Hind limb myology of the common hippopotamus, Hippopotamus amphibius (Artiodactyla: Hippopotamidae)
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1 Zoological Journal of the Linnean Society, 2010, 158, With 9 figures Hind limb myology of the common hippopotamus, Hippopotamus amphibius (Artiodactyla: Hippopotamidae) REBECCA E. FISHER 1,2 *, KATHLEEN M. SCOTT 3 and BRENT ADRIAN 1 1 Department of Basic Medical Sciences, University of Arizona, College of Medicine-Phoenix in Partnership with Arizona State University, Phoenix, AZ 85004, USA 2 School of Life Sciences, Arizona State University, Tempe, AZ 85287, USA 3 Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, NJ 08854, USA Received 20 September 2008; accepted for publication 18 December 2008 Based on morphological traits, hippos have traditionally been classified with pigs and peccaries in the suborder Suiformes. However, molecular data indicate that hippos and cetaceans are sister taxa. This study analyses muscle characters of the common hippo hind limb in order to clarify the phylogenetic relationships and functional anatomy of hippos. Several muscles responsible for propelling the body through water are robust and display extensive fusions, including mm. semimembranosus, semitendinosus, biceps femoris and gluteus superficialis. In addition, common hippos retain long flexor and extensor tendons for each digit, reflecting the fact that all four toes are weight-bearing. These flexor tendons, together with the well-developed intrinsic muscles of the pes, serve to adduct the digits, preventing splaying of the toes when walking on soft terrain. Lastly, common hippos retain a number of primitive features, including the presence of m. articularis coxae, a well-developed m. obturator internus, superficialis and profundus tendons to all digits, mm. flexor digitorum brevis, abductor digiti V, lumbricalis IV, adductores digitorum II and V, and two mm. interossei per digit. Pygmy hippos share these features. Thus, hippopotamids retain muscles that have been lost in the majority of artiodactyls, including other suiforms. These and previously reported findings for the forelimb support the molecular data in indicating an early divergence of the Hippopotamidae from the rest of the Artiodactyla.. doi: /j x ADDITIONAL KEYWORDS: artiodactyl functional anatomy limb musculature phylogeny pygmy hippopotamus. INTRODUCTION The common hippopotamus (Hippopotamus amphibius Linnaeus, 1758) is unique among the living artiodactyls, in terms of both its ecology and taxonomic position. The common hippo is distinguished from other living ungulates by its combination of large body size and aquatic habits; its aquatic habits are shared by the much smaller pygmy hippopotamus (Choeropsis liberiensis Leidy, 1853). Traditionally, hippos have been classified as Suiformes, together *Corresponding author. rfisher@ .arizona.edu with pigs and peccaries (Simpson, 1945) based on morphological similarities. However, the taxonomic position of the family Hippopotamidae has undergone a significant re-evaluation based on molecular analyses (e.g. Irwin & Arnason, 1994; Gatesy et al., 1996; Nikaido, Rooney & Okada, 1999), which indicate that hippos and cetaceans are sister taxa, forming a new clade, the Whippomorpha (Waddell, Okada & Hasegawa, 1999). Molecular studies also support a close relationship between the Whippomorpha and ruminants, further separating hippos from suids and tayassuids (e.g. Shimamura et al., 1997; Ursing & Arnason, 1998; Nikaido et al., 1999). These studies 661
2 662 R. E. FISHER ET AL. point to the need for a re-evaluation of the morphology of the hippos in the light of both their taxonomic position and unique habits. The musculoskeletal anatomy of the common hippopotamus was documented in several early monographs (Cuvier, 1850; Gratiolet, 1867; Humphry, 1872); however, these were based on dissections of fetal and newborn specimens. Windle & Parsons (1901, 1903) included these results in their classic studies of ungulate morphology, providing comparisons with a number of taxa. Subsequent studies have been more limited in scope; these include Maurer (1911) on the m. serratus posterior, Kajava (1923) on the flexor muscles of the forearm and manus, and Macdonald et al. (1985) on some comparative aspects of the fore and hind limb muscles of various suiforms. In addition, Jouffroy s (1971) review of appendicular myology included notes on the common hippo. Several studies provide comparative data for the pygmy hippo, including Milne Edwards (1868) on the osteology and Macalister (1873) on the myology; Campbell (1935, 1936, 1945) provides more detailed myology. Most recently, Macdonald et al. (1985) included the pygmy hippo in their comparative study of suiforms, and Fisher, Scott & Naples (2007) provided a detailed myology of the forelimb. Many studies have considered the myology of the Artiodactyla and, more broadly, the other ungulates and subungulates. The musculature of the domestic ungulates is described in detail in such sources as Sisson (1975a, b), Nickel et al. (1986) and Getty (1975). Comparative studies describing a range of artiodactyl and perissodactyl species include Windle & Parsons (1901, 1903), Jouffroy (1971) and Humphry (1872). In addition, Souteyrand-Boulenger (1968) and Smuts & Bezuidenhout (1987) describe the myology of camelids, and Macdonald et al. (1985) provide comparative data on suids. Additional studies on ungulate groups include descriptions of the Rhinocerotidae (Haughton, 1867; Beddard & Treves, 1889) and hyraxes and elephants (Miall & Greenwood, 1878; Fischer, 1986; Weissengruber & Forstenpointner, 2004). This study provides detailed myological descriptions and muscle maps of the common hippo hind limb, and reassesses the morphology of Hippopotamus considering both the relationships among the Artiodactyla suggested by the molecular data and the functional significance of the differences between hippos and other artiodactyls. The descriptions, muscle maps and functional notes reported here will provide comparative data for palaeontologists and anatomists engaged in the study of the living and fossil Hippopotamidae and, more broadly, the Artiodactyla. MATERIAL AND METHODS Dissections were conducted on the left hind limb of a captive-born common hippopotamus (Hippopotamus amphibius) housed at the National Zoological Park in Washington DC. The specimen was a 52-year-old female (accession no ), weighing 1680 kg, that died on October 25, The hind limb was