The Hindlimb Musculature of the Mousebirds (Coliiformes)

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THE HINDLIMB MUSCULATURE OF THE MOUSEBIRDS (COLIIFORMES)

SUSANL. gERMAN1 AND ROBERTJ. RAIKOW Departmentof BiologicalSciences, University of Pittsburgh,Pittsburgh, Pennsylvania 15260 USA

ABSTRaCT.---Thehindlimbs of two speciesof mousebirds (Colius striatusand C. leucocephalus)were dissectedin order to provide myologicaldescriptions, to elucidatethe mech- anism of digit rotationand other characteristiclocomotor habits, and possiblyto yield clues to the systematicposition of the order Coliiformes.Among the myologicalpeculiarities, the unusuallylarge M. iliofemoralisexternus, the accessorybelly of M. pubo-ischio-femoralis, and the extensive femoral insertion of M. flexor cruris lateralis and origin of M. flexor hallucislongus are featuresrelated to the hanging posturesof the Coliiformes.Digit rotation is accomplishedprimarily by enlargementand slight changesin the insertionsof four intrinsic foot muscles.Two small intrinsic foot muscles,not previously described in birds, also appear to be associatedwith digit rotation. In the speciesdissected, the extensordigitorum longus tendon sendsa branch to the hallux as well as to the three forward digits. This condition has previously been describedonly in the Psittaciformes,and may possibly suggesta commonancestry for the two orders. Received16 March 1981,accepted 21 July1981.

THE Coliiformes is an order of birds inhab- tion. This gives them the option of being an- iting scrub and lightly wooded areas of sub- isodactyl,zygodactyl, or parnprodactyl(Fig. 1). Saharan Africa. The single genus Colius in- Our extensive observations of living mouse- cludes six living species commonly called birds reveal no correlation between any digit colies or mousebirds. They are differentiated configuration and any particular activity. primarily on the basis of plumage (Sclater1903, Whatever position is most effective for the ob- Friedmann 1930, Chapin 1939, Mackworth- ject being grasped is the one put to use. As Praed and Grant 1962). Whereas the system- indicated in Fig. 1, the same configurationis atics within the order are not a problem, be- not necessarilymost appropriate for both feet causeof certainpeculiarities in their habits and at the same time. morphologythe relationshipof the Coliiformes In addition to the peculiarities of their feet, to other avian orders has always been uncer- mousebirdsare capableof a variety of very odd tain. At various times and for various anatom- movements and postures, which are accom- ical and behavioral reasons, affinities to the panied by some unlikely contortions of the Passeriformes, Piciformes, Psittaciformes, hind limb. They creep rapidly through dense Coraciiformes, Apodiformes, and Caprimul- vegetation in a rodent-like manner, with the giformes have been suggested(Murie 1872, longitudinal axis of the body parallel to the Garrod 1896, Pycraft 1907, Lowe 1948, Verhey- branch they are grasping. They are seldom en 1956). Ballman (1969: 192-195) studied fossil seen perching in a conventional position. mousebirds from the Miocene of France. He When resting, even for a moment, there is briefly described several skeletalelements, and usually a tendency for the body to drop below correctederrors of family allocation made by the feet, so that the bird is hanging to some earlier workers. degree (Fig. 1). The most conspicuous feature distinguish- Mousebirds use their hindlimbs extensively ing the Coliiformes from other birds is their in feeding. Small food items are held in one ability to rotate both the first and fourth hind- foot in a parrot-like manner, while the bird limb digits to either a cranial or caudal posi- hangs or supports itself by the other (Fig. 1). The foot has considerablemanipulative ability when used in this way, the digit configuration 1 Presentaddress: Department of Biology, College being modified as the item is consumed and of the Holy Cross, Worcester, Massachusetts01610 changes shape. USA. Finally, our observationsof the use of the

41 The Auk 99: 41-57. January1982 42 BERMANAND RAn

Fig. 1. A. Coliusstriatus "perching," with the right and left feet in anisodactyland zygodactylconfigu- rations, respectively.Note the tendencyfor the body to sink downward on the perch, and the useof the tail in bracing.B. Coliusstriatus in the typical hanging position. Note the pamprodactyldigit configuration.C. Coliusstriatus in a typical feeding posture.Note the use of the foot in holding food, and the use of only digits II and III in hanging. Drawn from photographswith the aid of a cameralucida.

hind limb during aggressive encounters are motor habits and the systematic position of noteworthy. A common sequencewas for one these birds. bird to approach another, raise its foot, and either use it in grasping the subordinatebird's MATERIALS AND METHODS head, or, if the latter began to move away, One hind limb of each of 4 preserved specimens grasp its tail and pull the bird off its perch. (3 Colius striatus and I C. leucocephalus)were dis- Despite the odd uses of the hind limb and sected under a stereomicroscope,using magnifica- the unique feet of mousebirds,there have been tions of 6-25x. Iodine stain (Bock and Shear 1972) no comprehensivemyological studies of this was used to elucidate fiber architecture and to dem- order. Previous anatomical studies deal only onstrate very small musclesmore clearly. Drawings were made with a camera lucida. Anatomical no- with those features considered relevant to the menclature follows the Nomina Anatomia Avium systematicposition of the Coliiformes (Murie (Baumelet al. 1979).Where it was necessaryto de- 1872, Garrod 1896, Pycraft 1907, Verheyen termine muscleactions by manipulation, freshly fro- 1956). One recent work (Decoux 1975) de- zen specimensof C. striatuswere used. Observations scribes the functional significance of the of postures, locomotion, and digit rotation were branching of the extensor digitorum longus made on individuals in a small colonyof C. striatus tendon, but gives no further myologicaldata. kept in a cage measuring 1.5 m x 1.5 m x 1.8 m. The presentstudy provides detailed descrip- tions of the hind limb muscles of two species DESCRIPTION OF HINDLIMB MUSCLES of Colius. This is followed by a discussionof M. iliotibialiscranialis (Fig. 2A, B).--This muscle the myological peculiarities encounteredand arises by fleshy fibers from the cranial 6 mm of the their possible bearing on the unusual loco- dorsalcrest of the synsacrum.The caudalborder of January 1982] MousebirdHindlimb Myology 43

