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Keywords:

  • pygmy hippopotamus;
  • common hippopotamus;
  • myology;
  • forelimb

Abstract

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

Based on morphological analyses, hippos have traditionally been classified as Suiformes, along with pigs and peccaries. However, molecular data indicate hippos and cetaceans are sister taxa (see review in Uhen, 2007, this issue). This study analyzes soft tissue characters of the pygmy hippo forelimb to elucidate the functional anatomy and evolutionary relationships of hippos within Artiodactyla. Two specimens from the National Zoological Park in Washington, D.C. were dissected, revealing several adaptations to an aquatic lifestyle. However, these adaptations differ functionally from most aquatic mammals as hippos walk along river or lake bottoms, rather than swim. Several findings highlight a robust mechanism for propelling the trunk forward through the water. For example, mm. pectoralis superficialis and profundus demonstrate broad sites of origin, while the long flexor tendons serve each of the digits, reflecting the fact that all toes are weight-bearing. Pygmy hippos also have eight mm. interossei and a well-developed m. lumbricalis IV. Retention of intrinsic adductors functions to prevent splaying of the toes, an advantageous arrangement in an animal walking on muddy substrates. Published descriptions indicate common hippos share all of these features. Hippo and ruminant forelimbs share several traits; however, hippos are unique among artiodactyls in retaining several primitive muscles (e.g., mm. palmaris longus and flexor digitorum brevis). These findings are consistent with the hypothesis that hippos diverged from other Artiodactyla early in the history of this group. Additional analyses of hindlimb and axial muscles may help determine whether this trajectory was closely allied to that of Cetacea. Anat Rec, 290:673–693, 2007. © 2007 Wiley-Liss, Inc.

There are two extant species of hippopotami, the common hippo (Hippopotamus amphibius) and the pygmy hippo (Choeropsis liberiensis). Based on morphological analyses, hippos have traditionally been classified as Suiformes, along with pigs and peccaries (Simpson, 1945). However, molecular studies indicate hippos and cetaceans are sister taxa (e.g., Irwin and Arnason, 1994; Gatesy et al., 1996; Nikaido et al., 1999). In addition, many molecular analyses support a close relationship between ruminants and the hippo and whale clade, further separating hippos from suids and tayassuids (e.g., Shimamura et al., 1997; Ursing and Arnason, 1998; Nikaido et al., 1999; see review in Uhen, 2007, this issue). In addition to their phylogeny, the functional anatomy of hippos is also of interest as they are the only semiaquatic artiodactyls and show marked morphological adaptations for this lifestyle.

Early monographs on the musculoskeletal anatomy of the common hippopotamus include Cuvier and Laurillard (1849), Gratiolet and Alix (1867), and Humphry (1872). These studies, based on dissections of a single fetal or newborn specimen, were summarized by Windle and Parsons in their classic treatises on ungulate anatomy (1901, 1903). In subsequent years, Maurer (1911) described m. serratus dorsalis, whereas Kajava (1923) analyzed the muscles of the flexor antebrachium and manus. More recently, Macdonald et al. (1985) published a brief discussion of their observations after the dissection of a 43-year-old female common hippo.

Fewer accounts exist on the musculoskeletal anatomy of pygmy hippos. Milne Edwards published a monograph on pygmy hippo osteology in 1868, and Macalister wrote a brief account of its myology in 1873. Campbell provided more in-depth myological descriptions in his dissertation (1935), parts of which were published later (1936, 1945). Macalister (1873) and Campbell (1935) each dissected a single fetal or newborn specimen. The only other account of pygmy hippo myology is a brief report published by Macdonald et al. (1985), based on their dissection of a 12-year-old male.

The goal of this study is to provide more detailed myological descriptions and muscle maps of the pygmy hippo forelimb. As noted above, most of the existing literature is based on neonates, and a detailed and comprehensive study of adult specimens is lacking. In addition, the functional significance of differences between hippos and other artiodactyls will be addressed, as previous accounts have failed to consider these implications. Furthermore, as molecular data now cast the phylogeny of the artiodactyls, and the placement of hippos in particular, in a new light, it is time to reassess the morphological data.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

Dissections were conducted on the left and right forelimbs of two pygmy hippopotami (Choeropsis liberiensis). Both hippos were captive-born, and lived at the National Zoological Park in Washington, D.C. The specimens include a 36-year-old female (accession no. 29218) weighing 184.5 kg that died on October 1, 1999, and a 9-year-old female (accession no. 110963) weighing 285 kg that died on January 27, 2003. After necropsy, the specimens were fresh-frozen and stored at the Osteopreparatory Laboratory at the Museum Support Center of the National Museum of Natural History (USNM) in Suitland, Maryland.

All dissections took place at the Osteopreparatory Laboratory. Standard dissection methods were employed, and digital photographs were taken at each level of the dissection using a Nikon Coolpix 995. To assist with muscle mapping, digital photographs were taken of the forelimb skeleton of a female pygmy hippo housed at the National Museum of Natural History (USNM 582095, captive-born). The scapula, humerus, radius, and ulna were photographed in lateral, medial, cranial, and caudal views, while an articulated manus was photographed in dorsal and ventral views. Muscle origins and insertions were then recorded on transparency film overlying these photographs.

The results of the pygmy hippo dissections were compared with previous accounts of this species (Macalister, 1873; Campbell, 1935, 1936; Macdonald et al., 1985) and the common hippo (Cuvier and Laurillard, 1849; Gratiolet and Alix, 1867; Humphry, 1872; Kajava, 1923; Jouffroy et al., 1971; Macdonald et al., 1985). The myology of the hippo forelimb was then compared with published accounts of other artiodactyls, including Sus (Windle and Parsons, 1901; Kajava, 1923; Campbell, 1935, 1936; Sisson, 1975a; Nickel et al., 1986), Potamochoerus (Windle and Parsons, 1901; Kajava, 1923), Babyrousa (Windle and Parsons, 1901; Macdonald et al., 1985; Kneepkens et al., 1989), Tayassu (Windle and Parsons, 1901), Pecari (Kajava, 1923; Campbell, 1935, 1936; Dalzell, 1970), domestic ruminants (Windle and Parsons, 1901; Getty, 1975; Nickel et al., 1986), Tragulus (Windle and Parsons, 1901; Kajava, 1923; Jouffroy et al., 1971), Hyemoschus (Windle and Parsons, 1901; Dalzell, 1970; Jouffroy et al., 1971), Giraffa (Windle and Parsons, 1901), Cervus (Windle and Parsons, 1901), Odocoileus (Dalzell, 1970), Ovibos (Windle and Parsons, 1901), Cephalophus (Windle and Parsons, 1901), Antilocarpra (Dalzell, 1970), and Camelus (Windle and Parsons, 1901; Smuts and Bezuidenhout, 1987). Myological differences between hippos and other artiodactyls were then compared with published accounts of perissodactyls, including Dicerorhinus (Beddard and Treves, 1889; Windle and Parsons, 1901; Jouffroy et al., 1971), Equus (Windle and Parsons, 1901; Sisson, 1975b; Nickel et al., 1986), and Tapirus (Windle and Parsons, 1901; Kajava, 1923; Campbell, 1935, 1936; Jouffroy et al., 1971). In cases where hippos differed from perissodactyls as well, comparisons were also made with hyraxes and elephants (Miall and Greenwood, 1878; Windle and Parsons, 1901). The terminology adopted in this manuscript conforms to the standards of the Nomina Anatomica Veterinaria (Waibl et al., 2005).

RESULTS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

Extrinsic Muscles of the Forelimb

M. trapezius.

The cranial aspect of this broad, triangular muscle was damaged by necropsy cuts in both cadavers. Nonetheless, it was possible to demonstrate its origin from the funicular portion of the nuchal ligament at the level of vertebrae C1 to T1, the supraspinous ligament from the level of T1 to T11, the fascia thoracolumbalis, and the fascia of m. latissimus dorsi. In addition, based on the cut edge observed on its cranial aspect, it is likely that m. trapezius also takes origin from the dorsal aspect of the occipital bone. M. trapezius originates by means of fleshy fibers from the supraspinous ligament, but it is thin and aponeurotic at its cranial and caudal ends. The pars cervicalis and pars thoracica are continuous, yet demonstrate different fiber directions, with the cervical fibers coursing caudoventrally and the thoracic fibers coursing cranioventrally. The fibers of the pars thoracica are at least twice as thick as those of the pars cervicalis. M. trapezius has a tendinous insertion onto the middle third of the scapular spine, ventral to the origin of m. infraspinatus, and dorsal to the insertion of m. omotransversarius (Fig. 1; Plate 1). The insertion extends to a minor degree onto the cranial and caudal aspects of the spine (Plate 1).

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Figure 1. Pygmy hippo shoulder in lateral view (superficial dissection).

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Figure Plate 1. Pygmy hippo scapula and associated muscle maps. A = lateral, B = medial, C = cranial, and D = caudal views.

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When the neck is fixed, m. trapezius pars cervicalis pulls the scapula dorsad and craniad, while m. trapezius pars thoracis draws the scapula dorsad and caudad. When the scapula is fixed, m. trapezius pars cervicalis flexes the head and neck laterally (with unilateral contraction). M. trapezius stabilizes the scapula and plays an important role in advancing the forelimb.

M. omotransversarius.

M. omotransversarius is a robust, flat, strap-like muscle. Its origin from the wing of the atlas and the articular process of the C2 vertebra is tendinous on its deep and superficial aspects, with fleshy fibers in between. In the cervical region, the belly of m. omotransversarius lies deep to that of m. brachiocephalicus (Fig. 1). As it approaches the scapula, it lies superficial to m. deltoideus and the insertion of m. trapezius pars cervicalis. M. omotransversarius inserts by means of a broad tendon onto the fascia of m. infraspinatus and m. deltoideus pars scapularis, and onto the base of the acromion process and scapular spine, superficial and just ventral to the insertion of m. trapezius pars cervicalis (Fig. 1; Plate 1). Its fibers of insertion are particularly difficult to separate from those of m. infraspinatus.

