from the posterior surface of the tarsometatarsus between the midline
and the posterior metatarsal crest beginning immediately below the
hypotarsus and ending a short distance above the first metatarsal
(sometimes more proximally).
INSERTION.--The slender tendon, which begins along the medial edge of
the distal part of the belly, passes through the groove on the
posterodistal surface of the first metatarsal and onto the proximal end
of the ventral surface of the hallux; the tendon widens considerably and
attaches by its edges to the ventral surface of the proximal end of the
first phalanx, forming a short "tunnel" through which the tendon of M.
flexor hallucis longus passes.
INNERVATION.--The paraperoneal branch of the tibial nerve sends one or
two twigs into the proximal part of the muscle (but distal to the
hypotarsus).
INDIVIDUAL VARIATION.--In two legs, the muscle arises in part from the
distal end of the lateral calcaneal ridge. The individual variation is
insignificant in _T. cupido_ and _P. p. jamesi_.
DISCUSSION AND CONCLUSIONS
_Analysis of Individual Variation_
Considerable individual variation occurs in both the muscles and the
nerves of the leg of the three species studied. The amount of variation
reported by a worker depends in large part on the degree of variation
that he considers significant.
Individual variation in the muscles and in the nerves will be discussed
separately; that of the muscles (excluding innervation) will be
considered first.
Muscles
Considering the number, rather than degree, of variations, the most
variable muscles are: Mm. flexor digitorum longus, obturator,
caudofemoralis, and extensor hallucis longus. The first-mentioned muscle
exhibits 14 different variations in the specimens studied. Mm. vastus
lateralis, flexor perforans et perforatus digiti II, and piriformis also
showed a considerable number of variations. The following muscles did
not exhibit any variations considered significant in this study: Mm.
vastus medialis, femoritibialis internus, flexor perforatus digiti III,
extensor brevis digiti III, and abductor digiti IV.
Muscles showing a great _degree_ of individual variation included the
following: M. extensor proprius digiti III was present in two legs of
_Pedioecetes_ but absent in the other legs studied. A fleshy muscle slip
connected M. caudofemoralis pars caudifemoralis with the tendinous raphe
between Mm. flexor cruris lateralis and femorocruralis in two legs,
whereas in others this connection was tendinous or even absent
altogether. M. caudofemoralis pars caudifemoralis had a tendinous area
within the belly in only three legs. A vinculum connected the
insertional tendons of Mm. flexor perforans et perforatus digiti II and
flexor perforatus digiti II in only one leg. The fleshy belly of M.
iliotrochantericus medius was completely split into two parts in one
leg. M. flexor cruris lateralis had an accessory slip arising from the
caudal musculature in one leg.
Certain individual variations reported in the accounts of the muscles
formed a graduated series, as far as degree is concerned, from the
typical to the extreme condition. Therefore it was difficult or
impossible in some cases to state whether or not certain specimens
exhibited such a variation. Elimination of the doubtful instances of
variation leaves a total of 50 different variations (excluding
variations between species) which can be attributed to a definite number
of specimens. The remainder of the discussion of individual variation in
the muscles concerns these 50 variations. See table 3.
The typical condition of any structure is considered to be the condition
of that structure in the majority of the legs studied. Some conditions
considered as typical in the present study might not be so considered if
a larger number of specimens had been studied. If exactly half of the
legs of one species shows a particular condition of a structure, the
condition typical for this species is considered (for purposes of the
following discussion) to be that found in the majority of the legs of
the other species.
In all instances except two (of 50) the typical condition of the muscles
in _T. pallidicinctus_ was also the typical condition in _T. cupido_.
The majority of the legs in _T. cupido_ had an additional dorsal slip on
the tendon of M. flexor digitorum longus in digits II and III. In all
instances except seven the typical condition in _T. pallidicinctus_ was
also the typical condition in _Pedioecetes_. In these seven instances a
variation in the former was the typical condition in the latter. These
were: an additional dorsal slip on the tendon of M. flexor digitorum
longus in each of three digits, a vinculum between the latter and M.
flexor perforatus digiti IV, a partly fleshy insertion of M. flexor
cruris medialis, an unossified lateral branch of the insertional tendon
of M. extensor digitorum longus, and an independent insertion of the
distalmost fibers of the distal head of M. extensor hallucis longus. For
all characters except the number of the dorsal slips on the tendon of M.
flexor digitorum longus in digits II and III, the typical condition in
_T. pallidicinctus_ was also the typical condition for all species
considered together. To facilitate comparison, in the following
discussion all of the above-mentioned characters are considered in all
species as variants from the typical condition.
