Zoological Journal of the Linnean Society, 2010, 158, 661–682. With 9 figures
Hind limb myology of the common hippopotamus,
Hippopotamus amphibius (Artiodactyla:
Hippopotamidae)
REBECCA E. FISHER1,2*, KATHLEEN M. SCOTT3 and BRENT ADRIAN1
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.
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158, 661–682.
doi: 10.1111/j.1096-3642.2009.00558.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. E-mail: [email protected]
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
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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. 25308), weighing 1680 kg, that
died on October 25, 2004. 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 162977,
wild-collected; USNM 25478, captive-born). The
femur, tibia and fibula of USNM 162977 were photographed in four views (lateral, medial, cranial and
caudal), and the articulated pes of USNM 254978 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,
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HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS
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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
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Figure 2. Common hippo hind limb in medial view with the fascia lata removed: dark grey indicates muscles dissected
in specimen no. 25308, 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. 25308, 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.
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Figure 3. Muscle maps for the common hippo femur: A, cranial; B, lateral; C, caudal; D, medial.
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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 &
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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
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(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,
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HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS
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)
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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
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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.
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.
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.
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.
MUSCLES
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.
OF THE LEG
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
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HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS
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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
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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. 4AC). 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
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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
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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).
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HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS
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
675
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.
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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
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158, 661–682
HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS
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
677
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).
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R. E. FISHER ET AL.
Comparative, functional and
phylogenetic implications
The intrinsic muscles of the hippo pes are characterized by the retention of a primitive mammalian
pattern, in contrast with the more derived pes of
other artiodactyls. A similar trend was documented in
the hippo manus (Fisher et al., 2007). Pygmy and
common hippos retain remnant fibres of m. flexor
digitorum brevis (Fig. 7A), m. lumbricalis IV (Figs 6B,
7A, B), a fleshy m. abductor digiti V, mm. adductores
digitorum II and V, and two mm. interossei per digit
(Figs 6B, 9). The m. flexor digitorum brevis is absent
in all other artiodactyls. In fact, among the ungulates
and subungulates, only hippos and hyraxes retain
this feature (Windle & Parsons, 1903). Apart from
hippos, m. abductor digiti V is absent in all other
artiodactyls, although it can be present in ligamentous form (e.g. in Sus; Campbell, 1935). Perissodactyls lack m. abductor digiti V, but it is present in
elephants (Miall & Greenwood, 1878; Windle &
Parsons, 1903) and in hyraxes, as m. abductor digiti
IV (Windle & Parsons, 1903).
The pattern is similar regarding the mm. lumbricales, which are absent in all other artiodactyls.
However, mm. lumbricales are present in perissodactyls (Windle & Parsons, 1903; Campbell, 1935; Sisson,
1975a; Nickel et al., 1986), elephants (Miall & Greenwood, 1878; Windle & Parsons, 1903) and hyraxes
(Windle & Parsons, 1903). Similarly, the mm. adductores digitorum II and V are reduced in size in suids
and tayassuids (Windle & Parsons, 1903; Campbell,
1935), and absent in camelids and ruminants (Windle
& Parsons, 1903; Getty, 1975; Nickel et al., 1986;
Smuts & Bezuidenhout, 1987). Tapirs and hyraxes do
have mm. adductores digitorum, but they serve digits
II and IV in these groups, whereas elephants have a
single m. adductor digiti V or mm. adductores digitorum IV and V (Miall & Greenwood, 1878; Windle &
Parsons, 1903; Campbell, 1935; Weissengruber & Forstenpointner, 2004).
Except in hippos, the mm. interossei are reduced in
artiodactyls. Tayassuids have lost the adductor
interossei for digits III and IV, whereas suids exhibit
a range of variation, but typically retain only one
(abductor) interosseus muscle per digit (Campbell,
1935; Windle & Parsons, 1903; Sisson, 1975b; Nickel
et al., 1986). Ruminants and camelids have a single,
highly derived m. interosseus that is muscular in
younger individuals, but becomes tendinous with age
(Getty, 1975; Nickel et al., 1986; Smuts & Bezuidenhout, 1987). In fact, among artiodactyls, only
tragulids (Hyemoschus), the most primitive living
ruminants, resemble hippos in having two mm.
interossei per digit (Windle & Parsons, 1903). Among
the perissodactyls, rhinos and tapirs have two mm.