When the scapula is fixed, m. omotransversarius flexes the neck laterally; however, if the neck is fixed, m. omotransversarius draws the scapula craniad, thus assisting in advancing the forelimb.

Mm. rhomboidei.

Mm. rhomboidei cervicis et thoracis are fused, forming a continuous sheet of muscle. M. rhomboideus cervicis is thicker than m. rhomboideus thoracis, which is relatively thin and triangular in shape. Fibers originate from the nuchal ligament down to the level of the spinous process of the T8 vertebra, and insert primarily by means of fleshy fibers onto the vertebral border of the scapula, from the cranial angle to just cranial to the caudal angle (Plate 1). Near the cranial angle of the scapula, fibers insert partially onto the fascia of m. serratus ventralis cervicis. In addition, at the cranial angle, there is a strong tendon of insertion just dorsal to the fleshy insertion of m. serratus ventralis cervicis. Along the vertebral border of the scapula, the fibers of mm. rhomboidei cervicis et thoracis intermingle with the fibers of mm. serrati ventrales cervicis et thoracis, and it is difficult to separate the two sheets of muscle. Finally, nearing the caudal angle, the muscle gives rise to a tendon that inserts adjacent to the insertion of m. serratus ventralis thoracis.

M. rhomboideus cervicis draws the scapula dorsad and craniad when the neck is fixed. Acting alone, it flexes the neck laterally, and acting bilaterally, it elevates the neck. M. rhomboideus thoracis draws the scapula dorsad and mediad. Together, the cervical and thoracic portions fix the scapula on the body wall.

M. latissimus dorsi.

M. latissimus dorsi arises from the fascia thoracolumbalis, by means of a thin aponeurosis, and from ribs 8 through 11, by means of fleshy strips (Fig. 1). Cranially, the fleshy fibers of m. latissimus lie approximately 10 cm from the dorsal midline; moving caudally, the fibers curve laterally. The muscle is thick craniodorsally and thins out caudoventrally. Slips of m. latissimus dorsi interdigitate with those of m. obliquus externus abdominis. The fleshy fibers of m. latissimus dorsi and m. teres major fuse to form a tendon of insertion. This tendon runs deep to m. coracobrachialis to insert on the teres major tuberosity on the craniomedial aspect of the middle third of the humerus (Fig. 2; Plate 2).

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Figure 2. Pygmy hippo forelimb in medial view.

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Figure Plate 2. Pygmy hippo humerus and associated muscle maps. A = cranial, B = lateral, C = caudal, and D = medial views.

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When the forelimb is advanced and fixed, m. latissimus dorsi draws the trunk craniad; when the limb is free, it is a powerful retractor of the forelimb. Thus, m. latissimus dorsi plays an important role in the propulsion of the body on the forelimb.

M. brachiocephalicus.

In suids and ruminants, m. brachiocephalicus is formed by the union of m. cleidocephalicus (including a pars mastoidea and a pars occipitalis) and m. cleidobrachialis. Mm. cleidocephalicus and cleidobrachialis are separated by a fibrous remnant of the clavicle, the intersectio clavicularis. In the pygmy hippo, m. brachiocephalicus is a very robust and flat, strap-like muscle. In the specimens dissected in this study, it lacked a clear intersectio clavicularis and was fused with the cranial edge of m. deltoideus pars acromialis. There are clearly two heads of origin (deep and superficial) but the exact origins are unclear due to necropsy damage in both cadavers. According to Campbell (1935, 1936), the deep head arises from the mastoid region (pars mastoidea) and is partially fleshy at its origin, whereas the superficial head originates primarily by means of an aponeurosis from the occipital crest (pars occipitalis). Although a clear intersectio clavicularis was not observed in this study, the deep and superficial heads clearly represent the pars mastoidea and pars occipitalis of m. cleidocephalicus. The pars mastoidea merges partially with the fibers of m. subclavius. However, in both specimens, the pars mastoidea and pars occipitalis fuse in the caudal half of the neck. The insertion of the resulting, fused belly (analogous to m. cleidobrachialis) is fleshy and broad, onto the cranial aspect of the deltoid tuberosity of the humerus (Fig. 1; Plate 2).

When the head and neck are fixed, m. brachiocephalicus plays a crucial role in advancing the forelimb craniad; when the forelimbs are fixed, it depresses the head and neck (with bilateral contraction) or laterally flexes the head and neck (with unilateral contraction).

Mm. serrati ventrales.

Mm. serrati ventrales cervicis et thoracis form a fan-shaped, continuous sheet of muscle, originating from the cervical transverse processes and continuing caudally off the first through ninth ribs. The cervical portion of the muscle (m. serratus ventralis cervicis) is massive, and originates by means of a series of slips from the wing of the atlas, adjacent to the origin of m. omotransversarius, and the transverse processes of all of the cervical vertebrae. The slip of origin from the atlas and axis is flatter and wider than the rest. The fibers of m. serratus ventralis cervicis insert onto: the fascia of m. supraspinatus near the cranial angle of the scapula, a triangular, rugose area on the lateral aspect of the scapula near the cranial angle, the cranial border of the scapula, and a fossa on the craniodorsal corner of the medial aspect of the scapula, becoming tendinous as it approaches m. subscapularis (Fig. 2; Plate 1).

The thoracic portion of the muscle (m. serratus ventralis thoracis) consists of robust slips arising from the ribs, and interdigitating extensively with m. obliquus externus abdominis (Fig. 1). The slips of m. serratus ventralis thoracis originate from the angle and lateral aspects of the first through sixth ribs, and the dorsal and lateral aspects of ribs 7 through 9. The slips are robust cranially, and become progressively thinner caudally. They converge to form a flat, stout tendon that inserts on the caudal angle of the scapula and the dorsal half of a longitudinal ridge on the medial aspect of the scapula (Plate 1). The insertion consists of tendon (externally) and fleshy fibers (internally) and becomes more tendinous as it approaches the origins of mm. teres major and subscapularis. In one specimen (no. 29218), the insertion extended onto the fascia of m. subscapularis. Along the vertebral border of the scapula, the fibers of mm. serrati ventrales cervicis et thoracis fuse extensively with those of mm. rhomboidei cervicis et thoracis.

Mm. serrati ventrales cervicis et thoracis suspend and support the trunk between the two scapulae. If the forelimb is free, m. serratus ventralis cervicis pulls the limb caudad (retraction) while m. serratus ventralis thoracis draws it craniad (protraction). When the forelimb is fixed, m. serratus ventralis cervicis elevates the neck (with bilateral contraction) or flexes it laterally (with unilateral contraction) while m. serratus ventralis thoracis propels the trunk craniad. M. serratus ventralis thoracis can also aid in forced inspiration.

M. pectoralis superficialis.

Although the pectoral muscles were damaged during both necropsies, the following observations are clear. M. pectoralis superficialis is a large, fan-shaped muscle. It originates from the sternum and the tunica flava abdominis, 5–8 cm caudal to the xiphisternum. The muscle is fused with m. pectoralis profundus at its origin. The cranial fibers of m. pectoralis superficialis are transverse in orientation, while its caudal fibers tend toward the diagonal; however, the muscle is not composed of two distinct parts (i.e., mm. pectoralis descendens and pectoralis transversus). M. pectoralis superficialis inserts by means of a broad, flat tendon onto: the cranial aspect of the middle third of the humeral shaft, just medial to the insertion of m. brachiocephalicus, with which it is partially fused; the fascia of the brachium, superficial to the lateral head of m. triceps brachii; and lastly, the fascia of the flexor compartment of the antebrachium (Plate 2).

M. pectoralis superficialis adducts the forelimb (or pulls the trunk to one side). It also assists in drawing the limb craniad or caudad, depending on the position of the forelimb relative to the trunk.

M. pectoralis profundus.

M. pectoralis profundus is a thick, fleshy muscle taking origin from the sternum and the tunica flava abdominis, extending 30–35 cm caudal to the xiphisternum. The muscle inserts on the cranial aspect of the greater tubercle, distal to m. supraspinatus, then arches across the intertubercular groove along with m. supraspinatus to insert on the lesser tubercle (Plate 2). In addition, part of its tendon of insertion joins the tendon of origin of m. coracobrachialis to attach onto the coracoid process (Plate 1).

M. pectoralis profundus works with mm. serrati ventrales cervicis et thoracis to support the trunk on the forelimbs. When the forelimb is free, m. pectoralis profundus is a powerful retractor.

M. subclavius.

M. subclavius originates deep to m. pectoralis superficialis, from the first rib, manubrium, and cranial half of the sternal body. Its fibers partially merge with those of the deep head of m. brachiocephalicus (m. cleidocephalicus pars mastoidea). M. subclavius inserts entirely onto the fascia of m. supraspinatus. M. subclavius may assist in stabilizing the scapula, preventing abduction of the forelimb.

Muscles of the Shoulder

M. supraspinatus.

A robust, multipennate muscle, m. supraspinatus projects beyond the cranial border of the scapula. It originates from the supraspinous fossa, the craniolateral aspect of the scapular neck, and the lateral surface of the coracoid process, adjacent to the insertion of m. pectoralis profundus and the origins of m. coracobrachialis and m. biceps brachii (Fig. 3; Plate 1). Its origin is primarily fleshy, but it arises by means of tendinous fibers from the cranial border of the scapula, where it is fused with m. subscapularis. In addition, the muscle is fused with the dorsal aspect of the glenohumeral joint capsule. M. supraspinatus inserts first on the dorsal and caudal aspects of the greater tubercle of the humerus (Plate 2). The tendon then crosses over the intertubercular groove, along with the tendon of m. pectoralis profundus, to insert on a ridge on the lateral aspect of the lesser tubercle (Plate 2). M. supraspinatus extends and stabilizes the shoulder joint, helping bear the weight of the body.

