PELVIC and THIGH MUSCLES of ORNITHORHYNCHUS by HELGA S

PELVIC AND THIGH MUSCLES OF ORNITHORHYNCHUS By HELGA S. PEARSON University College, London OF recent years attempts to establish homologies between the muscles found in one class of Vertebrates and those in another have been placed on a much sounder basis by the study of the fossil bones of common ancestral forms. These bones often show muscle insertions as well marked as those on the bones of animals living to-day. Moreover, being often intermediate in shape, they indicate how the skeletal differences between living groups have arisen, differences intimately connected with the different position and action of the muscles moving that skeleton. Watson in England, Gregory and Camp in America, were pioneers in this line of work. More recently Romer', using similar methods and also considering the nerve supply, has made a very careful comparative study of the locomotor apparatus in Amphibia, Reptiles and Mammals with especial reference to the mammalian line of descent. Of these three classes he himself dissected three living types, Cryptobranchus, Iguana and Didelphys, but at that time no Monotreme, relying on Westling's description of conditions in this group. Recently I have had the opportunity ofdissecting the hind limb musculature of two specimens of Ornithorhynchus (kindly lent me for this purpose by Prof. D. M. S. Watson). I find that, in the light of Romer's results from other groups of vertebrates, many of Westling's homologies can no longer be ac- cepted; moreover they are unaccompanied by any figures. Although since the days of Cuvier and Meckel there have been other, partially illustrated, descrip- tions by Mivart, Alix, Coues, Manners-Smith and Frets, the homologies of these investigators are for the most part equally unacceptable, so that a new and fully illustrated description of these muscles seems to be needed. I have myself dissected specimens of Romer's three types, and also of other lizards and of the marsupial Sarcophilus, and I have had the opportunity of discussing some of the difficult points with Dr Romer himself, convincing myself of the validity of almost all his homologies. Most of the pelvic and thigh muscles of Ornithorhynchus can readily be brought into line with these. As might be expected, they are essentially mammalian in their arrangement but sometimes still suggest a reptilian origin. A few appear to be unique.

1 Romer (1922), "The Locomotor Apparatus of Certain Primitive and Mammal-like Reptiles. Bull. Am. Mu8. Nat. Hist. XLVI. Pelvic and Thigh Mucltes of Ormithorhynchus 153

I. MUSCLES SEEN WITH THE ANIMAL ON ITS SIDE "Cruro-coccygeus." Origin. In front by a few fibres arising from the anterior end of the iliac blade at its internal corner. Then along a short tendinous raphe stretching between this and the spine of the first sacral vertebra superficial to spinalis and semispinalis lumborum. Then along the spines of the first sacral to the fifth caudal vertebrae. Then from the fascia of the tail external to all the tail muscles, and a little way on to the ventral surface of the tail beneath the transverse process of the fifth caudal vertebra (or thereabouts). Insertion. (a) By a wide, flat tendon which passes round the back of the ankle, onto the under surface ofthe foot internal to the origin of gastrocnemius and (in the male) external to the spine. Here it is superficial to all the tendons of the leg muscles. (b) By a partly fleshy, partly tendinous insertion on to the preaxial border of the tibia, internal to gracilis and just distal to the insertion of semimembranosus and semitendinosus. This enormous muscle is the hardest of all the monotreme muscles to inter- pret. I should judge it to be used by the animal in kicking back the earth scraped outfrom the burrow, and know of nothing that really corresponds to it in any reptile or higher mammal. Against its being part of glutaeus maximus, as it has usually been named (e.g. Manners-Smith', Westling2), is its insertion; this is on the lower leg, to which it passes superficially to biceps, instead of on the femur internal to biceps. Its mode of insertion would seem rather to relate it to a part of the reptilian flexor mass, the origin of which had not travelled down the ilio-ischiadic (mammalian sacro-ischiadic) ligament to the tuber ischii, as that of the semimembranosus and semitendinosus of most mammals has done. It may be related to the cruro-coccygeus of Didelphys, a slender muscle passing from the side of the tail to the lower leg, and represented in various other mammals by slips joining or accompanying semitendinosus or biceps (Romer, p. 573). This, Romer suggests, may further represent the long tendon of the reptilian caudi-femoralis (caudi-femoralis longus). The primitive caudi-femoralis is, as Romer points out, closely associated with the long flexor muscles, inserting into the flexor mass in Urodeles and primitive frogs. Frets3 calls the anterior part of the disputed muscle in Ornithorhynchus glutaeus maximus, the hinder part caudo-femoralis. Biceps [Reptilian ilio-fibularis; Romer, p. 564]. Origin. From the ischial tuberosity. Passes deep to "cruro-coccygeus" and superficial to all the femoral muscles. 1 Manners-Smith (1885), "On some points in the Anatomy of Ornithorhynchlu paradoxwu," Proc. Zool. Soc. 2 Westling (1889), "Anatomische Untersuchungen uber Echidna," Bihang k. Svenska Vet.- Akad. Handlingar, xv. 3 Frets (1910), "tOber den plexus Jumbo-sacralis, U.s.W.," AMorphol. Jahrb. xL. Anatomy ix 11 154 Helga S. Pearsron

