Comparative Myology of the Forelimb of Squirrels (Sciuridae)

Home , Callosciurus, Epixerus, Funambulus, Sciurinae, Spermophilus, Tamias

JOURNAL OF MORPHOLOGY 234:155-182 (1997)

RICHARD W. THORINGTON, JR.,* KAROLYN DARROW, AND AIMEE D.K. BETTS Department ofVertebrate Zoology, Smithsonian Institution, Washington, D.C. 20004

ABSTRACT The musculature of the shoulder, arm, and forearm was studied in 19 genera of squirrels, representing the Pteromyinae (flying squirrels) and all 7 tribes of the Sciurinae (tree and ground squirrels). The objective was to locate derived anatomical features of functional or phylogenetic significance and to determine how much morphological variation underlies the diverse locomotor behavior of squirrels, which includes terrestrial and arboreal bounding, climbing, digging, and gliding. The fossil evidence suggests that arboreality is primitive for squirrels, and in fact tree squirrels appear to represent the primitive sciurid morphology. Ground squirrels are less uniform and exhibit a few derived features, including a clavobrachialis muscle not seen in other squirrels. Pygmy tree squirrels, which have evolved independently in three tribes, exhibit convergence of forelimb anatomy, including the loss or reduction of several muscles in the shoulder and forearm. The forelimb anatomy of flying squirrels is the most derived and differs from that of tree squirrels in details of shoulder, arm, and forearm musculature. Some of these muscular differences among squirrels have phylogenetic significance, being shared by closely related genera, but none has significance above the tribal level. Many of the differences suggest a variety of changes in function that are amenable to further study. J. Morphol. 234:155-182,1997. © 1997 Wiley-Liss, Inc.*

Herein we present a study of the forelimb collected (Hight et al., '74; Ellis and Maxson, musculature of squirrels, which plays a key '80; Hafner, '84; Hafner et al., '94; Oshida et role in gliding, climbing, digging, and qua- al., '96). The muscular anatomy of squirrels drupedal locomotion. There are three pur- is well known for only 11 genera and 23 poses for this study. First, we are looking for species (Hoffmann and Weyenbergh, 1870; derived features that reflect functional Parsons, 1894; Alezais, 1900; Brizzee, '41; changes in the use of the forelimb, especially Peterka, '36; Bryant, '45), with a strong bias any that have evolved independently in dif- toward the two tribes of Holarctic taxa, and ferent taxa and that may be interpreted as no representation among three tribes of adaptations to particular ways of life. Sec- Asian and African squirrels. We have stud- ond, we are seeking myological characters ied the musculature of the forelimb in 19 that will be useful in formulating phyloge- genera and 25 species, including 6 genera of netic hypotheses about the genera of squir- flying squirrels and representatives of all 7 rels. Although we do not anticipate finding recognized tribes of the Sciurinae. enough forelimb characters to enable us to Modern squirrels occur in a diversity of conduct a phylogenetic analysis, we hope niches and present a number of cases of that a series of studies of squirrel anatomy convergent evolution. Pygmy tree squirrels (Ball and Roth, '95; Thorington et al., '96; have evolved independently in South Thorington and Darrow, '96; Thorington et America, Africa, and Southeast Asia, and al., in press) will provide adequate data for are members of three different tribes. Ground such an analysis in the future. Third, we squirrels (terrestrial squirrels that often live wish to compile morphological data that can be used to test phylogenetic hypotheses derived from the increasing amount of molecu- Contract grant sponsor: Smithsonian Institution. lar data on squirrels•immunological, elec- Correspondence to: Richard W. Thorington, Jr., NHB 390, trophoretic, sequencing, etc.•which is being MRC 108, Smithsonian Institution, Washington, D.C. 20004.