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Figure 3. Pygmy hippo forelimb in lateral view.

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M. infraspinatus.

M. infraspinatus originates from the dorsal third of the scapular spine, the infraspinous fossa, and the caudal aspect of the acromion process and scapular neck (Fig. 3; Plate 1). The muscle belly of m. infraspinatus extends over the caudal aspect of the scapula. Along the caudal border of the scapula, m. infraspinatus lies directly adjacent to the origin of the long head of m. triceps brachii, and a ridge of bone marks their junction (Plate 1). M. teres minor takes origin from the deep aspect of m. infraspinatus, and the fibers of the two muscles are intertwined. M. infraspinatus has a thick tendon of insertion, passing deep to m. deltoideus pars acromialis, and inserting extensively onto the caudal process of the greater tubercle, except for a small bare area (Plate 2). M. infraspinatus stabilizes the shoulder joint; it may also assist in extension or flexion of the shoulder joint, depending on the position of the humeral head relative to the glenoid cavity.

M. teres minor.

M. teres minor does not originate from bone; instead, the muscle arises from the fascia covering the deep aspect of m. infraspinatus (Fig. 3). The muscle fibers of m. teres minor are intimately blended with those of m. infraspinatus. In addition, its tendon of insertion is flatter and one third the size of the tendon of m. infraspinatus. It has a small site of insertion on the lateral aspect of the humeral shaft, just dorsal to the deltoid tuberosity (Plate 2). M. teres minor flexes the shoulder joint.

M. deltoideus.

M. deltoideus is composed of a pars acromialis and pars scapularis (Figs. 1, 3). M. deltoideus pars acromialis is a cylindrical muscle originating from the ventral tip of the acromion process (Plate 1). Its origin can be a mixture of superficial fleshy and deep tendinous fibers, or it can consist of a strong tendon only. The fascia on its superficial surface is continuous with that of m. supraspinatus. M. deltoideus pars scapularis does not originate from bone, arising from a thin but tough aponeurosis that is continuous with the fascia covering m. infraspinatus. In addition, a thick aponeurosis joins it to the long head of m. triceps brachii. Through these fascial connections, m. deltoideus pars scapularis arises indirectly from the scapular spine and the caudal half of the vertebral border, including the caudal angle. M. deltoideus pars scapularis fuses distally with m. deltoideus pars acromialis, and together, they insert on the caudolateral aspect of the deltoid tuberosity of the humerus (Plate 2). At its insertion, m. deltoideus pars acromialis is fused extensively with m. brachiocephalicus. M. deltoideus flexes and abducts the shoulder joint.

M. teres major.

M. teres major has an extensive origin from the fascia covering the caudal subdivision of m. subscapularis (Fig. 2). In addition, it arises from a triangular rugosity on the medial aspect of the caudal angle of the scapula (Plate 1). At its bony point of origin, m. teres major is tendinous on its superficial surface, and fleshy on its deep aspect. Distally, the fleshy fibers of m. teres major join the tendon of m. latissimus dorsi (Fig. 2). The resulting tendon courses deep to m. coracobrachialis to insert on the teres major tuberosity on the craniomedial aspect of the humeral midshaft (Plate 2). M. teres major flexes the shoulder joint; it may also assist in adduction.

M. subscapularis.

M. subscapularis has a fleshy origin from the subscapular fossa and cranial border of the scapula (Fig. 2; Plate 1). Its origin is bounded by the insertion of mm. serrati ventrales cervicis et thoracis and the origins of m. teres major and the long head of m. triceps brachii. Its ventral-most point of origin on the scapular neck is marked by a visible indentation (Plate 1). The muscle is partially subdivided into cranial and caudal bellies. The degree of division varies, but in all four limbs dissected, the subdivisions fuse toward the ventral aspect of the scapula. Along its cranial border, the belly of m. subscapularis is closely applied to the fascia of m. supraspinatus. In addition, m. teres major takes partial origin off the fascia of the caudal belly of m. subscapularis. The tendon of m. subscapularis runs deep to m. coracobrachialis to insert on the medial aspect of the lesser tubercle of the humerus, adjacent to the insertion of m. pectoralis profundus (Plate 2). A sesamoid bone may be located deep to the tendon of m. subscapularis. M. subscapularis stabilizes and adducts the shoulder joint; it also may participate in flexion (cranial part) or extension (caudal part) of the shoulder joint.

M. articularis humeri is absent.

Muscles of the Brachium-Flexor Compartment

M. coracobrachialis.

M. coracobrachialis arises by means of a tendon off the medial aspect of the coracoid process of the scapula (Fig. 2; Plate 1). At the coracoid process, the tendon of m. coracobrachialis is joined by some of the tendinous fibers of m. pectoralis profundus. M. coracobrachialis inserts on the cranial aspect of the middle third of the humeral shaft (Plate 2). The proximal part of the insertion is very tendinous, but it becomes fleshy distally. The insertion of m. coracobrachialis partially overlaps, and lies superficial to, the combined insertion of mm. teres major and latissimus dorsi. M. coracobrachialis adducts and flexes the shoulder joint.

M. biceps brachii.

M. biceps brachii is composed of a single, fusiform muscle belly (Fig. 2). The muscle originates by means of a thick, broad tendon off the craniolateral aspect of the supraglenoid tubercle and the scapular neck (Plate 1). The tendon lies deep to m. supraspinatus and courses through the intertubercular groove. In the cubital fossa, the bicipital aponeurosis expands to insert on the heavy fascia superficial to m. pronator teres. In addition, m. biceps brachii has a strong tendinous insertion onto the radial tuberosity and extending along a crest on the lateral aspect of the ulna (Plate 3). A bursa lies deep to the radial insertion. M. biceps brachii flexes the elbow joint; it also helps stabilize the shoulder joint.

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Figure Plate 3. Pygmy hippo radioulna and associated muscle maps. A = medial and B = lateral views.

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M. brachialis.

M. brachialis is a robust muscle, but its bony origin is quite minimal. The humeral attachment of m. brachialis begins medial and proximal to the insertion of mm. teres major and latissimus dorsi, continues proximally onto the medial aspect of the humeral shaft just distal to the lesser tubercle, onto the neck of the humerus, and toward the epiphyseal line of the humeral head (Plate 2). The belly then spirals onto the caudal surface of the humerus, encircling the inferior border of the humeral head and terminating on the caudal aspect of the deltoid tuberosity, adjacent to the origin of the lateral head of m. triceps brachii (Plate 2). Although it has a relatively limited bony origin, the belly of m. brachialis occupies the large sulcus on the caudolateral aspect of the humeral shaft. M. brachialis has a tendinous layer on its deep aspect, along its entire length. It inserts by means of fan-like fibers onto the proximal radius, at a tuberosity located just distal to the radial tuberosity of m. biceps brachii (Plate 3). M. brachialis flexes the elbow joint.

Muscles of the Brachium-Extensor Compartment

M. triceps brachii.
Caput longum.

The long head of m. triceps brachii has an extensive, thin, tendinous origin from the caudal border of the scapula (Figs. 1–3; Plate 1). Its origin includes the caudal angle, the entire caudal border, and the caudolateral aspect of the scapular neck. Near the caudal angle, the muscle takes partial origin from the fascia of m. infraspinatus. The origin widens at the scapular neck, and forms a thickened tendon, leaving a rugosity (Plate 1). The long head fuses with the lateral head of m. triceps brachii, and together they insert on the proximal, caudolateral, and caudomedial aspects of the olecranon process of the ulna (Plate 3). The muscle fibers of the long head continue until just proximal to its site of insertion. Distally, the tendon expands into a fascial layer and inserts on the very thick fascia covering the flexor compartment of the antebrachium. A bursa lies on the olecranon process, deep to the insertion of m. triceps brachii. The long head of triceps flexes the shoulder joint and extends the elbow joint; it also stabilizes the elbow joint when standing.

Caput laterale.

The lateral head of m. triceps brachii originates from the epiphyseal line of the humeral head, just proximal to the origin of m. brachialis, and continues distally along the tricipital line and onto the caudal aspect of the deltoid tuberosity, between the origin of m. brachialis and the insertion of the m. deltoideus pars acromialis et spinalis (Plate 2). In addition, the lateral head takes partial origin from the fascia of m. brachialis. In specimen 110963, the origin was tendinous throughout; in specimen 29218, the origin was tendinous off the tricipital line and deltoid tuberosity, but fleshy off the epiphyseal line of the humeral head. The muscle becomes tendinous just proximal to its site of insertion. As noted above, the lateral head fuses with the long head of m. triceps brachii to insert on the olecranon process (Plate 3) and antebrachial fascia. The lateral head of triceps extends the elbow joint and stabilizes the elbow joint when standing.

Caput mediale.

The medial head of m. triceps brachii is independent from the lateral and long heads (Fig. 2). For most of its length, the medial head parallels the spiral course of m. brachialis, and the belly of m. brachialis overlaps the proximal aspect of the medial head. The medial head originates from the medial and caudal aspects of the humeral shaft, just distal to the belly of m. brachialis (Plate 2). The origin of the medial head tapers distally, arising from the lateral aspect of the olecranon fossa of the humerus. The medial head of m. triceps brachii and m. anconeus are inseparable. The insertion of the medial head dives deep to that of the lateral and long heads, and attaches to the lateral and cranial aspects of the olecranon process (Plate 3). The insertion of the medial head is fan-shaped and fleshy, except for a tendinous portion attaching to a ridge on the cranial aspect of the olecranon (Plate 3). The fascia of the extensor compartment of the antebrachium also originates from this ridge. At its fleshy insertion, fibers of the medial head merge with the origin of the ulnar head of m. flexor digitorum profundus. The medial head of m. triceps brachii extends the elbow joint and stabilizes the elbow joint when standing.

Muscles of the Antebrachium-Flexor Compartment

Retinacula.

