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Variation in the Muscles and Nerves of the Leg in Two Genera of Grouse (Tympanuchus and Pedioecetes)

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Variation in the Muscles and Nerves
of the Leg in Two Genera of Grouse
(Tympanuchus and Pedioecetes)

BY
E. BRUCE HOLMES

PAGE Introduction 367 Materials and Methods 368 Terminology 369 Acknowledgments 375 Skeleton 375 Nerves 376 Lumbosacral Plexus 376 Femoral Nerve 377 Obturator Nerve 379 Sciatic Nerve 379 Peroneal Nerve 382 Tibial Nerve 384 Muscles 396 M. Extensor Iliotibialis Lateralis 398 M. Extensor Iliotibialis Anticus 405 M. Ambiens 408 M. Vastus Lateralis 408 M. Vastus Medialis 410 M. Piriformis 412 M. Gluteus Profundus 413 M. Iliacus 414 M. Iliotrochantericus Medius 415 M. Psoas 416 M. Flexor Cruris Lateralis 416 M. Flexor Cruris Medialis 417 M. Caudofemoralis 418 M. Flexor Ischiofemorali 420 M. Adductor Superficialis 420 M. Adductor Profundus 421 M. Obturator 422 M. Femorocruralis

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class="pginternal" tag="{http://www.w3.org/1999/xhtml}a">425 M. Gastrocnemius 426 M. Flexor Perforans et Perforatus Digiti II 427 M. Flexor Perforans et Perforatus Digiti III 429 M. Flexor Perforatus Digiti IV 430 M. Flexor Perforatus Digiti III 432 M. Flexor Perforatus Digiti II 433 M. Flexor Hallucis Longus 435 M. Plantaris 435 M. Flexor Digitorum Longus 436 M. Popliteus 438 M. Peroneus Longus 438 M. Tibialis Anticus 439 M. Extensor Digitorum Longus 440 M. Peroneus Brevis 441 M. Extensor Hallucis Longus 442 M. Abductor Digiti II 443 M. Extensor Brevis Digiti III 444 M. Extensor Proprius Digiti III 444 M. Extensor Brevis Digiti IV 445 M. Lumbricalis 445 M. Abductor Digiti IV 446 M. Flexor Hallucis Brevis 446 Discussion and Conclusions 446 Analysis of Individual Variation 446 Muscles 447 Nerves 449 Analysis of Variation Between Species 451 Comparison with Other Studies of Innervation 452 Summary 457 Literature Cited 473

