structural correlates of forelimb function in fur seals and sea lions

Structural Correlates of Forelimb Function in Fur Seals and Sea Lions

ARTHUR WM. ENGLISH Department of Anatomy, Emory Unioersity, Atlanta, Georgia 30322

ABSTRACT Dissections, manipulation of ligamentary preparations, analysis of limb proportions, and quantitative aspects of forelimb myology are used to correlate forelimb morphology in fur seals and sea lions (sub-family Otariinae) with pre- viously published data as to their locomotor function (English, '76a). Comparisons to structure and function in generalized fissiped carnivores are then used to elucidate locomotor adaptations in fur seals and sea lions. Unique features of forelimb function during swimming in these pinnipeds include the amounts of abduction-adduction and rotary movements used. Modifications of the size, attachments and fascicle architecture of the muscles and the structure and range of possible movement of the joints suggest that in fur seals and sea lions these movements (1) take place about the glenohumeral (shoulder) joints, (2) that the movements are probably finely controlled, and (3) that they contribute to the generation of massive forward thrust via the cooperative activity of muscles capable of generating large amounts of force throughout the range of movement. Recovery movements occur through a similarly large range, and modifications of forelimb anatomy either to minimize or overcome water resistance are noted. The adaptive significance of these modifications is interpreted as allowing fur seals and sea lions to swim at speeds necessary to feed on the fast swimming prey presumably abundant in their adaptive zone.

Fur seals and sea lions comprise a single carnivore sub-family, the Otariinae (sensu Mitchell and Tedford, '73). All are littoral, feeding on fish and large, mobile inverte- brates such as squid (Davies, '58; King, '64; North Pacific Fur Seal Commission, '75) whose capture may require considerable swimming speed. Indeed, swimming speeds of 18-37 km per hour have been reported (Lorenz, '69; Scheffer, '58; Walker, '68). Since all fur seals and sea lions swim using a bilateral paddling action of the forelimbs, their forelimbs might be expected to con- tain adaptive features associated with the production of rapid aquatic locomotion needed for the capture of elusive prey. To elucidate some of these locomotor adaptations, forelimb structure is correlated with locomotor function in fur seals and sea lions.

Previous attempts to correlate forelimb structure and locomotor function in fur seals and sea lions, notably the studies of

Gambarjan and Karapetjan ('61) and Howell ('29, '30), have relied heavily on interpretations of function which were derived from structure rather than from com- bined structural and functional studies. They also have been limited largely to qualitative studies of muscle attachments so that basic mechanical considerations of the muscle attachments and limb proportions, the movements and structure of the joints, the relative sizes of the muscles, and the implications of the arrangement of the muscle fascicles were not included. In addition, neither of the studies cited above considered forelimb anatomy and function in sea lions and fur seals in relation to that of less specialized forms, especially fissiped carnivores. Thus, attempts of these papers to identify adaptive specializations in the forelimbs of fur seals and sea lions were made on the basis of limited knowledge of structure and function.

This paper attempts to correlate fore-

J. MORPH., 151: 325-352. 325

326 ARTHUR WM. ENGLISH

limb structure with locomotor function in fur seals and sea lions on the basis of more detailed knowledge of both than the previous studies. Forelimb morphology of fur seals and sea lions is characterized by deviations from a morphological plan that is characteristic of generalized fissiped carnivores. These divergences are correlated with peculiarities of locomotor function, established primarily by recent cinemato- graphic study of locomotion in the Califor- nia sea lion (Zalophus californianus) (En- glish, '74; '76a). Less intense observation of locomotion in fur seals suggests that their forelimbs function similarly. The morphological plan was established by examination of the forelimbs of fissipeds such as the olingo (Bassaricyon alleni), the cacomistle (Bassariscus astutus), the wolverine (Gulo gulo), the marten (Martes americana), and the raccoon (Procyon lotor). These were chosen because their forelimb morphology is similar and because it resembles published descriptions of the forelimbs of such fossil fissipeds as Cynodictus gregarius (Wortman and Matthew, 1900) and Dapho- enus felinus (Hatcher, '03). The forelimbs of other fissipeds were considered to highly adapted to cursorial, arboreal, fossorial, semi-aquatic or semi-graviportal ways of life to form a basis for comparison. Forelimb morphology in the generalized forms presumably reflects the framework from which the forelimbs of fur seals and sea lions were derived. Departures from this framework thus are assessable in terms of adaptations to the unique type of locomotion required for their aquatic mode of life.

Analysis of locomotor behavior (English, '76a) suggests that modifications of forelimb structure in fur seals and sea lions might be related to the production of massive locomotor thrust and to the restructuring of the manus to form a flattened paddle or hydrofoil. Restructuring of the manus is brought about by a complex modification of the carpus and digits and is dealt with more cogently in separate com- munication (English, '76b). The result of

correlating forelimb structure and locomotor function in this paper is the elucidation of adaptive modifications associated with the specialized aquatic locomotor require- ments of fur seals and sea lions.

MATERIALS A N D METHODS

Specimens for gross dissection were obtained from a wide variety of sources and included captive and wild animals in approximately equal proportions. The specimens dissected were generally fixed in formalin, though some of the dissections and manipulations were performed on unfixed material. Pinniped forelimbs dissected included six Northern fur seals (Cal- lorhinus ursinus), five California sea lions (Zalophus calqornianus), two Steller sea lions (Eumetopias jubata) and one South American fur seal (Arctocephalus austra- l i d . Except for the Steller sea lion specimens, which were from a juvenile, all specimens were obtained from adult animals. For comparison, forelimbs of single specimens of a wolverine (Gulo gulo), a marten (Martes americana), and a raccoon (Procyon lotor) among the generalized fissipeds, and a river otter (Lutra lutra), a sea otter (Enhydra lutris), a least weasel (Mustela rixosa), a domestic cat (Felis catus), and a domestic dog (Canis fa- miliaris) among more specialized fissipeds were dissected.

In each dissection, the muscles were re- moved at their bony attachments and the investing fascia and connective tissue dissected free. This allowed correlation of sites of muscle attachment and bony land- marks that could be used as reference points in studies of osteological material. The length of centrally-located fascicles of each muscle was measured, the muscle was blotted to remove excess fluid, and weighed. Care was taken to avoid dessica- tion or excessive hydration of the muscles during these procedures.

After removal of all of the muscles and excess connective tissue, the resulting ligamentary preparations were manipulated to determine the types and ranges of move-

FUR SEAL AND SEA LION FUNCTIONAL ANATOMY 327

ment possible at each joint. The connective tissue structures limiting or controlling movements were noted. Joints were not forced into naturally impossible positions. In addition, radiographs taken at the ends of ranges of possible movements and manipulation of partially disrupted ligamentary preparations allowed determination of

the movements of the articular surfaces. Measurement of the anatomical limit of joint movements was made from the radiographs, directly from the manipulated specimens, or both.

Osteological material of all of the extant genera (sensu King, '64) of otariines was examined and supplemented by exam-

Zalophus califoonianus, right scapula. (a) Lateral and (b) medial views of the scapula. (c) and (d) muscle maps of same. Legend: vb, vertebral border; cb, cranial border; ab, caudal border; st, supraglenoid tuberosity; it, infraglenoid tuberosity; m, caudal aspect of acromion process; sr, scapular ridge; cr, caudal scapular ridge; Bi, Biceps brachii; AI, Atlantoscapularis; SSa, supraspinatus cranial; SSp, supraspinatus caudal; LS, anterior fibers of serratus ventralis (levator scapulae); RP, rhomboideus profundus; RC, rhomboideus capitis et cervicis; ST, spinotrapezius, AT, acromiotrapezius; IS, infraspinatus; D and dashed line on scapular spine, deltoideus; SM, posterior fibers of serratus ventralis (serratus magnus); TM, teres major; E, epitrochlearis; TLo, triceps longus; TLa, triceps lateralis; SBa, subscapularis cranial; SBm, subscapularis middle; SBp, subscapularis caudal; RD, rhomboideus dorsalis; the dashed line about the bottom of the bone marks the attachment of the capsule of the glenohumeral joint. Scale bar, 5 cm. See text for details.


ination of skeletons of generalized and specialized fissipeds. These examinations con- centrated on the sites of muscle attachment, shapes of articular surfaces, and relative limb proportions. Lengths of bones were measured according to their “functional length” as described by Howell (’44) and Hildebrand (’52) and were augmented by a series of linear measures that reflect sites of attachment of the muscles of the forelimb (see below). Nomenclature fol- lows Pierard (’71), except where noted.