removed at necropsy by reflecting muscles as close to their pelvic origin as possible. The specimen was freshfrozen and stored at the Osteopreparatory Laboratory at the Museum Support Center of the National Museum of Natural History (USNM) in Suitland, Maryland; dissection was also carried out at this facility. Each level of dissection was documented by digital photographs using a Canon PowerShot S3 IS. After each muscle had been described, it was reflected and the origins and insertions were recorded on transparency film overlying photographs of all appropriate views of the hind limb bones. For this purpose, digital photographs were taken of the hind limb skeletons of two female common hippos housed at the National Museum of Natural History (USNM , wild-collected; USNM 25478, captive-born). The femur, tibia and fibula of USNM were photographed in four views (lateral, medial, cranial and caudal), and the articulated pes of USNM was photographed in dorsal and plantar views. The muscle descriptions were supplemented by details from previous studies of common and pygmy hippos cited above. This was particularly the case for muscles that take origin from the pelvis, as the separation of the hind limb from the pelvis at necropsy damaged the origins of these muscles. The terminology adopted in this article conforms to the standards of the Nomina Anatomica Veterinaria (Waibl et al., 2005). As there has been little standardization of the nomenclature used for the hind limb musculature, a list of hind limb muscle synonymies is provided in the Appendix. MUSCLE DESCRIPTIONS, FUNCTIONAL AND PHYLOGENETIC CONSIDERATIONS GLUTEAL AND POSTERIOR THIGH MUSCLES The gluteal region is covered by a very thick layer of fascia. The extent of this gluteal fascia is consistent with that of other ungulates, with attachments on the tuber coxae, iliac crest, sacrum and tuber ischii (Nickel et al., 1986). M. tensor fasciae latae In artiodactyls, the typical origin for m. tensor fasciae latae is from the tuber coxae and iliac crest (Windle & Parsons, 1903); this is also the case for the pygmy hippo (Campbell, 1935). In the pygmy (Campbell,
3 HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS 663 Figure 1. Common hippo hind limb in lateral view. Asterisk (*) indicates the location of the patella deep to the fibres of the tensor fasciae latae. 1935) and common hippo, the muscle also takes origin from the fascia covering m. gluteus medius, and is partially fused with this muscle (Fig. 1). The cranial fibres of m. tensor fascia latae extend distal to the patella, where they insert on the fascia covering the cranial leg (Figs 1, 2). The caudal fibres insert more proximally onto the fascia lata (Fig. 1). The m. tensor fasciae latae flexes the hip joint, and contracts the fascia lata, thus assisting in extension of the stifle (knee) joint. The muscle also abducts the hind limb. Mm. gluteus medius et piriformis The m. gluteus medius originates from the dorsal aspect of the iliac blade, the fascia of the m. erector spinae and the sacrum, as described by Windle & Parsons (1903) for the common hippo and Campbell (1935) for the pygmy hippo. In the common hippo, the caudal fibres of m. gluteus medius are fused with fibres of m. gluteus superficialis, whereas its deep fibres are partially fused with m. gluteus profundus. In addition, m. piriformis is completely fused with the caudal edge of m. gluteus medius. The two muscles are inseparable. There are dense tendons located within the belly of m. gluteus medius, but it cannot be divided into distinct superficial and deep layers. The tendon of m. gluteus medius passes deep to m. vastus lateralis and partially fuses with its tendon of origin (Fig. 1). The tendon of m. gluteus medius inserts extensively on the greater trochanter (Fig. 3A C). At its cranial point of insertion, it is partly merged with the tendon of m. gluteus profundus. The m. gluteus medius is an extensor of the hip joint; when the hind limb is fixed, the muscle propels the trunk forward. In addition, working in concert with the erector spinae muscles, m. gluteus medius would serve to raise the trunk on the fixed hind legs, as in rearing onto the hind limbs. The m. gluteus medius also abducts the hind limb, and its cranial fibres medially rotate while its caudal fibres laterally rotate the femur, albeit weakly. M. gluteus profundus The deep gluteal originates from the dorsal aspect of the iliac blade and body and the ischial neck, as
4 664 R. E. FISHER ET AL. Figure 2. Common hippo hind limb in medial view with the fascia lata removed: dark grey indicates muscles dissected in specimen no , and light grey indicates muscle origins described by Gratiolet (1867) and Windle & Parsons (1903). As a result of necropsy damage, origins were not preserved in specimen no , but this information was available in the existing literature. Asterisk (*) indicates the location of the patella deep to the fibres of the tensor fasciae latae. reported by Gratiolet (1867) and Windle & Parsons (1903) for the common hippo and Campbell (1935) for the pygmy hippo. In the common hippo, the cranial aspect of m. gluteus profundus is fused with m. gluteus medius. The muscle becomes tendinous near its distal quarter, and inserts onto the greater trochanter (Fig. 3A, B). The tendon twists so that the most cranial fibres have the most distal insertion, adjacent to m. vastus lateralis (Figs 1, 3A, B). The m. gluteus profundus medially rotates the femur and abducts the hind limb. M. gluteobiceps Much of the lateral surface of the thigh is covered by the m. gluteobiceps, which is formed by the fusion of mm. gluteus superficialis and biceps femoris (Fig. 1). Their separate contributions to m. gluteobiceps are described below. The m. gluteus superficialis is triangular in shape (Fig. 1). It originates from the gluteal fascia and the fascia covering the mm. erector spinae as reported by Gratiolet (1867) for the common hippo and Campbell (1935) for the pygmy hippo. In the common hippo, m. gluteus superficialis is fused with the caudal fibres of m. gluteus medius and the cranial division of m. biceps femoris. The muscle does not show the partial subdivision seen in the pygmy hippo (Campbell, 1935). A broad, flat tendon forms on its deep surface and continues onto the deep surface of the cranial portion of m. biceps femoris.
5 HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS 665 Figure 3. Muscle maps for the common hippo femur: A, cranial; B, lateral; C, caudal; D, medial.