Certain legs showed a greater number of variations from the typical
condition than did others. The majority of legs showed from four to
seven variations in the muscles of the leg. The extremes were P.p. 1L,
which showed 11, and T.c.p. 2L, which exhibited only one variation.
Twenty-three of the 50 variations were found in only one leg (out of
23). It would be expected that if additional specimens were studied,
more kinds of variations would be found. Nine variations were found in
only two legs, five in three legs, five in four legs, and four in five
legs. One variation was found in nine legs, one in ten legs, and two in
12 legs; the last four variations were in the number of dorsal slips of
the insertional tendon of M. flexor digitorum longus in digits II, III,
and IV and in the ossification of the insertional tendon of M. extensor
digitorum longus.
Five of the variations were found only in specimens in which only one
leg was dissected. Considering only those eight specimens in which both
legs were dissected, five of the 45 variations were found in both legs
of each specimen exhibiting the variation; 28 variations were found in
only one leg of each specimen exhibiting the variation; 12 variations
were found in both legs of some specimens but in only one leg of other
specimens. Of the six muscle features showing the greatest degree of
individual variation (described previously), only two (both pertaining
to M. caudofemoralis) were found in both legs of the specimens
exhibiting the variation.
For one leg (the one showing the most variations) of each specimen of
which both legs were studied, the number of variations that this leg had
in common with every other leg (of all species) was determined. Then the
number of variations in common between the two legs of one individual
was compared with the number of variations in common between one leg of
this individual and each leg of every other individual. See table 4. One
leg of six of the eight specimens showed at least as many variations in
common with a leg of another individual as with the other leg of the
same individual. The two exceptions were T.p. 2R and T.c.a. 1R. Thus for
most specimens there was as much variation in the muscles between the
right and left legs of one individual as there was between individuals.
Of the 50 muscle variations seven were found only in _T. pallidicinctus_
(eight legs), 16 were found only in _T. cupido_ (nine legs), and ten
were found only in _Pedioecetes_ (six legs). Two were found in both
species of _Tympanuchus_ (but not in _Pedioecetes_). Fifteen were found
in both _Tympanuchus_ and _Pedioecetes_; of these, five were found in
all three species studied, eight were shared by _T. pallidicinctus_ and
_Pedioecetes_, and two occurred in _T. cupido_ and _Pedioecetes_.
Nerves
The lumbosacral plexus, femoral nerve, sciatic nerve, and tibial nerve
all showed numerous individual variations. The peroneal nerve, however,
was relatively constant. Variations in the obturator nerve were
considered to be insignificant. See table 5.
In all instances except one (of 40) the typical condition in _T.
pallidicinctus_ was also the typical condition in _T. cupido_. In most
of the legs of the latter the nerve to M. flexor cruris lateralis did
not perforate M. caudofemoralis. In all instances except four the
typical condition in _T. pallidicinctus_ was also the typical condition
in _Pedioecetes_. These exceptions were: prefixation of the lumbosacral
plexus, six roots of the sciatic nerve, femoral nerve formed mainly from
S2 to S4 and two twigs to M. flexor ischiofemoralis. In all instances
the typical condition in _T. pallidicinctus_ was also the typical
condition for all species considered together.
Certain legs showed a greater number of variations from the typical
condition of the nerves than did others. The greatest number of
variations was shown by P.p. 3L, which had 12. T.p. 1R and T.c.p. 1L
both showed only one.
All six variations in the lumbosacral plexus were found on both sides of
each specimen exhibiting the variation. In marked contrast to the other
nerves, there was no significant variation in the lumbosacral plexus
between the right and left sides of one individual. (This might not
always be true, however, if a larger number of specimens were studied.)