--BiC.

Fig. 1. The right pelvic and thigh muscles of Ornithorhynchu8, as seen with the animal on its side. BIC. =biceps; CLO. =cloacal pouch; COC. =ischio-coccygeus; GAS. =gastro-

cnemius; GLU. 1, 2. = glutaeals; PYR. = pyriformis; REC. = rectus; VAS. = vastus; X. = "cruro-coccygeus." Pelvic and Thigh Mumcle8 of Ornithorhynchus 155 Insertion. Into the fascia covering the lower leg muscles on the anterior and external surface of the lower leg. Glutaeals [Reptilian ilio-femoralis; Romer, p. 570]. In Ornithorhynchus there are two glutaeal muscles. (a) ( = " Glutaeus medius " of Westling and Frets). Origin. By a thin tendinous margin immediately under the fleshy origin of " cruro-coceygeus." Passes to the femur superficial to the axial musculature and to the other glutaeal. Insertion. On the posterior (external) border of the femur at the distal extremity of the crest running down that border from the great trochanter. The area of insertion is small, and distal to the long one of the other glutaeal. (b) ( = " Glutaeus minimus " of Westling and Frets). Origin. From nearly the whole of the glutaeal fossa of the ilium. Passes backwards and outwards, covering the origins of rectus and vastus. Insertion. On to the dorsal surface of the great trochanter and the crest running from that trochanter down the posterior (external) border ofthefemur. The first of these two glutaeals, (a), corresponds most nearly to the Eu- therian glutaeus maximus, the second, (b), to a fused glutaeus medius and minimus. In neither of my specimens was there any sign of a division of this second glutaeal into two, as described by Manners-Smith. Pyriformis [Reptilian caudi-ilio-femoralis? Romer, p. 572]. Origin. From the transverse process of the second caudal vertebra just dorsal to the anterior fibres of ischio-coccygeus. Insertion. On the ventral surface of the femur beyond the obturator insertions, and close to the most distally inserting part of the glutaeus, on the posterior (external) border of the bone. For this, as for the other muscles from tail to limb, it is hard to find the reptilian equivalent. The American workers have suggested that it is the reptilian caudi-ilio-femoralis (coccygeo-femoralis brevis). This in reptiles "inserts by a tendon into the femur part way down the shaft, reaching the bone between ilio-femoralis and the adductors" (Romer, p. 572). In higher mammals pyriformis inserts on the ventral surface of the great trochanter. The monotreme muscle, although undoubtedly representing the pyrifornis of higher forms, has an insertion some way down the shaft of the femur, in the position of the reptilian caudi-ilio-femoralis. This makes the suggested homology a very probable one. Rectus [= Reptilian caput iliacus triceps or extensor ilio-tibialis; Romer, p. 562]. Origin. From a small area on the ilium immediately in front of the acetabulum. There is a distinct tubercle for it at the acetabular end ofthe ridge between the glutaeal and iliac fossae of the ilium. f 11-2 156 Helga S. Pearson Passes between the glutaeals and ilio-psoas and then superficial to vastus. Its insertion may be taken with that of vastus below. Vastus [= Caput femoralis triceps or femoro-tibialis; Romer, p. 564]. Origin. From the whole of the dorsal surface of the femur except for the insertion places of the glutaeals and ilio-psoas on the dorsal surfaces of the two trochanters. The muscle has a thick fleshy body lying between vastus and the femur. Insertion. Together with rectus on the patella and patella ligament. Sartorius [= Caput acetab. triceps or Ambiens; Romer, p. 563]. Origin. From the extremity of the ilio-pectineal spine (the long process projecting forwards from the anterior border of the pubis just below the ilio- pubic symphysis). Insertion. On the front of the knee joint, proximally to and in a line with the insertion of gracilis, and at some little distance beyond the insertion of the adductors. As pointed out by Romer the sartorius of monotremes, like the ambiens of reptiles, arises from the pubis in front of and a little below the acetabulum, instead of from the superior iliac spine as in most higher mammals. Mono- tremes are unique, however, in having the anterior border of the pubis in this region drawn out into what I have termed above the ilio-pectineal spine, and it is from the tip of this spine that sartorius takes origin.