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Fig. 2. The thigh of Coliusstriatus. A. Lateral view. Note the absenceof the postacetabularpart of M. iliotibialis cranialis. B. Medial view. Note the accessorybelly of M. pubo-ischio-femoralis.C. Lateral view showing the deep muscles. The following musclesshown in Part A have been removed: M. iliotibialis cranialis, M. iliotibialis lateralis, M. femorotibialis externus, M. iliofibularis, and M. flexor cruris lateralis pars pelvica. Note the enlarged iliofemoralis externus. D. Medial view showing the deep muscles. The following musclesshown in Part B have been removed: M. iliotibialis cranialis, M. femorotibialis medius, M. femorotibialis internus, M. iliotrochantericus medius, M. caudiliofemoralis, M. flexor cruris mediails, and M. flexorcruris lateralis pars pelvica.Note the three belliesof M. pubo-ischio-femoralis.Abbreviations: CF, M. caudofemoralis;FCLA, M. flexor crurislateralis pars accessoria;FCLP, M. flexor crurislateralis pars pelvica; FCM, M. flexor cruris medialis; FHL, M. flexor hallucis longus; FTED, M. femorotibialis externus pars distalis; FTI, M. femorotibialisinternus; FTM, M. femorotibialismedius; IC, M. iliotibialis cranialis; IF, M. iliofibularis; IFE, M. iliofemoralis externus; IFI, M. iliofemoralis internus; IL, M. iliotibialis lateralis; ISF, M. ischiofemoralis; ITC, M. iliotrochantericus caudalis; ITCR, M. iliotrochantericus cranialis; ITM, M. iliotrochantericusmedius; LC, M. levatorcaudae; PIFA, M. pubo-ischio-femoralispars accessoria;PIFL, M. pubo-ischio-femoralispars lateralis; PIFM, M. pubo-ischio-femoralispars medialis. the origin lies deep to M. iliotibialis lateralis and M. iliotibialislateralis (Fig. 2A).--Only a preacetab- superficialto M. iliotrochantericuscranialis. No deep ular portion is present. It arisesby fleshyfibers from head is present, nor is there any area of origin from the dorsal crest of the synsacrum for about 2 mm the ilium, as in many birds. The strap-likebelly ex- caudal to the origin of M. iliotibialis cranialis, and tends down the cranialborder of the thigh, passing by an aponeurosisfrom the dorsalcrest of the syn- to the medial surface. It inserts by fleshy fibers on sacrumand from the dorsal iliac crest. The aponeu- the craniomedial surfaceof the pateliar crest of the rosis overlies M. iliofemoralis externus and the cau- tibiotarsus, after passing superficial to the medial domedial part of M. iliotrochantericuscaudalis. The side of the pateliar ligament. sheet-like belly extends down the lateral surface of 44 gERMANAND RAIKOW [Auk, Vol. 99 the thigh superficial to M. femorotibialis extemus chantericus caudalis. It does not appear to be named and, distally, to M. iliotibialis cranialis.It lies caudal in Baumel et al. (1979). to M. iliotibialis cranialis and cranial to M. iliofib- M. femorotibialisexternus (Fig. 2A).--This large, ularis. In the distal third of the thigh, M. iliotibialis fusiform muscle covers the craniolateral surface of lateralis gives rise to an aponeurosisthat fuseswith the thigh deep to M. iliotibialis lateralis. Both su- the lateral surface of M. femorotibialis extemus and perficial (pars proximalis) and deep (pars distalis) forms the superficialpart of the pateliarligament. heads are present. Pars proximalis arises semiten- M. iliotrochantericuscaudalis (Fig. 2C).--This orig- dinously from the craniomedialsurface of the femur inatesby fleshyfibers (partly aponeuroticin C. leu- just distal to the trochanter,and fleshyfrom the cra- cocephalus)from the dorsal crest of the synsacrum niolateral surfaceof the proximal three-fourthsof the deep to the origins of Min. iliotibialis cranialis and fernoral shaft. The semitendinous origin is shared lateralis, and from the dorsal iliac fossa, dorsal to the with that of M. femorotibialis medius. The much origins of Min. iliotrochantericus cranialis and me- smaller pars distalis arises fleshy from the middle dius, and cranial to the origin of M. iliofemoralis third of the lateral fernoral shaft and from the adja- externus.The fan-shapedbelly is bordered caudally cent surfaceof the superficialhead. It is somewhat by M. iliofemoralis extemus. It extends caudolater- fused with the superficial head throughout its ally to insert by a strong, flat tendon on the lateral length. Pars distalis is visible on the lateral surface surfaceof the fernoraltrochanter just cranial to that of the thigh, caudal to the superficialhead and cra- of M. iliofemoraiis extemus and distal to that of M. nial to M. iliofibularis. About halfway down the obturatorius mediaIls. This muscle is unusual in that thigh a denseaponeurosis forms on the lateral sur- its area of origin does not extend as far caudally as faceof M. femorotibialisextemus. Medially its fibers in most birds, owing to the unusually large size of are closelyassociated with thoseof M. femorotibialis the adjacentM. iliofemoralisextemus (see below). medius. Together these two musclesgive rise to the M. iliotrochantericuscranialis (Fig. 2B, C, D).--This pateIlar ligament, which inserts on the pateliar crest muscle originates by fleshy fibers from the ventro- of the tibiotarsus. lateral surfaceof the preacetabularilium from the tip M. femorotibialismedius (Fig. 2B).--The origin is of the cranial iliac processcaudally for about 4 min. continuous with that of M. femorotibialis extemus It lies deep to M. iliotrochantericuscaudalis and cra- from the craniomedialsurface of the femur just distal nial to M. iliotrochantericus medius. The narrowly to the trochanter.The unipinnate belly extendsdown fan-shaped belly tapers and fuses with that of M. the craniomedialsurface of the thigh, its deep fibers iliotrochantericus medius a short distance proximal being closelyassociated with those of M. femorotib- to their insertion. The common insertion is by a flat ialis externus. Its fibers insert on an aponeurosisthat tendon onto the lateral surface of the fernoral tro- arises from its roedial surface. Toward the distal end chanter just distal to that of M. iliotrochantericus of the femur the aponeurosisfuses with the caudo- caudalis. medial surface of M. femorotibialis extemus, and M. iliotrochantericusmedius (Fig. 2B).--This arises contributesto the pateliar ligament. by fleshy fibers from the ventrolateralborder of the M. femorotibialisinternus (Fig. 2B).--This arises preacetabular ilium caudal to M. iliotrochantericus from the roedial shaft of the femur just distal to the cranialis. The narrowly fan-shaped belly fuses with insertion of M. iliofemoralis intemus to the distal that of the latter muscle; their common insertion is end of the medial fernoralcondyle. A few fibers arise described above. from the surface of M. pubo-ischio-femoralisat its M. iliofemoralisexternus (Fig. 2C).--The origin is insertion on the fernoral shaft. The belly extends fleshy from the dorsal crestof the synsacrumcaudal down the roedial surfaceof the thigh, caudal to that to M. iliotrochantericus caudalis, the dorsal iliac of M. femorotibialis medius, the medial surface of crest, and the caudomedial surface of the iliac fossa. its distal half coveredby a dense aponeurosis.It in- The large, fan-shaped belly extends laterodistally serts by a short, strong tendon on the roedial end of and tapers to a flat tendon that inserts on the cau- the pateliar crestof the tibiotarsus,just roedial to the dolateral surface of the fernoral trochanter, superfi- insertion of the pateliar ligament. cial to the tendon of M. obturatorius medialis and M. iliofibularis(Fig. 2A, C; Fig. 4C, D).--The origin caudal to that of M. iliotrochantericus caudalis. Dis- is by fleshy fibers from the entire postacetabular tally M. iliofemoralis extemus lies deep to the cranial wing of the ilium, and aponeuroticallyfrom the cau- border of M. iliofibularis. This muscleis unusually dal end of the dorsal iliac crest; this aponeurosisis large in Colius compared to its condition in most continuous with that of M. iliotibialis lateralis. The birds. fan-shaped belly covers the lateral surface of the A wide, flat ligament lies superficial to the inser- thigh caudalto M. iliotibialis lateralisand cranialto tion of this muscle. This ligament passesfrom the M. flexor cruris lateralis. It lies superficial to the cau- ilium at the dorsocranial comer of the ilioischiadic dal border of M. iliofemoralis extemus, to Min. is- foramen to the femur, where it attaches between the chiofemoralis and caudofemoralis, to the distal end insertions of Min. iliofemoralis externus and iliotro- of M. flexor cruris lateralis, and to the origin of M. January1982] MousebirdHindlimb Myology 45 flexor hallucis longus. M. iliofibularis tapers to a strong, round tendon that passesthrough the biceps FCL•P Xi'. , loop (ansa M. iliofibularis), entering the shank between Min. gastrocnemius pars lateralis and flexor hallucis longus. It inserts on the iliofibular tubercle of the fibula. The ansa M. iliofibularis consists of three arms-- two fernoraland one fibular. The proximal fernoral arm is attached to the lateral fernoral shaft about 4 mm from the distal end of the bone. It lies just lateral to the origin of M. flexor digitorum longus, and passesroedial to the tendon of M. iliofibularis. The distal fernoralarm passeslateral to the tendon of M. iliofibularis and attaches to the caudolateral surface of the fernoralcondyle about 2 mm distal to the proximal fernoral arm. The fibular arm is attached to the GM cranial surfaceof the fibula just distal to its head. It is fused with the tendon of the fibular (distal) head Fig. 3. Medial view of the distal thigh and prox- of M. flexor perforatusdigiti III, and with the distal imal shank of Coliusstriatus showing the insertion head of M. flexor perforatusdigiti IV, then passes of M. flexor cruris lateralispars pelvica on the tibi- lateral to the iliofibularis tendon and joins the two otarsus. Its action as a flexor of the shank, as well as fernoralarms as they form a sling around the tendon. retractorof the femur, may be relatedto the hanging M. flexorcruris lateralis (Fig. 2A, B, C; Fig. 3; Fig. postureof mousebirds.Abbreviations are given with 4B).--Pars pelvica arises from an aponeurosis that Fig. 2. extends between the transverseprocesses of the first three free caudal vertebrae and from the terminal processof the ilium. The large, parallel-fiberedbelly the ischial body. A few fibers arise from the caudal lies on the lateral surface of the thigh caudal to M. end of the dorsolateral crest of the ilium. The caudal iliofibularis, cranial to M. flexor cruris medialis, and head arises fleshy from the caudolateraledge of the superficialto Min. pubo-ischio-femoralisand cau- ischium. The parallel-fiberedbelly is about 7 mm dofemoralis.About 10 mm caudalto the knee a lig- wide and extends cranially to insert by an aponeu- amentousraphe separatespars pelvica from pars ac- rosison the posterolateralsurface of the fernoralshaft cessoria. An extension from the caudal end of the for about 6 mm distal to the trochanter. raphe runs distally to fuse with the aponeurosison M. flexor cruris medialis(Fig. 2A, B, C; Fig. 3).-- the medial surfaceof M. gastrocnemiuspars inter- This muscle arises by fleshy and short, tendinous media. The main belly (pars pelvica) continuesdis- fibers from the ventrolateraledge of the caudal end tally from the raphe and narrows to a thin, flat ten- of the pubis for about 10 mm. The cranial edge of its don that passes into the shank lateral to M. origin lies deep to M. ischiofemoralis.The strap-like gastrocnemiuspars medialis and medial to the ac- belly extends distally as the most caudal of the thigh cessorybelly and pars media to insert by a tendon muscles.Its cranial border lies deep to M. flexor cru- about 3 mm wide on the medial surface of the tibio- ris lateralis.It givesrise to a flat tendon, about3 mm tarsus about 4 mm from its proximal end. Pars ac- wide, that entersthe shankbetween Mm. gastrocne- cessoriainserts by fleshy fibers on the caudalsurface mius intermedia and mediaIls. The tendon inserts of the femur for about 5 mm proximal to the condyles on the tibiotarsusabout 8 mm from its proximal end. (Fig. 2C). M. pubo-ischio-femoralis(Fig. 2B, D).--There are M. caudofemoralis(Fig. 2A, B, C).--M. iliofemor- three bellies, all of which arise from a dense apo- alis is lacking. M. caudofemoralisarises by an apo- neurosisextending from the ventraledge of the body neurosis from the ventrolateral surface of the caudal of the ischium to the adjacent surfaceof the pubis. end of the baseof the pygostyle.The strap-likebelly, The origin of the lateralbelly (parslateralis) extends about 4 mm wide, extends cranially to enter the for about 4 mm caudal to the obturator foramen. A thigh. It lies superficial to M. ischiofemoralis and smaller,caudal belly (parsaccessoria) originates from deep to Mm. iliofibularis and flexor cruris lateralis. the aponeurosisjust caudal to the lateral head for It tapers to a flat tendon about 2 mm wide that inserts about 3 min. The medial belly (pars mediaIls) orig- on the caudal surfaceof the femur about halfway inatesby an extensionof the aponeurosis,immedi- down the shaft. ately deep to both lateraland caudalheads. All three M. ischiofemoralis(Fig. 2B, C, D).--This largemus- are parallel-fiberedbellies. The lateralbelly extends cle arises by two heads. The cranial head arises by distally deep to Mm. ischiofemoralisand caudofem- fleshy fibers from the craniolateral surface of the oralis, and insertsby fleshy fibers on the caudal sur- wing of the ischium, and from the lateral surface of face of the femoral shaft, beginning about midway 46 BERMANAND RAIKOW [Auk, Vol. 99 down its length and extending down to the medial flat tendon that arises from the aponeurosis.The ten- surface of the medial condyle. The aponeurotic in- don continues to receive fibers on its medial surface sertion on the condyle is medial to the origin of M. after it has passedthrough the obturator foramen. It flexor cruris lateralis pars accessoria. extends laterally, passesdeep to the tendon of M. The medial belly extendsimmediately deep to the iliofemoralis externus, and inserts on the lateral sur- lateral belly and inserts medial to it on the caudal face of the proximal end of the femur just proximal surface of the femoral shaft. Its insertion ends just to that of M. iliotrochantericus caudalis. proximal to the medial condyle. The proximal half of M. iliofemoralisinternus (Fig. 2B, D).--M. iliofem- the insertion is aponeurotic, and the distal half is oralis internus arises by fleshy fibers from a small fleshy (entirely fleshy in C. leucocephalus). area on the dorsal surface of the ilium between the The accessorybelly remains on the same plane as iliosynsacralsuture and the ventral edge of the ilium the lateral belly, but extends distally to insert by a about 4 mm from the cranial border of this bone. It short, wide tendon onto the proximomedial corner extendslaterally as a band, less than 2 mm wide, to of the tibiotarsus, deep to the insertion of M. gas- insert fleshy on the medial surfaceof the femur about trocnemius pars intermedia. This belly appears to 3 mm from its proximal end. The muscle lies deep have no known counterpart in other birds (see Dis- to M. iliofemoralis externus. Caudally it is bordered cussion). by the insertion of M. ischiofemoralis. M. obturatoriuslateralis (not shown).--Pars dorsa- M. gastrocnemius(Fig. 3; Fig. 4A, B, C).--There are lis is absent. Pars ventralis arises fleshy from the three independentbellies. Parslateralis is by far the ventral and cranial margin of the lateral surface of largestof the bellies.It arisesby a strong,flat tendon the obturator foramen. It extends laterally to insert from the lateral epicondyleof the femur and the lat- by fleshy fibers on the caudal surfaceof the proximal eral surfaceof the distal arm of the biceps loop. Dis- end of the femur, just distal to the trochanter. The tally, the tendinous origin is continuous with an insertion is distal to that of M. obturatorius medialis, aponeurosison the medial surfaceof the muscle.The proximocaudalto that of M. iliofemoralis internus, fusiform belly extendsdown the caudolateralsurface and medial to that of M. ischiofemoralis. of the shank. It is bordered cranially by Mm. flexor M. obturatoriusmedialis (Fig. 2B, D).--This well- perforanset perforatusdigiti II and flexor perforans developed, fan-shaped muscle occupies the entire et perforatusdigiti III. M. flexor hallucislongus is medial surface of the postacetabularilium and the visible medially between pars lateralis and pars in- ischiopubic fenestra. The main part arises fleshy termedia and mediaIls. Distally pars lateralis tapers from the medial surfaces of the ischiopubic mem- to a very strong,broad tendon that fuseswith those brane and wing of the ischium, and from the caudal of pars intermedia and medialis about 5 mm from and ventral borders of the ilioischiadic foramen. Its the distal end of the tibiotarsus to form the common dorsalmostfibers are visible laterally through the il- tendon of insertion. ioischiadic foramen. A fairly distinct ventral part Pars intermedia arisesby fleshy and tendinous fi- (much more discrete in C. leucocephalus)arises by bers from the caudomedial surface of the median fleshy fibers from the ventral and medial bordersof femoral condyle.The weakly developedfan-shaped the pubis adjacent to the cranial half of the ischio- belly passesdistad for about 12 mm before tapering pubic fenestra.Both parts convergecranially toward to form a flat tendon that fuses with an aponeurosis the obturator fenestra, and extend through the ob- on the caudal surface of pars medialis. This tendon turator foramen, their fibers inserting on a strong, actually arises from the ligamentousraphe that sep-