6 666 R. E. FISHER ET AL. The m. biceps femoris consists of cranial and caudal subdivisions, which are partially fused. There is also extensive fusion between these two divisions and adjacent muscle bellies, with the cranial division of m. biceps femoris fused with m. gluteus superficialis, and the caudal division fused with m. semitendinosus (Fig. 1). The fibres of m. biceps femoris arise from the sacrotuberous ligament and the tuber ischii, as reported by Gratiolet (1867) for the common hippo and Campbell (1935) for the pygmy hippo. The fusion of muscle bellies and tendons of insertion essentially creates a single, broad insertion for mm. gluteus superficialis and biceps femoris, forming a single m. gluteobiceps. In the common hippo, m. gluteobiceps inserts superficially onto the fascia lata, the stifle joint, the crural fascia covering the lateral head of m. gastrocnemius and m. fibularis longus, and the common calcaneal tendon (Fig. 1). In addition, at the stifle joint, the combined tendon of m. gluteus superficialis and the cranial division of m. biceps femoris dives deep to m. vastus lateralis to insert on the lateral aspect of the femoropatellare laterale ligament and thus, indirectly, onto the patella. Finally, the cranial division of m. biceps femoris also inserts via tendinous fibres onto the lateral aspect of the cranial process of the lateral tibial condyle (Fig. 4B, C). The m. gluteobiceps extends the hip joint, abducts the hind limb, and extends the hock (ankle) joint. Its cranial fibres extend the stifle joint while its caudal fibres flex this joint. M. semimembranosus The m. semimembranosus originates from the tuber ischii, between the origins of mm. adductor communis and semitendinosus, as described by Windle & Parsons (1903) for the common hippo and Campbell (1935) for the pygmy hippo. In the common hippo, the bellies of mm. semimembranosus and adductor communis are entirely fused, and form a common insertion onto the superficial surface of the medial head of m. gastrocnemius, the medial collateral ligament, the medial meniscus and, via tendinous fibres, onto the medial tibial condyle and crural fascia (Figs 1, 2, 4C, D). The m. semimembranosus extends the hip joint and flexes the stifle joint, thus propelling the trunk forward. M. semitendinosus The m. semitendinosus arises from the tuber ischii, between the origins of m. semimembranosus and the caudal division of m. biceps femoris, as is typical of most artiodactyls (Windle & Parsons, 1903), and as described by Campbell (1935) for the pygmy hippo. In the common hippo, m. semitendinosus is fused with the caudal division of m. biceps femoris (Fig. 1). The m. semitendinosus inserts via a thin, flat tendon onto the medial aspect of the tibia, just distal to the tibial crest (Fig. 4A, D). In addition, the muscle inserts via a thin fascial layer onto the common calcaneal tendon. The m. semitendinosus extends the hip joint, flexes the stifle joint and extends the hock joint, thus propelling the trunk forward. Comparative, functional and phylogenetic implications Several features of the musculature in this region can be functionally related to the unique locomotor environment of both the common and pygmy hippos. Moving a large body through water would select for musculature that provides powerful propulsion rather than fine-tuned control. In fact, several muscles responsible for retracting the hind limb are not only robust, but display extensive fusions. These include mm. semimembranosus, semitendinosus, biceps femoris and gluteus superficialis (Figs 1, 2). The fusion of the m. gluteus superficialis with adjacent muscles is characteristic of the ungulates, and m. gluteobiceps, in particular, occurs in all of the artiodactyls as well as the tapir (Windle & Parsons, 1903; Campbell, 1935; Dyce, Sack & Wensing, 2002). However, compared to other artiodactyls, pygmy (Campbell, 1935) and common hippos exhibit more extensive fusions, involving not only m. gluteus superficialis, but all of the hamstring muscles as well. Another example of muscle fusion is m. gluteus medius, which is composed of a single robust belly in pygmy (Campbell, 1935) and common hippos (Fig. 1). This is in contrast with suids, camelids and ruminants, where m. gluteus medius is composed of a superficial and deep layer (m. gluteus accessorius), with distinct origins and insertions (Campbell, 1935; Getty, 1975; Sisson, 1975b; Nickel et al., 1986; Smuts & Bezuidenhout, 1987). In this respect, hippos resemble tapirs, rhinos and elephants, which also lack a distinct m. gluteus accessorius, although it is present in Equus (Miall & Greenwood, 1878; Beddard & Treves, 1889; Campbell, 1935; Sisson, 1975a; Nickel et al., 1986). The undivided m. gluteus medius, working in concert with the mm. erector spinae, also plays a crucial role in rearing the trunk onto the hind limbs. Considering the charging behaviour that characterizes hippo social interactions (Karstad & Hudson, 1986), a robust m. gluteus medius would be highly selected for in these species. DEEP MUSCLES OF THE PELVIS M. iliopsoas The damage at necropsy makes it impossible to confirm the origins of this muscle, but Windle &
7 HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS 667 Figure 4. Muscle maps for the common hippo tibia and fibula: A, cranial; B, lateral; C, caudal; D, medial. Parsons (1903) noted that it is very consistent among artiodactyls, with the muscle being composed of m. psoas major (magnus), arising from the transverse processes of the lumbar vertebrae and bodies of the thoracic vertebrae, and m. iliacus, arising from the iliac fossa. In the pygmy hippo, the origin of m. iliopsoas includes the last two ribs, the transverse processes of the lumbar vertebrae and the iliac fossa
8 668 R. E. FISHER ET AL. (Campbell, 1935). In both the common and pygmy hippo, the muscles fuse to form a common tendon of insertion onto the lesser trochanter (Figs 2, 3A, C, D). In the common hippo, the m. iliopsoas also fuses distally with the origin of the lateral belly of m. sartorius. The m. iliopsoas flexes the hip joint and laterally rotates the femur. M. articularis coxae Windle & Parsons (1903) reported that this muscle is absent in most artiodactyls, and it has not been previously described in the common hippo. However, it is clearly present in this specimen as a small cylindrical muscle with a fleshy insertion onto the craniolateral aspect of the proximal femoral shaft (Fig. 3A, B). Although the origin could not be determined due to necropsy damage, in the pygmy hippo this muscle originates from the craniodorsal aspect of the acetabular rim (Campbell, 1935). The m. articularis coxae stabilizes the hip joint when the hind limb is extended. Mm. obturator internus et gemelli The mm. obturator internus et gemelli consist of a single fused muscle mass with both intrapelvic (symphysis pubis, cranial ramus of the pubis, ischial ramus) and extrapelvic (sacrotuberous ligament, ischial body) origins, as described by Campbell (1935) and MacDonald et al. (1985) for the pygmy hippo. In the common hippo, the fused mm. obturator internus et gemelli fuse with the mm. obturator externus et quadratus femoris to insert as a single fleshy mass into the trochanteric fossa (Fig. 3D). The mm. obturator internus et gemelli laterally rotate the femur and extend the hip joint. Mm. obturator externus et quadratus femoris These muscles appear to be fused into a single mass. It is possible that they are more distinct at their origin; however, this cannot be confirmed due to extensive necropsy damage. The mm. obturator externus et quadratus femoris fuse with the mm. obturator internus et gemelli to insert into the trochanteric fossa (Fig. 3D). This complex of muscles laterally rotates the femur, adducts the hind limb and extends the hip joint, especially when the hip is