C 1997 WILEY-LISS, INC. *This article is a US Govern- ment work and, as such, is in the public domain in the United States of America. 156 R.W. THORINGTON ET AL. in subterranean burrows) occur in two tribes, of its divergent morphological and genetic the Holarctic Marmotini, including the chip- characteristics (Anthony and Tate, '35; munks, marmots, prairie dogs, and ground Moore, '59; Hafner et al., '94). The place- squirrels, and the Xerini, which includes ment of the Indian Funambulus in the same two African genera and one Asian genus. tribe with the African genera Paraxerus, Cursorial terrestrial squirrels (which do not Funisciurus, and Myosciurus is also ques- live in burrows) have evolved independently tionable (Hight et al., '74; Thorington and on Borneo (Rheithrosciurus, of uncertain Darrow, '96). The largest systematic prob- tribal allocation) and in Africa (Epixerus, of lem, however, is the relationship among the the tribe Protoxerini). Another terrestrial tribes. It is unclear how the flying squirrels squirrel, Rhinosciurus, of the Callosciurini, and the seven tribes of tree and ground specializes in eating ants and termites squirrels are related one to another. The (Askins, '77). Tree squirrels occur in five flying squirrels have long been recognized as tribes. Because arboreality is primitive for a separate subfamily based on their distinc- squirrels (Emry and Thorington, '82), it is tive morphology. Until recently, there was probable that it evolved only once. It is also no evidence relevant to when they diverged probable that gliding has evolved only once from other squirrels. Paleontological evi- in squirrels (Thorington, '84), but the phylo- dence has been used to argue for an early genetic relationships of the genera of flying date of divergence (Mein, '70; DeBruijn and squirrels are unclear (McKenna, '62). They Unay, '89), leading to the suggestion that occur in North America and Eurasia, with flying squirrels should be considered a sepa- the greatest diversity (12 genera) in South- rate family from other squirrels (Corbet and ern Asia. Hill, '92). However, Emry and Korth ('96) A trustworthy phylogenetic hypothesis of conclude that the fossil evidence, based just the family Sciuridae does not exist. Modern on teeth, is inadequate to determine whether squirrels comprise approximately 50 genera they are a distinct family. The immunodiffu- and 273 species (Hoffmann et al., '93). They sion evidence of Hight et al. ('74) suggests that the flying squirrels are more closely are usually aligned in 2 subfamilies, the related to the Sciurini than to other tribes of flying squirrels, in the Pteromyinae [14 gen- tree squirrels, but the analysis of Ellis and era, 43 species (Hoffmann et al., '93), but see Maxson ('80) suggests that they are diver- Thorington et al., '96, for justification that gent from other tribes of the Sciurinae. Vari- 15 genera should be recognized], and all ous hypotheses have been suggested about other squirrels in the Sciurinae, which is in the relationships between tribes of the Sci- turn divided into 7 tribes. Moore ('59) di- urinae, such as Moore's ('59) suggestion that vided the Sciurinae into eight tribes, but the the Protoxerini were derived from the Xe- number has since been reduced to seven by rini, and Hight et al.'s ('74) dendrogram that Black ('63), Hight et al. ('74), Hafner et al. suggests the sequential divergence of the ('94). The tribe Sciurini includes the tree Marmotini, Callosciurini, Ratufmi, and Sci- squirrels of South America, North America, urini, but none of these hypotheses is well and northern Eurasia. The Marmotini in- supported by morphological data, and some clude the Holarctic chipmunks, marmots, seem contradicted by it (Thorington and Dar- and ground squirrels. Three tribes occur row, '96). principally in Africa: ground squirrels of the Squirrels are first known from the fossil tribe Xerini, and tree squirrels of the tribes record of the North American Eocene, 35 Protoxerini and Funambulini. Two other mybp (Emry and Thorington, '82). Emry and tribes occur in southern Asia: Ratufmi, the Korth ('96) allocate the genus Douglassia to giant tree squirrels, and Callosciurini, which the tribe Sciurini. Paleosciurus occurred in includes a radiation of 13 genera of arboreal Europe in the early Oligocene, approxi- and terrestrial squirrels. mately 30 mybp (Vianey-Liaud, '74). By the Some genera are probably inappropriately late Oligocene, the Marmotini appear in the allocated to these tribes. Among these are fossil record of North America (Miosper- Rheithrosciurus, a terrestrial squirrel of Bor- mophilus) and the Xerini appear in the fossil neo, which is traditionally placed in the Hol- record of Europe (Heteroxerus) (Black, '72). arctic and