Fig.4. A.Lateral view of the shank ofColius striatus. Note the extensive origin of'M. flexor hallucis longusfrom the femoralshaft and the absenceof the longtendon of M. fibularislongus. B. Medialview of the shank.C. Lateralview of the shankshowing the retinaculumfor the tendonof M. tibialiscranialis caput femoraleand ansaM. iliofibularis.The followingmuscles shown in Part A havebeen removed:M. tibialis cranialisand M. gastrocnemiuspars lateralis. D. Lateralview of the shankshowing the deepmuscles and the three arms of ansaM. iliofibularis.The following musclesshown in Part C have been removed:M. flexor perforanset perforatusdigiti II and M. flexorperforans et perforatusdigiti III. Abbreviations:AIF, ansaM. iliofibularis;EDL, M. extensordigitorum longus; FB, M. fibularisbrevis; FDL, M. flexordigitorum longus; FHL, M. flexorhallucis longus; FL, M. fibularislongus; FPD3, M. flexorperforatus digiti III; FPD4,M. flexor perforatusdigiti IV; FPPD2,M. flexorperforans et perforatusdigiti II; FPPD3,M. flexorperforans et perforatusdigiti III; GI, M. gastrocnemiuspars intermedius;GL, M. gastrocnemiuspars lateralis;GM, M. gastrocnemiuspars mediaIls; R, retinaculum;TC, M. tibialiscranialis; TCF, M. tibialiscranialis caput fern- orale; TIC, tibial cartilage. January1982] MousebirdHindlimb Myology 47