II. MUSCLES SEEN WITH THE ANIMAL ON ITS BACK Gracilis [= Reptilian pubo-ischio-tibialis; Romer, p. 570]. Origin. Mid-ventrally from the whole length of the pelvic symphysis and forwards from here along the median border of the "marsupial" bone for about two-thirds of its length. Passes superficial to the adductors, completely concealing them. Insertion. On the anterior border of the tibia just external to the insertion of the adductors and of " cruro-coccygeus." The insertion is a long one, reaching about half way down the tibia from the insertion of sartorius on the knee joint. Semitendinosus and semimembranosus [= the Reptilian flexor tibialis internus and externus group; Romer, p. 570]. Origin. Along the hinder border of the ischium, between the origin of biceps on the ischial tuberosity and that of gracilis on the pelvic symphysis. The two muscles are imperfectly separated. They are hidden by gracilis ventrally and by biceps postero-dorsally. Semitendinosus has the more dorsal origin, spreading a little anteriorly to the ischial tuberosity until its area of origin borders on that of the dorsal obturator muscle. Insertion. Into the strong ridge that runs down the anterior (mesial) border of the tibia. The insertion reaches from that of the adductors at the knee joint, Pelvic and Thigh Muscles of Ornithorhynchus 157

/ bCLO,

,-ADD)3. S.MEM. ~~FN + 5.TEN.

k 'OBT.1 23.I \ =?YR X.

bS.MEM.+S.TEN.

Fig. 2. The right pelvic and thigh muscles of Ornithorhynehws, as seen with the animal on its back. ADD. 1, 2, 3. = adductors; BIC. = biceps; CLO. = cloacal pouch; COC. = ischio-coccygeus; F. = femur; GAS. = gastrocnemius; GRA. = gracilis; IL. PSO. = ilio-psoas; OBT. 1, 2, 3. = obturators (including gemelli, etc.); PEC. = pectineus; PYR. = pyriformis; REC. = rectus; SAR. = sartorius; S.MEM. = semimembranosus; S.TEN. = semitendinosus; T. = tibia; VAS. = vastus; X. = "cruro-coccygeus." 158 Helga S. Pearson downwards within those of sartorius and gracilis for about one and a half centimetres, where it touches the insertion of " cruro-coccygeus." Adductors [= Reptilian ischio-femoralis or pubo-ischio-femoralis; Romer, p. 571]. So much confusion exists in the use of the terms "brevis," "longus," "parvus," "magnus," differently applied by different writers to the several mammalian adductors, that I shall not here attempt to distinguish them by any of these names. The adductor mass in Ornithorhynchus is divided at its origin into three: 1. The most anterior adductor. Origin. From the little tubercle ("pubic tubercle") which projects from the pubis just lateral to its articulation with the "marsupial" bone. This muscle covers theventral surface ofpectineus and insertstogetherwith: 2. The median adductor. Origin. Along the articulation of the " marsupial " bone with the pubis, and on the anterior border of the pubis just behind this articulation and in front of the origin of obturator externus. It is covered externally by gracilis, bordered behind by semimembranosus, and in front by the anterior adductor. Insertion. Together with the anterior adductor on the inner side of the knee, on the medial condyle of the femur, just above the insertion of semimembranosus on the tibia. 