South American Sciurini, and Sci- Squirrels of undetermined tribal affinity are urillus, the South American pygmy squirrel, first recorded from Africa in the Miocene which is also placed in the Sciurini in spite (Lavocat, '73). On the basis of this evidence, SQUIRREL FORELIMB MUSCLES 157 Black ('63) suggested that the tribes of squir- Woods ('72) for "hystricomorphs," McEvoy rels diverged in the late Oligocene. However, ('82) for Erethizon and Coendou, Stein ('86, the paleontological record provides little in- '90) for arvicolids and dipodoids, and Ryan formation useful for showing how the tribes ('89) for heteromyids. are related one to another. RESULTS MATERIALS AND METHODS Trapezius group Animals dissected are listed in systematic M. sternomastoideus order in the Appendix. Dissectable museum Origin: Arises from the cranial surface of specimens of most of these taxa are rare. the manubrium. During dissection, muscles were bisected be- Insertion (Fig. 1): Inserts on the mastoid tween origin and insertion, so that origins process of the skull. The insertion is re- and insertions could be examined carefully. stricted to a small area of the mastoid in the We recorded our observations on camera lu- African genera. It extends from the mastoid cida drawings made of the appropriate bones slightly onto the nuchal line in other genera, in the collections of the National Museum of most extensively in Ratufa and Sciurus. Natural History. Innervation of the muscles Remarks: In squirrels, variation in the was verified, especially in cases in which origins and insertions of this muscle is slight there was a question about homology. Inner- (Parsons, 1894; Brizzee, '41; Bryant, '45). In vations are reported only where they dif- other rodents, variation is also slight. This fered with the observations of Hill ('37) and muscle originates slightly on the clavicle in Bryant ('45), or where they are of particular some cricetines (Rinker, '54). It inserts on interest. the posterior edge of the auditory meatus in Anatomical nomenclature remains a prob- cricetines (Rinker, '54), on the bulla in Dipod- lem. The Nomina Anatomica ('66) for hu- omys (Ryan, '89), and on the paraoccipital mans is inappropriate. The Illustrated Veteri- process in the hystricomorph rodent Myocas- nary Anatomical Nomenclature (Schaller, tor (Woods, '72). Woods ('72) suggests that '92) does not include rodents. Some terms the more extensive insertion on the nuchal normally used in comparative anatomy dif- line may simply reflect that the muscle is fer from both. Except where noted, we follow relatively stronger in some species. the terminology for muscles used by Hill ('37) to facilitate comparison. M. cleidomastoideus In the remarks sections, we first make comments on the comparative anatomy of Origin (Fig. 2): Arises from the ventral squirrels based on Hoffmann and Weyen- surface of the clavicle adjacent to the origin bergh (1870) for Sciurus vulgaris; Parsons of the sternomastoid and deep to the origin (1894) for Callosciurus prevostii, Pteromys of cleido-occipitalis. volans, Xerus getulus, Spermophilus mexi- Insertion (Fig. 1): Inserts on the mastoid cana, andMarmota marmota; Alezais (1900) process of the skull just caudal to the inser- for Sciurus vulgaris and Marmota marmota; tion of sternomastoid. In Spermophilus, the Peterka ('36) for Sciurus niger, Glaucomys insertion is dorsal to that of the sternomas- volans, and Cynomys ludovicianus; Hill ('37) toid, on the superior nuchal line. for Sciurus griseus and Spermophilus rich- Remarks: Like sternomastoid, the origin ardsonii; Brizzee ('41) for Spermophilus ar- and insertion of this muscle are quite conser- matus; Bryant ('45) for Spermophilus (seven vative in squirrels. Among other rodents, species), Ammospermophilus (two species), the insertion changes with the insertion of Tamias speciosa, Marmota flaviventer, Cyno- sternomastoid (Rinker, '54). This muscle is mys gunnisoni, Sciurus griseus, Sciurus ni- missing in Jaculus (Howell, '32; Klingener, ger, Tamiasciurus douglasii, Glaucomys '64). volans, and Glaucomys sabrinus. This is followed by comments on the com- M. cleido-occipitalis accessorius parative anatomy of other rodents based on Origin: Arises from the ventral surface of Parsons (1894, 1896) for diverse "hystrico- the clavicle immediately adjacent to the clei- morph" and "myomorph" rodents, Alezais domastoid. (1900) for Cavia, Mus, and Dipus, Howell Insertion: Inserts on the nuchal ridge for 2 ('26) for Neotoma, Hill ('37) for geomyids, mm adjacent to the mastoid process. Lewis ('49) for Aplodontia, Rinker ('54, '63) Remarks: Not recorded in other squirrels, for cricetines, Klingener ('64) for dipodoids, this muscle was found in only one specimen 158 R.W. THORINGTON ET AL.