interossei per digit. Equus is more derived, having
extremely reduced and ligamentous mm. interossei
associated with the rudimentary second and fourth
metatarsals, and a more prominent m. interosseous
medius, or suspensory ligament of the fetlock, which
is entirely ligamentous in the adult (Windle &
Parsons, 1903; Campbell, 1935; Sisson, 1975a; Nickel
et al., 1986). Elephants have four mm. interossei,
serving digits II to IV (Miall & Greenwood, 1878), or
five mm. interossei, serving digits I to V (Weissengruber & Forstenpointner, 2004). Thus, a clear pattern
emerges: hippos retain more primitive features in the
pes compared with other artiodactyls, including mm.
flexor digitorum brevis, lumbricalis IV, abductor digiti
V, adductores digiti II and V, and a full complement of
mm. interossei.
CONCLUSIONS
Hippos occupy a unique position among the ungulates, both phylogenetically and ecologically. Previously linked with pigs and peccaries, molecular
studies indicate that hippos are more closely related
to ruminants, and are the sister taxon of the Cetacea
(e.g. Shimamura et al., 1997; Ursing & Arnason, 1998;
Nikaido et al., 1999). If this is the case, hippos
diverged from the rest of the artiodactyls very early in
the history of this group, as fossil whales are known
from the early to middle Eocene (e.g. Bajpai & Gingerich, 1998; Gingerich et al., 2001; Thewissen et al.,
2001). In fact, the appendicular muscles of hippos
show more similarities to those of primitive ruminants than to those of suids or tayassuids (Table 1).
However, pygmy and common hippos share a number
of features that set them apart from most other
artiodactyls, including the absence of m. gluteus
accessorius, the presence of m. articularis coxae, a
well-developed m. obturator internus that retains its
intrapelvic origins, a variably present m. adductor
longus, long flexor and extensor tendons to all four
digits, and the retention of a nearly complete complement of intrinsic muscles of the pes (Table 1). The
flexor and extensor tendons serving digits II and V
and the well-developed intrinsic muscles are associated with the retention of functional lateral digits in
hippos (Fig. 8). The retention of these digits with full
functionality of movement and ability to control splay
would be highly adaptive, as it enhances the ability of
hippos to move along the soft substrates of lake and
river beds. Furthermore, these retained primitive features are consistent with an early divergence of
hippos from the rest of the Artiodactyla.
Functionally, the hippo hind limb shows few other
adaptations to their aquatic habitat. This is likely due
to the fact that hippos spend an appreciable amount
of time on land, foraging on terrestrial grasses from
dusk to dawn (Lock, 1972; Mackie, 1976), and
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158, 661–682
Absent
Absent
Absent
Absent
N = 1 (except
Hyemoschus, N = 8)
To digits II–V
To digits II–V
Remnant fibres
Present
To digit IV
To digits II & V
N=8
Flexores digitorum
profundi
Extensor digitorum
longus
Flexor digitorum brevis
Abductor digiti V
Lumbricales
Adductores digitorum
Interossei
Flexor digitorum
superficialis
Adductor longus
Well developed (intra
and extrapelvic
origins)
Present (Choeropsis) or
variable
(Hippopotamus)
To digits II–V
Obturator internus
Present
Absent (except
Tragelaphus and
Tragulus)
Absent or reduced (with
extrapelvic origins
only)
Absent (except
Tragelaphus and
Giraffa)
To digits III–IV (except
Hyemoschus, digits
II–V)
To digits III–IV (except
Hyemoschus, digits
II–V)
to digits III-IV
Absent
Present
Ruminants
Gluteus accessorius
Articularis coxae
Hippos
Table 1. Hind limb traits in hippos compared to other artiodactyls
Absent
Absent
Absent
To digits II & V but
reduced in size
Typically N = 4
To digits III–IV (weak
tendons to digits II &
V)
to digits II-V
To digits III–IV (fascia
only to digits II & V)
Absent or reduced (with
extrapelvic origins
only)
Absent
Present
Absent
Suids
Absent
Absent
Absent
To digits II & V but
reduced in size
N=6
To digits III–IV (weak
tendons to digits II &
V)
to digits II-V
To digits III–IV (fascia
only to digits II & V)
Absent or reduced (with
extrapelvic origins
only)
Absent
No data
Absent
Tayassuids
N=1
Absent
Absent
Absent
Absent
To digits III–IV
To digits III–IV
To digits III–IV
Well developed (intra
and extrapelvic
origins)
Absent
Present
Present
Camelids
HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158, 661–682
679
680
R. E. FISHER ET AL.
precluding the development of more restrictive
aquatic adaptations. In keeping with these constraints, hippos move through the water by walking
along the bottom, rather than swimming. In addition
to the retention of muscles that control the amount of
digital splay, most of the features that distinguish
hippos are adaptations for powerful propulsion
through water. The muscles responsible for retracting
the hind limb, including mm. gluteus superficialis,
gluteus medius, semimembranosus, semitendinosus
and biceps femoris, are not only robust, but display
extensive fusions and distal insertions, thus increasing their power.