Of the variations in the lumbosacral plexus, one was found in only one
specimen (of 15), one was found in three specimens, one in four
specimens, two in six specimens, and one in seven specimens. Of the 34
variations found in the other nerves, 14 were found in only one leg (of
23), six occurred in two legs, four in three legs, three in four legs,
three in five legs, two in six legs, one in seven legs, and one in nine
legs.
Four of the variations were found only in specimens in which only one
leg was dissected. Considering only those eight specimens in which both
legs were dissected, and excluding the lumbosacral plexus, ten of the 30
variations were found in both legs of each specimen exhibiting the
variation; 16 variations were found in only one leg of each specimen
exhibiting the variation; four variations were found in both legs of
some specimens but in only one leg of other specimens.
The number of variations in common between the two legs of one
individual was compared with the number between individuals in the same
manner as for the muscles; the lumbosacral plexus was excluded from
consideration. See table 6. One leg of six of the eight specimens showed
at least as many variations in common with a leg of another individual
as with the other leg of the same individual. The two exceptions were
T.p. 2L and T.p. 3R. Thus for most specimens there was as much variation
in the nerves other than the lumbosacral plexus between the right and
left legs of one individual as there was between individuals.
Of the 40 nerve variations (including the lumbosacral plexus) 11 were
found only in _T. pallidicinctus_, seven were found only in _T. cupido_,
and seven were found only in _Pedioecetes_. Four were found in both
species of _Tympanuchus_ (but not in _Pedioecetes_). Eleven were found
in both _Tympanuchus_ and _Pedioecetes_; of these, four were found in
all three species, three were shared by _T. pallidicinctus_ and
_Pedioecetes_ and four occurred in _T. cupido_ and _Pedioecetes_.
The average number of variations per leg in both muscles and nerves was
11 in _T. pallidicinctus_, nine in _T. cupido_, and 16 in _Pedioecetes_.
The high number in the last is in part the result of these being
variations from the typical condition of _T. pallidicinctus_ (rather
than from _Pedioecetes_).
_Analysis of Variation Between Species_
No constant differences in the muscles or nerves was found between _T.
cupido pinnatus_ and _T. cupido attwateri_. Only one constant difference
was found between _T. cupido_ and _T. pallidicinctus_: a thicker fleshy
origin of M. extensor iliotibialis lateralis in _T. cupido_ (associated
with a thicker edge of the lateral iliac process).
Although no constant differences in the nerves were found between
_Pedioecetes_ and _Tympanuchus_ (both species), 17 constant differences
in the muscles were found between these two genera. Seven of these
differences pertain to features of a single muscle--M. flexor cruris
medialis. Compared with the condition in _Tympanuchus_, M. flexor cruris
medialis in _Pedioecetes_ has a wider origin, a partly fleshy (instead
of entirely tendinous) origin, a more pronounced curvature of the line
of origin, a wider insertion, an insertion posterior (rather than
anterior) to the medial collateral ligament, an insertion that attaches
in part to the articular capsule, and a shorter tendon of insertion
(resulting in the fusion of the common insertional tendon of Mm. flexor
cruris lateralis and femorocruralis with the fleshy belly rather than
with the insertional tendon). Other differences include the following. A
more extensive posteroproximal aponeurosis of M. extensor iliotibialis
lateralis in _Pedioecetes_ (resulting in a narrower fleshy origin); a
more nearly straight line of origin of this muscle (associated with a
less pronounced lateral iliac process); a thinner fleshy origin of this
muscle (associated with a thinner edge of the lateral iliac process); a
wider M. flexor cruris lateralis that is fleshy up to the origin from
the vertebrae; a wider fleshy origin of M. iliacus; the origin of M.
caudofemoralis pars iliofemoralis not reaching the ventral edge of the
ischium; a narrower origin of M. adductor superficialis; a wider M.
femorocruralis; and a shorter belly of M. extensor digitorum longus.
Some additional differences between these two genera, which are slight
in degree, are given in the accounts of the muscles. If additional
specimens were studied, some of the differences listed above possibly
would prove to be subject to individual variation and so could not
properly be listed as constant differences between the two genera.