Sciurus Protoxerus [^| cleido-occipitalis

Irapezius

occipitoscapularis ^P rhomboid

Wh cleidomastoid

^ sternomastoid

Heliosciurus Myosciurus

Fig. 1. Posterior surface of the skull showing variations in the extent of the origins of trapezius, occipitoscapularis, and rhomboid, and the insertions of cleido-occipitalis, cleidomastoid, and sternomastoid in eight squirrel genera. Scale bar = 5 mm. of Atlantoxerus. It is probably derived from talis separated by several millimeters. In the immediately adjacent cleidomastoid, but genera with extensive cranial origins of tra- is completely separable from it. pezius (Xerus and Heliosciurus), the insertion is restricted to the lateral portion of the M. cleido-occipitalis nuchal line. In flying squirrels, which lack a Origin (Fig. 2): Arises from the caudal cranial origin of trapezius, the insertion is edge of the clavicle. In most genera, the much more extensive: in Belomys, Hylope- origin completely covers cleidomastoid. How- tes, and Pteromys, it extends from the inser- ever, in Nannosciurus, Myosciurus, Xerus, tion of sternomastoid nearly to the midline; Funambulus, Callosciurus, and Spermophi- inEoglaucomys, it extends to the midline; in lus variegatus, the origin was more lateral Glaucomys and Petaurista, it extends to the and only partly overlapped the origin of clei- midline and for a short distance on the nu- domastoid. chal ligament of the neck. In Atlantoxerus, Insertion (Fig. 1): Inserts on the nuchal Sciurus, and Spermophilus, the dorsal edge line on the cranium, usually between the of cleido-occipitalis is fused with the ventral sternomastoid and the trapezius (in Sper- edge of trapezius. mophilus, between the cleidomastoid and Remarks: In squirrels, this muscle is com- the trapezius). Only in Funisciurus are the pletely separable at its origin from the cleido- insertions of sternomastoid and cleido-occipi- mastoid. The degree of fusion of its insertion SQUIRREL FORELIMB MUSCLES 159

Glaucomys Petaurista

cl-occ

Spermophilus Xerus

Fig. 1. (Continued) with the ventral edge of the trapezius varies separable into distinct parts, although the in the Marmotini, being completely sepa- origin from the midline is aponeurotic oppo- rated in Marmota and Cynomys (Bryant, site the scapular spine in some genera (Pro- '45). Among other rodents, Woods ('72) notes toxerus, Heliosciurus, Paraxerus, Funisciu- that this muscle in hystricomorphs is not rus, Spermophilus, Atlantoxerus, and Ratufa). separable from the cleidomastoid at their Insertion (Fig. 3): Inserts on the scapular origins. spine from the metacromion almost to the vertebral border. Anterior fibers insert on M. trapezius the cranial border of the scapular spine; the Origin (Fig. 1): In most squirrels, trape- most posterior fibers insert on the caudal zius arises from the nuchal line of the cra- border of the scapular spine. In Myosciurus, nium and the midline of the neck and back. few fibers insert on the caudal border of the The origin extends for half the length of the spine. In Xerus, the most caudal fibers form nuchal line in Xerus and Heliosciurus and an "auricular slip," passing over the metacro- less than half in other tree and ground squir- mion and joining fibers of the M. sphincter rels. In the flying squirrels (Belomys, Eoglau- colli superficialis. comys, Glaucomys, Hylopetes, Petaurista, Remarks: Among squirrels, Bryant ('45) and Pteromys), it arises from the neck and described the insertion of trapezius extend- back, not from the nuchal line of the skull. In ing onto the base of the acromion in the all squirrels, the origin extends caudally to Marmotini. We did not observe this in any of the vicinity of T8 to T10. The muscle is not our dissections and therefore we do not use 160 R.W. THORINGTON ET AL.

cranial -~ medial C^rrrii^ lateral caudal Sciurus Funisciurus /7\^ [7] cleidomastoid

y////^w///////z^ HI cleido-occipitalis clavodeltoid £

Callosciurus Heliosciurus

•/?//•••••••,•••;,,;,...... ^.i*///. ^"--i-V,V,YW-y'w^

Atlantoxerus Spermophilus

clavobrachialis [~|

Petaurista Glaucomys

•iuimmi •\>>"/,",'"///'

Nannosciurus Myosciurus i • 1

-4V» Fig. 2. Ventral surface of the clavicle often squirrel genera showing the origin of subclavius and the insertions of cleidomastoid, cleido-occipitalis, clavodeltoid, and, in Spermophilus, clavobrachialis. Scale bar = 5 mm.