OBSERVATIONS

Scapula The scapula of fur seals and sea lions (fig.

1) is fan-shaped, largely because of expansion of its angles. The convex supraspinous fossa is more than twice the size of the infraspinous fossa and is divided by a scapular ridge, to which is attached an aponeurosis dividing the enlarged supraspinatus muscle. A low spine ends in a small caudad- projecting acromion process that does not extend past the level of the glenoid fossa. The infraspinous fossa is bordered caudad by a caudal scapular ridge coursing from near the vertebral border to the infraglenoid tubercle. The caudal scapular ridge

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marks the attachments of the long head of triceps brachii, epitrochlearis and infraspinatus, parts of the deltoid and lateral head of triceps brachii, and the caudal component of the subscapularis. The adjacent, expanded caudal scapular angle contains paired fossae housing the fleshy caudal fibers of the deltoid muscle and teres major. On the tip of the caudal angle is a third fossa, continuous with the medial surface of the scapula, that is a site of attachment of the caudal most fibers of the serratus ventralis muscle. The subscapular fossa is markedly concave except for more flattened areas along the cranial and caudal borders. The cranial flattened area serves as the site of origin of the cranial component of the subscapularis muscle. The caudal flattening, which is continuous with the caudal border and caudal scapular ridge, serves as origin to part of the fibers of the caudal component of the muscle.

In generalized fissipeds, the scapula is somewhat elliptical (fig. 2). The supraspinous fossa is only slightly larger than the infraspinous and contains no scapular ridge. The spine ends in prominent cranial and caudal projecting portions of the acromion process. The caudal margin of the infraspi-

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Fig. 2 Martes QfMriCQnQ, right scapula. The legend is the same as for figure 1 except that a, cranial aspect of acromion process; AD, acromoideltoideus; SD, spinodeltoideus. Scale bar, 5 em. See text for details.


nous fossa is marked by an upturned caudal border, the lateral margin of which forms an attachment of the long head of triceps brachii only. The caudal angle is not expanded and only the teres major inserts on its lateral surface. The deltoid muscle attaches to the caudal borders of the spine and acromion and not all onto the lateral surface or caudal angle. The serratus ventralis muscle attaches to the medial surface of the scapula only. The cranial portion of subscapularis occupies a small portion of the medial surface near the cranial border while the portion of the subscapular fossa housing the caudal component of the muscle is continuous with the caudal surface of the upturned caudal border.

Using many different methods, several workers have associated scapular shape in mammals at least in part with the attachments of the serratus ventralis muscle (mm. levator scapulae and serratus magnus of older literature) (e.g., Ashton and Ox- nard, '64; Davis, '64; Muller, '67; Oxnard, '67, '68; Roberts, '74; Wolffson, '50). Part of the fan-shape of the scapula of fur seals and sea lions is related to expansion of the scapular angles, on both sides of which this muscle inserts. The serratus ventralis forms a continuous muscle mass in all carnivores (Davis, '64), connecting the ribs and the transverse processes of the cervical ver- tebrae to the vertebral border of the scapula (fig. 3). Enlargement of the caudal part of the muscle can be associated with elongation of the caudal scapular angle, relative to that of fissipeds, and with reflection of its fibers onto the lateral surface of this angle. The cranial attachments are also more extesive than found in fissipeds and are reflected onto the lateral surface of the vertebral border. This latter reflection may be the source of the rhomboideus profundus muscle (m. atlantoscapularis superior of Howell, '29) which is very closely related to the most cranial slip of serratus ventrallis, much as suggested by Howell ('29), and by MacAlister (1873) and Barone and Deutsch ('53) in fissipeds. Since lateral reflection of the cranial fibers of the ser-

ratus ventralis muscle effectively reduces the area on the cranial portion of the vertebral border available for muscle attachment (where m. rhomboideus capitis et cervicis attaches in fissipeds), such reflection also might be associated with the insertion of the cranial rhomboids on the lateral surface of the scapula in fur seals and sea lions.

The attachments of other muscles are associated with scapular shape as well. Prox- imad and caudad migration of the scapular attachments of deltoideus found in fur seals and sea lions is also associated with expansion of the caudal scapular angle and with the relatively small size of the acromion process. The deltoid muscle (fig. 4) is found as a single mass, unlike the separation into acromiodeltoid and spinodeltoid in fissiped carnivores. Its proximal portion is aponeu- rotic and serves as a site of attachment of the superficial fibers of the acromiotrapezius muscle. Deep fibers of this muscle course from the first four thoracic ver- tebrae to the scapular spine, much as in fissiped carnivores, but the superficial fibers bypass the spine and insert onto the aponeurosis of the deltoid muscle. The distinct caudal scapular ridge found in fur seals and sea lions is correlated with the attachments of the deltoid and epitrochlearis and with the reflection of the caudal fibers of the caudal component of the subscapularis onto the lateral surface of the scapula. Enlargement of the supraspinous fossa and the development of a scapular ridge are correlated with enlargement of the supraspinatus (though as Howell "441 has noted, the extent of bony enlargement need not reflect the degree of muscular enlargement) and with development of an aponeurosis dividing the muscle. The orientation of pennate fascicles in the more cranial portion (fig. 5 ) is very complex, while the homologous portion in generalized fissipeds is smaller and often parallel-fibered (fig. 6). Differences in the more caudal division are less striking but the more complex orientation of fascicles in the pinnipeds is evident. The subscapu-

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FUR SEAL AND SEA LION FUNCTIONAL ANATOMY 33 1

Z M - Fig. 4 Right Deltoid muscle in Martes arnericana (M) and Zalophus cal i jhianus (Z). See text for

details. Scalebar, 5 cm

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Fig. 5 Cullorhinus ursinus, left intrinsic shoulder muscles, (a) lateral and (b) medial views. See text for details. Legend is as described above except: B, brachialis; MAF, musculature of antebrachial fascia (not described); LD, D and P refer to cut fragments of latissimus dorsi, deltoideus and pectoralis, respectively. Scale bar, 5 cm.


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Fig. 6 Gulo guEo, left intrinsic shoulder muscles; (a) lateral and (b) medial views. See text for details. Legend is as above except: CB, coracobrachialis. Scale bar, 5 cm.

laris muscle is so enlarged in fur seals and sea lions, that its cranial portion overlies much of the middle portion and was given a separate name, episubscapularis, in some previous studies (Miller, 1888; Howell, '29; Mori, '58).

Humerus The humerus of fur seals and sea lions

(fig. 7) is a short, massive bone whose most striking feature is its large deltoid crest, extending distad from the greater tuberosity for nearly two-thirds the length of the bone. Attached to the crest are the pectoralis, latissimus dorsi (pectoral portion), brachiocephalicus and deltoideus muscles. In small forms such as Callorhinus ursinus, the roughened apex of the crest is large and overhangs both its sides (Mitchell, '61), although it does not in large forms such as Eumetopias jubata. The humeral tuberosities, where the supraspinatus, infraspinatus and subscapularis muscles insert, are very large and the greater tuberosity extends above the level of the capitulum. Distal to the base of the lesser tuberosity is the site of attachment of the teres major and the teres portion of the latissimus dorsi muscle. Distad, the large medial epicondyle serves as an area for attachment of

fibers of the pronator teres, flexor carpi radialis, and internal anconeus muscles and sometimes part of the superficial portion of the digital flexor musculature, in addition to the medial collateral ligament of the elbow joint. The lateral epicondyle is less prominent than the medial and from it originates the superficial layer of carpal and digital extensors, the lateral collateral ligament of the elbow joint and, along the con- tiguous lateral supracondylar ridge, the brachioradalis and anconeus externus muscles.