A strong flexor retinaculum holds the flexor tendons in place.

M. pronator teres.

M. pronator teres arises by means of a narrow tendon from the medial epicondyle of the humerus, proximal to the origin of m. flexor carpi radialis (Fig. 4; Plate 2). The belly of m. pronator teres is small and is completely covered by a very thick layer of fascia. This fascia attaches to a ridge on the medial aspect of the distal third of the radius (Plate 3). In the cubital fossa, the bicipital aponeurosis expands to insert on this fascia. Distally, m. pronator teres gives rise to a thin tendon that is continuous with the flexor retinaculum. In the left forelimb of specimen 29218, a small accessory belly arose from the radial side of the humeral head of m. flexor digitorum profundus to join the tendon of m. pronator teres. Contraction of m. pronator teres tightens the fascia of the flexor compartment of the antebrachium and the flexor retinaculum, keeping the flexor tendons in place.

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Figure 4. Pygmy hippo antebrachium and manus in caudal view.

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M. flexor carpi radialis.

M. flexor carpi radialis is a robust, spindle-shaped muscle. It takes origin from the medial epicondyle of the humerus, distal to the origin of m. pronator teres (Fig. 4; Plate 2). Its tendon travels in its own fibrous tunnel in the distal third of the antebrachium, then dives between the os carpale II (os trapezoideum) and the os carpale III (os capitatum) to insert on the palmar process of the latter and the base of the second metacarpal (Plate 4; note: the insertion onto the os carpale III is not visible in palmar view). M. flexor carpi radialis extends the elbow joint and flexes the carpal and carpometacarpal joints of digit II.

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Figure Plate 4. Pygmy hippo manus and associated muscle maps. A = dorsal, B = palmar, and C = palmar detailed views.

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M. palmaris longus.

M. palmaris longus originates from the caudal aspect of the medial epicondyle of the humerus (Fig. 4; Plate 2). It is fused at its origin with m. flexor digitorum superficialis and the humeral head of m. flexor carpi ulnaris. In the right forelimb of specimen 110963, it was difficult to separate the bellies of m. palmaris longus and the humeral head of m. flexor carpi ulnaris. The tendon of m. palmaris longus lies superficial to the other flexor muscles and inserts partially onto the palmar fascia. However, the tendon continues distally, superficial to the palmar fascia, and sends a small slip to the lateral-most tendon of m. flexor digitorum superficialis to digit IV, while a larger slip (twice the size of the former) forms the superficialis tendon to digit V. This digit V tendon is joined by some muscle fibers from the m. abductor digiti V, forms a tunnel for the profundus tendon to travel through, and eventually inserts on the medial aspect of the base of the middle phalanx (Fig. 4; Plate 4).

M. palmaris longus weakly flexes the carpal joint. In addition, m. palmaris longus contributes to the flexion of digit IV, and flexes and adducts digit V at the metacarpophalangeal and proximal interphalangeal joints.

M. flexor carpi ulnaris.

M. flexor carpi ulnaris is composed of two heads of origin: ulnar and humeral. The ulnar head consists of a thin sheet of muscle fibers arising from the joint insertion of the long and lateral heads of m. triceps brachii and the fascia covering the ulnar head of m. flexor digitorum profundus (Fig. 4). The proximal fibers of the ulnar head fan out toward the medial epicondyle, but more distally, its fibers run parallel to those of the other flexors. The ulnar head becomes tendinous at one third to two thirds the length of the antebrachium. The humeral head of m. flexor carpi ulnaris shares an origin from the medial epicondyle with m. palmaris longus and the humeral head of m. flexor digitorum superficialis (Fig. 4; Plate 2). It is spindle-shaped, much more robust than the ulnar head, and remains fleshy almost to its point of insertion. It can be extensively fused with the belly of m. palmaris longus (right forelimb of specimen 110963). In three of the limbs dissected, the ulnar and humeral heads remained separate, and inserted separately, but in close proximity, on the palmar aspect of the os carpi accessorium (os pisiforme) (Plate 4). However, in the left forelimb of specimen 110963, the ulnar and humeral heads joined in the distal third of the antebrachium, and gave rise to a common, flat tendon of insertion. In all cases, the insertion onto the os carpi accessorium is partially fleshy, as the humeral head fibers extend quite distally. In addition, in the left forelimb of specimen 110963, some tendinous fibers also fanned out laterally, running superficial and lateral to the belly of m. abductor digiti V, to merge with the fascia overlying that muscle. Thus, in this limb, m. flexor carpi ulnaris also inserted, by means of this fascia, onto the lateral aspect of the fifth metacarpal shaft and head. M. flexor carpi ulnaris extends the elbow joint and flexes and weakly abducts the carpal joint.

M. flexor digitorum superficialis.

M. flexor digitorum superficialis originates from the medial epicondyle of the humerus, distal to the origin of m. flexor carpi radialis (Fig. 4; Plate 2). The muscle is completely fused at its origin with m. palmaris longus and the humeral head of m. flexor carpi ulnaris, and partially fused with the two humeral heads of m. flexor digitorum profundus. In three of the limbs dissected, there were no discernible subdivisions of m. flexor digitorum superficialis; however, in the right forelimb of specimen 29218, m. flexor digitorum superficialis was incompletely divided into two bellies.

M. flexor digitorum superficialis gives rise to three tendons, to digits II, III, and IV (Fig. 4). The digit II tendon is the smallest, whereas the digit III tendon can be slightly larger, or equal in size, to the digit IV tendon. The tendons of m. flexor digitorum superficialis form tunnels for the passage of the profundus tendons. The digit II tendon fans out at the metacarpophalangeal joint, contributes to the lateral aspect of the metacarpophalangeal retinaculum, and forms a tunnel for the profundus tendon. It then courses along the ventrolateral aspect of the proximal phalanx and inserts on the ventrolateral aspect of the base of the middle phalanx (Plate 4). The superficialis tendons to digits III and IV bifurcate at the level of the metacarpophalangeal joints, fuse with the metacarpophalangeal retinaculum, and form a complete tube through which the profundus tendon travels. At the midshaft of the proximal phalanx, the tendons divide once again, passing lateral and medial to the profundus tendon to fuse with the proximal interphalangeal joint retinaculum and joint capsule. The resulting slips insert on the palmolateral and palmomedial aspects of the base of the middle phalanx (Plate 4). Before its point of bifurcation at the metacarpophalangeal joint, the tendon to digit IV receives a slip from m. palmaris longus. M. flexor digitorum superficialis extends the elbow joint, flexes the carpal joint, and flexes the metacarpophalangeal and proximal interphalangeal joints of digits II–IV.

M. flexor digitorum profundus.

M. flexor digitorum profundus is composed of two partially fused humeral heads and a spindle-shaped ulnar head (Fig. 4). The humeral heads take origin from the medial epicondyle, just distal to the shared origin of mm. palmaris longus, flexor digitorum superficialis, and the humeral head of m. flexor carpi ulnaris (Plate 2). At their origin, the humeral heads of profundus are partially fused with m. flexor digitorum superficialis. In fact, a single scar on the medial epicondyle marks the origin of m. flexor digitorum superficialis, m. palmaris longus, the humeral head of m. flexor carpi ulnaris, and the humeral heads of m. flexor digitorum profundus. The humeral heads of m. digitorum profundus are fused at their origin, separable in their midsection, and fused distally, where they form a single tendon. The ulnar head of m. digitorum profundus originates from the medial surface of the olecranon process, distal to the insertion of the long and lateral heads of m. triceps brachii, and forms a single tendon (Fig. 4; Plate 3). The ulnar tendon is one fifth the size of the humeral tendon. The humeral and ulnar tendons fuse to form a thick, flattened tendon that provides a trough-like surface for the tendons of m. flexor digitorum superficialis.

The common tendon of m. flexor digitorum profundus divides to send strong tendons to insert on each of the four digits (Fig. 4). The tendons to digits III and IV are very robust and equal in size. The tendons to digits II and V are smaller than those to the central digits. The digit V tendon can be slightly larger, or equal in size, to the digit II tendon. The profundus tendons to digits II and V divide at the distal interphalangeal joint and fan out to insert on the palmar aspect of the distal phalanx (Plate 4). The profundus tendons to digits III and IV exhibit a midline groove, but the fibers are not separable. The tendons insert by means of a fan-shaped extension onto the palmar aspect of the distal phalanx (Plate 4).

M. flexor digitorum profundus extends the elbow joint, flexes the carpal joint, and flexes digits II through V at the metacarpophalangeal, proximal and distal interphalangeal joints. In addition, m. flexor digitorum profundus forcefully adducts digits II and V, and weakly adducts digits III and IV.

Mm. interflexorii are absent.

M. pronator quadratus is absent.

Muscles of the Antebrachium-Extensor Compartment

Retinacula.

The tendon of m. extensor digitorum lateralis travels through its own retinaculum at the carpus. The tendons of m. extensor digitorum communis are also held in place by a distinct retinaculum, while m. extensor carpi radialis and m. abductor digiti I longus share a retinaculum. The tendon of M. extensor carpi ulnaris does not travel under a retinaculum.

Mm. supinator and brachioradialis are absent.

M. extensor carpi ulnaris.

The origin of m. extensor carpi ulnaris is entirely tendinous, and creates an ovoid scar on the caudolateral aspect of the lateral epicondyle of the humerus, adjacent to the origin of m. extensor digitorum lateralis (Plate 2). M. extensor carpi ulnaris is mostly tendinous, although it does have a small muscle belly (Fig. 5). Its stout tendon inserts on the lateral aspect of the os carpi accessorium. M. extensor carpi ulnaris extends the elbow joint and flexes and abducts the carpal joint.

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Figure 5. Pygmy hippo antebrachium and manus in cranial view.

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M extensor digitorum lateralis.