the name acromiotrapezius for the anterior Extensor system portion of this muscle. It does not insert on Costo-spino-scapular group the acromion and it is not separable from the M. levator scapulae et M. serratus ventralis posterior portion (spinotrapezius) which in- Origin: Arises by slips from the ribs and serts on the caudal border of the scapular spine. In some rodents, the insertion ex- cervical vertebrae, converging to a single tends onto the clavicle: slightly in dipodoids sheet. An origin from the atlas is absent in and heteromyids, extensively in geomyids most genera. In Heliosciurus rufobrachium (Hill, '37; Klingener, '64; Ryan, '89). An au- (three of four specimens), there is a slip ricular slip of the trapezius is widely found originating from the ventral surface of the among rodents. Among the sciurids, it was atlas which passes superficial to the scale- noted in Marmota (Bryant, '45) and in Tami- nus (Fig. 4). asciurus (Rinker, '54). It also occurs in Insertion: Inserts on the vertebral edge of Aplodontia (Lewis, '49; Klingener, '64), in the scapula and the adjacent costal surface. hystricomorphs (Woods, '72), and among The insertion extends to the superficial sur- bathyergids, microtines, cricetines, and dipo- face of the scapula between rhomboid and doids (Klingener, '64, '70), but not geomyoids teres major in Sciurus, Callosciurus, Heli- (Hill, '37; Ryan, '89). osciurus, Paraxerus, and Funisciurus. SQUIRREL FORELIMB MUSCLES 161 Remarks: Contrary to our observations, by Parsons (1894) or Bryant ('45). It is found Bryant ('45) reported an origin from atlas as in some other rodents, e.g., cricetines the common condition for squirrels. Parsons (Rinker, '54) and arvicolids (Stein, '86). (1894) reported the atlantic origin present in Callosciurus, Pteromys, and Marmota, but M. occipitoscapularis absent in Xerus. It is present in a wide Origin (Figs. 1, 5): Arises from the supe- variety of other rodents as well (Parsons, rior nuchal line of the skull deep to the 1894; Ryan, '89). The occurrence of an atlan- cleido-occipitalis and medial to the insertion tic slip of levator scapulae, in addition to the of cleidomastoid. In the pygmy squirrels and atlantoscapularis dorsalis, was cited by in the flying squirrels, the origin is short and Woods ('72) as a reason for doubting that the is restricted to the lateral half or less of the latter muscle was derived from the former nuchal line. The origin extends medially to (see remarks for atlantoscapularis dorsalis). the cranial origin of the rhomboid in Atlan- M. rhomboideus toxerus, Xerus, Protoxerus, Paraxerus, and Origin (Figs. 1, 5): Arises from the supe- Heliosciurus, and almost to the midline in rior nuchal line, the cervical vertebrae, and the other genera. The origin is most exten- the first few thoracic vertebrae. Rhomboid sive in Funisciurus and Spermophilus. originates on the nuchal line vnAtlantoxerus, Insertion (Figs. 3, 5): Inserts on the dorsal Xerus, Paraxerus, Protoxerus, and Heliosciu- end of the scapular spine and on the verte- rus. In the other genera, there is no cranial bral border of the scapula anterior to the origin. In Xerus, the cranial origin is sepa- spine. It also inserts on the costal surface of rate from the vertebral origin and forms a the scapula in the flying squirrels, and in the distinct rhomboideus capitis. In Funambu- tree squirrels Callosciurus, Protoxerus, Fu- lus and Heliosciurus gambianus, the verte- nisciurus, and Paraxerus ochraceus. In Eo- bral origin is divided into anterior and poste- glaucomys, it also inserts on the surface of rior portions. the rhomboid. In Belomys, Petaurista, and Insertion (Figs. 3, 5): Inserts on the verte- Pteromys, the insertion is restricted to the bral edge of the scapula from the scapular cranial portion of the vertebral border of the spine nearly to the caudal angle. Rhomboid scapula. In Protoxerus, occipitoscapularis in- inserts on the costal side of the scapula in all serts on the surface of the supraspinatus. In genera except for Sciurus. In Funambulus Spermophilus variegatus, Ratufa, Paraxerus, and Heliosciurus gambianus, the posterior Funisciurus, and Heliosciurus, the inser- portion inserts superficial to the anterior tions of occipitoscapularis and atlantoscapu- portion and the fibers have a medial-lateral laris dorsalis are inseparable. orientation. The fibers of the anterior por- Remarks: The variation of this muscle in tion have a more cranial-caudal orientation. squirrels was not well documented hereto- The insertion does not extend to the caudal fore. A similar amount of variation occurs in angle of the scapula in Protoxerus, Ratufa, other rodents (Hill, '37; Rinker, '54; Klinge- and Spermophilus variegatus. ner, '64). The close association of occipito- Remarks: The part of the rhomboid origi- scapularis and atlantoscapularis dorsalis at nating on the nuchal line, as described above, their insertion was noted by Woods ('72). In should not be confused with the occipito- addition, he reported that the origins are scapularis (Fig. 5). The rhomboid and the contiguous in Thryonomys and argued that occipitoscapularis seem to us always to be atlantoscapularis dorsalis was derived from distinguishable in squirrels, contrary to the the occipitoscapularis. report of Bryant ('45). As reported by Par- sons (1894), and noted by us, they are least M. atlantoscapularis ventralis separable in Spermophilus, Bryant's princi- (omocervicalis) pal subject. They may not be separable at Origin (Fig. 4): Arises from the ventral the origin, but it is possible to allocate fibers arch of the atlas, medial to the attachment to their respective muscles on the basis of of scalenus. their separation more distally Woods ('72) Insertion (Fig. 3): Inserts on the metacro- describes them as forming a single sheet in mion of the scapula adjacent or partially most hystricomorphs. The two muscles are deep to the trapezius muscle. The trapezius obviously closely related. A distinct posterior significantly overlaps the atlantoscapularis portion of the rhomboid, seen by us in Fu- ventralis in Petaurista, Protoxerus, and nambulus and Heliosciurus, was not noted Ratufa. In the other genera, the muscles 162 R.W. THORINGTON ET AL.