LIST OF ILLUSTRATIONS

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PAGE Fig. 1. Pelvis of Tympanuchus pallidicinctus. A. Lateral view. × 1. B. Ventral view. × 1⅛. 370 Fig. 2. Ventral views of the lumbosacral plexus of Tympanuchus pallidicinctus. Sympathetic ganglionated chain removed. Numbers indicate synsacral spinal nerves. × 2. A. T.p. 1L. B. T.p. 2L. 386 Fig. 3. Ventral views of the lumbosacral plexus. Sympathetic ganglionated chain removed. Numbers indicate synsacral spinal nerves. × 2. A. Tympanuchus cupido pinnatus 3L. B. Pedioecetes phasianellus jamesi 4L. 387 Fig. 4. Semidiagrammatic ventral views of the femoral nerve, showing the distribution of the branches. × 3. 1,2, M. extensor iliotibialis anticus; 3, cutaneous; 4-6, M. extensor iliotibialis lateralis; 7,8, M. iliacus; 9, M. gluteus profundus; 10-12, fused Mm. vastus lateralis and vastus medialis; 13,14, M. vastus medialis; 15, M. ambiens; 16, M. femoritibialis internus; 17, nonmuscular; 18, M. psoas; 19, M. iliotrochantericus medius. A. Tympanuchus cupido pinnatus 3L. B. Pedioecetes phasianellus jamesi 3L. 388 Fig. 5. Semidiagrammatic ventral views of the femoral nerve, showing the distribution of the branches. × 3. 1,2, M. extensor iliotibialis anticus; 3, cutaneous; 5,6, M. extensor iliotibialis lateralis; 7,8, M. iliacus; 9, M. gluteus profundus; 10,11, fused Mm. vastus lateralis and vastus medialis; 13, M. vastus medialis; 15, M. ambiens; 16, M. femoritibialis internus; 17, nonmuscular; 18, M. psoas; 19, M. iliotrochantericus medius. A. Tympanuchus pallidicinctus 2L. B. Tympanuchus cupido attwateri 1R 389 Fig. 6. Semidiagrammatic dorsolateral view of the sciatic nerve of Pedioecetes phasianellus jamesi 3R, showing the distribution of the branches. × 2½. 1, M. gluteus profundus; 2, M. piriformis; 3, M. extensor iliotibialis lateralis; 4-7, M. extensor iliofibularis; 8, M. flexor cruris medialis; 9, cutaneous; 10, to pudendal plexus; 11, M. flexor cruris lateralis; 12, M. caudofemoralis pars caudifemoralis; 13-15, M. caudofemoralis pars iliofemoralis; 16,17, M. flexor ischiofemoralis; 18,19, M. femorocruralis (branch of tibial nerve); 20, cutaneous; 21, M. gastrocnemius pars media (branch of tibial nerve); 22, cutaneous. 390 Fig. 7. Semidiagrammatic dorsolateral view of the sciatic nerve of Tympanuchus pallidicinctus 2L, showing the distribution of the branches. × 2½. 1, M. gluteus profundus; 2, M. piriformis; 3, M. extensor iliotibialis lateralis; 4, 7, M. extensor iliofibularis; 8, M. flexor cruris medialis; 9, cutaneous; 10, to pudendal plexus; 11, M. flexor cruris lateralis; 12, M. caudofemoralis pars caudifemoralis; 13-15, M. caudofemoralis pars iliofemoralis; 17, M. flexor ischiofemoralis; 18, M. femorocruralis (branch of tibial nerve); 22, cutaneous; 23, nonmuscular (branch of peroneal nerve). 391 Fig. 8. Semidiagrammatic dorsolateral view of the sciatic nerve of Tympanuchus cupido pinnatus 3L, showing the distribution of the branches. × 2½. 1, M. gluteus profundus; 2, M. piriformis; 3, M. extensor iliotibialis lateralis; 4,7, M. extensor iliofibularis; 8, M. flexor cruris medialis; 9, cutaneous; 11, M. flexor cruris lateralis; 12, M. caudofemoralis pars caudifemoralis; 13, M. caudofemoralis pars iliofemoralis; 17, M. flexor ischiofemoralis; 18, M. femorocruralis (branch of tibial nerve); 20, cutaneous; 22, cutaneous. 392 Fig. 9. Semidiagrammatic dorsolateral view of the sciatic nerve of Pedioecetes phasianellus jamesi 3L, showing the distribution of the branches. × 2½. 1, M. gluteus profundus; 2,

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M. piriformis; 3, M. extensor iliotibialis lateralis; 4,5,7, M. extensor iliofibularis; 8, M. flexor cruris medialis; 9, cutaneous; 11, M. flexor cruris lateralis; 13,14, M. caudofemoralis pars iliofemoralis; 16,17, M. flexor ischiofemoralis; 18,19, M. femorocruralis (branch of tibial nerve); 20, cutaneous; 22, cutaneous. 393 Fig. 10. A,B. Semidiagrammatic drawings of the peroneal nerve of Tympanuchus pallidicinctus 1L, showing the distribution of the branches. × 2. C. Semidiagrammatic drawing of the distal part of the peroneal nerve of Tympanuchus cupido attwateri 1R, showing the distribution of the branches. × 2. 1,2, M. tibialis anticus (tibial head); 3,4, M. tibialis anticus (femoral head); 5, M. extensor digitorum longus; 6, nonmuscular; 7,8, M. peroneus longus; 9, M. peroneus brevis; 10,11, M. extensor hallucis longus (proximal head); 12, M. extensor hallucis longus (distal head); 13-15, nonmuscular (to toes); 16, M. abductor digiti II; 17, M. extensor brevis digiti III; 18, M. extensor brevis digiti IV. 394 Fig. 11. A,B. Semidiagrammatic drawings of the tibial nerve (excluding the paraperoneal branch) of Tympanuchus pallidicinctus, showing the distribution of the branches. × 2. A. T.p. 1L. B. T.p. 3R. C. Semidiagrammatic drawing of the distal part of the paraperoneal branch of the tibial nerve of Pedioecetes phasianellus jamesi 2L, showing the distribution of the branches. × 2. 1, M. femorocruralis; 2, M. gastrocnemius pars media; 3, M. popliteus; 4, M. plantaris; 5, M. flexor digitorum longus; 6-8, nonmuscular; 9-11, M. gastrocnemius pars interna; 12,13, M. flexor hallucis longus; 14-16, M. flexor perforatus digiti IV (medial head); 17, M. flexor perforatus digiti III (medial head); 18-20, M. flexor perforatus digiti II; 21, M. flexor perforatus digiti IV (lateral head); 22-24, M. flexor perforatus digiti IV (anterolateral head); 25, M. flexor perforatus digiti III (anterolateral head); 26, M. flexor perforans et perforatus digiti III; 27,28, M. flexor perforans et perforatus digiti II; 29, M. gastrocnemius pars externa; 30,31, M. abductor digiti IV; 32,33, M. flexor hallucis brevis; 34,35, nonmuscular (to toes). 395 Fig. 12. Tympanuchus pallidicinctus 2L. Lateral view of the superficial muscles of the left leg. × 1. 397 Fig. 13. Tympanuchus pallidicinctus 2L. Medial view of the superficial muscles of the left leg. × 1. Articular capsule shown by concentrically arranged dashes. 398 Fig. 14. Tympanuchus pallidicinctus 2L. Lateral view of the muscles of the left leg. The following muscles have been removed: extensor iliotibialis lateralis, extensor iliotibialis anticus, gastrocnemius pars externa and pars interna, and peroneus longus. × 1. 399 Fig. 15. Tympanuchus pallidicinctus 2L. Medial view of the muscles of the left leg. The following muscles have been removed: extensor iliotibialis lateralis, extensor iliotibialis anticus, ambiens, flexor cruris lateralis (in part), flexor cruris medialis (in part), gastrocnemius pars externa and pars interna, and peroneus longus. × 1. 400 Fig. 16. Tympanuchus pallidicinctus 2L. Lateral view of the muscles of the left leg. The following muscles, in addition to those listed for Fig. 14, have been removed: ambiens, vastus lateralis pars lateralis, vastus medialis (except for part of patellar tendon), extensor iliofibularis, flexor cruris lateralis (in part), flexor perforans et perforatus digiti II, and flexor perforans et perforatus digiti III. × 1. 401 Fig. 17. Tympanuchus pallidicinctus 2L. Lateral view of the muscles of the left leg. The following muscles, in addition to those listed for Fig. 16, have been removed: vastus lateralis pars postica, gluteus profundus, flexor