flexed. Comparative, functional and phylogenetic implications Common and pygmy hippos share a number of features of the deep pelvic muscles that set them apart from most artiodactyls. M. articularis coxae, a diminutive muscle spanning the ilium and proximal femur, is present in both pygmy (Campbell, 1935) and common hippos. Although m. articularis coxae has not been described previously in the common hippo, the muscle was present in this specimen. It is possible that this small muscle has been overlooked by some authors; nonetheless, m. articularis coxae appears to be absent in most artiodactyls. Apart from hippos, it is only known to be present in camelids (Camelus and Lama), one bovid (Tragelaphus) and one tragulid (Tragulus) (Windle & Parsons, 1903; Souteyrand-Boulenger, 1968; Smuts & Bezuidenhout, 1987). However, m. articularis coxae is found in all perissodactyls, the majority of carnivores and many primates (Campbell, 1935; Souteyrand-Boulenger, 1968, 1969). Thus, the presence of this muscle in hippos most likely represents a primitive retention. Several authors have considered the function of m. articularis coxae. Souteyrand-Boulenger (1969) found that the muscle is especially well developed in cursorial carnivores (e.g. Panthera onca, P. pardus and Acinonyx jubatus), and is reduced, or absent, in slowmoving carnivores. The small size of the muscle, coupled with range of motion experiments, led Kjaersgaard (1980) to conclude that m. articularis coxae in the horse has only minor relevance in hip flexion and in preventing the protrusion of the hip joint capsule between articular surfaces. However, he did find a high frequency of muscle spindles in the muscle, indicating that it is similar to muscles initiating fine movements with high precision (e.g. m. lumbricalis) or maintaining posture (e.g. m. soleus). He concluded that the muscle functions as a receptor organ, reporting on the torsion of the hip joint (Kjaersgaard, 1980: 27). It is probable that m. articularis coxae functions similarly in hippos. Both species of hippo possess a well-developed m. obturator internus with intrapelvic origins. This is also true of camelids (Smuts & Bezuidenhout, 1987). In contrast, m. obturator internus is either absent or very much reduced in suids, tayassuids and ruminants (Windle & Parsons, 1903; Campbell, 1935; Getty, 1975; Macdonald et al., 1985; Nickel et al., 1986). If present, the muscle arises from the ischial body only, as m. obturator externus has co-opted the intrapelvic site of origin off the pubis and ischium (Windle & Parsons, 1903) Getty (1975) argues that the intrapelvic part of m. obturator externus represents fibres of m. obturator internus; however, Nickel et al. (1986) note that the intrapelvic part is not homologous to m. obturator internus, as these fibres are innervated by the obturator, not the ischiatic nerve, and pass through the obturator, versus the lesser ischiatic, foramen. Thus, with the exception of the hippos and camelids, artiodactyls have lost a true m. obturator internus. Hippos exhibit the primitive condition, with m. obturator internus originating from the intrapelvic surface of the pubis and ischium,
9 HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS 669 as it does in perissodactyls and elephants (Miall & Greenwood, 1878; Windle & Parsons, 1903; Campbell, 1935; Sisson, 1975a; Nickel et al., 1986). Hyraxes are more derived and resemble the majority of artiodactyls in having a reduced m. obturator internus arising from the ischial body (Windle & Parsons, 1903). ANTERIOR AND MEDIAL THIGH MUSCLES M. quadriceps femoris This complex includes mm. rectus femoris, vastus medialis and vastus lateralis (Figs 1, 2). M. rectus femoris: This muscle has a tendinous origin from the base of the iliac body and the cranial aspect of the acetabular rim, as reported by Gratiolet (1867) for the common hippo and Campbell (1935) for the pygmy hippo. Distally, the belly of m. rectus femoris fuses extensively with m. vastus lateralis and, to a lesser extent, with m. vastus medialis (Figs 1, 2). The m. rectus femoris terminates on the common m. quadriceps tendon, inserting onto the patella (Fig. 2). It flexes the hip joint and extends the stifle joint. M. vastus medialis: The m. vastus medialis arises from the cranial aspect of the femoral neck and the craniomedial aspect of the femoral shaft (Figs 2, 3A D), and is partially fused with mm. vastus lateralis and rectus femoris. However, it is the most separable of the mm. quadriceps bellies. The m. vastus medialis inserts via fleshy fibres onto the common m. quadriceps tendon, which inserts onto the patella (Fig. 2). This muscle extends the stifle joint. M. vastus lateralis: The m. vastus lateralis originates from the dorsolateral aspect of the greater trochanter, the craniolateral and caudolateral aspects of the femoral shaft, and the surface of the combined tendon of mm. gluteus superficialis and biceps femoris (cranial division) (Figs 1, 3A C). Distally, it also takes partial origin from the surface of m. vastus medialis. The origin of m. vastus lateralis on the caudolateral femoral shaft is marked by a ridge, on the opposite side of which is the insertion of m. adductor communis (Fig. 3C). The m. vastus lateralis fuses with m. rectus femoris in the mid-thigh, and its deep aspect is fused with m. vastus medialis. The m. vastus lateralis terminates on the common m. quadriceps tendon, inserting onto the patella with both fleshy and tendinous fibres (Fig. 1). This muscle extends the stifle joint. M. sartorius The m. sartorius originates via two thin, strap-like heads. Gratiolet (1867) and Windle & Parsons (1903) described origins from the ilium and fascia of iliopsoas in the common hippo. Campbell (1935) recorded similar origins for the pygmy hippo, although he also observed an origin from the aponeurosis of m. obliquus externus abdominis. In the common hippo, the two heads fuse in the proximal third of the thigh, and give rise to a strong, flat tendon near the insertion (Fig. 2). The tendons of mm. sartorius and gracilis fuse to insert on the medial tibial condyle (Fig. 4A, D). The m. sartorius flexes the hip joint, adducts the hind limb and weakly extends the stifle joint. M. pectineus The m. pectineus lies cranial and deep to the origin of m. gracilis (Fig. 2). It originates on the intrapelvic surface of the pubis on the ilio-pectineal line, as described by Gratiolet (1867) and Windle & Parsons (1903). However, Humphry (1872) reported that m. pectineus was fused with m. adductor communis in one common hippo. The muscle is distinct in the pygmy hippo, taking origin from the cranial end of the pubic symphysis (Macalister, 1873; Campbell, 1935). In the common hippo, the muscle is robust proximally, but gradually flattens to form tendinous fibres on its cranial and caudal aspects. The m. pectineus inserts on the caudal aspect of the femoral shaft (Fig 3C, D), where it shares some tendinous fibres with m. adductor communis. The m. pectineus flexes the hip joint, medially rotates the femur and adducts the hind limb. M. gracilis The m. gracilis is a thin, poorly developed muscle, similar in appearance to m. sartorius (Fig. 2). The proximal end is extensive, consistent with an aponeurotic origin along the pubic symphysis superficial to m. adductor communis, as is typical for artiodactyls (Windle & Parsons, 1903), and as described by Campbell (1935) for the pygmy hippo. In the common hippo, the proximal end of m. gracilis is extensively fused with mm. semimembranosus and semitendinosus. Distally, it also fuses with m. sartorius to form a common tendon of insertion onto the craniomedial aspect of the medial tibial condyle (Figs 2, 4A, D). Further distally, gracilis inserts via a thin fascial layer onto the crural fascia on the medial aspect of the leg; this insertion extends to the level of the common calcaneal tendon and forms part of its sheath. The m. gracilis adducts the hind limb, flexes the stifle joint and extends the hock joint. M. adductor communis The common adductor mass is clearly separable proximally into two portions, but these subdivisions fuse in the distal third of the thigh (Figs 1, 2). This is contrary to Windle & Parsons (1903) observation that there are no subdivisions in the common hippo. The