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PD3 48 BERMAIq^ND R^•I•OW [Auk, Vol. 99 aratespars pelvica from pars accessoriaof M. flexor daily it merges with the lateral semilunar cartilage. cruris lateralis. Pars accessoriaand pars intermedia Two flat ligaments extend from the retinaculum me- are closely associatedat this point. Pars intermedia dially, acrossthe interior of the joint. One attaches passesmedial to M. flexorcruris medialis and lateral to the medial semilunar cartilage, the other to the to M. flexor cruris lateralis. craniomedialcorner of the tibiotarsus,just caudal to Parsmedialis arisesby fleshy and tendinousfibers the pateliar crest. After crossingthe knee the femoral from the craniomedial corner of the pateIlar crest of head extends down the craniolateral surface of the the tibiotarsus,just distal to the insertionof M. fem- shank, deep to the tibial head. About 8 mm proximal orotibialis internus, from the caudomedial surface of to the end of the tibiotarsus the two heads fuse and M. tibialis cranialis,and by a weak aponeurosisfrom taper to a very broad tendon. The tendon is held the medial surfaceof the proximal two-thirds of the against the cranial surface of the bone, along with tibiotarsus. A few fasicles also arise from the surface that of M. extensor digitorum longus, by a strong of M. femorotibialis internus at its insertion. The ligamentum transversum.As it crossesthe intertarsal unipennate belly is the most superficialmuscle on joint, the tendon turns slightly medially to insert on the medial surface of the shank. The fibers give rise the tuberosity of M. tibialis cranialis, about 4 mm to a tendon on the muscle's caudal border. This ten- from the proximal end of the tarsometatarsusand don arisesin part from an aponeurosison the medial just deep to the extensordigitorum longus tendon. surface of the muscle, and in part from the tendon M. fibularis longus (Fig. 4A).--Commonly also of pars intermedia. About 5 mm from the end of the called peroneus longus, this muscle overlies the lat- tibiotarsusit joins the tendonof parslateralis to form eral surface of M. tibialis cranialis. It is bordered the common tendon of insertion. caudally by M. flexor perforans et perforatus digiti The tendon of insertion of M. gastrocnemius III. M. fibularis longus arisesby an aponeurosisfrom passesover the tibial cartilage, attaching to its lateral the lateral corner of the patellar crest and the lateral and medial margins,thus forming a superficialcom- surfaceof the proximal third of M. tibialis cranialis. partment for the flexor tendons. It crossesthe inter- The cranial portion of the aponeurosis extends fur- tarsal joint and attachesto the lateral and medial ther distally than the caudal portion. The flat, par- margins of the hypotarsus,superficial to the flexor allel-fibered belly extendsalong the middle third of tendons. Distal to the hypotarsusit thins, but con- the shank, then tapers to a narrow tendon that in- tinues along the plantar surfaceof the tarsometatar- serts on the proximolateral corner of the tibial car- sus, having attachmentsalong the lateral and medial tilage. In most birds a branch of the tendon passes borders of this bone. About halfway down the length to the plantar surfaceof the tarsus,where it joins the of the tarsometatarsus a few fibers of M. flexor hal- tendon of M. flexor perforatus digiti III. Such a lucis brevis arise from the deep surfaceof the medial branch is lacking in Colius. border of the tendon. Distally the medial margin of M. extensordigitorum longus (Fig. 4C, D; Fig. 5; Fig. the gastrocnemiustendon thickens and runs deep to 8A).--This muscle lies deep to M. tibialis cranialis the lateral border of M. extensorhallucis longus. The and is bordered mediafly by M. gastrocnemiuspars lateral margin of the tendon of insertion in the distal medialis. It arises by fleshy fibers from the pateIlar third of the tarsometatarsusgives rise to a significant crest and the cranial and lateral cnemial crests of the number of fibers of the adjacentM. abductor digiti tibiotarsus, from the proximal third of the craniolat- IV. The tendon actsas a superficialaponeurosis cov- eral and craniomedial borders of the tibiotarsus, and ering lateral, medial, and plantar surfacesof the dis- from a raphe separating it from M. gastrocnemius tal end of the tarsometatarsus. pars medialis. The bipennate belly extendsdown the M. tibialiscranialis (Fig. 4).--This is a large, fusi- cranial surface of the tibiotarsus and tapers to a flat form musclelying superficiallyon the cranial surface tendon about 13 mm from the end of this bone. The of the shank. It is bordered medially by M. gas- tendon passesthrough the ligamentum transversum trocnemius pars medialis and laterally by the apo- deep to that of M. tibialis cranialis, and then through neurosis of origin of M. fibularis longus. M. tibialis a bony canal just proximal to the condyles. It then cranialis arisesby two heads. The tibial head (caput crossesthe intertarsaljoint, passesthrough another tibiale) arisesby fleshy fibers from the entire patellar bony canal on the cranial surface of the proximo- crestof the tibiotarsus,just distal to the insertionof medial corner of the tarsometatarsus, and extends the patellar ligament. Its lateral margin is deep to the along the cranial surface of the tarsometatarsus. aponeurosisof origin of M. fibularis longus. The About 10 mm from the distal end of the bone it gives femoral head (caput femorale) arises by a ligament off a medial branch to the hallux, a very unusual from the cranial surface of the lateral femoral con- condition among birds (see Discussion). After a dyle. As it passesacross the craniolateralsurface of short distance the main tendon bifurcates, sending the knee it is held in place by a retinaculum (Fig. a lateral branch to digit IV and a medial branch to 4C, D). Laterally and medially this retinaculum is the area between digits II and III. At the distal end reinforced by small sesamoidbones. It has a strong of the tarsometatarsus this medial branch bifurcates, lateral attachment to the head of the fibula, and cau- sending branchesto digits I! and III. January1982] MousebirdHindlimb Myology 49

The branch to the hallux extends to the proximal end of metatarsal I, where it is held in place by a ligamentousband. Near the distal end of this element, a secondligamentous band holdsthe tendon in place. It crossesthe metatarsal-phalangealjoint and passesthrough a third ligamentousband on the base of the first phalanx. The tendon inserts on a fibrouspad on the cranialsurface of the distal end of the first phalanx. The fibrous pad arises as a tendon from the cranial surfaceof the first phalanx about 2 mm from its distal end, deep to the tendon of M. extensordigitorum longus. It insertson the baseof the secondphalanx, after receivingthe insertionof the latter muscle. The branchto digit II crossesthe secondmetatar- sal-phalangealjoint and extendsbeneath a ligamentous band on the cranial surface of the base of the seconddigit. It is accompaniedby a smallertendon that arises from the branch to digit III. This smaller tendon extendsalong the cranialsurface of the first phalanx, superficialto the main branch to digit II, and ends as an expansionover the first interphalangealjoint. The main branchto digit II perforates this expansionand emergeson the cranialsurface of the second phalanx. It sends an attachment across the lateral surfaceof the first interphalangealjoint to insert on the joint pad on the plantar surface.The tendon continuesalong the cranial surfaceof digit II and inserts on a fibrous pad on the secondinter- phalangealjoint, in the samemanner as the tendon to the hallux. The branch to digit III is formed by extensions from both lateral and roedial divisions of the main tendon. It extendslaterally, acrossthe third metatarsal-phalangealjoint. In additionto the smalltendon given off to digit II, arisingfrom the medial extension is a narrow band extending to the ligamentous band that holds the tendonsin placeon the base of the seconddigit. About halfway along the cranial surface of the first phalanx the branch to digit III Fig. 5. Dorsalview of the left foot of Coliusstria- bifurcates into lateral and roedial divisions. The two tus showingthe divisionsof the tendonof M. exten- divisions extend along lateral and roedial borders, sordigitorum longus. Note the branchto the hallux, respectively,of the cranialsurface of the third digit. which has previouslybeen describedonly in parrots. They expandover the surfacesof the firstand second interphalangealjoints, forming attachmentsto the joint pads on the plantar surfaceas well as to each the main tendononto the plantarsurface of the distal other. Toward the distal end of the third phalanx end of the tarsometatarsus. The two branches unite they turn toward the center of the cranial surface, on the cranial surfaceof the baseof the first phalanx. and fuse. The tendon inserts on a fibrous pad at the As they do so, they form a sheatharound the con- third interphalangealjoint, in the same manner as tinuation of the main tendon. This accessorytendon the tendons to digits I and II. extendsalong the craniomedialsurface of the fourth There are actuallytwo tendonsof the EDL to digit digit, expandingand forming attachmentsat first, IV. One arises as a continuation of the main tendon second, and third interphalangeal joints. Distal to and crossesthe metatarsal-phalangealjoint, extend- the third interphalangealjoint, it becomesvery nar- ing onto the craniolateralsurface of the firstphalanx. row and tums onto the cranial surface of the fourth The other, more superficial, accessorytendon arises digit to inserton a fibrouspad at the fourth inter- from the union of two branches: a medial branch phalangealjoint. from the most proximal part of the branch to digit The continuation of the main tendon extends as a III, and a lateral branch from a broad extension of narrow band along the craniolateralsurface of digit 50 BERMANAND RAIKOW [Auk, Vol. 99