The humerus of generalized fissipeds (fig. 8) is longer and more slender than that of fur seals and sea lions. Its distinct but low deltoid crest extends to only about the

Zalophus calijbaianus, right humerus. (a) cranial and (b) caudal views of the humerus, (c) and (d) muscle maps of the same. See text for details. Legend as above except: dc, deltoid crest; gt, greater tuberosity; It, lesser tuberosity; me, medial epicondyle; le, lateral epicondyle; Br, brachioradialis; ECR, extensor carpi radialis; EDC, extensor digitorum communis; ED, extensor digitorum lateralis; A h , aconeus internus; AE, anconeus externus; FDC, flexor digitorum communis, FCR, flexor carpi radialis; PT, pronator teres; TMe, triceps medialis; the dashed lines mark the position of the articular capsules of the glenohumeral and elbow joints; large arrow marks the trochlear notch. Scale bar. 5 cm.

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a b Fig. 8 Martes americana, right humerus, muscle maps in (a) cranial and (b) caudal views. See text

for details. Legend as above except: FDS, flexor digitorum superficialis; FCU, flexor carpi ulnaris; PL, palmaris longus; ECU, extensor carpi ulnaris; ef, entepicondylar foramen. Scale bar, 5 cm.

proximal one-third of the bone. The greater and lesser tuberosities are small, and both lie below the level of the capitulum. Attached to the large medial epicondyle are the pronator teres, flexor carpi radialis, flexor digitorum superficialis, flexor carpi ulnaris, palmaris longus, and anconeus internus, and the medial collateral ligament of the elbow joint. On the lateral epicondyle, especially its caudal surface and the adjacent supracondylar ridge, are sites of attachment of carpal and digital extensor muscles and brachioradialis and anconeus externus.

The extraordinary development of the deltoid crest in fur seals and sea lions is unparalleled in any fissiped and is associated with enlargement of the sites of muscle attachment, especially those of the pectoralis muscle and the pectoral portion of the latissimus dorsi. Pectoralis is very much larger and its attachments more complex than found in fissiped carnivores. Its superficial portion (fig. 3) attaches to the distal tip of the deltoid crest and continues as an aponeurosis in the superficial layer of forearm fascia, finally attaching to the skin and connective tissues overlying the palm. Its

deep portion attaches to the length of the medial surface of the crest along with the tendons of pectoralis fibers arising from the xiphoid process and abdominal fascia, the posterior component of panniculus carnosus and the tendon of the pectoral portion of latissimus dorsi. The four muscles together form the lower ramus of an axil- lary arch about the brachial plexus, the upper ramus being formed by the teres major and the associated tendon of latissimus dorsi. This insertion of latissimus dorsi as pectoral and teres portions is also found in fissiped carnivores (LDt is cov- ered by the crest in fig. 8) but the relative proportion of muscle associated with each

Fig. 9 Zalophus californianus, right ulna and radius. (a) lateral and (b) medial views of the bones; (c) and (d) muscle maps of the same. See text for details. Legend as above except: rf, radial fovea; bt, bicipital tubercle; r, radial styloid process; u, ulnar styloid process; large arrow marks attachment of medial collateral ligament of elbow joint; small arrows mark grooves for tendons of flexor carpi radialis (fcr) ; flexor digitorum communis (fdc), extensor carpi radialis (ecr), extensor pollicis longus (epl), abductor pollicis longus (apl); S, supinator; EPL, extensor pollicis longus; APL, abductor pollicis longus. Scale bar, 5 cm.

FUR SEAL AND SEA LION 335 FUNCTIONAL ANATOMY


insertion is more variable. In generalized fissipeds, approximately half of the fibers of the muscle attach to each tendon; in fur seals and sea lions, about 80% of the muscle fibers are associated with the more distal pectoral insertion.

The enlarged medial epicondyle of fur seals and sea lions is also of note, since relatively little musculature originates there. The pronator teres, flexor carpi radialis and internal anconeus muscles arise there but the flexor carpi ulnaris, palmaris longus, and most of flexor digitorum communis, which take origin from the medial epicondyle of generalized fissipeds, do not (see below). The very large medial collateral ligament of the elbow joint may be a more significant occupant of the medial epicondyle since both its humeral and antebrachial attachments are more extensive than in any fissiped examined.

Ulna and radius The bones of the forearm of all members

of the Otariinae (fig. 9) are dorsoventrally flattened. The ulna is broadened proximad by its large olecranon process and narrows distad, terminating in its styloid process.

. P Q S

The radius is narrow and rounded near its fovea and broad and flat near its distal end. Mediad the concave olecranon process contains a prominent ridge that divides the fibers of origin of the flexor carpi ulnaris and flexor digitorum communis muscles. Along the radial border of the ulna, the medial surface is rugose from the attachment of the medial collateral ligament of the elbow joint. The lateral and caudal sides of the olecranon process are roughened and serve as sites of insertion of the muscles of the triceps complex. More distad a ridge divides depressions which house fibers of the abductor pollicis longus and extensor carpi ulnaris muscles. The medial surface of the radius contains a prominent bicipital tubercle where the biceps brachii inserts and a roughened area along its radial border for insertion of the pronator teres. Distad are prominent fossae in which the tendons of flexor carpi radialis and flexor digitorum communis lie. Three similar grooves are found on the lateral surface and house tendons of abductor pollicis longus and the paired tendons of extensor carpi radialis. The lateral surface contains a prominent lip marking the

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Fig. 10 Procyon lotor, right ulna and radius, muscle maps showing (a) lateral and (b) medial views. See text for details. Legend as above except: FDP, flexor digitorum profundus; PQ, pronator quandratus; LI, interosseous ligament. Scale bar, 5 cm.


attachment of the tendon of the brachioradialis.

In the antebrachial skeleton of fissipeds the bones are not flattened but cross each other, since the manus is pronated at rest (fig. 10). Along the radial border of the ulnar shaft are located a pit where the brachialis muscle attaches, a line marking the extent of the interosseous ligament, and a bony plate marking the ulnar attachment of the pronator quadratus muscle. The radius is bent into a sigmoid curve that allows pronation of the manus to place the digits in a sagittal plane during quadrupe- dal support and locomotion. Other muscle attachments are substantially similar to those of fur seals and sea lions.

The more extensive flattening of the forearm bones of fur seals and sea lions in comparison to generalized fissipeds may reflect a trend toward overall limb flattening associated with flipper formation but also may be related to providing an extensive area for muscle attachment. The olecranon process forms the sole source of origin of flexor and extensor carpi ulnaris, both of which display some humeral origin in fissipeds (cf. figs. 7 and 9 ,8 and 10). The digital flexors and extensors also have more extensive humeral origin in fissipeds than in fur seals and sea lions. The antebrachial musculature exerts less influence on the elbow joint than in fissiped carnivores since fewer muscles cross the joint. The elbow joint might thus display less tendency to be disrupted by simultaneous palmar flexion of the wrist and digits and elbow extension, as proposed by Jenkins ('73), than in fissipeds.