3. The posterior adductor. Origin. Immediately lateral to the pelvic symphysis (which is occupied by gracilis) and near to its posterior end, where it is practically confluent with semimembranosus. A small muscle, almost entirely concealed by semimembranosus and by the median adductor. Insertion. Its fibres are lost among those of the median adductor before reaching the knee. The ischio-femoralis of lizards inserts towards the proximal end of the femur. In higher mammals the adductors usually have a long insertion area on the ventral (posterior) surface of the femur, but more distally than in lizards. This area is left bare in Ornithorhynchus, where the adductors insert entirely at the distal end of the femur. In Echidna, however, Frets finds that they insert " on the distal third of the median margin and onthe tibial condyle." Professor Watson has suggested to me that the condition in Ornithorhynchus is associated with the swimming habits of that animal. Pectineus [= part of Reptilian pubo-ischio-femoralis internus; Romer, p. 565]. Origin. From the anterior border of the girdle between the attachment of the " marsupial" bone and the extremity of the ilio-pectineal spine. Pelvtc and Thigh Mu&cles of Ornithorhynchus 159 Lies between the more superficial sartorius and the deeper ilio-psoas. Insertion. About midway along the anterior (median) border of the femur at the distal end of the ridge leading down that border from the lesser trochanter. The area of insertion is sometimes marked by a slight prominence on the femur. It is probable, as Romer has shown, that most of the reptilian pubo-ischio- femoralis internus has in mammals migrated upwards on to the ilium and lumbar vertebrae as the ilio-psoas, but that the small pectineus represents a portion that has retained almost its original position. Ilio-psoas [= main part of Reptilian pubo-ischio-femoralis internus; Romer, p. 565]. Psoas and iliacus form practically one continuous mass. Origin. The ventral surface of the presacral vertebrae from about half way along the animal's back to the sacrum (= psoas minor), from the anterior sacral vertebrae (= psoas major) and from the whole of the iliac fossa of the ilium (= iliacus). Insertion. The more anterior part representing psoas minor inserts on the ilio-pectineal spine alongside sartorius. The more posterior part (psoas major and iliacus) inserts on the dorsal surface and anterior (median) border of the femur. This latter area of insertion is a triangular one, reaching from the extremity of the trochanter minor to about half way down the shaft of the femur. Obturators. The obturator externus, quadratus femoris, gemelli and obturator internus of higher mammals are represented by the following muscles inOrnithorhynchus. A. A mass which lies beneath the adductors and arises partly from the membrane covering the obturator foramen but chiefly from the bordering parts of the girdle. At its origin this mass is divided into: (1) The most anterior obturator muscle ("obturator intermedius" of Westling). Origin. From the pubis anterior to the obturator foramen, between the latter and the base of the marsupial bone. A few fibres may take origin from the membrane covering the foramen itself. Insertion. Together with (2) described below. (2) The median obturator ("obturator externus" of Westling). Origin. From a large area on the ventral part of the ischium and pubis, below and posterior to the obturator foramen, under cover ofsemimembranosus and gracilis. Lies immediately over the obturator foramen and some of its fibres may take origin from the membrane covering the latter. Insertion. Together with the anterior obturator on to a wide area on the ventral surface of the femur at its proximal end. Most of the fibres of the 160 Helga S. Pearson