ACKNOWLEDGEMENTS
The authors would like to thank Charley Potter, John
Ososky, Linda Gordon, James Mead and Richard
Thorington, from the National Museum of Natural
History, for their continued support of this project.
Charley Potter and John Ososky were very helpful in
facilitating the logistical aspects of this project at the
Smithsonian’s Osteopreparatory Laboratory in Suitland, MD. We would particularly like to thank John
Ososky for his efforts in securing the specimen. We
are also extremely grateful for the reviewer comments, which greatly improved the manuscript.
R.E.F. wishes to thank Eric Sargis (Yale University)
for his assistance in obtaining data for Camelus.
Brent Adrian produced the muscle drawings for the
manuscript (Figs 1, 2, 5, 7, 9) and revised the muscle
maps (Figs 3, 4, 6). Brandon Ehrfurth produced the
original artwork for the muscle maps (Figs 3, 4, 6)
and Melissa Cortez produced Figure 8. R.E.F. and
K.M.S. are Research Collaborators in the Division of
Mammals, National Museum of Natural History,
Smithsonian Institution.
REFERENCES
Bajpai S, Gingerich PD. 1998. New Eocene cetacean from
India and the time of origin of whales. Proceedings of the
National Academy of Sciences of the United States of
America 95: 15 464–15 468.
Beddard FE, Treves F. 1889. On the anatomy of Rhinoceros
sumatrensis. Proceedings of the Zoological Society (London)
1: 7–25.
Campbell B. 1935. The comparative myology of the hippopotamus, pig, and tapir. Ph.D., Johns Hopkins University
Medical School.
Campbell B. 1936. The comparative myology of the forelimb
of the hippopotamus, pig and tapir. American Journal of
Anatomy 59: 201–247.
Campbell B. 1945. The hindfoot musculature of some basic
ungulates. Journal of Mammalogy 26: 421–424.
Cuvier G. 1850. Anatomie comparée. Recueil de planches de
myologie dessinées par Georges Cuvier ou exécutées sous ses
yeux par M. Laurillard. Paris: Imprimerie d’E. Duverger.
Dyce KM, Sack WO, Wensing CJG. 2002. Textbook of veterinary anatomy. Philadelphia, PA: W.B. Sanders.
Fischer MS. 1986. Die stellung der schliefer (Hyracoidea)
im phylogenetischen system der Eutheria. Courier Forschungsinstitut Senckenberg 84: 1–132.
Fisher RE, Scott KM, Naples VL. 2007. The forelimb
myology of the pygmy hippo (Choeropsis liberiensis). Anatomical Record 290: 673–693.
Gatesy J, Hayshi C, Cronin MA, Arctander P. 1996.
Evidence from milk casein genes that cetaceans are close
relatives of hippopotamid artiodactyls. Molecular Biology &
Evolution 13: 954–963.
Getty R. 1975. Myology (Ruminant). In: Getty R, ed. Sisson
and Grossman’s the anatomy of the domestic animals, 5th
edn. Philadelphia, PA: W. B. Saunders, 791–860.
Gingerich PD, Ul-Haq M, Zalmout IS, Khan IH, Malkani
MS. 2001. Origin of whales from early Artiodactyls: hands
and feet of Eocene Protocetidae from Pakistan. Science 293:
2239–2242.
Gratiolet L-P. 1867. Rechereches sur l’anatomie de
l’hippopotame. Paris: Victor Masson et Fils.
Haughton S. 1867. On the muscular anatomy of the rhinoceros. Proceedings of the Royal Irish Academy Series 2 9:
515–523.
Humphry GM. 1872. On the disposition of muscles in vertebrate animals. Journal of Anatomy & Physiology 6: 293–
376.
Irwin D, Arnason U. 1994. Cytochrome b gene of marine
mammals: phylogeny and evolution. Journal of Mammalian
Evolution 2: 37–55.