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cruris medialis (in part), caudofemoralis, flexor perforatus digiti IV, and tibialis anticus. × 1. 402 Fig. 18. Tympanuchus pallidicinctus 2L. Lateral view of the muscles of the left leg. The following muscles, in addition to those listed for Fig. 17, have been removed: patellar tendon, iliacus, iliotrochantericus medius, flexor cruris lateralis, flexor cruris medialis, flexor ischiofemoralis, adductor superficialis, femorocruralis, gastrocnemius pars media, flexor perforatus digiti III, flexor perforatus digiti II, flexor hallucis longus, plantaris, flexor digitorum longus, popliteus, and extensor digitorum longus. × 1. 403 Fig. 19. Tympanuchus pallidicinctus 2L. A. Posterior view of the muscles of the left shank. The following shank muscles, in addition to those listed for Fig. 17, have been removed: gastrocnemius pars media, flexor perforatus digiti III, and flexor perforatus digiti II. × 1. B. Posterior view of the proximal end of the shank, showing the most deeply situated muscle. × 1. C. Lateral view of the head of the left femur and the middle part of the pelvis, showing the deepest part of M. obturator. × 1. D. Medial view of the posteroventral part of the left side of the pelvis, showing the intrapelvic part of M. obturator. × 1. E. Anterior view of the left tarsometatarsus, showing the dorsal intrinsic muscles of the foot. × 1½. F. Posterior view of the left tarsometatarsus, showing the ventral intrinsic muscles of the foot. × 1½. 404 Fig. 20. A-D. Dorsal views of M. iliotrochantericus medius, showing its relationship to femoral notch. × 1. In D, note absence of femoral notch and location of branch of femoral nerve. A. Tympanuchus pallidicinctus 2L. B. T. cupido pinnatus 4L. C. Pedioecetes phasianellus jamesi 1L. D. T. pallidicinctus 3L.
E. Medial view of distal end of M. flexor cruris medialis of P. p. jamesi 4L. × 1. Part of insertion is covered by medial collateral ligament.
F,G. Lateral views of posteroproximal corner of M. extensor iliotibialis lateralis (removed from specimen). × 1. F. T. pallidicinctus 2L. G. P. p. jamesi 3L.
H,I. Dorsolateral views of M. piriformis. × 1. H. P. p. jamesi 1L. I. T. cupido attwateri 1L.
J. Lateral view of M. caudofemoralis pars caudifemoralis (removed from specimen) of T. c. pinnatus 4L. × 1. K. Lateral view of extrapelvic part of M. obturator of T. pallidicinctus 3L (bones not shown). × 2.
L,M. Region surrounding obturator foramen of T. pallidicinctus 3L, showing points of attachment of three parts of M. obturator (muscles removed). × 3. L. Lateral view. M. Medial view.
N. Anterior view of left tarsometatarsus of P. p. jamesi 4L, showing dorsal intrinsic muscles of foot. × 1½. Tendon of M. extensor digitorum longus has been removed. 406

