Variation in the Muscles and Nerves of the Leg in Two Genera of Grouse Part 1

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

by E. Bruce Holmes.

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.

att.w.a.teri_ (Att.w.a.ter'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 ill.u.s.trated only two. Gadow (1880) described the nerves in _Struthio_, _Rhea_, and _Casuarius_; his paper contains some excellent ill.u.s.trations 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 ill.u.s.trations.

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 ill.u.s.trations 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 ill.u.s.trations. 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 of vultures, but did not include the lumbosacral plexus. Wilc.o.x (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 Att.w.a.ter's Prairie Chicken (_T. cupido att.w.a.teri_), 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 KU38524 P.p. 2L KU38527 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. att.w.a.teri_, which were frozen; the latter were later injected with embalming fluid. Injection in all the birds was by hypodermic syringe into all major muscle ma.s.ses, 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 ill.u.s.trated in fig. 1. Most of the remaining terms are ill.u.s.trated 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 _ant.i.trochanter_, 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 ant.i.trochanter, where the crest is continuous with the lateral iliac process. The _lateral iliac process_ is a p.r.o.nounced, laterally or ventrolaterally, projecting ridge on the ventrolateral surface of the ilium posterior to the level of the ant.i.trochanter; 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 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 p.r.o.nounced 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.

[Ill.u.s.tration: FIG. 1. Pelvis of _Tympanuchus pallidicinctus_. A.

Lateral view. 1. B. Ventral view. 1-1/8.]

The terminology applied to the synsacral vertebrae by different authors varies. The terminology proposed by DuToit (1913) is employed in the present account. See my fig. 1B. This terminology differs considerably from that used by Howard (1929). DuToit divides the fused synsacral vertebrae into the following five groups, listed in anteroposterior sequence: (1) _synsacro-thoracic_, which bear movable ribs; (2) _synsacro-thoraco-lumbar_, which lack movable ribs but possess well developed laterally directed parapophyses, in addition to the more dorsally directed diapophyses; (3) _synsacro-lumbar_, which lack parapophyses, although possessing inconspicuous diapophyses; these vertebrae are shortened anteroposteriorly and are so firmly fused together that often the number present can be determined only by counting the intervertebral foramina; (4) _synsacro-sacral_, which have much more p.r.o.nounced transverse processes than do the synsacro-lumbar vertebrae; these transverse processes are expanded distally where they fuse with the ilium and represent both parapophyses and diapophyses partly or completely fused together plus sacral ribs (detectable only in the embryo); there are considered to be two of these vertebrae; they are situated at approximately the level of the acetabulum; (5) _synsacro-caudal_, which include the remainder of the fused vertebrae; no marked gross morphological features differentiate the synsacro-sacral and the synsacro-caudal groups of vertebrae. The boundaries between all but the last two groups of vertebrae are usually, but not always, easily determined. It may be difficult to determine whether a vertebra with rudimentary parapophyses belongs to the synsacro-thoraco-lumbar or the synsacro-lumbar group. Sometimes a parapophysis will be better developed on one side of a vertebra than on the other.

FEMUR

The _trochanter_ is a large squarish tuberosity on the lateral surface of the proximal end of the femur. The _trochanteric ridge_ is a sharp, longitudinal (relative to the femur) ridge forming the anterior edge of the trochanter. The _obturator ridge_ is a short, blunt, longitudinal ridge forming the posterior edge of the trochanter. The _anterior intermuscular line_ is a slight ridge extending distally from the trochanteric ridge. The _posterolateral intermuscular line_ is a slight ridge extending distally from the obturator ridge. The _posterior intermuscular line_ is a slight, longitudinal ridge on the mid-posterior surface of the femur. The _internal condyle_ is a large rounded articular prominence on the medial side of the distal end of the femur.

On the lateral side of the distal end of the femur are two articular prominences--the lateralmost, smaller one is the _fibular condyle_, separated by the _fibular groove_ (visible from posterior aspect only) from the larger and more medial _external condyle_. The _popliteal area_ is a depression on the posterior surface of the distal part of the femur immediately proximal to the condyles.

TIBIOTARSUS AND FIBULA

The _inner cnemial crest_ is p.r.o.nounced and directed anteriorly on the anterior surface of the proximal end of the tibiotarsus. The _outer cnemial crest_ is p.r.o.nounced and directed anterolaterally on the anterolateral surface of the proximal end of the tibiotarsus. The _rotular crest_ is transverse and forms the anterior border of the proximal end of the tibiotarsus; the crest extends between the dorsal ends of the two cnemial crests and also extends medial to the inner cnemial crest. The _fibular crest_ is longitudinal on the lateral surface of the tibiotarsus and fuses with the middle part of the fibula.