Limb proportions During locomotion the limb bones of

quadrupeds are said to act as rigid levers which are operated by the limb muscles about their joints and therefore are amena- ble to analysis by Newtonian mechanics (Gray, '44). Forward thrust is generated by the application of a muscular force to the limb. The force may produce a torque whose magnitude is dependent on the amount of force applied by the muscle (fig. 11) and its moment arm-the perpendicu-

lar distance between the line of action of any force capable of inducing rotation (in this case that produced by the muscle) and the center of rotation of the limb. The ground on which a terrestrial quadruped stands usually resists the torque by a reaction which causes the body to be propelled past the limb. In water the reaction of the

duction of thrust in a similar manner Pro- En- water on moving limbs contributes to

glish, '76a). The magnitude of this pro-

I h

Fig. 11 Mechanics of forelimb thrust production. See text for details. Fr, force vector of a retractor muscle; m, moment arm of muscle; h, resistance arm of limb; R, resistance of ground; H, propulsive force applied to the body by the limb.


pulsive reaction force depends on the magnitude of the torque applied to the limb and the vertical distance between the center of rotation of the limb and the reaction force (its moment arm), the resistance arm of the limb. The ratio of the moment arm of each limb muscle to the resistance arm of the limb (Maynard Smith and Savage, ’56) is thus an indicator of the extent of conver- sion, by geometry, of the effort of that muscle into a propulsive force. These measures of limb geometry also determine to some extent the rate with which a limb can be moved, both in terms of average velocity (elapsed time between two positions), and the velocity at various points in a movement (see Stern, ’74, for further discussion). At a constant rate of muscular shortening and constant load, muscles with small moment arms are said to be advantageous in producing a high velocity at some point during the movements via a small, but prolonged angular acceleration. Muscles with large moment arms are favorable for producing limb movements to be accomplished in short periods of time by a short but large angular acceleration (Stern, ’74) * The diagram in figure 11 portrays the

point of rotation of the entire forelimb as passing through the glenohumeral (shoulder) joint, much as suggested by Gray (’44) and Maynard Smith and Savage (’56). Although the position of the axis of rotation of the forelimb of fur seals and sea lions is not now known, recent work in cats (Miller and van der Meche, ’75; English, ’75 and unpublished data) supports an earlier observation of Hildebrand (’61) that the axis of rotation of the forelimb lies proximal to the glenohumeral joint in fissipeds. One effect of this more proximal point of rotation of the forelimb would be a change in the value of the moment arm of the muscle in figure 11 (and, indeed, all other muscles) and the resistance arm of the limb. However, the definitions of moment arms of muscles, the resistance arm of the limb and their functional implications would remain the same.

Accordingly, the proportions of the

forelimb of fur seals and sea lions and generalized fissipeds were analyzed with regard both to the functional lengths of the bony elements and to bony lengths that are correlated with the moment arms of forelimb muscles (fig. 12). Each length is expressed as a function of published average values of head and body length (Walker, ’68) for purposes of comparison and is listed in table 1. Values for sea lions and fur seals and for generalized fissipeds are grouped rather than listed according to genus because within each group, one-way analysis of variance proved insignificant at the 0.05 level. In other words, variation between genera of each group was no greater than variation within samples of each genus. Statistical significance between means of the two groups was tested using a t-test.

Use of single published values of head and body length as a comparable measure of body size in the two groups might be questioned, since these average values of

Fig. 12 Measurements taken on (a) scapula, (b) humerus, and (c) ulna and radius. All measures of length were “functional” length as described by Howell (’44). Legend: DC, length from humeral capitulum to distal end of deltoid crest; TM, length from humeral capitulum to distal insertion of fibers of teres major; 0, length of olecranon from insertion of triceps musculature to center of ulnar articular surface; BT, distance from ulnar center to center of bicipital tubercle.


TABLE I

RelatiGe forelimb proportions in fur seals and sea lions and generalizedfissipeds. Limb proportions expressed as a function of head and body length

Fur seals and Generalized sea lions * fissipeds

N =21 N =21

Scapula 9.45 (1.82) Humerus 8.11 (1.66)4 Radius 8.26 (1.63)4 Forelimb 16.37 (3.26)4

Deltoid crest 5.48 (1.13)4 Teres major 1.82 (0.69)' Olecranon 2.91 (0.67)4 Bicipital tubercle 1.49 (0.33)

(humerus and radius)

9.01 (1.12) 15.91 (0.78) 12.41 (0.81) 27.90 (3.87)

7.35 (0.57) 3.65 (0.19) 1.91 (0.69) 1.59 (0.17)

Numbers in parentheses refer to standard deviation. ' After Walker ('68).

Average of Arctocephalus australis (2). Callorhinus ursinus (6), Eumetopias jubata (4), Oturin hyronia (2), and Zalophus culifornianus (7) .

Average of Martes umericana (8), Bassariscus astutus (4) and Bassarccyon alleni (9).

Indicates that difference hetween groups is significant at 0.05 level.

TABLE 2

Forelimb indices in fur seals and sea lions and generalized jissipeds

Fur seals and Generalized

N=21 N =21 sea lions fi s s i p e d s

Scapular 82.18 (8.14)2 133.23 (10.07) Humeroradial 102.58 (8.58)2 78.95 (2.37) Deltoid crest' 32.60 (2.38)2 25.84 (3.24) Teres major' 9.86 (2.36)2 12.91 (1.45) Olecranonl 16.94 (1.81)2 7.44 (0.96) Bicipital tubercle' 8.81 (0.83)2 5.66 (0.99)

Numbers in parentheses refer to standard deviations. ' Expressed as a function of forelimb (= humerus + radius)

' Indicates that difference between groups is significant at length.

0.05 level.

body size do not reflect size variability in each of the genera involved (see e.g. Gould, '75, for discussion). A more favorable and commonly used measure of body size, available with each full skeleton, pre- sacral vertebral length, was not used because results of regression analysis suggested that the relationship of this length to other indices of body size (body weight and head and body length) was different in the two groups.

Howell ('44) has suggested that the use of indices is a more accurate method of comparing limb proportions than the method employed above, since it compares one bony length to another without res ect to body size. However, Hildebrand f52) and Huxley ('32), among others, have stressed caution when comparing organ- isms of widely different sizes because the use of such indices may be misleading, since the component bony parts may scale differently with respect to body size. Fore- limb indices for fur seals and sea lions and generalized fissipeds are listed in table 2. Differences in indices were determined by t-tests and were evaluated in light of relative differences in the size of their component parts.

The most obvious feature of forelimb proportions in fur seals and sea lions is their overall shortening, though this shortening is not uniform. Shortening of the humerus is more marked than that of the antebrachium, as noted in the different humeroradial indices. Overall shortening of the forelimbs reduces their resistance arms and, thus, increases the ability of their muscles to produce forward thrust during locomotion. The greater degree of humeral shortening found in fur seals and sea lions may also allow much of their forelimbs to be incorporated into the surrounding loose skin and contribute to general streamlining of the body despite the enlarged foreflip- pers. Such streamlining might reduce the effects of drag on aquatic movements significantly, especially at the fast (ca. 18-37 km/hr) swimming speeds reported for fur seals (Scheffer, '50, '58) and sea lions (Lorenz, '69; Scheffer, '58; Walker, '68).

Bony lengths associated with the attachments of the latissimus dorsi, pectoralis and teres major muscles are also significantly shorter in fur seals and sea lions but, as shown by the limb indices, shortening of the total limb length is greater than that of the attachments of the muscles. Thus, the moment arm-resistance arm ratios for these muscles, at least as indicated by these measures, are larger than in generalized fissipeds. Olecranon length, which is associ-


ated with the moment arm of the triceps muscles, is significantly longer in fur seals and sea lions so that the moment arm-resistance arm ratios of these muscles are especially larger. Thus, on the basis of limb proportions, the ability of the forelimbs of fur seals and sea lions to convert the effort of their muscles into a propulsive force is greater than that of generalized fissipeds (see also below).

The moment arms of the cranial- and caudal-most portions of the serratus ventralis muscle as scapulothoracic rotators, regardless of the position of the axis of rotation of the scapula on the thorax, are said to be related to the length of the scapula and the extent of elongation of the scapular angles (Ashton and Oxnard, '64). In sea lions and fur seals, relative scapular length does not differ significantly from that of generalized fissipeds, but, as shown by the scapular index, the angles are more expanded. Thus, the two portions of the serratus ventralis attaching to these angles operate with greater moment arms than in generalized fissipeds. The implication of these differences in moment arms lies in the proposed use of scapulothoracic rotation in the production of thrust. If these parts of the muscle are used to rotate the scapula on the thoracic wall and contribute to propulsive thrust, then their contribution is greater in fur seals and sea lions than in generalized fissipeds.

