of morphological differences. Anatomical differences between G. gangeticus and all other crocodylian species reinforce the perception that gavialoids are the oldest and most primitive of the crocodylians (see Brochu, 1997, for a review). Documentation of the anatomy of the crocodylian forelimb has provided the basis for functional interpretations of the osteology of Crocodylia (Meers, 1999) and, combined with data from Aves, other archosaurs as well (Meers et al., 1993; unpublished results). Their phylogenetic importance to the inference of function in extinct archosaurs cannot be overemphasized. Since Crocodylia is the extant sister taxon to birds, the study of crocodylian anatomy provides unique insights into the evolution of forelimbs in all archosaurs (Bryant and Russell, 1992; Witmer, 1995).

Acknowledgements

This work could not have been completed without the substantial contributions of several individuals and organizations. In particular, thanks are due to D. Weishampel, P. Dodson, M. Worrell, P. Brazaitis, C. Ruff, K. Carpenter, and an anonymous reviewer for comments that greatly improved and shortened this manuscript. P. Dodson and D. Weishampel provided an unpublished preliminary description of the anatomy of the forelimb in Alligator mississippiensis that was invaluable in the preparation of this work. Several individuals and organizations provided dissection specimens for this research, including M.B. Worrell, D.B. Weishampel, L.M. Witmer, the St. Augustine Alligator Farm (L. Kirkland and K. Vliet), Florida Wildlife Research (P. Moler), the New England Aquarium, and the American Museum of Natural History (C.J. Cole, L. Ford, and T. Trombone). The value of the opportunities provided by these individuals and institutions cannot be overstated, and a sincere debt of gratitude is owed them for this research. Facilities for specimen storage were also generously provided by J.T. Richtsmeier and D.B. Weishampel. M.B. Worrell also provided dissection equipment and invaluable advice on specimen acquisition.

Ancillary