Pars internabipartiteVireoSeiurusIcterusMolothrusPirangaRichmondenaGuiracaPasserinaSpizaChloruraPipiloCalamospizaChondestesJuncoSpizellaZonotrichiaPasserellaCalcarius
The two parts of them. gastrocnemiusare most distinct inVireo.Icterus,Molothrus,Richmondena,Guiraca, andPasserinalack the fibrous band that passes around the front of the knee. InSpizathis band of fibers is smaller than in the other species.
Pars internaundividedPasserEstrildaPoephilaHesperiphonaCarpodacusPinicolaLeucosticteSpinusLoxia
InLeucosticte, although thepars internais undivided, there is a band of fibers which extends around the front of the knee (see discussion, p.183).
Musculus plantaris(Fig.5).—Small and slender, this muscle lies on the posteromedial surface of the crus, beneath thepars internaof them. gastrocnemiusand originates by fleshy fibers from the posteromedial surface of the proximal end of the tibia immediately distal to the internal articular surface. The belly extends approximately one-sixth of the way down the crus and gives rise to a long, slender tendon that inserts on the proximomedial edge of the tibial cartilage.
Action.—Extends tarsometatarsus.
Comparison.—No significant differences noted among the species studied.
Musculus flexor perforatus digiti II(Figs.3,9).—This is a slender muscle which lies on the lateral side of the crus beneath thepars externaof them. gastrocnemiusand is intimately connected anteromedially with them. flexor digitorum longusand posteromedially with them. flexor hallucis longus. The origin is by a strong tendon from the lateral surface of the external condyle of the femur at the point of origin of them. flexor perforans et perforatus digiti II. This tendon serves also as the origin of the anterior head of them. flexor hallucis longus. The tendon connects also by a broad tendinous band with the distal arm of the loop for them. biceps femorisand by a similar band with the lateral edge of the fibula immediately distal to the head. The tendon of insertion passes distally, perforates the tibial cartilage near its lateral edge, traverses the middle medial canal of the hypotarsus (Fig.6), and passes distally to the foot. At the distal end of the tarsometatarsus the tendon is held against the medial surface of the first metatarsal by a straplike sheath. The tendon then passes over a sesamoid bone between the first metatarsal and the base of the second digit and is bound to this bone by a sheath. The tendon inserts mainly along the posteromedial edge of the proximal end of the first phalanx of the second digit, although the termination is sheathlike and covers the entire posterior surface of this phalanx. This sheathlike termination is perforated by the tendons of them. flexor perforans et perforatus digiti IIand the branch of them. flexor digitorum longusthat inserts on the second digit.
Action.—Flexes second digit.
Comparison.—InVireothis muscle is larger and more deeply situated than it is in the other species examined and has no connection with them. flexor hallucis longus.
Musculus flexor perforatus digiti III(Fig.5).—Long and flattened, this muscle lies on the posteromedial side of the crus beneath them. gastrocnemius. The belly is tightly fused laterally with the belly of them. flexor hallucis longusand posteriorly with the belly of them. flexor perforatus digiti IV. The origin is by a long, strong tendon from a small tubercle just medial to, and at the proximal end of, the external condyle of the femur. Below the middle of the crus this muscle terminates in a strong tendon which perforates the tibial cartilage near its lateral edge. In this region the tendon is sheathlike and wrapped around the tendon of them. flexor perforatus digiti IV. These two tendons together pass through the posterolateral canal of the hypotarsus (Fig.6). Immediately distal to the hypotarsus the two tendons separate, and the tendon of them. flexor perforatus digiti IIIreceives a branch of the tendon of them. peroneus longus. The tendon passes distally over the surface of the second trochlea, and its insertion is sheathlike on the posterior surface of the first phalanx, and on the proximal end of the second. In the area of insertion this tendon is perforated by that of them. flexor perforans et perforatus digiti IIIand by that of them. flexor digitorum longusto the third digit.
Action.—Flexes digit III.
Comparison.—InPasser,Estrilda,Poephila,Hesperiphona,Carpodacus,Pinicola,Leucosticte,Spinus, andLoxiathe edges of the sheathlike tendon are thickened at the points of insertion, so that the tendon appears to have two branches which insert along the posterolateral edges of the first phalanx and are connected medially by a fascia.