INTRODUCTION

The purposes of this study were: (1) to obtain information on individual variation in the anatomy of the muscles and nerves of the leg of Tympanuchus cupido pinnatus (Greater Prairie Chicken), T. c. attwateri (Attwater's Prairie Chicken), T. pallidicinctus (Lesser Prairie Chicken), and Pedioecetes phasianellus jamesi (Sharp-tailed Grouse); (2) to determine whether or not the two species of the genus Tympanuchus differ constantly in the myology of the leg; and (3) to determine what constant differences in the myology of the leg exist between the two closely related genera Tympanuchus and Pedioecetes.

These particular birds were chosen because they are closely related, and closely resemble one another in habitats occupied and in patterns of behavior. It was desired to study examples that showed as few adaptive differences as possible among the grouse. Series of each of the three species of grouse were readily obtainable, making it possible to draw comparisons at the level of individuals, subspecies, species, and genera.

The study here reported on was begun in the spring of 1957 and was completed in the autumn of 1961.

Prior work on the muscles of the leg of birds has been reviewed by Hudson (1937) and Hudson, et al. (1959). Only papers dealing with the innervation of the leg in birds are reviewed below.

DeMan (1873) treated the nerves of Paradisea papuana, Corvus monedula, and the chicken; he also commented briefly on a few other species. Jhering (Ihering, 1873) briefly described the lumbosacral plexus in approximately a dozen birds, but illustrated only two. Gadow (1880) described the nerves in Struthio, Rhea, and Casuarius; his paper contains some excellent illustrations of nerves. Unfortunately, the text is marred by numerous confusing typographical errors. Carlsson (1884) described the nerves of Eudyptes chrysolopha, Alca torda, Mergulus alle, and Mormon arcticus. Gadow (1891) described the nerves in a study that included a large variety of birds, but published few illustrations. DuToit (1913) described the lumbosacral plexus of the chicken. Romer (1927) gave the innervation of the hip and thigh muscles in the chicken, but did not cover the lumbosacral plexus. Appleton (1928) gave the innervation, in various birds, only of those muscles of the hip and thigh that are supplied by the tibial and peroneal nerves; he did not include the lumbosacral plexus. Sudilovskaya (1931) described the nerves of Struthio, Rhea, and Dromaeus (Dromiceius). Unfortunately, his illustrations are almost useless as far as the nerves are concerned. Boas (1933) described the lumbosacral plexus in a large number of birds. His extensive account includes numerous good illustrations. Howell (1938) listed the innervation of the hip and thigh muscles in the chicken; he did not include the lumbosacral plexus. Fisher (1946) listed the innervation of the muscles

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of vultures, but did not include the lumbosacral plexus. Wilcox (1948) gave the innervation of the muscles of Gavia immer, but did not include the lumbosacral plexus. Fisher and Goodman (1955) described the nerves in the Whooping Crane. Papers by Chomiak (1950) and Yasuda, et al. (1959), both dealing with the chicken, were not examined.

MATERIALS AND METHODS

Complete dissections of the muscles and nerves were made in eight legs (of five specimens) of the Lesser Prairie Chicken (Tympanuchus pallidicinctus), six legs (of four specimens) of the Greater Prairie Chicken (T. cupido pinnatus), three legs (of two specimens) of Attwater's Prairie Chicken (T. cupido attwateri), and six legs (of four specimens) of the Sharp-tailed Grouse (Pedioecetes phasianellus jamesi).

For convenience and simplicity of reference, each specimen has been designated by a symbol consisting of the first letter of the genus and of the species (and also of the subspecies in T. cupido) plus a number. The letter "L" or "R" is added to indicate the left or right leg. Thus the symbol T.p. 1L refers to the left leg of specimen number one of T. pallidicinctus.

All specimens are in the University of Kansas Museum of Natural History. The catalogue number of each specimen, and the legs of it that were dissected, are listed below.