M. extensor digitorum lateralis arises from the humerus and ulna (Fig. 5). The tendinous humeral origin creates a large scar on the lateral epicondyle, adjacent to the origin for m. extensor carpi ulnaris (Plate 2). The ulnar origin is initially tendinous, arising from the lateral aspect of the middle third of the ulna, but becomes fleshy distally, near the origin of m. abductor digiti I longus (Plate 3). The fleshy ulnar origin creates a depression on the shaft of the ulna (Plate 3). The ulnar and humeral fibers fuse to form a single belly proximally, but this divides again, forming medial and lateral subdivisions in the distal two thirds of the antebrachium. Near its origin, m. extensor digitorum lateralis is fused with m. extensor digitorum communis. However, in the distal half of the antebrachium, the lateral extensor lies in its own fascial compartment, separated from the common extensor by a thick fascial septum that attaches to a tuberosity on the distal ulna (Plate 3).

M. extensor digitorum lateralis gives rise to two tendons of insertion, to digits IV and V (Fig. 5). The digit IV tendon is derived from fibers of the medial belly, while the digit V tendon is derived from those of the lateral. The tendon to digit IV is slightly larger than its counterpart. The digit IV tendon travels deep to the common extensor tendon to digit V, and crosses dorsolaterally over the metacarpophalangeal joint of digit IV, where it is joined by the tendon of m. abductor interosseus digiti IV. The tendon then courses lateral to the digit, and inserts on the lateral aspect of the distal half of the proximal phalanx and base of the middle phalanx (Plate 4). In the right forelimb of specimen 29218, the digit IV tendon was joined by a slip from m. extensor digitorum communis. The tendon to digit V passes dorsolaterally over the metacarpophalangeal joint, travels lateral to the digit, and inserts on the lateral aspect of the distal half of the proximal phalanx and base of the middle phalanx (Plate 4).

M. extensor digitorum lateralis extends the carpal joint and the metacarpophalangeal and proximal interphalangeal joints of the fourth and fifth digits. In addition, m. extensor digitorum lateralis abducts digits IV and V. The lateral fibers of m. extensor digitorum lateralis extend the elbow joint, but the medial fibers flex this joint.

M. extensor digitorum communis.

M. extensor digitorum communis takes origin from the craniolateral aspect of the lateral epicondyle of the humerus, adjacent to the origin of m. extensor digitorum lateralis, with which it is fused (Fig. 5; Plate 2). On its lateral aspect, m. extensor digitorum communis is also fused extensively with the belly of m. extensor carpi radialis. As a result, the common extensor also takes origin indirectly from the radial fossa. This muscle and its tendons of insertion were variable in the limbs dissected. The belly was incompletely divided into two portions in one limb, but demonstrated three or four bellies in the others, each with a tendon. Figure 6 illustrates the variation observed in the tendon arrangements of these specimens. In all of the limbs, tendons of insertion served digits III, IV, and V; in all but one limb there was also a tendon of insertion to digit II. The tendons of m. extensor digitorum communis insert on the distal phalanx, although in some cases slips also insert more proximally. M. extensor digitorum communis flexes the elbow joint, extends the carpal joint, and extends the metacarpophalangeal, proximal and distal interphalangeal joints of digits II–V.

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Figure 6. Variation in the distribution of the tendons of m. extensor digitorum communis to digits 2–5. A: Specimen 29218 (dotted line indicates fibers joining m. extensor digitorum lateralis). B: Left forelimb of specimen110963 (dotted line indicates minor contribution of fibers). C: Right forelimb of specimen 110963.

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M. extensor carpi radialis.

M. extensor carpi radialis is very robust and has an extensive origin off the lateral epicondylar crest, the craniolateral aspect of the lateral epicondyle, the radial fossa, and the tendon of origin of m. extensor digitorum lateralis (Fig. 5; Plate 2). The origin is fleshy off the lateral epicondyle. The origin off the lateral epicondylar crest may be tendinous (specimen 29218) or fleshy (specimen 110963), and the origin off the radial fossa may be tendinous (specimen 29218) or a mixture of tendinous and muscular fibers (specimen 110963). M. extensor carpi radialis has the appearance of having two subdivisions, but this is only due to its bipennate nature, with fibers running in two different directions. Fibers from the lateral epicondyle curve across the cranial aspect of the humerus to insert on the medial side of the central tendon, while more distal fibers course in the opposite direction to insert on its lateral aspect. The tendon of m. extensor carpi radialis is crossed superficially by the tendon of m. abductor digiti I longus at the level of the carpal joint. M. extensor carpi radialis has a robust, broad, and flat tendon which fans out to insert primarily on two tubercles on the dorsal aspect of the base of the third metacarpal (Fig. 5; Plate 4). In addition, a small slip extends onto a tubercle on the dorsomedial aspect of the base of the fourth metacarpal (Fig. 5; Plate 4). M. extensor carpi radialis flexes the elbow joint and extends and stabilizes the carpal joint.

M. abductor digiti I longus.

M. abductor digiti I longus is a small, fusiform muscle lying deep to m. extensor digitorum communis (Fig. 5). The muscle has a fleshy origin from the lateral aspect of the radius and ulna, distal to the proximal interosseous space (Plate 3). Its belly courses diagonally across the extensor compartment to insert on the medial side of the carpus. At the level of the carpus, its tendon passes superficial to the tendon of m. extensor carpi radialis. It inserts on the ventromedial aspect of the os carpale II (Fig. 5; Plate 4). M. abductor digiti I longus flexes and abducts the carpal joint; this finding is in contrast to its usual action in artiodactyls, where its more dorsal insertion makes it an extensor of the carpal joint (Getty, 1975; Nickel et al., 1986).

M. extensor digiti II.

M. extensor digiti II is not present as a distinct muscle in the pygmy hippo. It is possible that it has been incorporated into m. extensor digitorum communis.

Intrinsic Muscles of the Manus

Retinacula.

There are thick retinacula for the long flexor tendons at the metacarpophalangeal and proximal and distal interphalangeal joints of each digit. The metacarpophalangeal retinacula are especially robust and well-developed.

Sesamoid bones.

There are two sesamoid bones (lateral and medial) located on the palmar aspect of the metacarpophalangeal joints in all four digits.

M. flexor digitorum brevis.

M. flexor digitorum brevis is represented by fibers arising from the deep aspect of the tendon of m. palmaris longus (Fig. 4). The muscle fibers do not give rise to a tendon.

M. lumbricalis IV.

The single lumbrical originates from the m. flexor digitorum profundus tendon serving digits III and IV, proximal to its subdivision (Fig. 4). M. lumbricalis IV inserts by means of a tendon onto the medial aspect of the base of the proximal phalanx of digit IV (Plate 4). M. lumbricalis IV flexes the metacarpophalangeal joint of digit IV and weakly adducts the digit.

M. abductor digiti V.

M. abductor digiti V originates from the palmar surface of the os carpi accessorium and adjacent connective tissue (Plate 4). Distally, some of its fibers join the superficialis tendon to digit V, which is derived from m. palmaris longus. However, m. abductor digiti V primarily inserts by means of a fan-shaped tendon onto the palmolateral aspect of the base of the proximal phalanx (Plate 4). It inserts partially onto the lateral aspect of the metacarpophalangeal joint capsule and is largely fused with m. abductor interosseous digiti V at its insertion. M. abductor digiti V abducts digit V and weakly flexes its metacarpophalangeal joint.

M. adductor digiti V.

This muscle lies superficial to mm. adductor interosseus digiti V and abductor interosseus digiti IV (Fig. 7). It has a fleshy origin from the palmar aspects of the os carpale III and os carpale IV (os hamatum) and inserts onto the medial aspect of the base and shaft of the proximal phalanx of digit V (Plate 4). In one limb (specimen 110963), the tendon also inserted on the medial aspect of the metacarpophalangeal joint capsule. M. adductor digiti V adducts digit V and weakly flexes its metacarpophalangeal joint.

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Figure 7. Pygmy hippo manus in palmar view.

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M. adductor digiti II.

This muscle lies superficial to mm. adductor and abductor interossei digiti III and m. adductor interosseus digiti II (Fig. 7). It has a fleshy origin from the palmar aspect of the os carpale III (Plate 4). The tendon crosses the metacarpophalangeal joint medially to insert on the medial aspect of the base of the proximal phalanx of digit II (Plate 4). In the right manus of specimen 110963, the insertion extended onto the base of the middle phalanx. M. adductor digiti II adducts digit II and weakly flexes its metacarpophalangeal joint.

Mm. interossei (Fig. 7; Plate 4).

M. abductor interosseus digiti II consists of either one or two bellies. It arises from the palmar aspect of the os carpale II and the base of the second metacarpal. If two bellies are present, they fuse distally to insert. The muscle inserts on the medial sesamoid, medial aspect of the metacarpophalangeal joint capsule, base of the proximal phalanx, and extensor expansion of digit II. The connection to the extensor expansion may be very weak. The muscle abducts digit II, flexes its metacarpophalangeal joint, and weakly extends its interphalangeal joints.

M. adductor interosseus digiti II lies deep to m. adductor digiti II and originates from the palmar aspect of the os carpale III and the base of the second metacarpal. The muscle inserts on the lateral sesamoid and the lateral aspect of the metacarpophalangeal joint capsule and base of the proximal phalanx. It also has a weak connection to the extensor expansion on the lateral aspect of the digit. The muscle adducts the second digit and flexes its metacarpophalangeal joint. It may also weakly extend the interphalangeal joints.

M. abductor interosseus digiti III lies deep to m. adductor digiti II and is partially fused at its origin with m. adductor interosseus digit III. It arises from the palmar aspect of the os carpale III and the base of the third metacarpal, and inserts on the medial sesamoid and the medial aspect of the metacarpophalangeal joint, base of the proximal phalanx, and extensor expansion. The muscle abducts digit III, weakly flexes its metacarpophalangeal joint, and weakly extends its interphalangeal joints.