Originally all of the measurements of bony features of fur seals and sea lions were considered separately with regard to sex because of the large sexual size dimorphism reported for these pinnipeds (Fiscus, '61; Scheffer and Wilke, '53; Scheffer, '58). Differences in means of limb proportions of the sexes expressed as a function of head and body length were tested using a t-test. In every instance, differences in limb proportions between sexes were not significant. Similar results were obtained in test- ing differences in limb indices between sexes. The lack of significant distinction between the limb proportions and indices of male and female sea lions and fur seals is striking since the adult males are up to five

times heavier than the adult females (Scheffer and Wilke, '53). However, the samples used were small so that further sampling is indicated before the very interesting possible effects of sexual size dimorphism on locomotion in fur seals and sea lions can be investigated.

Glenohumeral (shoulder) joint The glenohumeral (shoulder) joint of fur

seals and sea lions is a ball and socket joint and, as such, the movements of flexion, extension, abduction, and rotation are possible there. The ranges of possible glenohumeral joint movements in representative fur seals and sea lions and generalized fissipeds are shown in table 3. Movements are described here in comparison to an anatomical reference position approximat- ing the position of the forelimb at the onset of aquatic locomotor cycles (English, '76a). The humeral shaft and the scapular spine form an angle slightly greater than 90". In a transverse plane the blade of the scapula and the intertubercular groove of the humerus are nearly aligned.

Flexion and extension of the humerus on the scapula are movements limited mainly by tension in the investing articular capsule and attached supraspinatus, infraspinatus and subscapularis muscles. Extremes of flexion in fur seals and sea lions also may be limited, in ligamentary preparations, by bony contact between the scapula and the enlarged humeral tuberosities projecting above the capitulum. Abduction and adduction are limited by capsular and muscular tension but abduction is inhibited addi- tionally by a medial glenohumeral ligament (fig. 13). This oblique band of collagen fibers connects the cranial portion of the medial glenoid lip with the caudal portion of the proximal humerus, just caudal to the lesser tuberosity. In smalI forms such as Callorhinus ursinus it is little more than thickened capsular fibers but in larger forms like Eumetopias jubata, it is prominent. When the limb is flexed, the enlarged humeral tuberosities may also inhibit possible abduction-adduction movements. In ligamentary preparations, the range of

FUR SEAL AND SE.4 LION FUNCTIONAL AKATOMY 34 1

possible medial glenohumeral rotary movements is greater than lateral movements, probably because of inhibition of lateral rotation by the medial glenohumeral ligament. The oblique course of the fibers of this ligament inhibit lateral humeral rotation at nearly any posture of the arm. Com- bined movements (e.g., flexion with lateral rotation), which may increase the tension in the articular capsule over that found in

, Fig. 13 Zalophus califomianus, right glenohu-

meral joint, medial view. The articular capsule is stippled and the medial glenohumeral ligament (LGHM) is shown. S, scapula, H, humerus. See text for details. Scale bar. 5 cm.

simple movements, have a smaller possible range in ligamentary preparations.

In generalized fissipeds, glenohumeral joint movements are similar to those of fur seals and sea lions, though the ranges of possible movements are different. Al- though Parsons (1900) described small intrascapular glenohumeral ligaments in fissipeds, most of the resistance to glenohumeral movements in ligamentary preparations of the fissipeds in this study was found to come from the articular capsule. Liga- ments as prominent as the medial glenohumeral ligament of fur seals and sea lions were not observed in any fissiped examined.

Elbow joint The elbow is actually a double joint. It is

a modified hinge joint between the humerus and ulna and a pivotal joint between the proximal radius and ulna. Though the movements of each articulation are most easily discussed separately, the movements of one articulation affect those of the other. The range of possible elbow joint movements of representative fur seals and sea lions and generalized fissipeds is given in table 3.

During flexion and extension of the elbow in all mammals, the ulna moves craniad and caudad with respect to the humerus, but in doing so the path of movement of the two articular surfaces is along an oblique depression of the humeral surface called the trochlear notch (figs. 7 , 8: large arrow). The oblique course of the trochlear notch and the large, convex, radial portion of the humeral trochlea

TABLE 3

Ranges of possible movements of forelimb joints from ligamentary preparations of representatitie fur seals, sea lions, and generalized fissipeds

Glenohumeral joint Elbow joint

Flexion- Abduction- Flexion Pronation- extension supination extension adduction Rotation

Callorhinus ursinus 65" 136" 80" 66" 42" Zalophus californianus 71" 180" 114" 76" 40" Martes americana 79" 60" 60" 90" 70"

Procuon lotor 60" 65" 60" 120" 62" Gulo gulo 57" 49" 54" 96" 73"


a

\

b Fig, 14 Zalophus c ~ l i j ~ r n i ~ n ~ . ~ , left elbow joint in (a) lateral and (b) medial views. The articular

capsule is stippled and the ligaments are labeled. Legend: LCL, lateral collateral ligament; LTL, lateral transverse ligament; LRL, lateral radial ligament (cut and reflected); LRA, annular radial ligament; LI, interosseous ligament; LCM, medial collateral ligament; S, cut origin of m. supinator. See text for details. Scale bar, 5 cm.


cause the ulna to be displaced mediad and rotated mediad about its long axis during flexion. This causes the brachium to be slightly adducted and rotated mediad as the humerus rotates anteriorly on the antebrachium during extension. This cam action of the mammalian elbow 'oint has been described by Jenkins ('73j and is found at the elbow joint of all otariine pinnipeds. Since the described accessory movements are part of humeroulnar joint movements and are a consequence of the shapes of the articular surfaces, this phe- nomenon has been termed conjunct rotation (Barnett et al., '61).

As a hinge joint, however, modified, the main movements possible at the humeroulnar articulation of fur seals and sea lions are flexion and extension. These movements are limited mainly by tension in the articular capsule and the collateral ligaments (fig. 14) in ligamentary preparations.

The primary movements of the radioulnar articulations are pronation and supination. In fur seals and sea lions, these movements are limited mainly by tension in the annular radial ligament but also by tension in the articular capsule, the collateral ligaments, the interosseous ligament and the lateral transverse ligament. The annular ligament connects the ulna with the cranial parts of the articular capsule and lateral epicondyle. Fibers attaching to the capsule are tensed when the radial fovea is rotated on the proximal-lateral portion of the articular surface of the ulna during pronation. This movement causes the long diameter of the elliptical radial fovea to change its orientation from a transverse plane to one more longitudinal. At first this relaxes the cranial articular capsule, but as pronation continues, it tenses the cranial capsule and the fibers of the annular ligament attaching to it. During supination the radial fovea turns on the ulna and the radial portion of the trochlea of the humerus with which it articulates. This tenses the portions of the articular capsule and annular ligament attaching to the cranial portion of the lateral epicondyle, the interosseous liga-

ment, and the large medial collateral ligament.

In generalized fissipeds conjunct movements at the humeroulnar articulation are much as described above. Flexion and extension are limited by the same structures in both groups. Pronation and supination likewise involve the same movements of the articular surfaces, but the range of possible movements is noticeably smaller in fur seals and sea lions (table 3). This difference may be accounted for by the peculiar attachments of the annular radial ligament. In generalized fissipeds the annular ligament forms a ring about the neck of the radius, attaching to the sides of the articular surface of the ulna-the semi-lunar notch-and, presumably, helps to maintain approximation of the proximal radioulnar articular surfaces. In fur seals and sea lions the annular ligament is not continuous but ends craniad on the articular capsule and lateral epicondyle. Although in generalized fissipeds it apparently plays little role in inhibiting or stopping rotary forearm movements, the annular ligament of fur seals and sea lions is prominent in this regard.

Z M Fig. 15 Ulnar articular surfaces of Zalophus cali-

fornianus (Z) and Martes americana (M) are shown in cranial view. The anconeal (a) and coronoid (c) processes are labeled. Drawn to same length, not to scale. See text for details.