Jouffroy FK. 1971. Musculature des membres. In: Grassé P,
ed. Traité de zoologie: anatomie, systématique, biologie,
Volume 16 (3). Paris: Masson et Cie Éditeurs.
Kajava Y. 1923. Die volare handmusckulatur der huftiere.
Acta Societatis Medicorum Fennicae Duodecim 4: 1–184.
Karstad EL, Hudson RJ. 1986. Social organization and
communication of riverine hippopotami in southwestern
Kenya. Mammalia 50: 153–164.
Kjaersgaard P. 1980. M. articularis coxae – a possible
receptor organ. Zentralblatt fur Veterinarmedizin Reihe C.
Anatomia Histologia. Embryologia 9: 21–28.
Leidy J. 1853. On the osteology of the head of hippopotamus
and a description of the osteological characters of a new
genus of Hippopotamidae. Journal of the Academy of
Natural Sciences of Philadelphia 2: 207–224.
Lewis OJ. 1989. Functional morphology of the evolving hand
and foot. New York: Oxford University Press.
Linnaeus C. 1758. Systema naturae per regna tria naturae,
secundum classis, ordines, genera, species cum characteribus, differentiis, synonymis, locis, Volume 1. Stockholm:
Laurentii Salvii.
Lock JM. 1972. The effects of hippopotamus grazing on
grasslands. Journal of Ecology 60: 445–467.
Macalister A. 1873. The anatomy of Chaeropsis liberiensis.
Proceedings of the Royal Irish Academy 1: 494–500.
Macdonald AA, Kneepkens AFLM, Kolfschoten TV,
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158, 661–682
HIND LIMB MYOLOGY OF THE COMMON HIPPOPOTAMUS
Houtekamer JL, Sondaar PY, Badoux DM. 1985. Comparative anatomy of the limb musculature of some Suina.
Fortschritte der Zoologie 30: 95–97.
Mackie C. 1976. Feeding habits of the hippopotamus on the
Lundi River, Rhodesia. Arnoldia 7: 1–16.
Maurer F. 1911. Die musculi serrati postici bei Hippopotamus amphibius. Anatomischer Anzeiger 38: 145–156.
Miall L, Greenwood F. 1878. The anatomy of the Indian
elephant. Journal of Anatomy & Physiology 12: 261–287.
Milne Edwards MH. 1868–1874. Des observations sur
l’hippopotame de Liberia et des études sur la faune de la
Chine et du Tibet oriental. In: Milne Edwards MH, ed.
Recherches pour servir à l’histoire naturelle des mammifères:
comprenant des considérations sur la classification de ces
animaux. Paris: G. Masson, 43–66.
Nickel R, Schummer A, Seiferle E, Wilkens H, Wille K-H,
Frewein J. 1986. The anatomy of the domestic animals.
volume i. The locomotor system of the domestic animals.
Berlin: Verlag Paul Parey.
Nikaido M, Rooney AP, Okada N. 1999. Phylogenetic relationships among cetartiodactyls based on insertions of short
and long interspersed elements: hippopotamuses are the
closest extant relatives of whales. Proceedings of the
National Academy of Sciences of the United States of
America 96: 10 261–10 266.
Shimamura M, Yasue H, Ohshima K, Abe H, Kato H,
Kishiro T, Goto M, Munechika I, Okada N. 1997.
Molecular evidence from retroposons that whales form a
clade within even-toed ungulates. Nature 388: 666–670.
Simpson GG. 1945. The principles of classification and a
classification of the mammals. Bulletin of the American
Museum of Natural History 85: 1–350.
Sisson S. 1975a. Myology (Equine). In: Getty R, ed. Sisson
and Grossman’s the anatomy of the domestic animals, 5th
edn. Philadelphia, PA: W.B. Saunders, 376–453.
Sisson S. 1975b. Myology (Porcine). In: Getty R, ed. Sisson
681
and Grossman’s the anatomy of the domestic animals, 5th
edn. Philadelphia, PA: W.B. Saunders, 1256–1267.
Smuts MM, Bezuidenhout AJ. 1987. Anatomy of the dromedary. Oxford: Clarendon Press.
Souteyrand-Boulenger JD. 1968. Muscle articulaire de la
hanche chez les camélidés. Revue d’Elevage et de Medecine
Veterinaire des Pays Tropicaux 21: 289–292.
Souteyrand-Boulenger JD. 1969. Le muscle articulaire de
la hanche chez les carnivores. Mammalia 33: 276–284.