M. adductor interosseus digiti III lies partially under the origin of m. adductor digiti II and is fused proximally with mm. abductor interosseus digiti III and adductor interosseus digiti IV. It originates from a tubercle on the palmar aspect of the base of the third metacarpal, and inserts onto the lateral sesamoid and the lateral aspect of the metacarpophalangeal joint capsule, base of the proximal phalanx, and extensor expansion of digit III. The muscle adducts the third digit, weakly flexes its metacarpophalangeal joint, and weakly extends its interphalangeal joints.

M. adductor interosseus digiti IV lies deep to m. adductor digiti V, and is fused proximally with mm. adductor interosseus digiti III and abductor interosseus digiti IV. It originates from the palmar aspect of the os carpale IV, the base of the third metacarpal, and a tubercle on the palmar aspect of the base of the fourth metacarpal. The muscle inserts onto the medial sesamoid and the medial aspect of the metacarpophalangeal joint capsule, base of the proximal phalanx, and extensor expansion of digit IV. In the right manus of specimen 110963, a very small accessory belly lies palmar to the main muscle, and inserts solely into the fascia overlying the metacarpophalangeal joint capsule. The muscle adducts digit IV, weakly flexes its metacarpophalangeal joint, and extends its interphalangeal joints.

M. abductor interosseus digiti IV lies deep to m. adductor digiti V and is fused proximally with m. adductor interosseus digiti IV. It originates from the palmar aspect of the os carpale IV and a tubercle on the palmar aspect of the base of the fourth metacarpal and inserts onto the lateral sesamoid and the lateral aspect of the metacarpophalangeal joint capsule, base of the proximal phalanx, and extensor expansion of digit IV. When it inserts onto the extensor expansion, its tendon joins that of the m. extensor digitorum lateralis to digit IV. The muscle abducts digit IV, weakly flexes its metacarpophalangeal joint, and weakly extends its interphalangeal joints.

M. adductor interosseus digiti V lies between m. adductor digiti V and m. abductor interosseus digiti V. The muscle originates from the palmar aspect of the os carpale IV and the base of the fifth metacarpal. It inserts onto the medial sesamoid and the medial aspect of the metacarpophalangeal joint capsule and base of the proximal phalanx. It then continues distally to insert on the proximal interphalangeal joint capsule, the medial aspect of the base of the middle phalanx (immediately adjacent to the insertion of the digit V superficialis tendon), and the medial aspect of the extensor expansion of digit V. The muscle adducts digit V, weakly flexes its metacarpophalangeal joint, and weakly extends its interphalangeal joints.

M. abductor interosseus digiti V lies deep to m. abductor digiti V and may have two divisions, although they are not completely separable. It originates from the palmar aspect of the os carpale IV, but it has a more extensive origin from the palmar aspect of the base of the fifth metacarpal. It inserts by means of fleshy fibers onto the tendon of m. abductor digiti V and then inserts by means of a tendon onto the lateral sesamoid and the lateral aspect of the metacarpophalangeal joint capsule and base of the proximal phalanx of digit V. The muscle abducts digit V and weakly flexes its metacarpophalangeal joint.

DISCUSSION

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

Range of Variation in Choeropsis

The results of the Choeropsis dissections in this study differed in some respects from previous accounts, reflecting a range of variation in the myology of the pygmy hippo. For example, the origins of mm. rhomboidei and m. trapezius vary in Choeropsis. The mm. rhomboidei may originate in the neck (Campbell, 1935, 1936; this study) or from the occiput (Macalister, 1873). Similarly, Campbell (1935, 1936) describes m. trapezius originating from the C6 or C7 vertebral level, whereas this study and Macalister (1873) indicates that an occipital origin is present in some individuals. In fact, longer-necked artiodactyls tend to lose the occipital origin of m. trapezius; common hippos, ruminants, and camels lack an occipital origin. In contrast, a cranial attachment is present in suids and tayassuids. Pygmy hippos appear to lie in an intermediate position, demonstrating variable origins for this muscle.

The insertion of m. brachialis also appears to vary in the pygmy hippo. According to this study, Macalister (1873), and Macdonald et al. (1985), the muscle inserts on the radius only; however, Campbell (1935, 1936) recorded both radial and ulnar insertions. Most artiodactyl species also demonstrate a wide variety of insertions. For example, in Sus, the muscle may insert on the radius and ulna, or on one bone only. Because the radius and ulna are functionally or actually fused in artiodactyls, the reasons for this variation are unclear.

M. flexor digitorum profundus also exhibits a range of variation. According to this study, it arises by means of an ulnar and two humeral heads; however, Campbell (1935, 1936) also describes a weak radial head in the pygmy hippo. Three or four bellies of origin are present in the common hippo, including an ulnar head and two or three humeral heads. In suids, tayassuids, and ruminants, there is a radial, an ulnar, and one to three humeral heads. Finally, in Camelus, radial and ulnar heads are joined by a humeral head with two subdivisions. The functional significance of these variations is unclear. The muscles of the extensor antebrachium are particularly variable, not only in hippos, but in all artiodactyls. Each of the extensor muscles vary in terms of the number of muscle bellies and tendons present. For example, in Choeropsis, m. extensor carpi radialis may insert on the third and fourth metacarpals, or solely on the former. In common hippos, insertions also vary and may include second and third metacarpal, third metacarpal, or third and fourth metacarpal attachments. Other artiodactyls display a range of metacarpal insertions (Sus: third, or third and fourth; Babyrousa: second and fourth; Pecari: third; ruminants and Camelus: homologue of the third). Extensor variations that are functionally or phylogenetically relevant are discussed below.

Functional and Phylogenetic Considerations

The muscles of the forelimb offer several insights into the functional anatomy and phylogenetic relationships of hippos relative to other artiodactyls. Among the extrinsic muscles, m. brachiocephalicus is noteworthy. Choeropsis demonstrates typical artiodactyl origins and insertions for this muscle; however, a clear intersectio clavicularis is absent. Published accounts of common hippos are ambiguous regarding this trait. Interestingly, among artiodactyls, the intersectio clavicularis is also absent in Hyemoschus and Tragulus. Thus, hippos are similar to tragulids in this regard.

The pectoral muscles of hippos also differ from those of other artiodactyls. While published descriptions of common hippos are unclear on the matter, illustrations indicate the pectoral muscles are similarly arranged in the two species. Hippos resemble Babyrousa, ruminants, and camels in lacking a clear subdivision of the superficial pectoral. In contrast, m. pectoralis superficialis is clearly divided into two parts (mm. pectoralis descendens and pectoralis transversus) in Sus and Pecari. Most importantly, hippos are distinct among the artiodactyls in having a more extensive origin for m. pectoralis superficialis; in other artiodactyls, the muscle is restricted to the first three to six costal cartilages, while in hippos, m. pectoralis superficialis extends up to 8 cm caudal to the xiphisternum. M. pectoralis profundus is also characterized by a broad origin in hippos compared with other artiodactyls, extending up to 35 cm caudal to the xiphoid process. Both pectoral muscles are crucial parts of the suspensory apparatus of the trunk. The pectoral muscles support the trunk on the limbs, retract the unsupported limb, and advance the trunk over the fixed limb. They are also capable of moving the trunk laterally over a fixed limb. The well-developed pectoral muscles in hippos reflect a capacity for powerful retraction of the forelimb; this may be an adaptation for charging (a staple of intraspecific interaction), climbing the steep inclines of muddy river and lake banks, and propelling the body forward against the resistance of water during underwater locomotion.

The four muscles that stabilize the hippo shoulder joint (mm. infraspinatus, supraspinatus, subscapularis, and teres minor) are similar to those of most artiodactyls, although there are a few points of difference. For example, in pygmy and common hippos, m. infraspinatus inserts by means of a single tendon onto the caudal aspect of the greater tubercle of the humerus. Babyrousa and Camelus resemble the hippos; however, in Sus and ruminants, the tendon divides into a deeper, fleshy insertion and a superficial, tendinous insertion. The deeper limb inserts on the medial surface of the humerus in pigs, and on the caudal aspect of the greater tubercle in ruminants, whereas the more superficial inserts on a depression lateral to the caudal aspect of the greater tubercle. M. subscapularis is partially subdivided in pygmy hippos and may have up to three divisions in the common hippo. Suids and camels lack subdivisions; however, ruminants may have three or four parts. Thus, pygmy hippos appear to be intermediate between suids and ruminants, whereas common hippos approximate the ruminant condition.

M. deltoideus is subdivided into a pars acromialis and a pars scapularis in both pygmy and common hippos. Due to the reduction of the acromion process in suids, m. deltoideus is undivided in these artiodactyls. However, ruminants and camels have distinct acromial and scapular parts, thus resembling hippos. M. articularis humeri is not described in accounts of common hippos, suggesting that it is absent in all hippos. The muscle is also absent in ruminants. In contrast, m. articularis humeri is constant in Babyrousa and variably present in Sus. It is also present in Camelus. Yet again, the hippos resemble ruminants more closely than other artiodactyls.

The muscles of the hippo brachium differ from those of most artiodactyls in only a few significant ways. M. coracobrachialis consists of a single belly in pygmy and common hippos. In contrast, two bellies are present in suids, ruminants, and camels. In addition, pygmy and common hippos have an undivided medial head of m. triceps brachii. In Sus, the medial head is divided into two parts by the conjoined tendon of mm. latissimus dorsi and teres major. This tendon also divides the medial head in Babyrousa, although the two parts fuse distally. In ruminants, an accessory medial belly is also present to a variable extent. In this case, hippos resemble Camelus, which also lacks an accessory triceps muscle. Lastly, in the pygmy hippo, m. anconeus is fused with the medial head of m. triceps brachii. However, it forms a distinct muscle in the common hippo. M. anconeus is also independent in Sus and Camelus. In Babyrousa, it is fused with both medial and lateral heads, and in ruminants it is fused with the lateral head.