W, passing beneath ligamentous bands at each of of the shank, caudal to M. flexor perforans et per- the first three interphalangealjoints. Distal to the foratusdigiti III. It arisesfrom the superficialsurface third joint it expands and tums onto the cranial sur- of the caudal limb of the latter muscle's tendon of face of digit IV to insert on the fibrous pad at the origin, from the caudolateralsurface of the lateral fourth interphalangealjoint, just lateral to the inser- femoral condyle, just distal to the distal limb of the tion of the accessorytendon. The attachmentsof the ansaM. iliofibularis, and from the superficialsurface fibrous pad are as thoseof digits I, II, and III. of the aponeurosisof origin of M. flexor perforatus M. fibularis brevis (Fig. 4A, C, D).--Often called digiti IV. The belly is parallel-fiberedproximally, peroneus brevis, this muscle arises by fleshy and becomingbipennate distally. It extendsone-third of tendinous fibers from the distal end of the fibula and the way down the shank before tapering to a flat from the craniolateral surface of the tibiotarsus from tendon. At the distal end of the tibiotarsus the ten- just distal to the insertion of M. iliofibularis to about don turns caudallyand passesthrough a superficial 4 mm from the end of this bone. The roughlybipen- compartmentin the tibial cartilage,lying roedial to nate belly lies deep to M. tibialis cranialis. About 3 the tendon of M. flexor perforanset perforatusdigiti mm from the distal end of the tibiotarsus, M. fibu- III and superficialto that of M. flexorperforatus digiti laris brevistapers to a flat tendonthat passesthrough II. As it crosses the intertarsal joint and passes a retinaculum on the craniolateral surface of the tib- through a fibrouscanal in the hypotarsus,it lies lat- iotarsusjust proximal to the condyle. It crossesthe eral to the tendon of M. flexorperforatus digiti II and intertarsal joint and turns onto the plantar surfaceof roedial to that of M. flexor perforans et perforatus the tarsometatarsusto insert on the proximolateral digiti III. It extends down the plantar surfaceof the corner of the hypotarsus. tarsometatarsus,turning to lie superficial and then M. flexor perforanset perforatusdigiti III (Fig. 4A, deep to the tendon of M. flexor perforatusdigiti II. C).--This is a superficialmuscle on the lateral surface At the distal end of the tarsometatarsus it turns me- of the shank. It lies superficialto M. fibularislongus dially and crossesthe metatarsal-phalangealjoint of and cranialto Mm. flexorperforans et perforatusdig- the seconddigit. About halfway down the plantar iti II and gastrocnemiuspars lateralis. It arises by surface of the first phalanx the tendon is perforated two short tendons, one from the sesamoid bone of by that of M. flexor digitorum longus. Resulting lat- the retinaculum for the tendon of the femoral head eral and roedial branches extend distally to insert on of M. tibialis cranialis, the other from the caudolat- caudolateraland caudomedialsurfaces, respectively, eral surface of the lateral fernoral condyle. As the of the fibrous pad on the plantar surfaceof the first two tendonsjoin they overlie the head of the fibula. interphalangealjoint. The roedial branch is some- The deep surfaceof the tendon provides the surface what larger than the lateral. The tendon of M. flexor of origin for part of M. flexor perforatusdigiti W. perforans et perforatus digiti II does not perforate The parallel-fibered belly of M. flexor perforans et that of M. flexor perforatusdigiti II as it doesin some perforatus digiti III extends down the shank super- other groupsof birds. ficial to M. flexorperforatus digiti IV. About halfway M. .flexorperforatus digiti IV (Fig. 4C, D).--There down the shank it tapers to a flat tendon that turns are two headsof origin. The proximal (femoral)head caudad and passesthrough a superficialcompart- arisesby a long, flat tendonshared with the proximal ment in the tibial cartilage, lateral to the tendon of head of M. flexor perforatusdigiti III, from the cau- M. flexorperforans et perforatusdigiti II and roedial domedial surface of the lateral fernoral condyle. It to that of M. flexorperforatus digiti IV. It crossesthe lies just distal and medial to the distal fernoral arm intertarsaljoint superficialto the tendon of M. flexor of the ansa M. iliofibularis. The tendon extends deep perforatus digiti III and runs through a shallow to the fibular arm of the latter. The distal (fibular) groove in the hypotarsus. As the tendon extends head arisesfrom an aponeurosisshared with the dis- down the plantar surface of the tarsometatarsusit tal head of M. flexor perforatus digiti III. This apo- tums to lie deep to that of M. flexorperforatus digiti neurosisoriginates from the lateralmargin of the fib- III. About 2 mm from the distal end of metatarsal III ular head. It extends as a broad sheet superficial to it perforatesthe tendon of M. flexor perforatusdigiti the fibular arm of the ansa M. iliofibularis, to which III. It crossesthe metatarsal-phalangealjoint, extend- it has attachments. The tendon of insertion of M. ing onto the plantar surfaceof digit III. Justdistal to iliofibularispasses between the proximal and distal the first interphalangealjoint the tendon is held in heads of M. flexor perforatus digiti IV about 6 mm place by a ligamentousband as it is perforated by from the proximal end of the fibula. The two parallel- the tendon of M. flexor digitorum longus.The lateral fibered bellies extend distal, the proximal head lying and medial branches thus formed insert on lateral caudal to the distal head. As a whole, the muscle lies and medial surfaces,respectively, of a fibrous pad superficialto the cranial part of M. flexor perforatus on the plantar surfaceof the second interphalangeal digiti III. About halfway down the shank(one-third joint. in C. leucocephalus)the bellies fuse and taper to a M. flexor perforanset perforatusdigiti II (Fig. 4A, flat tendon. The tendon passesthrough a superficial C).--This is a superficialmuscle on the lateral surface compartment in the tibial cartilage and crossesthe January1982] MousebirdHindlimb Myology 51

intertarsaljoint, lying lateralto that of M. flexorperforans et perforatusdigiti III and superficialto that of M. flexor perforatus digiti III. Maintaining the same relationships to these tendons, the tendon runs througha shallowgroove in the hypotarsusand extends along the plantar surfaceof the tarsometatarsus as the most lateral of the long flexor tendons. It passesthrough a ligamentousband at the distal end of the tarsometatarsus,adjacent to digit IV, and as FHL it crossesthe metatarsal-phalangealjoint it bifurcates.Both lateral and medial branchespass through a thick, ligamentousband on the plantar surfaceof the first interphalangealjoint, superficialto the tendon of M. flexordigitorum longus. The tendonof M. flexordigitorum longus passes between them as they emerge on the plantar surfaceof the secondphalanx. The lateral branchinserts on the proximolateralcor- ner of the secondinterphalangeal pad. The medial branch inserts on the medial corner of the base of the fourth phalanx. M. flexorperforatus digiti III (Fig. 4C, D).--This lies deep to M. flexorperforatus digiti W and superficial to Mm. flexor perforatusdigiti II and flexor hallucis longus. The muscle has two bellies. The proximal belly originates in common with the proximal head of M. flexorperforatus digiti W by a long, flat tendon from the intercondylararea, lateral to the origin of M. flexor hallucis longus and medial to the distal Fig. 6. Medial view of the shank of Coliusstriatus femoral arm of the ansaM. iliofibularis. The parallel- showing the two headsof M. flexorhallucis longus. fibered belly developsabout 5 mm distal to the ori- Note the extensiveorigin of the proximalhead from gin. The smaller distal belly arises proximally by a the fernoral shaft. Abbreviations are as in Fig. 4. long tendon (13 mm) in common with that of the distal head of M. flexor perforatusdigiti IV. Distally it arises from an aponeurosison the medial surface origin of M. flexor perforatusdigiti IV. The distal of the fibularis brevis. Its parallel-fibered belly be- head lies superficialto the proximal head. About comes closely associatedwith that of the proximal one-third of the way down the shank the two heads belly about 9 mm from the distal end of the tibio- fuse and taper to a slender tendon that runs super- tarsus. The two bellies fuse near the intertarsal joint. ficial to M. flexordigitorum longus and cranialto M. The tendon passesthrough the lateralmostcompart- flexor hallucislongus. It passesthrough the tibial ment of the tibial cartilage, crossesthe intertarsal cartilage, crossesthe intertarsal joint, and passes joint, and extendsover a shallowgroove in the hy- through a fibrous canal in the hypotarsus.As it ex- potarsus.It runs medial and then superficialto the tends along the plantar surfaceof the foot, it lies first tendon of M. flexorperforans et perforatusdigiti III. medial to the tendon of M. flexor perforanset per- As it crossesthe metatarsal-phalangealjoint it is perforatus digiti II, then crossesit superficially to lie forated by the tendons of Mm. flexor perforans et lateral to it. The tendon inserts on the caudolateral perforatusdigiti III and flexordigitorum longus.The corner of the base of the proximal phalanx of digit lateral and roedial branches thus formed extend dis- II. It is not perforatedby the tendonsof Mm. flexor tad to insert on lateral and medial surfaces,respec- perforanset perforatusdigiti II or flexor digitorum tively, of the first interphalangealjoint pad. longus as in some birds. M. flexor perforatusdigiti II (not shown).--This M. flexorhallucis longus (Fig. 2C, Fig. 4, Fig. 6, Fig. small muscle is visible on the lateral surface of the 7).--This muscle lies on the caudal surface of the shankbetween the two headsof M. flexor perforatus shank,superficial to M. flexordigitorum longus. The digiti III. There are two heads of origin. The more origin is by two heads. The proximal head arises by proximal head arisesby fleshy fibers from the caudal fleshy fibers from the caudal surfaceof the femur in surfaceof the lateral femoral condyle, the caudolat- the distal half of the shaft (an unusually extensive eral corner of the tibiotarsus, and the adjacenthead origin) in the intercondylararea. The distalhead aris- of the fibula. The distal head arisesby a 4 mm long, es by a tendon from the intercondylararea. The two slender tendon from the deep surfaceof the fibular headsfuse about halfway down the shank, their fi- arm of ansa M. iliofibularis and from the tendon of bers converging on a tendon that arises on the mus- 52 gERMAN AND RAIKOW [Auk, Vol. 99