The picture of the differences between _Tympanuchus_ and _Pedioecetes_
that the present study presents is radically different from that
presented by the study of Hudson, _et al._ (1959). These authors
reported the following differences between these two genera. (I am using
my terminology.) The origin of M. piriformis is narrower in
_Pedioecetes_ and is more posteriorly situated; the belly of M. extensor
iliotibialis anticus is broader in _Pedioecetes_; the belly of M.
tibialis anticus is longer; the belly of M. peroneus brevis is shorter;
the insertional tendon of the anterolateral head of M. flexor perforatus
digiti III is shorter; the belly of M. flexor digitorum longus is
shorter; only two (rather than three) of the branches of M. extensor
digitorum longus on the tarsometatarsus are ossified; the posterior
metatarsal crest is shorter; M. flexor perforans et perforatus digiti II
has two heads in _Pedioecetes_ but only one in _Tympanuchus_; the roof
over the hypotarsal canal enclosing the tendon of M. flexor digitorum
longus is bony in _Pedioecetes_ but fibrous in _Tympanuchus_; M. flexor
cruris lateralis is wider in _Pedioecetes_; and the origin of M.
femorocruralis is wider. I paid particular attention in my study to
these 13 features given by Hudson, _et al._; of these the only
differences that I found to be constant were the last two. The apparent
reason for this great discrepancy is the small number of legs of
_Tympanuchus_ studied by Hudson, _et al._ They studied eight legs of
_Pedioecetes_ but only two legs of _Tympanuchus_. This emphasizes the
danger of making comparisons based on a very small number of specimens
(a criticism which may prove to apply to the present study as well). The
reason why Hudson, _et al._ did not report most of the differences found
by me is not so apparent. Either the specimens studied by the former
workers showed a greater variation in these characters than did my
specimens or else those workers overlooked the differences. Probably
both factors are involved. It remains to be determined how many
specimens need to be studied in order to obtain a fairly accurate
picture of variation.
_Comparison with Other Studies of Innervation_
I accept the following concept of muscle-nerve relationship. All muscles
of the pelvic limb of birds have developed phylogenetically from either
the dorsal extensor muscle mass or the ventral flexor muscle mass. The
former was (at least originally) supplied by only the femoral and
peroneal nerves ("dorsal" nerves), the latter by only the obturator and
tibial nerves ("ventral" nerves). The best guide for determining which
muscles are phylogenetically dorsal and which are ventral seems to be
their embryogeny (as shown in the studies of Romer, 1927, and Wortham,
1948). In the phylogenetic changes undergone by the muscles under
consideration, the innervation may have changed in some instances,
although this is less likely to occur than changes in the attachment or
function of the muscles. If a change in innervation has occurred, it
would be more likely to be a change from one dorsal nerve to the other
or from one ventral nerve to the other rather than from a dorsal nerve
to a ventral one or _vice versa_.
Thus, in my opinion, a report of a dorsal muscle supplied by a ventral
nerve, or _vice versa_, should be viewed with suspicion until it is
verified. I suspect that many previous workers have ignored this concept
of muscle-nerve relationship, or else do not accept it, since they
report, without comment, dorsal muscles (as determined embryologically)
innervated by ventral nerves, or _vice versa_. Owing to the intimate
association between the proximal parts of the tibial and peroneal
nerves, the true relationship may be difficult to determine. I suspect
that this relationship has been misinterpreted by a number of workers. I
found in _Tympanuchus_ and _Pedioecetes_ a branch of the tibial nerve
that is closely associated with, and distributed with, the peroneal
nerve and has been mistakenly considered a part of the peroneal nerve by
some workers. In the study here reported on, I have found no definite
exceptions to the expected innervation. The only possible exception is
an extra branch, which could not be traced to its origin, supplying M.
extensor iliofibularis in one leg. Thus my study of innervation agrees
with the embryological determination of the (phylogenetic) dorsal and
ventral muscles and lends strong support to the above-stated concept of
muscle-nerve relationship.