Musculus flexor perforatus digiti IV(Fig.3).—Extending along the posterior edge of the crus, this slender muscle lies beneath them. gastrocnemius. The belly is fused with those of them. flexor hallucis longusandm. flexor perforatus digiti III. Its origin is fleshy from the intercondyloid region of the distal end of the femur and has a few fibers arising from the tendon of origin of them. flexor perforatus digiti III. Near the distal end of the crus the muscle gives rise to the strong tendon of insertion which perforates the tibial cartilage near its lateral edge and in this region is ensheathed by the tendon of them. flexor perforatus digiti III. The two tendons pass together through the posterolateral canal of the hypotarsus (Fig.6). The tendon continues distally along the tarsometatarsus and the posterior surface of digit IV. The tendon bifurcates at approximately the middle of the first phalanx. A short lateral branch inserts on the posterolateral edge of the proximal end of the second phalanx. The long medial branch is perforated by a branch of them. flexor digitorum longus; the distal end is flattened, has thickened edges, and inserts over the posterior surfaces of the distal end of the second phalanx, and over the proximal end of the third phalanx.
Action.—Flexes digit IV.
Comparison.—No significant differences noted among the species studied.
Musculus flexor perforans et perforatus digiti II(Figs.2,9).—Small and spindle-shaped, this muscle lies on the posterolateral side of the crus immediately beneath thepars externaof them. gastrocnemius. The origin is fleshy and arises in company with them. flexor perforans et perforatus digiti IIIfrom a point on the posterolateral surface of the distal end of the femur between the point of origin of thepars externaof them. gastrocnemiusand the fibular condyle. The belly extends approximately one-fourth of the way down the crus and gives rise to the tendon of insertion which passes distally and superficially through the posterior edge of the tibial cartilage. The tendon traverses the posteromedial canal of the hypotarsus (Fig.6) and continues along the posterior surface of the tarsometatarsus. Between the first metatarsal and the base of the second digit the tendon is enclosed by the medial surface of a sesamoid bone. This tendon then perforates that of them. flexor perforatus digiti IIat the level of the first phalanx and in turn is perforated by the tendon of them. flexor digitorum longusat the proximal end of the second phalanx. The insertion is on the posterior surface of the second phalanx.
Action.—Flexes digit II.
Comparison.—InPasser,Estrilda,Poephila,Hesperiphona,Carpodacus,Pinicola,Leucosticte,Spinus, andLoxiathe proximal portion of this muscle is more intimately connected with the posterior edge of them. flexor perforans et perforatus digiti IIIthan it is in the other species examined.
Musculus flexor perforans et perforatus digiti III(Fig.2).—Long and pinnate, this muscle lies on the lateral surface of the crus beneath them. peroneus longusandpars externaof them. gastrocnemius. There are two distinct heads. The origin of the anterior head is fleshy from the proximal edge of the outer cnemial crest and from the internal edge of the distal end of the patellar tendon. The posterior head arises by a tendon from the femur in company with them. flexor perforans et perforatus digiti II, is connected also with the tendon of origin of them. flexor perforatus digiti II, and is loosely attached to the head of the fibula. Fibers from the belly of the muscle attach throughout its lengthto the lateral edge of the fibula, and the muscle is tightly fused also with adjacent muscles. The tendon of insertion is formed approximately one-half the way down the crus. The tendon perforates the posterior surface of the tibial cartilage and passes through the posteromedial canal of the hypotarsus (Fig.6). At the base of the third digit the tendon ensheathes that of them. flexor digitorum longusand the two together perforate the tendon of them. flexor perforatus digiti III. Immediately distal to this perforation the tendon of them. flexor perforans et perforatus digiti IIIceases to ensheath that of them. flexor digitorum longus. The latter passes beneath that of the former. Near the distal end of the second phalanx the tendon of them. flexor digitorum longusperforates that of them. flexor perforans et perforatus digiti III. The latter inserts on the posterior surface of the distal end of the second phalanx and the proximal end of the third.
Action.—Flexes digit III.
Comparison.—InPasser,Estrilda, andPoephila, and in all the cardueline finches examined the proximal portion of this muscle is more intimately connected with the anterior edge of them. flexor perforans et perforatus digiti IIthan it is in the other species examined.