A second major structural peculiarity of the elbow joint of otariine pinnipeds lies in the shape of the articular surface of the ulna. In most fissipeds both the medial and lateral margins of this surface are well-developed and contribute to a distinct semi- lunar notch. The proximal-lateral and distal-medial portions of the surface are upturned as are the humeral surfaces with which they articulate. Jenkins ('73) has suggested that in most fissipeds the anconeal and coronoid processes (fig. 15) have developed in response to normal loading of the joint such as found during walking. These processes are well-situated to resist compressile loading applied by the humerus as the wrist and digital flexors, acting about the elbow, tend to rotate the humerus laterad on the ulna as the elbow is extended and the wrist and digits are palmar flexed simultaneously during the stance phase of normal locomotion. Promi- nent lateral collateral and lateral transverse ligaments found in generalized fissipeds would be tensed by this movement.

In fur seals and sea lions the lateral half of the semi-lunar notch is poorly developed, but a prominent coronoid process (fig. 15) forms the medial border of an expanded trough for articulation with the radius. The lateral ligaments are only mod- erately developed but the medial collateral ligament is very large (fig. 14) and together with the well-developed medial portion of the annular ligament, forms a strong medial bracing of the elbow joint against tension. This modification of joint structure may be of advantage in loading of the joint that occurs during normal locomotion. During aquatic propulsion, the limb is adducted and rotated mediad (English, '76a). The density of the water exerts a re- sistive thrust on the limb (fig. 16) while the action of the limb muscles presumably tends to adduct and rotate it mediad. This theoretically would give rise to loading of the elbow joint from lateral to medial, placing the lateral portion of the joint under compression, forcing the humeral trochlea and radial fovea medially and

b f .

1

Fig. 16 Loading of the elbow joint during aquatic locomotion in sea lions and fur seals is shown in cranial view in (a) and on the bones in (b). Adductor and retractor muscles apply a force (P) to the forelimbs which is resisted by the water (W) giving rise to a loading of the elbow (E) from lateral to medial, compressing the joint laterally, tensing the medial ligaments. After English ('76a) modified. See text for details. Legend: h, humerus; r, radius; u, ulna.


together. The compression of the trochlea and fovea would be opposed by the wall- like lateral surface of the ulnar coronoid process with which it articulates. Medially, tension would be resisted by the large medial collateral ligament and the medial portion of the annular ligament.

Quantitative aspects of forelimb myology

Muscle weight has been used as an index of muscle force in several comparative morphological studies (e.g., Stern, '71). However, most physiologists and functional anatomists (e.g., Schumacher, '61) agree that the cross-sectional area of the muscle fibers is a better index of muscle force since it is said to be related to the number of cross bridges forming between myofila- ments in parallel (Helander and Thulin, '62). Heiimae ('71) and Rayne and Craw- ford ('72) sought to combine these positions by the use of the ratio of weight to central fascicle length as an index of the maximum isometric force that the muscles of mastication of rats could exert. They considered this parameter a more reliable estimate of force than muscle weight alone and, especially in the case of pennate muscles, it is more readily and accurately ob- tainable than cross-sectional area. Accord- ingly, weight-fascicle length ratios were calculated for each of the muscles of the forelimb and expressed as a function of

body weight. The animals investigated were grouped into otariine pinnipeds and generalized fissipeds. Table 4 displays the relative distribution of forelimb muscles in the two groups compared by expressing the total of weight-fascicle length ratios for the muscles of various anatomical seg- ments of the limb as a function of body weight. Differences in ratios of individu- al muscles and muscle groups between fissipeds and otariine pinnipeds were tested with a t-test. Differences in individ- ual muscles are shown in the APPENDIX.

Many limitations to the use of anatomical data as predictors of physiological parame- ters such as muscle force are found. Morphologists such as Stern ('71) who have realized these limitations, either place little emphasis on such anatomical parame- ters or have not relied on these data in assessing possible muscle functions. Weight-fascicle length data are included here realizing the many assumptions which must be met concurrently before they can be used to reflect the actual ability of the muscles to produce force. Because weight- fascicle length ratios are doubtful predictors of muscle force and because of the statistical limitations imposed by the small sizes of the sample groups, no attempt was made to evaluate the allegedly more accurate dry weight of the muscles (cf. e.g., Tuttle, '73). It is hoped that the differences noted between groups, when present, are

TABLE 4

Distribution of forelimb musculature. Groups of weight-fascicle length ratios as a function of body weight (gm/cm/lO kg)

Extrinsic Intrinsic limb limb Pectoral Brachial Antebrachial Total

~ ~ ~ ~ ~ ~

Average, 16.2S2 48.162 16.612 9.8Y 15.5g2 106.462 fur seals (1.59) (10.23) (3.68) (0.84) (1.79) (16.91) and sea lions (N=13) Average, 13.19 22.00 5.35 17.89 21 42 79.86 generalized (1.84) 65.79) (0.77) (2.75) (6.47) (11.35) fissipeds (N =4)

Numbers in parentheses are standard deviations. ' Composition of muscle groupings is explained in the APPENDIX. * Indicates that the difference between groups is significant at the 0.05 level


great enough to offset some of these limitations. Differences in the ratios are used to suggest that more or less force can be produced by a muscle in otariines than in generalized fissipeds. The differences noted reflect neither the absolute magnitude of the difference in force nor the magnitude of the force actually used during forelimb function.

The weight-fascicle length ratios of many of the muscles of the forelimb of fur seals and sea lions do not differ significantly from those of fissiped forelimb muscles. Among the 37 muscles or parts of muscles analyzed, only 13 have weight-fascicle length ratios which are significantly greater in fur seals and sea lions despite the fact that the total of weight-fascicle length ratios is substantially larger than in fissipeds (table 4). However, the distribution of forelimb musculature does differ between the groups. In fur seals and sea lions, more than half of the musculature lies in the proximal portion of the forelimbs, but in generalized fissipeds the musculature is more evenly distributed. Of the 13 muscles whose weight-fascicle length ratio is larger in fur seals and sea lions, ten are found in the proximal portion of the limb. In some cases where differences occur, such as supraspinatus and subscapularis, part of the difference in weight-fascicle length ratios can be associated with differences in fascicle architecture between the two groups, since pennate-fascicled muscles may be associated with larger weight-fascicle length ratios than parallel-fascicled muscles of approximately the same size. In other muscles, such as the pronator teres and supinator, differences in muscle attachment between the groups suggest that the central fascicles are relatively shorter in the pinnipeds and account for at least some of their differences in weight-fascicle length ratios. However, in most cases differences in weight-fascicle length ratios between the groups reflect differences in relative size of the muscle.

DISCUSSION

The major peculiarities of forelimb func-

tion during aquatic locomotion in sea lions and fur seals involve large ranges of abduction-adduction and rotary movements (En- glish, ’76a). Protraction and retraction of the limbs are said to predominate during aquatic locomotion in fissipeds. The cycle of forelimb movements used by swimming sea lions and fur seals can be divided into recovery and propulsive phases (Gambar- jan and Karapetjan, ’61; English, ’76a). Recovery phase movements include lateral rotation and abduction of the forelimbs in addition to protraction while propulsive phase movements include medial rotation and adduction as well as retraction. Lateral rotation during recovery phase movements orients the flattened radial margin of the forelimb in the line of movement such that the drag on abduction and protraction is reduced (English, ’76a). Medial rotation of the forelimb during the propulsive phase orients the enlarged palmar surface of the manus in the direction of movement. This exposure of a relatively large surface to the water via medial forelimb rotation has been postulated as a modification to aid in thrust production via either paddling or hydrofoil activity in sea lions (English, ’76a). Thus, rotary movements of the forelimbs during aquatic locomotion enable sea lions and fur seals to employ large ranges of abduction and adduction to hydromechanical advantage. These important rotary movements of the forelimb can take place only at the radioulnar or glenohumeral (shoulder) joints. The glenohumeral joints of fur seals and sea lions are remarkably mobile, especially in abduction-adduction and rotary movements. Surrounding the glenohumeral joint are muscles capable of rotating the forelimb through a sizeable excursion- the teres major, latissimus dorsi, pectoralis, and deltoideus. With one

I Protraction and retraction are used here as defined by En- glish (’76a). Protraction is “movement of a limb anteriorly in a vertical longitudinal or sagittal plane” (p. 343) and retraction as its opposite. These terms were chosen to describe limb movements in swimming sea lions because it was not always possible to determine to what extent forelimb movements were due to glenohumeral flexion and extension, to scapulothoracic rotation in a sagittal plane or to cranial and caudal translation of the scapula on the lateral thoracic wall.