I have compared my findings on the nerves with those of other workers,
who have studied the nerves with a varying degree of thoroughness. The
important differences in innervation between these studies and the
present one are discussed below.
In neither of Gadow's works did he distinguish tibial and peroneal
components in the thigh. In his later work (1891), covering a wide
variety of birds, he found that M. piriformis sometimes has a femoral
innervation in addition to the constant sciatic one and that M. gluteus
profundus may or may not have a sciatic supply in addition to the
femoral one. A comparison of Gadow's terminology of the sciatic nerve
branches in the shank and foot (in both works) with mine shows that his
branch I represents my peroneal nerve plus my paraperoneal branch of the
tibial nerve (Ic); his branch II represents my medial division of the
tibial nerve; and his branch III represents my posterior (IIIa) and
lateral (IIIb) divisions of the tibial nerve.
Gadow's study (1880) on the ratites included _Struthio_, _Rhea_, and
_Casuarius_. Only in _Casuarius_ did Gadow find a branch (IIe) of the
sciatic nerve supplying Mm. lumbricalis, adductor digiti II, and
abductor digiti II. The two former muscles are typically supplied (as in
_Rhea_) by the paraperoneal branch of the tibial nerve; Gadow's branch
IIe presumably represents a segregated branch of this nerve. More
surprising is his finding that M. abductor digiti II is innervated in
_Casuarius_ by both the deep peroneal nerve and branch IIe and in _Rhea_
by branch Ic (paraperoneal branch of tibial nerve). The deep peroneal
innervation is typical. Also unexpected is his finding that the
posterior division of the femoral nerve gives minute twigs into M.
gastrocnemius pars interna in _Struthio_ and _Casuarius_. Since the
other terminal branches of this nerve in these birds are nonmuscular,
since this muscle is chiefly supplied by other nerves, and since the
innervation from the femoral nerve is apparently atypical for most
birds, the possibility should be considered that the femoral twigs are
sensory rather than motor.
Sudilovskaya (1931), studying _Struthio_, _Rhea_, and _Dromaeus_
(_Dromiceius_), used the same terminology as Gadow except that he
designates as branch III Gadow's branch Ic. Sudilovskaya's discussion of
the main branches of the sciatic nerve is confusing. He states that in
_Struthio_, branches I, II, and III all pass through the tendinous guide
loop for M. extensor iliofibularis; this is hard to believe. As near as
I can determine, he has mistakenly given the same designation (branch
III) to two separate branches (Gadow's Ic and III). There is no problem,
however, in determining to which of these two branches he is referring
when he is describing the innervation of a particular muscle, since one
supplies only muscles of the shank and the other only intrinsic foot
muscles. Sudilovskaya found M. abductor digiti II to be innervated by
branch III (Ic of Gadow); thus the innervation of this muscle
corresponds to that found in _Rhea_ by Gadow. Although M. adductor
digiti II had the expected innervation from branch III (paraperoneal
branch of tibial nerve) in _Dromaeus_, that muscle was found to be
supplied by branch II in _Rhea_. (Gadow, on the other hand, reports a
typical innervation for this muscle in _Rhea_.) Sudilovskaya found M.
peroneus brevis to be supplied by the deep peroneal branch (in contrast
to the superficial peroneal supply that I found in _Tympanuchus_ and
_Pedioecetes_). He found M. gastrocnemius pars interna to be supplied in
_Struthio_ by twigs of the femoral nerve in addition to its typical
innervation from branch II of the sciatic nerve; this agrees with
Gadow's findings in the same genus. Sudilovskaya reports that M.
gastrocnemius pars externa was innervated by branches II and III in
_Struthio_ and _Rhea_ and by branches I and III in _Dromaeus_. (Gadow
found only the typical innervation--branch III.)
In the Whooping Crane, Fisher and Goodman (1955) found a peroneal,
rather than a femoral, nerve supply for pars postica of M. vastus
lateralis. They also report a peroneal nerve supply for M. flexor
ischiofemoralis (in contrast to the usual tibial nerve supply) and for
M. adductor superficialis (in addition to the usual supply from the
obturator nerve). The innervation was not given for the intrinsic foot
musculature.