10 670 R. E. FISHER ET AL. typical artiodactyl origin is off the caudal aspect of the pubic symphysis continuing onto the ischium (Windle & Parsons, 1903); a similar origin has been documented in the pygmy hippo (Campbell, 1935). M. adductor communis inserts on the caudal femoral shaft, the medial aspect of the stifle joint, the superficial surface of the medial head of m. gastrocnemius, the medial collateral ligament and the patella (Fig. 3B, D). The caudal half of the m. adductor communis is fused extensively with m. semimembranosus (Figs 1, 2). Together, they insert on the superficial surface of the medial head of m. gastrocnemius, the medial collateral ligament, the medial meniscus and, via tendinous fibres, onto the medial tibial condyle and the crural fascia (Fig. 4C, D). The m. adductor communis primarily adducts the hind limb, but also extends the hip joint. Through its fusion with m. semimembranosus, it also assists in flexion of the stifle joint. M. adductor longus A distinct m. adductor longus was not found in this specimen. Windle & Parsons (1903) also noted its absence in the common hippo; however, Humphry (1872) claimed it was present in his specimen. Thus, it appears that common hippos exhibit intraspecific variation in this regard. In contrast, in the pygmy hippo, m. adductor longus is a clearly defined, robust, fusiform muscle with an extensive origin from the caudal aspect of the transverse pelvic ligament, the rectus sheath at the midline and a depression on the ventral aspect of the cranial pubic ramus, extending to the acetabular rim (R. Fisher, K. M. Scott, V. L. Naples, unpubl. data). M. adductor longus lies cranial to the transverse pelvic ridge, whereas m. obturator externus lies caudal to it, clearly separable, with the obturator nerve coursing between the two muscles, and innervating both. Although some fibres merge with the tendon of m. obturator externus, most of its fibres form a separate, rounded tendon that inserts onto the base of the trochanteric fossa, distal to the insertion of m. obturator externus. Comparative, functional and phylogenetic implications The quadriceps complex in ungulates generally provides little in the way of phylogenetic or functional interest; there is some variation in the degree to which the heads of the vasti are separable, but in all artiodactyls, this complex arises from cranial, medial and lateral aspects of the femur. In both common and pygmy (Campbell, 1935) hippos, the vasti follow this pattern, with extensive fusions and lacking a separable intermediate head. The adductor complex in ungulates generally is much less differentiated than in other mammals; most typically, m. gracilis, m. pectineus and a fused common adductor mass are readily identifiable (Windle & Parsons, 1903). The most significant distinction among the ungulates is the presence or absence of m. adductor longus. The presence of a distinct m. adductor longus in the Hippopotamidae, even if only variably present in common hippos, is an important distinction from most other artiodactyls. Among the artiodactyls, m. adductor longus has been documented only in Tragelaphus and Giraffa (Windle & Parsons, 1903). In contrast, m. adductor longus is distinct in perissodactyls, hyraxes and elephants (Haughton, 1867; Miall & Greenwood, 1878; Beddard & Treves, 1889; Windle & Parsons, 1903). Thus, hippos and some ruminants seem to have retained the primitive condition. MUSCLES OF THE LEG Fasciae and retinaculae The strikingly robust crural fascia inserts along the tibial crest, forming a ridge located medial to that marking the origin of m. tibialis cranialis. There is a common extensor retinaculum for the tendons of mm. tibialis cranialis, extensor digiti I longus, fibularis tertius and extensor digitorum longus. In addition, a strong lateral retinaculum forms a single tunnel for the tendons of mm. fibularis longus and extensor digitorum lateralis. Distal to this retinaculum, a smaller retinaculum secures the tendon of the m. extensor digitorum lateralis. One flexor retinaculum surrounds the combined tendon of mm. flexor digitorum lateralis and tibialis caudalis, while another encloses the tendon of m. flexor digitorum medialis. M. tibialis cranialis The m. tibialis cranialis has a broad site of origin off the patellar ligament, the tibial crest and the depression adjacent to the tibial crest (Figs 4A, B, D, 5). The belly of m. tibialis cranialis is robust, and terminates in a stout tendon. The tendon inserts on the plantarmedial aspect of the base of the second metatarsal, the plantar aspect of the os tarsale I (os cuneiforme mediale) and the sesamoid associated with this tarsal bone (Fig. 6B). This muscle is similar in the pygmy hippo (Campbell, 1935). The m. tibialis cranialis flexes the hock joint and inverts the pes. M. extensor digiti I longus This slender muscle lies deep to mm. fibularis longus and fibularis tertius (Fig. 5). The m. extensor digiti I longus arises from the interosseous membrane and the craniomedial aspect of the proximal two-thirds of the fibular shaft (Figs 4A, B, 5). The cranial tibial
11 HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS 671 tendons of mm. tibialis cranialis and fibularis tertius (Fig. 5). It passes medial to the m. extensor digitorum longus tendon to digit II, to insert on the dorsomedial aspect of the shaft and head of the distal phalanx of digit II (Fig. 6A). This muscle is also described by Campbell (1935) in the pygmy hippo; its origin and insertion are identical to those in the common hippo. The m. extensor digiti I longus weakly flexes the hock joint and extends the metatarsophalangeal and interphalangeal joints of digiti II. M. fibularis tertius The m. fibularis tertius is a robust, fusiform muscle that lies superficial to, surrounds and is fused with the belly of m. extensor digitorum longus (Fig. 5). The mm. fibularis tertius and extensor digitorum longus take origin from a single stout, round tendon. This tendon arises from a depression located adjacent to the lateral rim of the patellar groove of the femur (Fig 3B, C). The tendon occupies a distinct groove between the tibial crest medially and the cranial process of the lateral tibial condyle laterally. This tibial groove is characterized by a smooth surface, similar to that seen in the bicipital groove of the humerus, and is associated with a synovial bursa surrounding the tendon (Fisher et al., 2007). Distally, m. fibularis tertius gives rise to a tendon that inserts on the medial aspect of the os tarsale I (os cuneiforme mediale) and the dorsomedial aspect of the base of the second metatarsal (Fig. 6A). Campbell (1935) described an identical muscle in the pygmy hippo, although he identified this as the extensor hallucis longus, and considered there to be a true fibularis tertius only in the tapir among the species he dissected. The m. fibularis tertius flexes the hock joint. It may also invert the pes. Figure 5. Common hippo leg in cranial view. vessels and deep fibular nerve lie directly medial to m. extensor digiti I longus and run parallel to its muscle belly and tendon. The thin tendon of m. extensor digiti I longus emerges at the ankle, between the M. extensor digitorum longus The m. extensor digitorum longus originates via a common tendon with m. fibularis tertius, as described above (Fig 3B, C). The muscle lies deep to m. fibularis tertius, and is surrounded by, and fused with, that muscle (Fig. 5). The m. extensor digitorum longus gives rise to a robust tendon that trifurcates just distal to the origin of m. extensor digitorum brevis, forming three main m. extensor digitorum longus tendons, each of which bifurcates, thus forming six secondary tendons (Fig. 5). One secondary tendon serves digit V, two each serve digit IV and digit III, and one serves digit II. At the level of the proximal interphalangeal joint, the secondary tendons form the extensor expansions of the digits, which insert on the distal phalanges (Figs 5, 6A). This muscle is similar in the pygmy hippo (Campbell, 1935). The m. extensor digitorum longus flexes the hock joint and extends the metatarsophalangeal and interphalangeal joints of