FUR SEAL AND SE.4 LIOh FUNCTIONAL ASATOMY 347

exception, teres major, all of these long humeral rotators attach to the enlarged deltoid crest on the humerus, which makes their moment arms large as humeral rotators. In contrast, the radioulnar joints are fairly rigid. A modified annular radial ligament is largely responsible for the relatively small range of possible pronation and supination found in fur seals and sea lions. The pronator and supinator muscles have relatively larger weight-fascicle length ratios than generalized fissipeds, but their attachments suggest that their fascicles are relatively shorter so that the range of movements they can produce is theoretically smaller. Even though the large medial epicondyle of fur seals and sea lions might indicate that the moment arm of the pronator teres muscle is large, the muscles surrounding their radioulnar joints seem better suited to control than produce movement. While rotation at the glenohumeral joint might produce lateral bulging of the elbow, such as noted in swimming sea lions (English, '76a), radioulnar rotation could contribute to distortion of the desira- ble flattening of the forelimb and disrupt the hydromechanical advantages of such flattening.

If glenohumeral rotation functions to ori- ent the forelimbs of fur seals and sea lions for favorable hydromechanical perfor- mance, then these rotary movements must be well-controlled. Control of glenohumeral rotation could be achieved by antagonistic activity of the long humeral rotators mentioned above or by cooperative activity of these muscles with the supraspinatus, infraspinatus and subscapularis muscles. The latter muscles are probably better suited to resist or control glenohumeral rotation than produce it; their ex- treme size and the complex orientation of their fascicles are generally associated with the production of large amounts of tension but over a short range of slow movement. Cans and Bock ('65) have also suggested that if such complexly pennate muscles are appropriately innervated, their arrangement of fascicles is particularly advantageous to precise control of movement. Al-

though electromyographic analysis is necessary to substantiate that the proposed long glenohumeral rotators and the supraspinatus, infraspinatus, and subscapularis muscles actually act in concert to control rotary movements of the forelimbs in sea lions and fur seals, modifications of the size, attachments and fascicle architecture of these muscles and of the joints about which they act suggest such cooperative use.

During the recovery phase of aquatic locomotion in sea lions and fur seals, modifications of potential limb abductors to accommodate the large range of limb abduction used might be predicted. Only the acromiotrapezius and deltoideus have lines of action appropriate to be considered forelimb abductors. The line of action of the acromiotrapezius lies such that the muscle can effect forelimb abduction by adduction of the vertebral border of the scapula and, thus, abduction of the glenoid fossa; the deltoideus has a line of action such that it abducts the arm. Proximal and caudal migration of the origin of the deltoideus is probably responsible for its peculiar single-headedness and makes its fascicles relatively longer than in generalized fissipeds. Expansion of the origin of this muscle also brings about its association with the acromiotrapezius so that in fur seals and sea lions the fibers of the two muscles are continuous over the scapular spine. Abduction of the forelimb could probably be accomplished by each muscle acting independently, but this association of the two muscles suggest that they might act together. Such in-series synergism would make the functional length of the composite muscle fibers greater than if either acted alone and especially greater than if the two muscles were arranged as in fissipeds. Potential advantages of such a longer muscle in abducting the forelimbs would include a larger range and relatively more rapid rate of movement and the ability of the composite muscle to maintain tension over a larger range of movement than if the muscles acted independently or were arranged as in fissipeds. Although neither the acromiotrapezius nor deltoide-

348 ARTHUR WM.

us has a weight-fascicle length ratio significantly greater in fur seals and sea lions than in generalized fissipeds, and the proposed in-series synergism does not necessarily suggest an increase in the force that the two muscles exert, their modification in otariines does have the advantage of allowing abduction of the forelimbs through a greater range of movement, at a more rapid rate, and with more constant force than hypothetically possible in fissiped carnivores. The potential adaptive value of this modification in swimming fur seals and sea lions lies in allowing a large range of rapid forelimb abduction and in overcoming water resistance during recovery phase movements.

Overall shortening of the forelimbs shortens their resistance arms and thus reduces water resistance to recovery phase movements. In addition, modifications of the muscles capable of producing forelimb protraction in fur seals and sea lions reflect movement against possible water resistance. The muscle most likely to function in forelimb protraction, the brachiocephalicus, has a relatively larger weight-fascicle length ratio than in fissipeds, suggesting its use in overcoming water resistance during the recovery phase. If forelimb protraction is produced by scapular movements as well, cranial movement of the scapula on the thorax, both by ventral rotation of its caudal angle and cranial translation, could contribute substantial force to recovery phase movements. The muscles most likely to produce them are modified accordingly. The caudal-most component of the serratus ventralis muscle has a line of action making it a scapulothroacic rotator. The large size and moment arm of this muscle in fur seals and sea lions are consistent with a significant contribution to overcoming water resistance during the recovery phase. If the axis of rotation of the forelimb lies proximal to the glenohumeral (shoulder) joint in these pinnipeds, as it does in fissipeds, then the contribution of the atlantoscapularis to recovery movements as a couple with the caudal portion of the serratus ventralis also must be considered. The cranial and deep

ENGLISH

rhomboid muscles may act to move the scapula, and thus the forelimb, craniad by translation and the more extensive attachments of these muscles to the scapula in otariines may reflect their active role in recovery phase movements. The resulting proposed protraction and abduction of the forelimbs via a cooperative muscular effort can be produced with theoretically greater and more constant force than in fissipeds. Further, if the activity of the muscles is appropriately controlled, such cooperation might be used to obtain optima of muscular power or limb speed, as the results of the modelling of Stern ('74) suggest. (See also below.)

The inclusion of medial rotation and adduction of the forelimbs during early aquatic propulsive phase movements in fur seals and sea lions has been interpreted as a means of including more of the force generated by the pectoralis muscle into the production of forward thrust than in fissiped carnivores (English, '76a). The greater thrust so developed is presumed to enable sea lions and fur seals to swim with speed. The large size and extensive antebrachial attachments of the pectoralis muscle as well as overall forelimb shortening certain- ly are consistent with this hypothesis.

During later propulsive phase movements, retraction of the forelimbs aug- ments adduction and, as might be expected, modifications of forelimb structure associated with the production of massive thrust via retraction are found. The latissimus dorsi, which lies in an appropriate position to retract the forelimbs, not only has a greater weight-fascicle length ratio in fur seals and sea lions, but relatively more of its fibers insert with pectoralis than in fissipeds. Although the moment arm of latissimus dorsi is relatively shorter in fur seals and sea lions, whether measured at teres or pectoral insertion (see above), more of its fibers act about the larger moment arm of the pectoral insertion. Thus since the moment arm-resistance arm ratio for either insertion is larger, the overall mechanical advantage of latissimus dorsi as a retractor is greater in fur seals and sea


lions. The panniculus carnosus and the abdominal component of pectoralis, which have lines of action that make them capable of forelimb retraction, also insert with part of latissimus dorsi onto the deep surface of the sternal component of pectoralis. Both muscles have extensive attachments in fur seals and sea lions which suggests that their cooperative use with latissimus dorsi could bring about very powerful forelimb retraction. If panniculus carnosus and the abdominal part of pectoralis are used along with latissimus dorsi, then a smooth tran- sition between forelimb adduction and retraction during propulsive movements also might be facilitated. Additional thrust via forelimb retraction could be produced by scapulothoracic movement. Expansion of the cranial angle of the scapula of fur seals and sea lions increases the moment arm of the cranial most portions of the large serratus ventralis muscle as a scapulothoracic rotator and is consistent with production of forward thrust in this manner.

