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The Hindlimb Musculature of the Mousebirds (Coliiformes)

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The Hindlimb Musculature of the Mousebirds (Coliiformes) 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. leuco- cephalus)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 in- trinsic foot muscles.Two small intrinsic foot muscles,not previously described in birds, also appear to be associatedwith digit rotation. In the speciesdissected, the extensordig- itorum 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<OW [Auk, Vol. 99 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 •iFFCLP C D 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
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