The _fibular tubercle_ is small and on the lateral surface of the fibula near the level of the middle of the fibular crest. The _anteromedial intermuscular line_ is a slight ridge extending from the inner cnemial crest down the anteromedial surface of the tibiotarsus. The _anterolateral intermuscular line_ is a slight ridge extending from the fibular crest down the anterolateral surface of the tibiotarsus. The _supratendinal bridge_ is a transverse bony arch over a longitudinal groove near the distal end of the anterior surface of the tibiotarsus.

TARSOMETATARSUS

The _hypotarsus_ is a large, p.r.o.nounced, squarish protuberance on the posterior surface of the proximal end of the tarsometatarsus and contains grooves and ca.n.a.ls for the pa.s.sage of the flexor tendons. The longitudinal ridges forming the lateral and medial edges of the posterior surface of the hypotarsus are termed _calcaneal ridges_. The _posterior metatarsal crest_ is long and sharp; it is continuous with the medial calcaneal ridge that extends most of the way down the posterior surface of the tarsometatarsus medial to the midline; there is an opening between this crest and the tarsometatarsus immediately distal to the hypotarsus. The _medial metatarsal depression_ is large; it is on the medial surface of the proximal end of the tarsometatarsus. The _anterior metatarsal groove_ is a longitudinal groove in the midline of the proximal part of the anterior surface of the tarsometatarsus. The three _trochleae_ are large rounded articular prominences at the distal end of the tarsometatarsus; there is one at the base of each of the digits II, III, and IV. The term _distal foramen_ (as used by Howard) refers to a short, anteroposteriorly directed ca.n.a.l that perforates the tarsometatarsus a short distance proximal to the intertrochlear notch between the trochleae for digits III and IV. Beginning at the middle of this ca.n.a.l and extending distally at a right angle to it is the _intertrochlear ca.n.a.l_, which opens via the terminal foramen into the intertrochlear notch between the trochleae for digits III and IV.

_Nerves_

For ease of description I have coined terms for the major divisions of the femoral and sciatic nerves.

_Muscles_

My terminology follows that of Fisher (1946) and Fisher and Goodman (1955) except for Mm. femoritibialis externus, flexor cruris lateralis (accessory head), and obturator internus et externus. Fisher (1946:547) states that most of his names for the hip and thigh muscles are those of Howell (1938) and the names for the shank and foot muscles are those of Hudson (1937). Fisher deviates, without explanation, from Howell's terminology in respect to Mm. vastus medialis and femoritibialis internus, M. caudofemoralis, M. flexor cruris lateralis, and Mm.

obturator internus and obturator externus. Fisher's synonymy of these muscles (1946: table 42) is in error. Fisher understandably deviates from Hudson in respect to Mm. extensor brevis digiti III and extensor proprius digiti III (see Holmes, 1962), although Fisher's synonymy is in error here. See my table 1.

I am not using Fisher and Goodman's term femoritibialis externus; this muscle is here considered as a part of M. vastus lateralis. A great deal of confusion surrounds the terminology of the muscle complex here termed Mm. vastus lateralis and vastus medialis.

Hudson (1937), Hudson, _et al._ (1959), Fisher (1946), and Fisher and Goodman (1955) have used different terminology for this complex. Most of the confusion stems from Gadow's (1891) unclear description of this complex, which he subdivided into two units termed Mm. femori-tibialis externus and femori-tibialis medius.

Many birds have three parts to this complex. It is difficult to determine how to apply Gadow's two terms to these three parts. As nearly as I can determine, the correct method is that of Hudson, _et al._ (1959); but because Gadow's terms have been used in different ways (even by the same worker), it seems best to abandon these terms. Berger (1956:272) believes that the muscle unit that Fisher and Goodman term M. femoritibialis externus represents a head of M. vastus lateralis; I am accepting his opinion. For the three parts of the complex under discussion, I am using the terms M. vastus medialis and M. vastus lateralis pars lateralis and pars postica.

Fisher (Fisher, 1946; Fisher and Goodman, 1955) considers the muscle here termed M. femorocruralis as an accessory head of M.

flexor cruris lateralis. The two muscle units in question are closely a.s.sociated; they insert broadly on opposite sides of a common tendinous raphe. Howell (1938:73) considers this to be a secondary fusion of unrelated muscles. Romer (1927:366) states that in the chick embryo M. femorocruralis is in reality a shank muscle that migrates into the thigh during development. Therefore, Fisher's usage of a single name for these two unrelated muscles is unsatisfactory. I am using Howell's terminology in which the name flexor cruris lateralis represents the main head only of Fisher's M. flexor cruris lateralis and the name femorocruralis represents Fisher's accessory head.