The flexor muscles of the hippo antebrachium show some interesting contrasts to other artiodactyls. M. palmaris longus is present in pygmy hippos and variably present in common hippos. In the pygmy hippos dissected for this study, m. palmaris longus inserted onto the palmar aponeurosis, contributed fibers to the superficial flexor tendon to digit IV, and formed the entire superficialis tendon to digit V. However, Macalister (1873) and Campbell (1935, 1936) recorded an insertion only onto the palmar aponeurosis in their pygmy hippos. Although Gratiolet and Alix (1867) claimed it was absent in the common hippo, Macdonald et al. (1985) and Kajava (1923) observed m. palmaris longus in the larger species. Kajava (1923) describes m. palmaris longus inserting onto the palmar aponeurosis, with extensions to the long flexor tendon sheaths and the base of the proximal phalanx of digit II. M. palmaris longus is absent in all other artiodactyls and all perissodactyls; however, it is present in elephants and hyraxes. Thus, hippos are unique among ungulates in retaining this feature.

In both hippo species, m. flexor carpi ulnaris exhibits two separate bellies: ulnar and humeral. These bellies may give rise to a common tendon or independent tendons of insertion. The primary insertion is the os carpale accessorium; however, this may be accompanied by a secondary insertion onto the metacarpal or proximal phalanx of digit V. In Sus, the ulnar head can be absent, or, if present, much reduced. The ulnar head is also absent in Potamochoerus and Babyrousa, while it is much reduced in Pecari and Camelus. In ruminants, there are two heads of origin, but the ulnar head is weak and largely tendinous. Therefore, m. flexor carpi ulnaris is more developed in hippos versus suids and tayassuids, and to a lesser extent, ruminants. Perissodactyls also vary in the degree of development of the ulnar head; it is reduced in Tapirus, variably absent in Equus, and present in Dicerorhinus. Both heads are present and well developed in hyraxes and elephants. Thus, compared with other artiodactyls, hippos demonstrate a more primitive condition in retaining the ulnar head of m. flexor carpi ulnaris.

The digital flexors of hippos also show several interesting features. M. flexor digitorum superficialis usually consists of a single muscle belly in pygmy and common hippos. However, in suids, tayassuids, and ruminants, the muscle has superficial and deep parts. M. flexor digitorum superficialis is very derived in Camelus, lacking a muscle belly altogether; this tendinous structure originates from the os carpale accessorium and metacarpal bone. In hippos, the muscles contributing to the long flexor tendons differ from those in other artiodactyls. M. flexor digitorum superficialis does not provide a tendon to digit V in Choeropsis; instead, the superficial tendon to this digit is provided by m. palmaris longus (this study) or m. flexor digitorum brevis V (Campbell, 1935, 1936). A digit V contribution from m. flexor digitorum superficialis is usually present in the common hippo; however, when absent, this tendon is provided by m. flexor digitorum brevis V (Macalister et al., 1985). In addition, m. flexor digitorum profundus supplies tendons to all four digits in hippos. Thus, a pair of long flexor tendons serves each of the digits in the Hippopotamidae. In suids and tayassuids, there are strong superficial and deep tendons to digits III and IV, and weak deep tendons to digits II and V only. However, deep tendons do serve all four digits in Potamochoerus. In camels and most ruminants, there are strong superficial and deep tendons to digits III and IV only; however, Ovibos, Tragulus, and Hyemoschus have deep tendons to all four digits. Thus, the flexor tendons of hippos resemble those of Potamochoerus, Ovibos, and tragulids. In most artiodactyls, digits II and V are not typically weight-bearing, as they are in hippos (Fig. 8). In addition, the presence of long flexor tendons to all four digits in hippos would assist in adducting the toes to help prevent splaying, especially on soft terrain. The condition in Tapirus and Dicerorhinus parallels that of hippos, with superficial and deep tendons serving digits II–IV. In contrast, single superficial and deep tendons serve the central digit in Equus. Interestingly, the mm. interflexorii are absent in pygmy and common hippos. Mm. interflexorii are present in suids, tayassuids, and ruminants; however, they are absent in camels. Mm. interflexorii are also absent in perissodactyls. In short, the digital flexor apparatus of hippos is relatively primitive compared with that of other artiodactyls.

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Figure 8. A–C: Lateral view of forelimb in the (A) ox, (B) common hippo, and (C) pig. Whereas hippos have four weight-bearing digits, the pig and ruminant have reduced lateral digits.

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In all artiodactyls, pronators and supinators are reduced or absent. In rare instances, these muscles are variably expressed, as is the case for m. pronator teres in pygmy and common hippos. The muscle was present in this and Campbell's (1935, 1936) study; however, it was absent in Macalister's (1873). Similarly, m. pronator teres was present in Kajava's (1923) common hippo, but absent in those dissected by Cuvier and Laurillard (1849) and Gratiolet and Alix (1867). M. pronator teres is also variably developed in Sus and Potamochoerus; when present, it inserts on the middle to distal thirds of the radius. However, in Babyrousa, m. pronator teres is reduced to a completely tendinous state and inserts more proximally on the radius. In tayassuids, it is a mixture of fleshy and tendinous fibers, and inserts on the midshaft of the radius. With the exception of the tragulids, m. pronator teres is poorly developed in ruminants, and inserts on the proximal third of the radius. The muscle is absent altogether in Camelus. M. pronator teres is variably developed in the perissodactyls, being fibrous or absent in equids, weakly developed or absent in tapirs, and absent in rhinos. M. supinator and m. pronator quadratus are absent in pygmy and common hippos, although Macalister (1873, p. 498) claimed a “barely detectible” m. pronator quadratus was present in his pygmy hippo. Apart from this report, the muscle is absent in all artiodactyls, and there is only a single account of its presence among perissodactyls, in the tapir (Murie, cited in Windle and Parsons, 1901). M. supinator is occasionally present in reduced form in Sus. When present, it is a thin slip of muscle that blends with the radial head of m. flexor digitorum profundus. However, m. supinator is absent in other artiodactyls, and in perissodactyls. Interestingly, m. brachioradialis is absent in the pygmy hippo but variably present in the common hippo. M. brachioradialis is absent in all other artiodactyls and among perissodactyls, it is present in the tapir and rhino. Therefore, the common hippo once again retains a primitive feature that has been lost by other artiodactyls.

As noted above, the antebrachial extensor muscles show considerable variation, both within species and across the Artiodactyla. M. extensor carpi ulnaris is similarly disposed in both species of hippo, although it may be entirely tendinous with a secondary insertion onto the base of the fifth metacarpal in the common hippo. In suids, the muscle is composed of a superficial tendinous and a deep fleshy part; the superficial tendinous part is homologous to the muscle in hippos, but the fleshy belly inserts on the fifth metacarpal, or more rarely, the fourth, and is absent in the hippo (although common hippos can have a similar secondary insertion). In Pecari, the muscle is similar to suids, although the fleshy belly can insert on the os carpale IV and fourth and fifth metacarpals in some individuals. In ruminants, m. extensor carpi ulnaris also inserts more distally, on the fourth or the rudimentary fifth metacarpal, and in Camelus, the insertion reaches the fused metacarpal bone. Therefore, compared with other artiodactyls, m. extensor carpi ulnaris is reduced in the pygmy hippo, losing its connection to the fifth metacarpal. A more distal insertion indicates the muscle acts on the carpometacarpal joint as well as the carpal joint, whereas in the pygmy hippo, it only acts on the latter. This arrangement may allow the carpometacarpal joint to be independent of the carpal joint, allowing for more controlled movement of the digits in the pygmy hippo.

M. extensor digitorum lateralis is incompletely subdivided in the pygmy hippo. Published accounts of the common hippo do not comment on the relative degree of subdivision. In suids and Pecari, the muscle is composed of two distinct bellies, while in ruminants and camels, the muscle is undivided. M. extensor digitorum lateralis sends tendons to digits IV and V in the pygmy hippo, but tendon insertions vary in the common hippo, with fourth and fifth digit tendons, or a single fourth digit tendon. In suids and tayassuids, insertion is onto the fourth and fifth digits; however, a single fifth digit tendon may be present in Sus. In ruminants, it inserts on the fourth digit (giraffids, cervids, most bovids), fourth and third digits (Bos), or fourth and fifth digits (tragulids). Finally, in Camelus, the tendon serves digit IV. Thus, the hippo m. extensor digitorum lateralis most closely resembles that of the tragulids.

M. abductor digiti I longus is similar in its morphology in the common and pygmy hippo, although it may take sole origin from the ulna in the larger species. Campbell (1935, 1936) and Macalister (1873) claim that m. abductor digiti I longus inserts on the vestige of the first metacarpal in the pygmy hippo, but this study revealed an insertion on os carpale II. Humphry (1872, p. 373) also lists the “rudimentary trapezium” as the site of insertion in the common hippo. M. abductor digiti I longus inserts further distally in other artiodactyls, terminating on the base of the second metacarpal in suids, tayassuids, and tragulids, and on the fused third and fourth metacarpals in camels and most ruminants. The proximal insertion of m. abductor digit I longus in hippos mirrors that seen for m. extensor carpi ulnaris. Both muscles flex and abduct the carpal joint; in the case of m. abductor digiti I longus, this function is quite unusual, as it is a carpal extensor in other artiodactyls. As noted above, decoupling the carpal and carpometatacarpal joints may allow for more controlled digital movement in hippos.

M. extensor digiti II is absent in hippos and Camelus, but a rudimentary version of this muscle is present in Sus, where it arises from the ulna, deep to m. extensor digitorum communis, and gives rise to a tendon that fuses with that of the common extensor or inserts on or near the second digit. In Babyrousa, the muscle is quite small and originates from the lateral aspect of the ulna, proximal to the origin of m. abductor digiti I longus and deep to the common extensor. It gives rise to two tendons, one joining a tendon from m. extensor digitorum communis to digit II, and the other inserting onto the fascia covering the third metacarpal. In ruminants, m. extensor digiti II helps form the lateral belly of m. extensor digitorum communis, sending tendons to digits III and IV.