Thewissen JGM, Williams EM, Roe LJ, Hussain ST.
2001. Skeletons of terrestrial cetaceans and the relationship
of whales to artiodactyls. Nature 413: 277–281.
Ursing B, Arnason U. 1998. Analyses of mitochondrial
genomes strongly support a hippopotamus–whale clade.
Proceedings of the Royal Society of London, Series B: Biological Sciences 265: 2251–2255.
Waddell PJ, Okada N, Hasegawa M. 1999. Towards resolving the interordinal relationships of placental mammals.
Systematic Biology 48: 1–5.
Waibl H, Gasse H, Hashimoto Y, Budras K-D, Constantinescu GM, Saber AS, Simoens P, Sotonyi P, Augsburger H, Bragulla H. 2005. Nomina anatomica
veterinaria. Hannover: International Committee on Veterinary Gross Anatomical Nomenclature, World Association of
Veterinary Anatomists.
Weissengruber GE, Forstenpointner G. 2004. Musculature of the crus and pes of the African elephant (Loxodonta
africana): insight into semiplantigrade limb architecture.
Anatomy and Embryology 208: 451–461.
Windle BCA, Parsons FG. 1901. On the muscles of the
Ungulata. Part I. Muscles of the head, neck, and fore-limb.
Proceedings of the Zoological Society (London) II: 656–
704.
Windle BCA, Parsons FG. 1903. On the muscles of the
Ungulata. Part II. Muscles of the hind-limb and trunk.
Proceedings of the Zoological Society (London) 1: 261–298.
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158, 661–682
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APPENDIX
SYNONOMY
OF HIND LIMB MUSCLE NAMES
Nomina Anatomica Veterinaria terms in bold, followed by synonyms used in Windle & Parsons (1903)* or Campbell
(1935)†
Gluteal and lateral thigh muscles
m. tensor fasciae latae; tensor fasciae femoris*
m. gluteus medius; mesogluteus*
m. gluteus profundus; entogluteus*; gluteus minimus*,†
m. gluteobiceps
m. gluteus superficialis; ectogluteus*; gluteus maximus*,†
m. biceps femoris (cranial division); femoro-coccygeus*; agitator caudae*
m. biceps femoris (caudal division); flexor cruris lateralis*
m. semimembranosus; semimembranosus + presemimembranosus*
Deep muscles of the pelvis
m. psoas major; psoas magnus*
m. psoas minor; psoas parvus*
m. articularis coxae; gluteus profundus*; gluteus quintus*; ilio-capsularis*; capsularis†
m. obturator externus; obturator externus + obturator tertius*
Quadriceps and adductor groups
m. rectus femoris; rectus head of quadriceps extensor cruris*
m. vastus medialis; vastus internus*
m. vastus lateralis; vastus externus*
m. sartorius; ilio-tibialis*
m. gracilis; adductor cruris*
m. adductor communis; adductor mass*, adductor femoris communis†
Leg muscles
m. tibialis cranialis; tibialis anticus*; m. tibialis anterior†
m. extensor digiti I longus; extensor proprius hallucis*, part of extensor longus digitorum*; extensor primi
internodii digiti secundi (et tertii) pedis†
m. fibularis tertius; part of extensor longus digitorum*; extensor hallucis longus†
m. extensor digitorum longus; extensor longus digitorum*
m. fibularis longus; peroneus longus*,†
m. extensor digitorum lateralis; peroneus quarti et quinti digiti*; peroneus digiti quarti et peroneus digiti quinti†
m. flexor digitorum superficialis; plantaris*,†
mm. flexores digitorum profundi
m. tibialis caudalis; tibialis posticus*; accessory head of m. flexor digitalis†
m. flexor digitorum lateralis; flexor fibularis*; flexor digitorum fibularis†; flexor hallucis longus†
m. flexor digitorum medialis; flexor tibialis*; flexor digitorum tibialis†; flexor digitorum longus†
Intrinsic muscles of the pes
m. extensor digitorum brevis; extensor brevis digitorum*; extensor digitorum brevis pedis†
m. lumbricalis IV; lumbricales*; lumbricales pedis†
m. abductor digiti V; abductor minimi digiti*; m. abductor digiti quinti pedis†
m. adductor digiti V; contrahentes digitorum pedis†
m. adductor digiti II; contrahentes digitorum pedis†
mm. interossei; flexores breves*; flexores breves profundi pedis†
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158, 661–682