12 672 R. E. FISHER ET AL. Figure 6. Muscle maps for the common hippo pes: A, dorsal; B, plantar. digits II to V. Owing to the fact that the tendons travel medial or lateral to the metatarsophalangeal joints, they can also serve as abductors or adductors of the digits. M. fibularis longus The m. fibularis longus lies superficial to the smaller m. extensor digitorum lateralis (Fig. 5), and the two muscles are separated by the superficial fibular nerve. It originates from the cranial aspect of the proximal tibial shaft, the lateral tibial condyle and the fibular head (Fig. 4A-C). As its tendon crosses the ankle, it courses lateral to the lateral malleolus, and not caudal to it (Fig. 5). The tendon then passes between the base of the fifth metatarsal and os tarsale IV (os cuboideum), courses through a tunnel between the os tarsale IV and the plantar processes of the third and fourth metatarsals, and, finally, inserts on the proximal surface of these plantar processes, as well as on the base of the third metatarsal (Fig. 6B). In this specimen, the tendon gave rise to a small accessory tendon that inserted onto the retinaculum for the tendon of the m. extensor digitorum lateralis. This muscle is similar in the pygmy hippo, except that, according to Campbell (1935), it inserts on the first and second metatarsals. The m. fibularis longus flexes the hock joint and everts the pes. M. extensor digitorum lateralis The m. extensor digitorum lateralis lies deep and caudal to m. fibularis longus (Fig. 5). The muscle is fused with the fascial septum, separating the lateral and caudal compartments of the leg. In addition, it is fused at its origin with m. flexor digitorum lateralis. The m. extensor digitorum lateralis originates from the lateral collateral ligament, the fibular head and the proximal two-thirds of the fibular shaft (Fig. 4A- C). Its origin from the fibular shaft is marked by a long groove. The belly gives rise to two adherent but separate tendons. The tendons travel through a retinacular tunnel in close apposition and diverge in the pes. One tendon passes along the dorsolateral aspect of digit V to insert on the distal phalanx (Figs 5, 6A). The other tendon fuses with the belly of m. extensor
13 HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS 673 Figure 7. Common hippo leg in caudal view: A, superficial; B, deep. digitorum brevis proximally, passes deep to the tendon of m. extensor digitorum longus to digit V, and joins the longus tendon to digit IV at the head of the fourth metatarsal. This combined tendon fans out to insert on the dorsolateral aspect of the distal phalanx of digit IV (Figs 5, 6A). The m. extensor digitorum lateralis is similarly arranged in the pygmy hippo (Campbell, 1935). This muscle flexes the hock joint and extends the metatarsophalangeal and interphalangeal joints of digits IV and V. M. gastrocnemius Common hippos do not possess an m. triceps surae, as the m. soleus is absent. The m. soleus is also absent in the pygmy hippo (Campbell, 1935). In the common hippo, the m. gastrocnemius is composed of two bellies, an exceptionally robust medial and a much more slender lateral belly, which fuse in the proximal third of the leg (Figs 1, 2, 7A, B). The medial head originates from the medial supracondylar ridge and the popliteal fossa (Fig. 3B D). The smaller lateral head lies superficial to m. flexor digitorum superficialis and originates from the lateral supracondylar ridge, the popliteal fossa, the surface of the m. flexor digitorum superficialis tendon of origin and the femoral shaft (Fig. 3B, C). The heads do not contain sesamoid bones and, according to Windle & Parsons (1903), fabellae are absent in all of the ungulates. The lateral and medial heads converge to form a tendon in the distal third of the leg (Fig. 7A). Shortly thereafter, tendinous fibres from mm. gluteobiceps, semitendinosus and gracilis join this tendon to form the common calcaneal tendon. The common calcaneal tendon is robust on its lateral aspect, but is thin and diffuse
14 674 R. E. FISHER ET AL. medially. It encloses the tendon of m. flexor digitorum superficialis, forming a sheath around it and creating a tunnel for its passage into the pes. The common calcaneal tendon is partially fused with the tendon of m. flexor digitorum superficialis at the midline, but most of its fibres divide to insert onto the calcaneal tuberosity on its proximal, medial and lateral aspects (Fig. 6B). The muscle is similar in the pygmy hippo, although the lateral head appears to have a more extensive origin; the insertion is similar (Campbell, 1935). The m. gastrocnemius flexes the stifle joint and extends the hock joint. Mm. flexor digitorum superficialis et flexor digitorum brevis The m. flexor digitorum superficialis originates from the supracondylar fossa via a very robust tendon, which, in its proximal quarter, is fused with the deep aspect of the lateral head of m. gastrocnemius (Figs 3B, C, 7A, B). The muscle lacks a distinct belly, but the tendon of origin becomes fleshy at the level of the femoral condyles and steadily increases in bulk, and there are muscle fibres within the tendon in the distal third of the leg. The m. flexor digitorum superficialis tendon is enclosed in a sheath that is formed by the common calcaneal tendon in the distal part of the leg (see above). The stout tendon passes along a deep groove on the plantar surface of the calcaneus. As it enters the pes, muscle fibres are present on the tendon (Fig. 7A). The largest bundle of fibres is located on the lateral side of the common tendon plate and continues onto the tendon of digit V, with a few fibres on the tendon of digit IV; these fibres are located on the plantar, lateral and dorsal aspects. Additional fibres are present on the dorsal and plantar aspects of the medial border of the common tendon plate, continuing onto the dorsal midline of the common tendon plate. We concur with Windle & Parsons (1903) and Campbell (1935) in identifying these scattered muscle fibres as remnants of the m. flexor digitorum brevis in hippos. The m. flexor digitorum brevis is the only muscle in mammals that is associated with the superficial aspect of the common tendon plate distal to the calcaneus, and which contributes to the digital tendons (Lewis, 1989). The m. flexor digitorum superficialis has a similar origin and course in the pygmy hippo, and also includes these remnant muscle fibres (Campbell, 1935). Within the pes, the tendon of m. flexor digitorum superficialis gives rise to four tendons, one to each digit (Fig. 7A). The tendons to digits III and IV are equal in size and larger than their lateral counterparts to digits II and V. These tendons form impressive tunnels, known as the manica flexorum, for the passage of the m. flexor digitorum profundus tendons. Each manica flexoria lies within a deep tunnel formed by a pair of sesamoid bones at the metatarsophalangeal joints. The tendon to digit II forms a manica flexoria at the metatarsophalangeal joint, courses to the lateral side of the digit, and inserts on the plantar-lateral aspect of the base of the