T.p. 1L,R KU38520 T.c.p. 4L KU38518 T.p. 2L,R KU38521 T.c.a. 1L,R KU36617 T.p. 3L,R KU38522 T.c.a. 2L KU36618 T.p. 4L KU38523 P.p. 1L,R KU38526 T.p. 5R KU38527 P.p. 2L KU38518 T.c.p. 1L,R KU38515 P.p. 3L,R KU38528 T.c.p. 2L,R KU38516 P.p. 4L KU38529 T.c.p. 3L KU38517

The specimens were injected in the field either with formalin (10%) or embalming fluid, except for those of T. c. attwateri, which were frozen; the latter were later injected with embalming fluid. Injection in all the birds was by hypodermic syringe into all major muscle masses, into the body cavities, and subcutaneously in the neck, wings, and feet. In those specimens injected with embalming fluid, the body cavities were injected with formalin. The embalming fluid consisted of 70 per cent alcohol, glycerin (or propylene glycol), and formalin (full strength) in the approximate ratio of 78:20:2, respectively. This fluid gave good preservation; these specimens had the advantages of lacking almost entirely the irritating odor of formalin and of having pliable tissues. The skin of those specimens originally injected with formalin was slit in several places and they were transferred to crocks containing embalming fluid (without the formalin). After a period of many weeks, with two changes of fluid, most of the formalin odor was eliminated and the muscles were sufficiently pliable to be easily dissected. All specimens were kept in containers filled with embalming fluid. No mold ever appeared, even though no phenol or other chemical was added.

To facilitate comparison, two or three specimens were frequently dissected simultaneously. The nerves and smaller muscles were dissected with the aid of a stereoscopic microscope mounted on a long movable arm. In order satisfactorily to expose the lumbosacral plexus the posterior half of the sternum and pectoral muscles, as well as the abdominal viscera, were removed.

To insure more nearly accurate proportions, drawings of the pelvis and of some of the muscles were made with the aid of photographs of the several specimens listed above.

TERMINOLOGY

Skeleton

The majority of the osteological terms used in the present paper are those used by Howard (1929); however, many skeletal features are not named by Howard. Since names for most of these parts were not found in the other literature examined, it was necessary for me to propose terms for them. Most of this new terminology pertains to the pelvis. All of the osteological terms used in the present paper, whether used by Howard or not, are briefly defined below. Those of the pelvis are illustrated in Fig. 1. Most of the remaining terms are illustrated by Howard (1929).

Pelvis

The median dorsal ridge is the blunt ridge in the midline of the anterior part of the synsacrum formed by the neural spines of the vertebrae. The antitrochanter, on the posterodorsal rim of the acetabulum, is a pyramid-shaped projection that articulates with the proximal end of the femur. The anterior iliac crest is a ridge along the dorsomedial border of the ilium, beginning almost at the anterior end of that bone; the crest curves laterally as it extends posteriorly and (for purposes of the present definition) ends at the level of the posterior edge of the antitrochanter, where the crest is continuous with the lateral iliac process. The lateral iliac process is a pronounced, laterally or ventrolaterally, projecting ridge on the ventrolateral surface of the ilium posterior to the level of the antitrochanter; the process does not extend as far as the posterior end of the ilium. The lateral ischiatic ridge is a relatively slight ridge continuous with the posterior end of the lateral iliac process and curves posteroventrally across the lateral surface of the posterior part of the ischium; the ridge extends to the ventral edge of the ischium in some individuals and not in others. The dorsolateral iliac ridge begins at the lateral edge of the ilium near the posterior end of the lateral iliac process and curves posteromedially and

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somewhat dorsally, extending to the posterior edge of the ilium. The lateral iliac fossa is the concavity below the overhanging lateral iliac process. The ilio-ischiatic fenestra is a large oblong opening behind the acetabulum between the ilium and the ischium. The obturator foramen is a small oval opening posteroventral to the acetabulum between the ischium and the pubis. The ventral ischiatic tubercle is the angle formed by the ventrally projecting ischium at the point (near its midlength) where the ischium overlaps and lies lateral to (and fused to) the pubis. The pectineal process is an anterolaterally directed projection of the ventrolateral edge of the ilium anteroventral to the acetabulum. The femoral notch of the ilium is a shallow notch in the ventrolateral edge of the ilium approximately halfway between the last rib and the pectineal process. The oblique iliac crest is a pronounced blunt ridge on the ventral surface of the ilium and extends from the posterolateral corner of the last synsacro-thoraco-lumbar vertebra to near the anteroventral border of the ilio-ischiatic fenestra. The internal ilio-ischiatic crest is more or less continuous with the oblique iliac crest and extends posteriorly along the dorsal border of the ischium (forming the ventral border of the ilio-ischiatic fenestra), and then curves sharply dorsomedially onto the ventral surface of the ilium. The iliac recess is a concavity dorsolateral to the sharply curving posterior end of the internal ilio-ischiatic crest.