Musculus flexor digitorum longus(Figs.3,5).—This strong, pinnate muscle is deeply situated along the posterior surfaces of the tibia and fibula. There are two distinct heads of origin. The lateral head arises by means of fleshy fibers from the posterior edge of the head of the fibula. The medial head arises by means of fleshy fibers from the region under the ledgelike external and internal articular surfaces of the proximal end of the tibia. Neither head has any connection with the femur in contrast to the condition, described by Hudson (1937: 46-47) in the crow,Corvus brachyrhynchos, and in the raven,Corvus corax. Near the point of insertion of them. biceps femoristhe two heads fuse. The common belly is attached by fleshy fibers to the posterior surface of the tibia and fibula for two-thirds of the distance down the crus. Near the distal end of the crus the muscle terminates in a strong tendon which passes deeply through the tibial cartilage and traverses the anteromedial canal of the hypotarsus (Fig.6). About midway down the tarsometatarsus this tendon becomes ossified. Immediately above the bases of the toes it gives rise to three branches, one to the posterior surface of each of the foretoes. These branches perforate the other flexor muscles of the toes as described in the accounts of those muscles and insert as follows: The branch to digit II inserts on the base of the ungual phalanx and by a stout, tendinous slip on the distal end of the second phalanx (Fig.9). The branch to digit III inserts on the base of the distal end of the third phalanx and a stronger slip to the distal end of the second or proximal end of the third. The branch to digit IV inserts on the base of the ungual phalanx, with one tendinous slip to the distal end of the third phalanx and another to the distal end of the fourth.
Action.—Flexes foretoes.
Comparison.—No significant differences noted among the species studied.
Musculus flexor hallucis longus(Fig.3).—Situated immediately posterior to them. flexor digitorum longus, the belly of this large, pinnate muscle is intimately connected anteriorly to that of them. flexor perforatus digiti II. Them. flexor hallucis longusarises by two heads which are separated by the tendon of insertion of them. biceps femoris. The smaller anterior head arises fromthe same tendon as does them. flexor perforatus digiti II. The larger posterior head arises by means of fleshy fibers from the intercondyloid region of the posterior surface of the femur along with them. flexor perforatus digiti IIIandIV. The two heads join just distal to the point of insertion of them. biceps femoris. There is no trace of a tendinous band connecting the two heads as there is in the crow and in the raven (Hudson, 1937:49). Near the distal end of the shank the muscle gives rise to a strong tendon which perforates the tibial cartilage along its lateral edge and passes through the anterolateral canal of the hypotarsus (Fig.6). The tendon crosses over to the medial surface of the tarsometatarsus, passes distally, and perforates the sheathlike tendon of them. flexor hallucis brevisbetween the first metatarsal and the trochlea for digit II. The tendon continues along the posterior surface of the hallux and has a double insertion; the main tendon attaches to the base of the ungual phalanx and a smaller branch inserts on the distal end of the proximal phalanx.
Action.—Flexes hallux.
Comparison.—InVireothis muscle has only the posterior head of origin and is not connected with them. flexor perforatus digiti II. The muscle is proportionately smaller and weaker than in any of the other species studied.
Musculus extensor hallucis longus(Fig.4).—One of the smallest muscles of the leg, the origin is fleshy from the anteromedial edge of the proximal end of the tarsometatarsus. The belly is long and slender and terminates distally in a slender tendon which passes distally along the posterior surfaces of the first metatarsal and the first digit. The insertion is on the base of the ungual phalanx. Near the distal end of the proximal phalanx, the tendon passes between two thick bands of fibro-elastic tissue which insert also on the ungual phalanx. These bands of tissue function as automatic extensors of the claw.
Action.—Extends hallux; action must be slight.
Comparison.—InVireothis muscle is proportionately larger and better developed than it is in any of the other species examined.
Musculus flexor hallucis brevis(Fig.4).—This minute muscle has a fleshy origin from the medial surface of the hypotarsus. The short belly terminates in a weak, slender tendon which passes down the posteromedial surface of the tarsometatarsus and into the space between the first metatarsal and the trochlea for digit II. In this region the tendon envelops the tendon of them. flexor hallucis longusand inserts on the distal end of the first metatarsal and on the proximal end of the first phalanx of the first digit.