middle phalanx (Fig. 6B). Similarly, the tendon to digit V forms a manica flexoria, courses to the medial side of digit V, and inserts on the plantar-medial aspect of the base of the middle phalanx (Fig. 6B). The superficialis tendons to digits III and IV give rise to a manica flexoria and divide just distal to the start of the tunnel, at the level of the metatarsophalangeal joints. The resulting slips insert onto the plantar-medial and plantar-lateral processes on the bases of the middle phalanges (Fig. 6B). The superficialis tendons send fibres to fuse with the metatarsophalangeal and proximal interphalangeal joint capsules in all four digits. Although the insertions and relationship to the tendons of m. flexor digitorum profundus are similar in the pygmy hippo, Campbell (1935) noted that the tendon to digit II is markedly smaller. The m. flexor digitorum superficialis extends the hock joint and flexes the metatarsophalangeal and proximal interphalangeal joints of digits II to IV. In addition, the superficialis tendons to digits II and V are strong digital adductors. M. popliteus The m. popliteus originates via a stout tendon from a depression on the lateral femoral condyle, and via fleshy fibres from the lateral meniscus and the articular capsule (Figs 3B, 7B). The muscle passes deep to the lateral collateral ligament to enter the leg. The belly of m. popliteus is fused extensively with m. flexor digitorum medialis and is incompletely subdivided into a superficial and a deep layer. The m. popliteus inserts on the medial tibial condyle and along a ridge on the caudal aspect of the tibial shaft, and continues onto the fascia of the leg almost to the hock joint (Figs 4C, D, 7B). At its most distal insertion, the fibres of m. popliteus fuse with the retinaculum for the tendon of m. flexor digitorum medialis. This muscle has a similar origin and insertion in the pygmy hippo (Campbell, 1935). The m. popliteus flexes the stifle joint. Mm. flexores digitorum profundi This complex includes: mm. tibialis caudalis, flexor digitorum lateralis and flexor digitorum medialis (Fig. 7A, B). M. tibialis caudalis: The m. tibialis caudalis arises from the caudal aspect of the lateral tibial condyle (Fig. 4C). It is fused in its proximal half with m. flexor digitorum lateralis, which lies deep to it (Fig. 7A, B).
15 HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS 675 Just proximal to the hock joint, the muscle belly gives rise to a tendon that fuses with the tendon of m. flexor digitorum lateralis. M. flexor digitorum lateralis: This muscle arises from the lateral intermuscular septum and the caudal aspect of the fibular head and shaft, interosseous membrane, lateral tibial condyle and tibial shaft (Fig. 4B, C). It is fused along its medial border with m. flexor digitorum medialis (Fig 7A, B). The m. flexor digitorum lateralis becomes tendinous at the level of the hock joint, where it immediately joins the tendon of m. tibialis caudalis. This combined tendon courses in the midline of the hock joint, travels into the pes within its own retinaculum, lateral to the tendon of m. flexor digitorum medialis, and courses along the plantar aspect of the sustentaculum tali (Fig. 7B). M. flexor digitorum medialis: The m. flexor digitorum medialis takes origin from the caudal aspect of the tibial shaft (Fig. 4C, D). It is fused along its lateral border with m. flexor digitorum lateralis. It gives rise to a tendon just proximal to the hock joint. This tendon travels in its own retinaculum, medial to the hock joint and well separated from the combined tendon of mm. tibialis caudalis and flexor digitorum lateralis (Fig. 7B). The tendon of m. flexor digitorum medialis travels through its own osseofibrous tunnel and joins the other long flexor tendons at the level of the midshafts of the metatarsals. This common tendon plate then forms four tendons, one to each digit (Fig. 7B). Each tendon travels through a manica flexoria, formed by the m. flexor digitorum superficialis tendon, to insert on the plantar aspects of the distal phalanges (Figs 6B, 7A). There is a midline furrow on each of the deep flexor tendons, but they do not bifurcate. The flexor tendons are held in place by plantar annular ligaments at the metatarsophalangeal joints and proximal digital annular ligaments at the proximal interphalangeal joints. The mm. flexores digitorum profundi are similar in origin and extent in the pygmy hippo (Campbell, 1935), although Campbell considered m. tibialis caudalis to be an accessory head of m. flexor digitorum lateralis. The mm. flexores digitorum profundi extend the hock joint and flex the metatarsophalangeal and interphalangeal joints of digits II to V. Comparative, functional and phylogenetic implications The arrangement of the long flexor tendons distinguishes hippos from other artiodactyls. The mm. flexor digitorum superficialis and flexores digitorum profundi provide tendons to all four digits in hippopotamids (Figs 6B, 7A, B). A similar arrangement was observed in the hippo manus (Fisher et al., 2007). In suids and tayassuids, m. flexor digitorum superficialis serves digits III and IV, with only fascial connections to digits II and V, whereas m. flexores digitorum profundi sends robust tendons to digits III and IV, and weak tendons to digits II and V (Windle & Parsons, 1903; Campbell, 1935; Nickel et al., 1986). In ruminants and camelids, superficialis and profundus tendons typically serve digits III and IV only (Windle & Parsons, 1903; Getty, 1975; Nickel et al., 1986; Smuts & Bezuidenhout, 1987). However, the long flexors do serve all four digits in Hyemoschus, as in the hippo (Windle & Parsons, 1903). The extensor tendons show a similar pattern in the common and pygmy hippos, although the tendons to the lateral digits are not as well developed as are the flexors. In suids and tayassuids, these tendons also serve all four digits, whereas, in the other artiodactyls, they mirror the flexors in serving only digits III and IV. Thus, most artiodactyls exhibit a reduction in the long flexor and extensor tendons to the lateral digits, a feature tied to the fact that the lateral digits are no longer weight-bearing in these species (Fig. 8). In contrast, hippos and tragulids have strong superficial and deep flexor tendons. A pair of long flexor tendons serves all existing digits in perissodactyls (Haughton, 1867; Beddard & Treves, 1889; Windle & Parsons, 1903; Campbell, 1935; Sisson, 1975a; Nickel et al., 1986), demonstrating that hippos and, in this case, tragulids preserve the primitive condition. Retention of strong flexor and extensor tendons to the lateral digits in hippos is probably also functionally related to the control of digital splay on the soft substrates of their aquatic habitats. The more robust flexor tendons suggest that hippos are actively controlling splay through the use of the flexor muscles, and that active extension is a less critical function. INTRINSIC MUSCLES OF THE PES M. extensor digitorum brevis The m. extensor digitorum brevis originates from the dorsal aspect of the talus via a broad tendon (Figs 5, 6A). The deep fibular nerve and cranial tibial vessels lie just medial to m. extensor digitorum brevis, and dive deep to the muscle near its tendon of origin. The m. extensor digitorum brevis does not form a tendon of insertion. Instead, the belly inserts onto the metatarsophalangeal joint capsules of digits II, III and IV, terminating as broad aponeurotic extensions onto the dorsum of the proximal phalanges of these digits (Fig. 5). In addition, the belly of m. extensor digitorum brevis is fused with the medial and middle tendons of m. extensor digitorum longus. This muscle is also present in the pygmy hippo, although it is partially divided into superficial and deep bellies, and inserts on all four digits (Campbell, 1935). The m.