one-third of the way down the shank. The common belly is bipennate, its fibers inserting on a tendon that developson its caudal surface.About 6 mm from the distal end of the tibiotarsus the muscle tapers to a flat tendon that extends distally to run through the tibial cartilage. The tendon of this muscleis the most medial of the flexor tendons. It crosses the intertarsal joint and passesthrough a superficialfibrous compartment in the medial side of the hypotarsus. As it extends along the caudal surface of the foot, it lies medial and superficialto the tendon of M. flexor hallucis longus. About one-third of the way down the tarsometatarsusthe tendons of Mm. flexor digitorum longus and flexor hallucis longus fuse. The common tendon then divides to send a branch to each of the four digits, making it Type V of Gadow's (1893-1896) classification. The distribution of the branch tendons is described below. Flexor hallucis longus/flexordigitorum longusinser- tion.--The common tendon of these two muscles divides into four branches. The branch to digit I (the hallux) arises from the medioplantar surface of the tendon and runs superficialto the branch to digit II. The branchesto digits II, III, and IV arisefrom about the sameplane, slightlydeep to the branchto digit I. The branch to the hallux extends along a groove in the lateral surface of the first metatarsal, and is Fig. 7. Dorsal (left) and ventral (right) views of held in place by a retinaculum. The tendon lies su- the flexor hallucis longus/flexordigitorum longus perficial to that of M. flexor hallucis brevis. It crosses tendon in the right foot of Coliusstriatus. Although the medial surfaceof the metatarsal-phalangealjoint the tendons do fuse, making it type V in Gadow's and passesdown the plantar surface of the proximal classification,branches to digits II, III, and 1V are in phalanx. It is enclosed in a fibrous sheath in the the same plane, separatefrom that of the branch to proximal two-thirds of the bone. Distally the deep the hallux. Abbreviations are as in Fig. 4. surface of the tendon gives rise to a vinculum that extends distally to insert on the interphalangealjoint pad. The tendon passesthrough a retinaculum and cle's craniolateralsurface. The belly ends about 9 mm inserts on the plantar surfaceof the base of the ter- from the distal end of the tibiotarsus. The very large, minal phalanx (flexor tubercle). flat tendon passesthrough a deep compartmentin The branch to digit II arisesfrom the main tendon the tibial cartilagelateral to that of M. flexor digito- deep to the branch to digit I and medial to the rum longus. It crossesthe intertarsaljoint, passes branches to III and IV. It extends through a cartilag- through a deep, fibrous compartmentin the hypo- inous canal to the distal end of the dorsal surface tarsus,and emergeson the plantarsurface of the foot of the metatarsal II, and then crossesthe metatarsal- as the deepestof the long flexor tendons.About one- phalangealjoint, lying in a grooveformed by the two third of the way down the tarsometatarsusthe ten- condyles on the proximal end of the first phalanx. dons of this muscleand M. flexor digitorum longus The tendon perforatesthat of M. flexor perforans et fuse. The distribution of the branches of the fused perforatus digiti II before reaching the first inter- tendons is described below. phalangealjoint. It passesthrough a fibrous sheath M. flexordigitorum longus (Fig. 4B, Fig. 6, Fig. 7).-- on the proximal two-thirds of the secondphalanx. This muscle lies deep to M. flexor hallucis longus As it approachesthe end of the secondphalanx, the and is the deepest muscle on the caudal surfaceof deep surfaceof the tendon gives rise to a vinculum the shank. There are two headsof origin. The lateral that extendsdistally to insert on a fibrouspad on the head arisesby fleshy fibers from the caudalsurface dorsal surface of the second interphalangealjoint. of the fibula. The medial head arisesby fleshy fibers The tendon inserts on the flexor tubercle at the base from the caudal and medial surfaces of the tibiotar- of the terminal phalanx. sus, and the flexor fossa to about halfway down the The branch to digit III passesthrough a cartilagi- length of the bone. It runs lateralto the tendonof M. nous canal at the base of the third digit and crosses iliofibularis and Mm. flexor cruris medialis and gas- the metatarsal-phalangealjoint, extending onto the trocnemiuspars mediaIls.The two belliesfuse about plantar surfaceof the proximal phalanx.The tendon January1982] MousebirdHindlimb Myology 53 perforatesthat of M. flexorperforatus digiti III about A B halfwaydown the phalanx.At the baseof the second phalanxit perforatesthe tendon of M. flexor perforans et perforatusdigiti III. The tendon of M. flexor digitorum longus is held in place at the interphalangeal joints by ligamentousbands. Toward the middle of the third phalanxa vinculum arisesfrom the deep surfaceof the tendon. It extendsdistally to insert on the third interphalangealjoint pad. The main tendon inserts on the flexor tubercle at the base of the terminal phalanx. The branchto digit IV passesthrough a cartilagi- •EHLA nous canal at the base of digit IV onto the dorsal surface of digit IV. About halfway down the first phalanxit perforatesthe tendon of M. flexor perforatus digiti IV. It continuesalong the plantar surface of the digit, being held in place at each interphalangealjoint by ligamentousbands and by a fibrous sheath on the surfaceof digit IV. The tendon inserts on the flexortubercle at the baseof the terminalpha- lanx. A vinculumfrom its deep surfaceinserts on the distalinterphalangeal joint pad as in the other digits. M. flexorhallucis brevis (Fig. 8B).--This bipennate Fig. 8. A. Dorsal view of the left foot of Colius musclelies on the plantar surfaceof the tarsometa- striatus showing two muscles not previously de- tarsus medial to the flexor digitorum longus/flexor scribed in birds, Mm. extensorhallucis longus pars hallucis longus tendon. It has an extensiveorigin accessoriusand extensorproprius digiti IV. Mm. ex- from the medial hypotarsalcrest, medial half of the tensor hallucis longus pars distalis and extensor flexor sulcus,and the medial plantarcrest. About 6 brevis digiti IV are unusually large and have under- mm from the distal end of the tarsometatarsus the gone changes in their insertions. These deviations belly gives way to a flat tendon that passesalong a from the typical avian condition are related to their groove in the lateral surface of the first metatarsal. functions. B. Plantar view of the left foot. Mm. flexor It is held in placeat the baseof this bone by a reti- hallucisbrevis and abductor digiti IV are well-de- naculum,and insertson the plantarsurface of the base veloped and have undergoneslight changesin in- of the proximalphalanx of the hallux.Throughout its sertion associated with their modified functions. course this tendon remains entirely separatefrom Abbreviations: ABD4, M. abductor digiti IV; EBD4, that of M. flexor hallucislongus. M. extensorbrevis digiti IV; EDL, M. extensordig- Mm. extensorhallucis longus and extensorhallucis itorum longus; EHLA, M. extensorhallucis longus longusaccessorius (Fig. 8A).--Pars proximails, the accessorius;EHLD, M. extensorhallucis longus pars major and often only componentof this musclepres- distalis;EPD3, M. extensorproprius digiti III; EPD4, ent in many birds, appearsto have been lost in Co- M. extensorproprius digiti IV; FHB,M. flexorhallucis lius, exceptthat its tendon of insertion may be rep- brevis; TC, M. tibialis cranialis. resented by the branch of the extensor digitorum longus tendon to the hallux (see Discussion). Pars distalis is a roughly unipennate muscle originating accessorybelly of M. extensorhallucis longus be- by fleshyfibers from the craniomedialsurface of the causeof its positionand becauseM. extensorhallucis distal three-fifths of the tarsometatarsus. Its fibers longus is a rather variable musclein birds (George insert onto a flat tendon that extends onto the medial and Berger 1966: 455). surface of the first metatarsal, where it is held in M. extensorproprius digiti III (Fig. 8A).--This orig- place by a ligamentousband. Distal to this the ten- inates by fleshy fibers from the entire dorsalsurface don crossesthe metatarsal-phalangealjoint and in- of the tarsometatarsus, medial to M. extensor brevis sertson the medial surfaceof the baseof the proxi- digiti IV and lateral to M. extensor hallucis longus mal phalanx of the hallux, where it blends with the pars distalis. The fibers insert onto a broad tendon joint capsule. that arises on almost the entire dorsal surface of the A tiny musclearises on the dorsolateralsurface of muscle. At the distal end of the tarsometatarsus the metatarsal! and sendsa tendon to insert on the lig- tendon inserts on the dorsal surface of the base of amentousband connectingthe basesof the proxi- the proximal phalanxof digit III. mal phalangesof digits I and II. The identity of this M. extensorbrevis digiti IV (Fig. 8A).--This muscle structureis uncertainas it does not appear to have arisesby fleshy fibers from the craniolateralsurface been describedpreviously. We have termed it an of the tarsometatarsusextending from the lateral co- 54 BERMAi•Ai•D RAIKOW [Auk, Vol. 99 tyla to the trochleafor digit IV. A flat tendon arises it would be expectedthat the musclesbringing along the dorsal surface of the muscle, passesbe- about theseactions might be modified in some neath a bony bridge between the trochleaefor digits way. III and IV, and inserts on the medial surface of the The thigh.--M. iliofemoralis externusis usu- base of the proximal phalanx of digit IV. M. extensorproprius digiti IV (Fig. 8A).--This small, ally small and often absent in birds (George bipennate muscle arises over the dorsal surface of and Berger 1966). Its very large size in Colius the distal one-fourth of the belly of M. extensorbrev- (Fig. 2C) is almost certainly related to its action is digiti IV, and inserts by a flat tendon onto the as a retractor of the femur. Likewise, the ex- proximodorsalsurface of the first phalanxof digit IV. tensive femoral insertion of M. flexor cruris lat- This appearsto be a previouslyundescribed muscle. eralis (Fig. 3) is probably related to the need Three musclesarising from the tarsometatarsusand for powerful retraction of the femur. inserting on digit IV are listed in the compilations The accessorybelly of M. pubo-ischio-fem- of Hudson (1937), George and Berger (1966), and oralis(Fig. 2B, D) has not been reportedin any Baumel et al. (1979). Extensor brevis digiti IV and other group of birds. Whereas pars lateralis abductor digiti IV are present in Colius, while ab- and medialis insert on the femur in a conven- ductor digiti IV is locatedon the plantar surfaceof the tarsometatarsusin those few birds that possess tional manner, pars accessoriusinserts on the it, and thus is probably not homologouswith the tibiotarsus, thus functioning both in retraction present muscle. We have therefore provided the of the femur and in flexion of the tibiotarsus. above new name for this muscle because its relation Becauseboth actionsare important in elevation to the fourth digit is similar to that of M. extensor of the body, it seemslikely that the presence proprius digiti IlI to the third. of this unique third belly is also related to the M. abductordigiti IV (Fig. 8B).--This lies on the habit of hanging. plantar surfaceof the tarsometatarsuslateral to the There are other peculiar featuresof the thigh deep flexor tendons. It originates by fleshy fibers for which the significanceis uncertain. M. ob- from the lateral hypotarsalcrest, the adjacentlateral surface of the tarsometatarsus, and from the lateral turatorius medialis is much enlarged and con- plantar crest to about 3 mm from the distal end of sists of two bellies (Fig. 2B, D). Whereas the the element. The fibers insert on a flat tendon arising latter feature is not uncommonamong birds, on the lateral surface of the muscle. The tendon the enlargement of this muscle in Coliusmay crosses the lateral surface of the fourth metatarsal- be a compensationfor the loosely articulated phalangealjoint and insertson the baseof the prox- hip joint. The second head of origin for M. imal phalanxof digit IV. ischiofemoralishas not previously been re- M. lumbricalis.--Thiswell-developed muscle arises ported among birds. But as the muscle as a by fleshyfibers from the caudalsurfaces of the fused whole is not noticeably enlarged, nor has it tendons of Mm. flexor digitorum longus and flexor changed its areas of origin or insertion, the hallucis longus in the central third of the tarsomet- significanceof this variation is obscure. Like- atarsus. Distally it narrows to a short tendon that inserts on the proximal end of a joint pad on the wise, this study provides no explanation for medial surfaceof the trochlea of digit IV. the lossof M. iliofemoralisand the postacetabular portion of M. iliotibialis lateralis in Colius. The shank.--At least two unusual features of DISCUSSION the shankare probably relatedto hanging. The Several notable features of the thigh and large size of the tibialis cranialis and the pe- shank of Coliusare very likely related to their culiar retinaculumjust distal to its femoral or- propensity for hanging. In this position (Fig. igin (Fig. 4) may reflect this muscle'sfunction 1), elevation of the body to an upright position as a flexor of the tarsometatarsus. The arthrol- requires retraction of the femur, flexion of the ogy of the hindlimb was not included in this shank, and flexion of the tarsometatarsus. study, but observations on living birds and Muscles bringing about these actions must fresh specimensindicate a very loose articu- counteractthe weight of the entire body. Han- lation both at the hip and the knee. The reti- dling captive C. striatusrevealed it to be a sur- naculum, with its complex attachmentsto the prisingly heavy bird for its size. Rowan (1967) proximal end of the tarsometatarsus,may serve recordsan averagelength of 326 mm, 204 mm to stabilize the tendon when it is under con- of which is tail, and an averageweight of 56.4 siderable stress,as would be the caseduring g. Wallace (cited by Murie 1872) was also im- body elevation. pressed by the weight of these birds. Hence, The extensive origin of M. flexor hallucis January1982] MousebirdHindlimb Myology 55