Action.—Flexes hallux; action must be slight.
Comparison.—The small size of this muscle makes it exceedingly difficult to study. The muscle is larger inVireothan in any of the other species examined. This may be correlated with the smaller size of them. flexor hallucis longusin this species. The muscle does not seem to be so well developed in the cardueline finches as it is in the other species.
Musculus abductor digiti IV(Fig.2).—Extremely small, delicate and difficult to demonstrate, this muscle arises in a fleshy origin immediately from underneath the posterior edge of the external cotyla of the tarsometatarsus. The tendon of insertion is long and slender and inserts along the lateral edge of the first phalanx of digit IV.
Action.—Abducts digit IV.
Comparison.—No significant differences noted among the species studied.
Musculus lumbricalis.—Semitendinous throughout its length, this muscle arises from the ossified tendon of them. flexor digitorum longusat a point immediately proximal to the branching of this tendon. The insertion is on the joint pulleys and capsules at the base of the third and fourth digits.
Action.—Hudson (1937:57) states that: "Meckel (videGadow—1891, p. 204) considered this muscle as serving to draw the joint pulley behind in order to protect it from pinching during the bending of the toes. It perhaps also tends to flex the third and fourth digits."
Comparison.—No significant differences noted among the species studied.
Discussion of the Myological Investigations
Simpson (1944:12) and others have emphasized that different parts of organisms evolve at different rates. Beecher (1951b:275) in stating that "... the hind limb is very similar in muscle pattern throughout the Order Passeriformes and seems to have become relatively static after attaining a high level of general efficiency ..." implies that the muscle pattern of the leg must be one of long standing and slow change. This concept was emphasized by Hudson (1937) who found but little variation in muscle pattern among members of the several families of passerine birds. The concept is further confirmed by the present investigation. The intricate patterns of origin and of insertion seem to remain almost the same throughout the order in spite of adaptive radiation which has occurred.
Two major differences in patterns of leg-musculature, however, were found among the species studied, and these differences are significant since they are consistent between subfamilies. The muscles involved are them. obturator externusand thepars internaof them. gastrocnemius.
Them. obturator externusis bipartite, consisting of dorsal and ventral parts, in the passerine species studied by Hudson (1937) and in all of the species examined by me except the ploceids and the cardueline finches. In the ploceids and cardueline finches this muscle is undivided and resembles in its position, origin, and insertion only the ventral portion of the muscle found in the other birds studied. It is difficult to imagine what advantage or disadvantage might be associated with the bipartite or with the undivided condition. The action of this muscle is to rotate the femur (right femur clockwise, left femur counterclockwise), and certainly the greater mass of the bipartite muscle could lend greater strength to such action. The possible significance of this is discussed below.
List of Abbreviations Used in Figures
Abd. dig. IV
M. abductor digiti IV
Acc.
M. accessorius semitendinosi
Add. long.
M. adductor longus et brevis
Anterolat. can. Anterolateral canal of hypotarsus
Anteromed. can. Anteromedial canal of hypotarsus
Bic. fem.
M. biceps femoris
Bic. loop Loop for
m. biceps femoris
Ext. cot. External cotyla
Ext. dig. l.
M. extensor digitorum longus
Ext. hal. l.
M. extensor hallucis longus
Fem. tib. ext.
M. femorotibialis externus
Fem. tib. int.
M. femorotibialis internus
Fem. tib. med.
M. femorotibialis medius
F. dig. l.
M. flexor digitorum longus
F. hal. brev.
M. flexor hallucis brevis
F. hal. l.
M. flexor hallucis longus
F. p. et p. d. II
M. flexor perforans et perforatus digiti II
F. p. et p. d. III
M. flexor perforans et perforatus digiti III
F. per. d. II
M. flexor perforatus digiti II
F. per. d. III
M. flexor perforatus digiti III
F. per. d. IV
M. flexor perforatus digiti IV
Gas.
M. gastrocnemius
Iliacus
M. iliacus
Il. tib.
M. iliotibialis
Il. troc. ant.
M. iliotrochantericus anticus
Il. troc. med.
M. iliotrochantericus medius
Il. troc. post.