GLU.1 2 Fig. 3. Deep lateral aspect. H.F. = head of femur. Other letters as in preceding figures.

Fig. 4. Deep ventral aspect. Lettering as in fig. 2. Pelvic and Thigh Mwucles of Ornithorhynchus 161

:-*.3 ,/ _w~;

S'A R.

pIC. , 'ADD.1.

FirEN ADD2 AUD2 G;RA

Fig. 5. Pelvis of Ornsithorlychu from the right side with muscle areas indicated by dotted lines. ADD. 1,2,3. = adductors; BIC. = biceps; GRA. = gracilis; GLU. 2 = deeper glutaeal mediums + minimus); ILPSO.

= ilio-psoas; OBT. 1, 2. = obturator externus (+ quadratus femoris?); OBT. 3. = ?obturator "internus" + gemelli; PEC. = pectineus; REC. = rectus; SAR. = sartorius; S.MEM. = semimembranosus; S.TEN. = semitendinosus.

R.N N\. -T R- TMi- M. "I .3.

\' RsiN

-'CTD3 L<.##'-OE'y O-,T. X t

Fig. 6. Dorsal (to the left) and ventral (to the right) aspects of the right femur of OrnithorhynchuA. Muscle areas indicated by dotted lines.

ADD. = adductors; GAS. = gastrocnemius (internal head); GLU. 1. = glutaeus "maximus"; GLU. 2. = glutaeus "medius + minimus"; IL.PSO. = ilio- psoas; OBT. 1, 2. = obturator externus (+ quadratus femoris?); OBT. 3 = ? obturator "internus" + gemelli; PEC. = pectinus; PYR. = pyriformis; TR.MAJ. = trochanter major; TR.MIN. - trochanter minor; VAS. = vastus. 162 Helga S. Pearson median obturator, which has large fleshy origin but tapers distally, insert on to a low crest bounding this wide area posteriorly and dividing it from the smaller area of insertion of the " obturator internus " to be described below. This mass (headed A above) clearly represents the obturator externus of higher mammals and probably also the quadratus femoris. B. A smaller but nevertheless quite stout muscle. Origin. Along the dorsal border of the ischium from just behind the acetabulum to the origin of semitendinosus and biceps on the tuber ischii. Insertion. On the ventral surface of the trochanter major and of the crest passing from the latter down the posterior (external) border of the femur. This muscle has been variously homologised with obturator internus, the gemelli, quadratus femoris and the superior part of obturator externus. By its insertion it would appear to represent obturator internus and the gemelli of higher mammals. Unlike the latter, Ornithorhynchus has no true obturator internus taking origin from the inner surface of the ischium. The muscle just described is completely excluded from that surface by the broad insertion of ischio-coccygeus. Romer (p. 569) wishes to derive the typical obturator internus from the reptilian ischio-trochantericus (pubo-ischio-femoralis posterior), a small muscle arising from within the pelvis posteriorly and passing out over the dorsal border of the ischium to insert into the proximal end of the femur. He shows that in primitive fossil reptiles such as Diadectes and Dimetrodon, and in some Therapsid (or "mammal-like") reptiles such as Moschops, there is a small but well-marked fan-shaped muscle area "just within the dorsal border of the ischium and converging to the representative of the 'lesser sciatic notch'." In other words, he thinks that a femoral muscle arising from within the pelvis posterior to the ilium is far older in origin than the mammals, although in many of these it acquires a new importance, becoming much larger and spreading down within the pelvis over the obturator region. If this view is correct the monotreme condition cannot be intermediate between primitive reptiles and higher mammals, for the monotremes have either lost the ischio-trochanteric muscle or it has been pushed up on to the dorsal border of the ischium by ischio-coccygeus. I have elsewhere suggested that the disputed muscle in monotremes might well, both from its origin and from its insertion, represent the postero-dorsal division of the big reptilian pubo-ischio-femoralis externus (the other divisions of which become obturator externus). Yet, except that it does not reach down within the pelvis at its origin, it has undeniably the appearance of an obturator internus muscle'. It is therefore possible that the modern placental obturator 1 It may be noted that even in some marsupials the obturator internus consists of only a few insignificant fibres. Macalister, 1870 and 1872, Mag. Nat. Hist. 4th ser. vols. v and x, reports that there is no obturator internus in either Phascolomys or Sarcophilus. In a Sarcophilus which I myself dissected, however, I found a thin slip of muscle arising from well within the pelvis. This became tendinous where it rested on the surface of another muscle ("gemelli") arising from the postero-dorsal border of the pelvis by an origin almost as extended as that in monotremes. The ischio-coccygeus muscle inserted, as in placentals, anterior to the slender obturator interns but not completely anterior to the representative of the gemelli. Pelvic and Thigh Mwmcles of Ornithorhynchus 163 internus was notderivedfromthe modern reptilian ischio-trochantericus (in this case anindependentandsomewhat parallel development), butfrom amuscletak- ingorigin from the outersurface anddorsalborderofthehinderpartofthegirdle. The gemelli of placentals would represent some fibres of that muscle which did not migrate down within the pelvis. This might help to solve the problem of ischio-coccygeus, which inserts in placentals anterior to obturator internus, permitting its derivation from the reptilian ischio-caudalis, a powerful muscle passing from the tail to the ischial tuberosity and inserting posterior to ischio- trochantericus. The monotremes would represent an intermediate condition, for in them ischio-coccygeus has so wide an insertion within the girdle that there is no room for any other muscle to arise there, be its origin that of an ischio-trochantericus or that of an obturator internus. Might not the muscle area in Permian reptiles which Romer ascribes to the origin of an ischio- trochantericus equally well be the insertion of an ischio-caudalis? Certainly in Romer's figures of Dimetrodon and Moschops it lies in the position of the insertion area of ischio-coccygeus in Ornithorhynchus. Ischio-coceygeus [= all or part of Reptilian ischio-caudalis?]. Origin. From the transverse processes of the second, third, fourth and fifth caudal vertebrae. The fibres arising from the second caudal vertebra are beneath those of pyriformis. Insertion. On the inner surface of the ischium close to the origin of the dorsal obturator along its dorsal border. The homologies of this muscle I have just discussed in relation to those of the obturators. If it really represents ischio-caudalis it has become very much shortened, but that is true of all tail muscles in the change from reptile to mammal, when the tail ceases to be of importance in locomotion.