TABLE1. Summary of muscularmodifications associated with rotation of digits I and IV in Colius.

Digit Action Muscle Modification I Cranial rotation M. flexor hallucis brevis Well-developed; insertion on lateral rather than plantar surfaceof digit Caudal rotation M. extensor hallucis Well-developed;insertion on longus pars distalis medial rather than dorsal surfaceof digit IV Cranial rotation M. extensor brevis digiti Well-developed IV Caudal rotation M. abductor digiti IV Well-developed;insertion more plantar than lateral longus from the femoral shaft (Fig. 6) might groups have shared a common ancestor. It also be correlatedwith hanging. Examination must be borne in mind, however, that both of this muscle on a fresh specimen revealed parrotsand mousebirdsuse their feet in a pe- that in this position its action has some role in culiar manner, thus providing an equally flexion of the shank. Alternatively, the enlarge- strong argument for convergence.Parrots are ment of this musclemay simply reflect the im- permanently zygodactyl, while mousebirds portance of maintaining a strong grip under only occasionallyhold their digits in this con- very diverse circumstances. figuration. The ability to extend both caudally Pycraft (1907) contended that in the Coli- directed digits with the action of one muscle iformesthe tendon of M. flexorhallucis longus would seem to be an advantage. The normal never fuses with that of M. flexor digitorum arrangement, with branches only to digits II, longus, but bifurcates, sending branches to Ill, and IV, is most efficient for the anisodactyl digits I and II. This is incorrect, for although configuration.The hallux, the caudallydirected the distinction between the two tendons can digit, is often the only digit that actsin grasp- be seen throughout their length, they are in ing during perching; hence its operation apart fact fused. There is no doubt that the branch from the other three digits is necessary.In ad- to the hallux is derived from that part of the dition, both parrots and mousebirds have tendon formed by the flexor hallucis longus many more complex uses of their feet than tendon. When viewed dorsally (Fig. 7) the perching. It is possiblethat the manipulative branch to digit II cannot be seen unless those ability of the foot is enhancedby having ex- to digits I and III are separated slightly, be- tension of all four digits controlledby a single cause it is deep to the branch to the hallux. muscle. Mousebirds have lost pars proximaIls Becauseit arises from the most medial part of of the extensorhallucis longus, and the entire the tendon, as does the branch to the hallux, muscle is absent in at least one parrot (Mel- from this view it could be interpreted as aris- opsittacusundulatus). In both casesit appears ing from the part of the tendon derived from that the tendon of insertion of pars proximaIls M. flexor hallucis longus. The ventral view, has been shifted to the extensordigitorum lon- however, clarifiesthe picture (Fig. 7). In spite gus. of its medial origin, the branch to digit II arises Although this character alone cannot dem- in the sameplane as thoseto digits III and IV. onstratea commonancestry for the Coliiformes In this view it really looks as if the tendon of and Psittaciformes, it is more substantial evi- M. flexor digitorum longus trifurcates,and the dence than any single feature previously of- branch to the hallux is the exceptionalone, in fered in relating the Coliiformes to other that it arises from the dorsal surface of the com- groups. Thus, the possibility of this relation- mon tendon. ship should be kept in mind when considering One of the most distinctive features of the other aspectsof the anatomy of these two or- entire hind limb of Colius is the branch of the ders. extensordigitorum longus tendon to the hallux The foot.--Cranial and caudal rotation of (Fig. 5). This condition has been found in only digits I and IV is accomplishedby several de- one other order, the Psittaciformes, and could viations from the basic avian plan (Table 1). thus be taken as evidence that these two Considering first the hallux: The extensor 56 BERMANAND RAIKOW [Auk, Vol. 99 hallucis longus consistsof two parts in many that some modification of the fourth metatar- birds, a pars proximalis and a pars distalis. sal-phalangealjoint is also involved in this ac- Pars proximalis is typically the larger compo- tion. nent, pars distalis being reduced or often absent (George and Berger 1966). In Colius, pars ACKNOWLEDGMENTS proximalis has been lost and pars distalis is We are grateful to Kenneth C. Parkes,Carnegie well-developed.Furthermore, while pars dis- Museum of Natural History, for providing the pre- talis typically inserts on the dorsal surface of served and frozen specimens for dissection, and to the base of the hallux, in Colius the insertion Norman Suhoski,Pittsburgh Aviary-Conservatory, has moved to the medial surfaceof this digit. for furnishing the live mousebirds. Thanks are also In this position its contraction brings about due to Jonathan Treasure for his technical assistance. caudal rotation of the hallux. StorrsL. Olson,Joel Cracraft, and an anonymousre- The action of the very small extensorhallucis viewer provided constructivecriticisms of the manu- longus accessoriusis difficult to demonstrate. script.The figureswere drawn by William R. Filer. This study was supportedby N.S.F. grantsDEB- As it is known only in Coliiformes, it seems 7810715 and DEB-8010898 to R. J. Raikow. Studies of likely that it is related to digit rotation. From the frozenspecimens and the colonyof living birds its location it looks as if it might feebly aug- were supportedby the Collegeof the Holy Cross. ment cranial rotation. M o flexor hallucis brevis is often small or absent in birds. When present, it normally inserts LITERATURE CITED on the plantar surfaceof the base of the hallux BALLMAN, P. 1969. Les oiseaux Miocenes de la (Georgeand Berger1966). This muscleis well- Grive-Saint-Alban (Isere). Geobios 2: 157-204. developed in mousebirds, and the insertion BAUMEL,J. J., A. S. KING, A.M. LUCAS,J. E. BREA- has shifted to the lateral surfaceof this digit, ZILE, & H. E. EVANS (Eds). 1979. Nomina An- so that its contractionbrings about cranial ro- atomica Avium. London, Academic Press. tation of the hallux. BOCK,W. J., & R. SHEAR.1972. A stainingmethod for gross dissection of vertebrate muscle. Anat. Caudal rotation of digit IV is less pro- Anz. 130: 222-227. nounced than that of the hallux. It can be ac- CHAPIN,J.P. 1939. The birds of the BelgianCongo. tively rotated to only about 100ø . Beyond this, Bull. Amer. Mus. Nat. Hist. 75: 469-479. its distal four phalanges can be rotated pas- DEcovx, J.P. 1975. Le dispositif d'accrochagedes sively by contactagainst the substrateto about griffes de Colius striatus (Coliiformes). Alauda 160 ø. 43: 271-278. M. extensorbrevis digiti IV is typicallysmall FRIEDMANN,H. 1930. Birds collectedby the Childs or absent in birds. When present, it inserts on Frick expeditionto Ethiopia and Kenya colony. the dorsal surface of the base of digit IV Part 1. Bull. U.S. Natl. Mus. 153: 321-337. (Georgeand Berger1966). In Colius,this mus- GADOW,H. 1893-1896. Muscular System.Pp. 602- cle is unusually large and its insertion has 620 in A. Newton (Ed.). A dictionary of birds, Part III. London, Adam and Charles Black. shifted medially. Its action in this position is GARROD,A. H. 1896. Notes on the anatomyof the not extension, but cranial rotation of digit IV. colies (Colius). Proc. Zool. Soc. London 1896: Mo extensorproprius digiti IV, however, does 416-419. insert on the dorsal surfaceof this digit. This GEORGE,J. C., & A. J. BERGER.1966. Avian myol- muscle, not previously described in birds, may ogy. New York, AcademicPress. have replaced M. extensor brevis digiti IV as HUDSON, G. E. 1937. Studies on the muscles of the the short extensorof this digit. pelvic appendagein birds. Amer. Midi. Natur. The caudal rotator of digit IV is M. abductor 18: 1-108. digiti IV, and its action probably accountsfor LowE, P. 1948. What are the Coraciiformes? Ibis 90: 572-582. its enlargementin Colius.The insertion, nor- MACKWORTH-PRAED, C. W., & C. H. B. GRANT. mally on the lateral surface of the base of the 1962. Birds of the southern third of Africa, Vol. digit (Georgeand Berger 1966), has shifted to 1. London, Longmans, Green & Co., Ltd. a slightlymore plantarposition in mousebirds, MuRIE, J. 1872. On the genus Colius, its structure so that the action of this musclegoes beyond and systematicplace. Ibis 1872:263-280. abduction to caudalrotation. This is not a very PYCRAFT,W. P. 1907. On the anatomyand system- pronounced change, however, and it is likely atic position of the colies. Ibis 1907: 229-253. January1982] MousebirdHindlimb Myology 57