M. iliotrochantericus posticus
Int. cot. Internal cotyla
Isch. fem.
M. ischiofemoralis
Midmed. can. Midmedial canal of hypotarsus
Obt. ext.
M. obturator externus
Obt. int.
M. obturator internus
P. ant.
Pars anticus
P. ext.
Pars externa
P. int.
Pars interna
P. med.
Pars media
P. post.
Pars posticus
Per. brev.
M. peroneus brevis
Per. long.
M. peroneus longus
Pirif.
M. piriformis
Plan.
M. plantaris
Posterolat. can. Posterolateral canal of hypotarsus
Posteromed. can. Posteromedial canal of hypotarsus
Sar.
M. sartorius
Semim.
M. semimembranosus
Semit.
M. semitendinosus
Tib. ant.
M. tibialis anticus
Tib. cart. Tibial cartilage
Superficial Leg MusclesFig. 1.Pipilo erythrophthalmus.Lateral view of the superficial muscles of the left leg, × 1.5.
Fig. 1.Pipilo erythrophthalmus.Lateral view of the superficial muscles of the left leg, × 1.5.
Deeper Leg MusclesFig. 2.Pipilo erythrophthalmus.Lateral view of the left leg showing a deeper set of muscles. The superficial musclesiliotibialis,sartorius,gastrocnemiusandperoneus longushave been removed, × 1.5.
Fig. 2.Pipilo erythrophthalmus.Lateral view of the left leg showing a deeper set of muscles. The superficial musclesiliotibialis,sartorius,gastrocnemiusandperoneus longushave been removed, × 1.5.
Still Deeper Leg MusclesFig. 3.Pipilo erythrophthalmus.Lateral view of the left leg showing the still deeper muscles. In addition to those listed for figure2, the following muscles have been wholly or partly removed:iliotrochantericus posticus,femorotibialis externus,femorotibialis medius,biceps femoris,semitendinosus,tibialis anticus,flexor perforans et perforatus digiti II, andflexor perforans et perforatus digiti III, × 1.5.
Fig. 3.Pipilo erythrophthalmus.Lateral view of the left leg showing the still deeper muscles. In addition to those listed for figure2, the following muscles have been wholly or partly removed:iliotrochantericus posticus,femorotibialis externus,femorotibialis medius,biceps femoris,semitendinosus,tibialis anticus,flexor perforans et perforatus digiti II, andflexor perforans et perforatus digiti III, × 1.5.
Medial View Superficial Leg MusclesFig. 4.Pipilo erythrophthalmus.Medial view of the superficial muscles of the left leg, × 1.5.
Fig. 4.Pipilo erythrophthalmus.Medial view of the superficial muscles of the left leg, × 1.5.
Medial View Deeper Leg MusclesFig. 5.Pipilo erythrophthalmus.Medial view of the left leg showing a deeper set of muscles than those seen in figure4. The following superficial muscles have been removed:iliotibialis,sartorius,femorotibialis internus,obturator internus,adductor longus (pars posticus),gastrocnemius, andperoneus longus, × 1.5.
Fig. 5.Pipilo erythrophthalmus.Medial view of the left leg showing a deeper set of muscles than those seen in figure4. The following superficial muscles have been removed:iliotibialis,sartorius,femorotibialis internus,obturator internus,adductor longus (pars posticus),gastrocnemius, andperoneus longus, × 1.5.
Figure 6
Fig. 6.Pipilo erythrophthalmus.Proximal end of left tarsometatarsus and the hypotarsus, × 4.
Fig. 7.Pipilo erythrophthalmus.Lateral view of proximal end of left femur and a portion of the pelvis, × 3.5.
Fig. 8.Pipilo erythrophthalmus.Upper surfaces of the phalanges of the foretoes of the left foot showing insertions of theM. extensor digitorum longus, × 3.
Fig. 9.Pipilo erythrophthalmus.Medial view of the second digit of the left foot, showing insertions of the flexor muscles, × 3.