Propulsive movements in fur seals and sea lions end with forelimb retraction which is produced by elbow extension and palmar flexion of the manus (English, '76a). Since the moment arms of the muscles of the triceps complex are relatively large in fur seals and sea lions, production of substantial thrust also might be associated with these movements. Palmar flexion of the manus is nearly coincident with elbow extension during propulsive movements but since few of the carpal and digital flexors cross the elbow joint, little tendency toward disarticulation of the elbow, such as described for fissipeds (Jenkins, '73), might be expected. Instead, the elbow joint of otariines is braced against the loading proposed to occur during aquatic locomotion by bony reinforcement of the coronoid process and an enlarged medial collateral ligament.

The magnitude of the forward thrust produced during swimming is dependent on the amount of water moved and velocity to which it is accelerated (by Newton's second law). Since the forelimbs of fur seals

and sea lions are enlarged to form flippers, it has been hypothesized (English, '76a) that propulsive thrust is generated by accelerating a large amount of water to a relatively slow velocity rather than by accelerating a small quantity of water to a relatively large velocity. The latter method is considered more inefficient because the kinetic energy involved varies as the square of the velocity (Alexander, '68). The modifications of forelimb structure in fur seals and sea lions that are associated with the production of large amounts of propulsive thrust are consistent with this view. En- largement of the moment arms of muscles, such as the serratus ventralis and triceps, increases the torque they can produce from a given amount of generated force and also enhances their ability to move the bones to which they are attached with large average velocity (Stern, '74). However these potential advantages come at the expense of the production of large amounts of generated force through the entire range of contraction. Muscles with smaller moment arms such as latissimus dorsi and pectoralis are said to favor more prolonged periods of large amounts of force generation (Stern, '74). Thus, in fur seals and sea lions, where shortening of the resistance arm of the forelimb enhances thrust production from its muscles, muscles with relatively short moment arms (but large moment arm-resistance arm rations) might be associated with production of relatively slow movements with large amounts of force throughout the movement. Other muscles with large moment arms might be used to produce larger values of thrust in short periods at particular points during the propulsive phase, but not throughout. These muscles could be considered to act advantageously in reversing recovery phase movements and overcoming the ini- tial inertial load of the water at the onset of propulsive movements, (e.g., serratus ventralis) or in adding to forward thrust near the end of the range of contraction of other propulsive muscles near its termina- tion (e.g., triceps). Such propulsive movements are capable of accelerating a rela-


tively large amount of water to a relatively slow velocity to produce rapid forward propulsion. During the recovery phase of forelimb movement, enlargement of the moment arms of muscles or moment arm- resistance arm ratios and cooperative muscle activity similarly might be considered to contribute to the production of these apparently non thrust-producing movements against water resistance over a short period of time.

Thus, structural modifications of the forelimbs of fur seals and sea lions can be associated with peculiarities in aquatic locomotor behavior. Specifically, forelimb structure reflects orientation of the forelimbs for favorable hydromechanic per- formance, overcoming water resistance during recovery phase movements and producing massive thrust during the propulsive phase. Together, these specializations of structure and function can be regarded as adaptations to the aquatic life- style of the animals. Their significance, I feel, lies in enabling fur seals and sea lions to swim with speed and presumably to capture elusive, fast-swimming pre . It has been noted (Lips and Mitchell, '69y that the origin and rapid radiation of sea lions and fur seals and their proposed early relatives was coincident with changes in ocean CUT- rents favoring offshore development of a littoral fauna rich in such prey items (Mitchell, '66, '72). Following such environ- mental changes and early exploitation of the new adaptive zone by coastal fissipeds, it is not difficult to imagine selection pres- sures favoring fast-swimming aquatic pre- dators such as sea lions and fur seals and development of locomotor adaptations of the sort discussed above.

ACKNOWLEDGMENTS

This work formed part of a thesis for the degree of Doctor of Philosophy in Anat- omy at the University of Illinois at the Medical Center in 1974. For their help in obtaining pinniped specimens, I thank DOC- tor Burney LeBoeuf of the University of California at Santa Cruz and Ancel Johnson, Clifford Fiscus, and Albert Wolman of the

US. Department of Commerce. Doctors James Mead and Luis de la Torre very gen- erously made specimens under their care available to me, and Doctors Robert Sca- pino and Ursulla Rowlatt allowed me to dis- sect specimens from their personal collec- tions. Appreciation is due to Sue English, Ladonna Compton and Janis Brockschmidt who typed various forms of the manuscript. I am thankful to Doctor Herbert R. Barg- husen for supervising this work and for reading earlier drafts of the paper.

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FUR SEAL AND SEA LION FUNCTIONAL ANATOMY 35 1

SEE APPENDIX ON PAGE 352


APPENDIX

Weight-fascicle length ratios o f forelimb muscles as a function of body weight (gm/cm/lO kg)

Average, generalized fissipeds (N =4) I

Average fur seals and sealions (N=13)*

Extrinsic limb muscles Brachiocephalicus 1.46 (0.47) 2.41 (0.38)' Acromiotrapezius 1.16 (0.39) 1.31 (0.35) Spinotrapezius 0.85 (0.43)" 0.58 (0.11)

Rhomboideus dorsalis 1.05 (0.59) 1.08 (0.14) Rhomboideus profundus 0.28 (0.04) 0.23 (0.02) Atlantoscapularis 0.57 (0.24) 0.63 (0.05) Serratus ventralis 4.60 (0.92) 7.09 (1.61)" Latissimus dorsi (pectoral) 0.94 (0.38) 1.42 (0.05)' Latissimus dorsi (teres) 1.54 (0.43) 0.76 (0.22)'

Teres major 1.52 (0.47) 1.35 (0.43) Del toideus 1.25 (0.22) 1.85 (0.18)" Supraspinatus cranial 1.26 (0.68) 7.98 (1.07)" Supraspinatus caudal 4.68 (l.06)* 3.92 (0.50) Infraspinatus 4.89 (2.09)' 1.74 (0.43) Subscapularis cranial 2.60 (1.93) 15.68 (1.11)' Subscapularis middle 5.06 (0.48) 14.13 (3.47)" Subscapularis caudal 1.90 (0.79) 3.01 (1.49)"

Pectoralis 5.35 (0.77) 16.61 (3.68)'

Triceps longus 4.32 (1.41)" 2.00 (0.30) Triceps lateralis 4.74 (2.71)O 1.17 (0.09) Triceps medialis 2.15 (0.94) 1.60 (0.13) Epitrochlearis 1.35 (0.48) 1.57 (0.30) Anconei 0.78 (0.37) 0.69 (0.43) Biceps brachii 3.12 (0.46)' 0.84 (0.44) Brachialis 1.23 (0.54) 1.49 (0.14) Brachioradialis 0.33 (0.06) 0.52 (0.17)"

Extensor carpi ulnaris 1.69 (0.47)' 0.35 (0.16) Extensor carpi radialis 1.38 (0.47)" 0.59 (0.08) Extensor digitorum communis 1.63 (0.84) 0.46 (0.34) Extensor digitorum lateralis 1.22 (0.31)O 0.54 (0.16) Extensor pollicis longus 0.53 (0.14) 1.48 (0.08)' Abductor pollicis longus 1.55 (0.27) 1.72 (0.27)

Flexor carpi ulnaris 2.46 (1.59) 3.87 (1.64) Flexor carpi radialis 1.21 (0.97) 0.63 (0.07) Flexor digitorum communis 7.46 (3.62) 2.71 (0.16) Pronator teres 1.26 (0.19) 1.15 (0.24)

Numbers in parentheses are standard deviations, asterisks denote significant differences between the groups. I Average of Gulo gulo ('I, Martes americana"', and Procyon lotor(*'. * Average of Callorhinus ursinus'6', Eumetapias jubata (2), and Zalophus ~a1ifornianu.d~'.

Rhomboideus capitis et cervicis 0.89 (0.13) 0.90 (0.22)

Intrinsic limb muscles

Pectoral muscles

Brachial muscles

Antebrachial muscles

Supinator 0.60 (0.10) 1.02 (0.21)"

structural correlates of forelimb function in fur seals and sea lions

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