16 676 R. E. FISHER ET AL. Figure 8. Lateral view of hind foot skeleton in the ox, common hippo and pig. The hippo has four weight-bearing digits, whereas pigs and ruminants have reduced lateral digits. extensor digitorum brevis extends the metatarsophalangeal and interphalangeal joints of digits II to IV and, acting via its connection to the m. extensor digitorum longus tendons, extends digits II, III and IV. M. lumbricalis IV The m. lumbricalis IV originates from the common tendon of mm. flexores digitorum profundi, just proximal to its branches to digits III and IV (Fig. 7A, B). It then inserts via a fan-like extension of its tendon onto the plantar-medial aspect of the midshaft of the proximal phalanx of digit IV (Fig. 6B). This insertion may be variable, as Gratiolet (1867) reported that it inserted on digit III, although both Humphry (1872) and Macdonald et al. (1985) support the findings of this study. It appears to be constant in serving digit IV in the pygmy hippo (Macalister, 1873; Campbell, 1935; Macdonald et al., 1985). The pedal lumbrical flexes and adducts the metatarsophalangeal joint of digit IV. M. abductor digiti V The m. abductor digiti V arises from the plantar aspect of the calcaneus, on the transverse ridge just distal to the groove for m. flexor digitorum superficialis (Fig. 6B). The robust belly gives rise to a stout tendon that joins the tendon of m. abductor interosseous digiti V (Fig. 9). This combined tendon inserts onto the lateral sesamoid at the metatarsophalangeal joint and the lateral aspect of the base of the proximal phalanx (Fig. 6B). This muscle is also present in the pygmy hippo (Campbell, 1935). The m. abductor digiti V abducts digit V. M. adductor digiti V The m. adductor digiti V lies superficial to the mm. abductor and adductor interossei digiti IV (Fig. 9). It originates from the plantar aspect of the distal os tarsale IV (Fig. 6B) and inserts on the medial side of the base of the proximal phalanx (Fig. 6B). This muscle is similar in the pygmy hippo (Campbell, 1935). It adducts digit V and weakly flexes its metatarsophalangeal joint. M. adductor digiti II The m. adductor digiti II lies superficial to the mm. abductor interosseus digiti III and adductor interosseus digiti II (Fig. 9). The muscle takes origin from the surface of m. abductor interosseus digiti III and from the plantar aspects of os tarsale III and IV (Fig. 6B). The m. adductor digiti II inserts onto the lateral aspect of the base of the proximal phalanx of digit II (Fig. 6B). This muscle is also present in the pygmy hippo (Campbell, 1935). It adducts digiti II and weakly flexes its metatarsophalangeal joint. Mm. interossei (Fig. 9) The m. abductor interosseus digiti II originates from the plantar surface of the base of the second metatarsal and the tendon of m. tibialis cranialis (Fig. 6B). The muscle is composed of multiple small bellies that
17 HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS 677 Figure 9. Common hippo pes in plantar view. converge to form a single tendon. The tendon inserts equally onto the medial sesamoid and the medial aspect of the base of the proximal phalanx of digit II. The muscle abducts digit II and flexes its metatarsophalangeal joint. The m. adductor interosseus digiti II consists of an extremely small bundle of muscle fibres that takes origin from the medial aspect of the plantar process of the third metatarsal (Fig. 6B). It inserts primarily onto the lateral sesamoid and also slightly onto the lateral aspect of the base of the proximal phalanx of digit II. The muscle adducts digit II and flexes its metatarsophalangeal joint. The m. abductor interosseus digiti III originates from the base of the plantar process on the third metatarsal, and slightly off the fibrocartilage lying between the adjacent plantar processes (Fig. 6B). The muscle inserts on the medial sesamoid, the medial aspect of the base of the proximal phalanx and the extensor expansion of digit III, formed by the tendon of m. extensor digitorum longus. The muscle abducts digit III, flexes its metatarsophalangeal joint, and helps extend its interphalangeal joints. The m. adductor interosseus digiti III originates from the plantar aspect of the bases of the third and fourth metatarsals, in the depression between the plantar processes of these metatarsals, and from the fibrocartilage lying between the adjacent plantar processes (Fig. 6B). At its origin, the muscle is fused with mm. abductor interosseus digiti III and adductor interosseus digiti IV. It inserts on the lateral sesamoid, the lateral side of the base of the proximal phalanx and the extensor expansion of digit III. The muscle adducts digit III, flexes its metatarsophalangeal joint and helps extend its interphalangeal joints. The m. adductor interosseus digiti IV originates from the base of the plantar process of the fourth metatarsal, and slightly from the fibrocartilage between the plantar processes of digits IV and III (Fig. 6B). The belly is fused at its origin with mm. abductor interosseus digiti IV and adductor interosseus digiti III. It inserts on the medial sesamoid, the medial aspect of the base of the proximal phalanx and the extensor expansion of digit IV. The muscle adducts digit IV, flexes its metatarsophalangeal joint and helps extend its interphalangeal joints. The m. abductor interosseus digiti IV originates from the base of the plantar process on the proximal fourth metatarsal (Fig. 6B). It is fused at its origin with m. adductor interosseus digiti IV. It inserts on the lateral sesamoid, the lateral aspect of the base of the proximal phalanx and weakly onto the extensor expansion of digit IV. The muscle abducts digit IV, flexes its metatarsophalangeal joint and helps extend its interphalangeal joints. The m. adductor interosseus digiti V originates from a pit on the plantar-medial aspect of the base of the fifth metatarsal, as well as the distal-most tip of os tarsale IV (Fig. 6B). The muscle inserts on the medial sesamoid and the medial aspect of the base of the proximal phalanx. It adducts digit V and flexes its metatarsophalangeal joint. The m. abductor interosseus digiti V originates from a ridge on the plantar surface of the base of the fifth metatarsal and the os tarsale IV (Fig. 6B). The muscle inserts via a joint tendon with m. abductor digiti V onto the lateral sesamoid and the lateral aspect of the base of the proximal phalanx. Its tendon has a diffuse attachment to the extensor expansion, but the connection is very weak. The muscle abducts digit V and flexes its metatarsophalangeal joint. Two mm. interossei per digit are also present in the pygmy hippo (Campbell, 1935).
lesser trochanter of femur lesser trochanter of femur iliotibial tract (connective tissue) medial surface of proximal tibia
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