The division of thepars internaof them. gastrocnemiusinto anterior and posterior parts has not been reported by previous authors yet the division is quite distinct in those birds in which it occurs. Hudson (1937:36) points out that in some non-passerine birds thepars internais double, but that in these species them. semimembranosusinserts between the two parts. This is not the condition in those species studied by me. Only the ploceids and the cardueline finches in the present investigation fail to show such a division. The undivided muscle in these birds resembles, in its origin and position, the posterior portion of the muscle found in those species showing the bipartite condition. The greater mass of the bipartite muscle probably makes possible a stronger extension of the tarsometatarsus.
Thus, the divided or undivided conditions of them. obturator externusand thepars internaof them. gastrocnemiusseem to be correlated with the degrees of strength of certain movements of the leg. It is conceivable that these differences in structure are correlated with the manner in which food is obtained, the birds having the bipartite muscles being those which spend the most time on the ground searching and scratching for seeds and other sorts of food. Yet, inLeucosticte, a cardueline, and inCalcarius, an emberizine, whose foraging habits are rather similar, the structure is unlike.Leucostictedoes resemble the emberizines and alsoPirangaandSpziain the extension of a band of muscle fibers from thepars internaof them. gastrocnemiusaround the front of the knee. A band of muscle fibers of this sort strengthens the knee joint and gives still more strength to thepars interna. This condition has been reported in a number of birds by Hudson (1937) and is, in all probability, an adaptation for greater strength of certain leg movements. The development of this band inLeucosticteseems to parallel that in the other birds studied and does not indicate relationship, since inLeucostictethis band arises from the undivided muscle which (as stated above) resembles only the posterior portion of the bipartite muscle described for the other birds. In the latter, the muscular band arises from the anterior part of the muscle.
Minor differences in muscle pattern, like those already mentioned, are consistent also between subfamilies, but correlation of these minor differences with function is difficult. There is the implication, however, that in all the groups except the carduelines and ploceids, the emphasis is on greater strength and mobility of the leg. In the carduelines that were studied the origin of them. sartoriusdoes not extend so far craniad as in the other species. In the latter, at least half of the origin is from the last one or two free dorsal vertebrae; in the carduelines no more than one third of the origin is anterior to the ilium. It is conceivable that the more craniad the origin, the stronger the forward movement of the thigh would be.
InPasser,EstrildaandPoephila, and in all the cardueline finches examined, the bellies of them. flexor perforans et perforatus digiti IIand them. flexor perforans et perforatus digiti IIIare more intimately connected than they are in the other species studied. Thus, the amount of independent action of these muscles inPasser, in the estrildines, and in the carduelines probably is reduced.
InPasser, the estrildines, and the carduelines the edges of the sheathlike tendon of insertion of them. perforatus digiti IIIare thickened; as a result the insertion appears superficially to be double but closer examination reveals that there is a fascia stretched between the thickened edges. In the other species examined, the insertion is sheathlike throughout and there are no thick areas. I cannot explain this on the basis of function. The difference, however, is obvious and constant.
Aside from the differences noted above, there were variations of muscle pattern that seem to be significant only inVireo olivaceus. In this species the central, aponeurotic portion of them. iliotibialisis absent. The origin of them. adductor longus et brevisis from the dorsal edge of the ischiopubic fenestra and not from the membrane covering this fenestra. The origin of thepars posticusof this muscle, furthermore, is fleshy and not tendinous as it is in the other species. Them. flexor perforatus digiti IIis larger and more deeply situated inVireoand has, furthermore, no connection with them. flexor hallucis longus. The latter muscle is smaller and weaker than in any of the other species and has only one (the posterior) head of origin. Them. flexor hallucis brevis, on the contrary, is larger than in the other birds, compensating, probably, for the smallm. flexor hallucis longus. In those differences, however, which separate the carduelines and ploceids from the other birds studied,Vireoresembles, in every instance, the richmondenines, emberizines, tanagers, warblers, and blackbirds.
On the basis of differences in leg-musculature the species which are now included in the Family Fringillidae may be separated into two groups. One group includes the richmondenines and the emberizines; the other, the carduelines. The muscle patterns of the legs of the birds of the first group are indistinguishable from those ofSeiurus,Icterus,Molothrus, andPiranga, and except for the differencesnoted are similar to those inVireo. The carduelines, on the other hand, are similar in every point of leg-musculature to the ploceids which were studied. Thus, the heterogeneity of the Family Fringillidae, as now recognized, is emphasized by differences in the muscle patterns of the leg.