ROWAN,M. K. 1967. A study of the coliesof south- VERHEYEN, R. 1956. Note sur L'anatomie et la clas- ern Africa. Ostrich 38: 63-115. sificationdes Coliiformes.Inst. Roy. Sci. Natur. SCLATER, W. L. 1903. The birds of South Africa, Belgique, Bull. 32(47): 1-7. Vol. 3. London, R. H. Porter.

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Altitudinal gradients in speciationof Andean forest tion of WesternGrebe colorphases in Mexico; Sally birds; Susan Hannon, Female spacingbehaviour in Olson,Habitat selection,breeding biology, and den- the Willow Ptarmigan and its relation to population sity of the Mountain Plover on the CharlesM. Russell regulation;Douglas B. Hay, Physiologicaland social National Wildlife Refuge;Paula Peters,Vocal com- ecologyof roostingPygmy Nuthatches(Sitta pyg- municationsystem of the SantaCruz IslandScrub Jay; maea); JamesL. Hayward, Reproductivestrategies Ted N. Pettit, Incubation strategiesof tropical sea- used by homosexualand heterosexualgulls; Linda birds on ChristmasIsland; Nina Pierpont, Foraging Heald, Behavioralplasticity in a Tyrannidflycatcher: behavior of woodcreepers (Dendrocolaptidae) in effects of environmental variability; Carlos M. Her- AmazonianPeru; Melinda Pruett-Jones,Vocal copy- rera, Ecologyand evolution of avian frugivory in ing in Macgregor's Bowerbird (Amblyornis mac- Spanishmediterranean habitats; Eve SevierHiatt, gregoriae);Stephen Glen Pruett-Jones,Ecology and Annual cycle of plasma prolactin and follicle- evolution of social organization in Parotia lawesii, stimulatinghormone in a free-living populationof the Lawes Six-wired Bird of Paradise; JamesScott Quinn, White-crowned Sparrow, Zonotrichia leucophrys; Pairbond integrity, mate fidelity, and parental in- Wendy L. Hill, Effectof resourceproductivity on the vestment in Caspian Terns (Sterna caspia); Terry intraspecificvariation in reproductivebehavior of the Edwin Quinney, Relationshipbetween food abun- American Coot (Fulica americana); Anne E. Houde, danceand breeding performancein the Tree Swallow Effects of nest site choice on the survival of Common (Iridoprocnebicolor); Susan St. Clair Raye, Bobwhite Tern chicks;Peter Houde, Paleognathousbirds from Quail (Colinus virginianus)vocalizations: ontogeny the Lower EoceneLondon clay; Karen E. Innes, Be- and function in sibling recognition;Mark F. Riegner, havioral ecologyof the White-throated Magpie Jay Foraging ecology of the Yellow-crowned Night (Calocittaformosa) of Santa Rosa National Park, Costa Heron; Diane E. Riska, Breedingbiology and com- Rica;Joel F. Jerabek,Territories of Vesper, Savannah, munication behavior of the Brown Noddy, Anous and Grasshopper Sparrows on reclaimed surface stolidus,Dry Tortugas, Fla.; ScottK. Robinson, Ecol- mines;Alan CharlesKemp, Systematicinvestigation ogy and social behavior of the Yellow-rumped of hornbills (Bucerotidae)and birds of prey (Fal- Caciquein southeasternPeru; StephenR. Sabo,Ecol- coniformes); E. N. Kurochkin, Avian fossils from the ogyand behavior of the Maul Parrotbill;Lilian J. Saul, tertiary of the USSR and Mongolia; BarbaraE. Kus, Ecologyand behavior of Red-headedand Red-bellied Raptorpredation on wintering shorebirds;Stewart T. Woodpeckers in south-central Florida; William A. Levinson, BirdSfruit interactions in northern Florida; Searcy,Female choice of matesand male singingbe- CharlesS. Luthin, Comparativemorphologies of 4 haviorin SongSparrows; Erik Skadhauge,Activation subspecies of the Buff-necked Ibis, Theristieus of salt-gland function and regulation of coprodeal caudatus;Timothy D. Manolis, Reproductiveinterac- transportin the ostrich;Martin Luther Stephens,Pa- tions betweenShiny Cowbirdsand actualand poten- rental behavior and ecology of the polyandrous tial hostsin Trinidad and Tobago; Leslie F. Marcus, Northern Jacana; Henry M. Stevenson, Birds of Ecomorphologicalanalysis of birds from Mediterra- Florida; F. G. Stiles, Handbook of Costa Rican birds; nean habitats in Chile, California, and France; Ken- Theresa A. Thompson, Social organization within neth D. Meyer, Sexualdifferences in the behavioral easternWild Turkeyflocks; Diana F. Tomback,Role of ecology of the Sharp-shinned Hawk (Accipiter visual cues in seed cacheretrieval by Clark's Nut- striatus);Bruce Wayne Miller, Revisionof the bird cracker;Wayne Trivelpiece,Etho-ecology of the Mag- family Pittidae; Michael T. Murphy, Variability in nificent Frigatebird(Fregata magnificens); Robert F. insect abundance, foraging ecology, and nestling Tintie, Influence of male multiple nest building on growthin the EasternKingbird; EricaNol, Reproduc- female mate choicein Long-billed Marsh Wrens (Tel- tive strategiesin two speciesof oystercatcher;Christ- matodytespalustris); Alan Tye, Foodsupply, feeding opher J. Norment, Avian communitiesof the alpine behaviour, and territorial behaviour of the Wheatear tundra/subalpine forest ecotone, Beartooth Mts., (Oenantheoenanthe) in Africa; EvelynH. Weinstein, Wyoming; Gary L. Nuechterlein,Reproductive isola- Nest site selectionin Arctic Terns (Sternaparadisaea)

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