M. flexor digitorum brevis is present in pygmy hippos, although it appears to vary in form. Campbell (1935, 1936) describes this muscle as a small, flat muscle belly arising from the tendon of m. palmaris longus, forming the perforated tendon to the fifth toe, and inserting on the proximal phalanx. He also observed tendinous fibers originating from the os carpi accessorium and joining the m. flexor digitorum superficialis tendon to digit IV as well as the m. flexor digitorum brevis tendon to digit V, and includes these tendinous fibers in the m. flexor digitorum brevis complex. In the two specimens dissected for this study, m. flexor digitorum brevis was represented by muscle fibers on the deep aspect of the m. palmaris longus tendon; a brevis tendon was not present. Elements of m. flexor digitorum brevis are also present in common hippos. Kajava (1923) describes three accessory muscles arising from the m. flexor digitorum superficialis tendons to digits II–IV, as well as m. flexor digitorum brevis digiti V arising from the tendon of m. palmaris longus. The description by Macdonald et al. (1985) is less complete. According to these authors, the muscle originates on “the carpal bone” and inserts on the fifth toe. M. flexor digitorum brevis is absent in other artiodactyls, and among the perissodactyls, it is variably developed in Tapirus. M. flexor digitorum brevis is constant in the hyrax and elephant. This muscle is thus only present in those taxa that retain the more primitive arrangement of lateral weight-bearing digits, but even among these ungulates it is reduced.

The intrinsic muscles of the manus are much more developed in hippos than in other artiodactyls, although the patterns of reduction in different groups are complex. M. lumbricalis IV is present in pygmy and common hippos. In common hippos, the lumbrical may arise from the m. flexor digitorum profundus tendon to digit IV, or before the division of the profundus tendon. Interestingly, Kajava (1923) describes a single lumbrical with insertions on the fourth and fifth digits in his common hippo. For Sus, many authors describe m. lumbricalis II arising from either the common tendon of m. flexor digitorum profundus or the profundus tendon to digit II. However, according to Nickel et al. (1986) and Sisson (1975a), the mm. lumbricales are represented by a few muscle fibers running between the deep flexor tendon and the deep belly of the superficial flexor. Kneepkens et al. (1989) argue that m. lumbricalis II is present in Sus, but is mislabeled “m. flexor digiti II (brevis)” (e.g., sensu Nickel et al., 1986). M. lumbricalis II is also present in Potamochoerus, but mm. lumbricales are absent in Babyrousa and Pecari. In addition, they are absent in camels and most ruminants, although Getty (1975a) describes muscular bundles in domestic ruminants that may be regarded as mm. lumbricales; these arise from m. flexor digitorum profundus and insert onto the digital tendon at the carpus. Although most ruminants lack these muscles, Tragulus may have a lumbrical to the third and fourth digits, or solely to the fourth, while Hyemoschus has m. lumbricalis II. Thus, once again, hippos most closely resemble tragulids, particularly Tragulus. Among perissodactyls, Tapirus has three mm. lumbricales (one to each digit), while Equus has two, each arising from the single profundus tendon. Mm. lumbricales are not present in Dicerorhinus.

M. abductor digiti V is similarly arranged in the pygmy and common hippo; however, Kajava (1923) records an insertion onto the fibrous digital sheath of digit V, rather than a bony insertion in his common hippo. In Sus and Potamochoerus, m. abductor digiti V is similar to that seen in the pygmy hippo. However, Nickel et al. (1986) describe an abductor of the fifth digit in the domestic pig that originates from the palmar aspect of the fifth metacarpal and inserts on the lateral aspect of the metacarpophalangeal joint and proximal phalanx; this muscle could represent m. abductor interosseus digiti V. In Babyrousa, m. abductor digiti V has superficial and intermediate heads. These muscles represent the m. abductor digiti V and the abductor interosseus digiti V described here for the pygmy hippo. M. abductor digiti V is present in tayassuids and resembles the condition present in the pygmy hippo, although Campbell (1935, 1936) did not observe a fleshy representative in his collared peccary. M. abductor digiti V is absent in camels and in all of the ruminants except the tragulids. Among the perissodactyls, m. abductor digiti V is present in Tapirus and Dicerorhinus.

Mm. adductores digiti II et V are present in pygmy and common hippos; however, Kajava (1923) indicates a more distal origin off the metacarpals in his common hippo. Adductors for the lateral digits are present in suids and Pecari. According to some accounts, Sus demonstrates origins and insertions similar to those in the pygmy hippo (Kajava, 1923; Campbell, 1935, 1936). However, Nickel et al. (1986) describes the adductors as arising from the third and fourth metacarpals, as in Kajava's (1923) common hippo. These muscles are absent in Camelus and most ruminants; however, mm. adductores digiti II et IV are present in Tragulus. Among the perissodactyls, the tapir has three mm. adductores, to digits II, IV, and V.

Pygmy and common hippos have eight mm. interossei (two per digit). Campbell (1935, 1936) describes four mm. interossei in Sus, including one to each toe (radial side of digits II and III; ulnar side of digits IV and V); these represent the digit II–V abductores interossei. Kajava (1923) provides a similar account for Sus, although he also describes a digit II adductor interosseus. Getty (1975) and Nickel et al. (1986) describe two mm. interossei in Sus, for digits III and IV. However, according to these authors, the second and fifth digits each have a flexor, adductor, and abductor. Most likely, the adductors to digits II and V represent mm. adductores digiti II et V, rather than mm. interossei. In addition, as the flexor of the second digit arises from the deep flexor tendon, this represents m. lumbricalis II (sensu Kneepkens et al., 1989). In addition, the flexor of the fifth digit described by these authors represents a second muscle belly of m. abductor interosseus digiti V, as described by Campbell (1935, 1936). In light of these considerations, the abductors to digits II and V would represent true mm. interossei. According to these calculations, Sus lacks an adductor interosseus for the second (variable), third, fourth, and fifth digits. Whatever the precise homologies, Sus has a reduced number of intrinsic muscles compared with the hippo manus.

In Potamochoerus, the mm. adductores interossei are entirely tendinous, as is m. abductor interosseus digiti IV. Compared with Sus and Potamochoerus, Babyrousa demonstrates only a slight reduction, as it lacks m. adductor interosseus digiti II. In Pecari, m. adductor interosseus digiti II is absent; mm. adductores interossei digiti III et V are entirely tendinous, and mm. abductor and adductor interosseus digiti IV are reduced. The intrinsic musculature is further reduced in ruminants; there is only a single middle interosseous muscle. This muscle divides into five tendons of insertion, inserting on the sesamoid bones of digits III and IV as well as uniting with the tendons of the superficial flexor, contributing to the cuff around the deep flexor tendon. An exception to this rule, once again, are the tragulids, which have four interossei muscles, corresponding to each digit. In camels, a single, entirely tendinous interosseous element is present, arising from the distal carpus and proximal metacarpus, and inserting onto the proximal sesamoid bones. Thus, compared with other artiodactyls, hippos have more extensively developed intrinsic muscles of the manus, including a full complement of mm. interossei (two per digit).

Although hippos are semiaquatic, the musculature does not show extreme modifications as they have maintained typical terrestrial patterns of locomotion; hippos walk underwater rather than use lateral or dorsoventral movements of the trunk to swim. Nonetheless, hippos do display some unique characteristics related to their lifestyle. Because of their large size and the increased resistance of movement against water, the musculature shows several adaptations for increased power, including increased muscle size and fusions and reductions in number of muscle bellies. Especially noteworthy are the modifications of the pectoral muscles to propel the trunk forward and the arrangement of the long flexor tendons to serve each of the four weight-bearing digits, providing increased control of splay on soft ground. In addition, many of the intrinsic muscles of the manus are retained in hippos, including m. lumbricalis IV, mm. adductores digiti II et V, and a full complement of interossei, once again indicating that control of the digits is functionally important in these animals.

This study also indicates that, although the forelimb musculature of hippos shares some similarities with suids, hippos more closely resemble ruminants, especially tragulids. This finding supports the molecular data (e.g., Shimamura et al., 1997; Ursing and Arnason, 1998; Nikaido et al., 1999) (Fig. 9). Moreover, pygmy and common hippos are unique among artiodactyls in retaining several primitive features in the forelimb (e.g., mm. palmaris longus and flexor digitorum brevis). These findings are consistent with the hypothesis that hippos diverged from other Artiodactyla early in the history of this group. Additional studies of hindlimb, facial, and trunk muscles may help determine whether this unique family of artiodactyls was indeed closely allied to the Cetacea (see Cooper et al., 2007, this issue).

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Figure 9. Cladogram for the Artiodactyla. This cladogram is supported by numerous molecular analyses, and is consistent with the findings in the current study (Nikaido et al., 1999).

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Acknowledgements

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

We thank Charley Potter, John Ososky, Linda Gordon, James Mead, and Richard Thorington (National Museum of Natural History, Smithsonian Institution) for their generous support of this project. In addition, we also thank Charley Potter and John Ososky for facilitating the logistical aspects of this project at the Smithsonian's Osteopreparatory Laboratory in Suitland, Maryland. We acknowledge Glenn Feldhake (IUCN Hippo Specialists Subgroup) for the information he provided on the behavior of the pygmy hippos formerly under his care. In addition, we thank the reviewers for their comments on the manuscript. R.E.F. thanks Ken Rose, Dave Weishampel, and Mark Teaford (Johns Hopkins University School of Medicine) for supporting this project during the tenure of her postdoctoral fellowship, and Andrew Hill (Yale University) for fostering an interest in hippos during her graduate career. R.E.F., K.M.S., and V.L.N. are research associates, with the Division of Mammals, National Museum of Natural History, Smithsonian Institution.

LITERATURE CITED

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED
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