costal dorsal

Fig. 3. Costal and dorsal surfaces of the scapula of tions of occipitoscapularis, rhomboid, atlantoscapularis six squirrel genera showing the origins of teres major, ventralis, atlantoscapularis dorsalis, and trapezius. Scale teres minor, and the long head of triceps, and the inser- bar = 5 mm.

may be adjacent or trapezius may slightly insertion. Hill ('37) reports its origin on the overlap the insertion of atlantoscapularis basioccipital in Spermophilus, but that is ventralis. Only in one specimen of Sper- not reported for Spermophilus in other stud- mophilus richardsonii did some fibers of tra- ies (Brizzee, '41; Bryant, '45). The primitive pezius lie deep to fibers of atlantoscapularis morphology of the origin for rodents is sub- ventralis. The separability of the two muscles ject to debate. Parsons (1894) suggests that at their insertion is variable. the primitive origin is on the basioccipital, Remarks: Among squirrels, this muscle as seen in diverse rodents, and that the exhibits very little variation in origin or origin from the atlas is derived. In many SQUIRREL FORELIMB MUSCLES 163

costal dorsal

I. h. triceps trap t. minor atlantoscap. vent Callosciurus

Petaurista \]> -f£>

Fig. 3. (Continued.)

other mammals, e.g., Didelphis (Stein, '81), and that this primitive condition is retained and primates (Howell and Straus, '33), the in Heteromys and Neotoma. However, the origin is on the transverse process of the origin is on the ventral arch, not the trans- atlas. If we use these as out-groups, the verse process of the atlas, in Heteromys basioccipital origin in some rodents would (Ryan, '89) andNeotoma (Howell, '26; Rinker, appear to be the most derived, not the primi- '54), thus destroying Hill's ('37) hypothesis. tive condition as suggested by Parsons Woods ('72) argues that the origin from the (1894). ventral arch of the atlas is the primitive Hill ('37) suggests that the primitive ori- morphology for rodents, as seen in hystrico- gin is the transverse process of the atlas, morphs and sciurids. 164 R.W. THORINGTON ET AL.

serratus ventralis atlantoscapularis - atlantic slip - dorsalis

atlantoscapularis ventralis

Sciurus carolinensis Heliosciurus rufobrachium

Fig. 4. Ventral surface of the atlas of Sciurus carolin- rus. In S. carolinensis, as in most squirrel genera, serra- ensis and Heliosciurus rufobrachium illustrating the tus ventralis does not have an origin on the atlas. Scale origin of an atlantic slip of serratus ventralis inHeliosciu- bar = 5 mm.

This muscle inserts on the metacromion of all squirrels, most muroids, and most hystri- Funambulus comorphs. In the dipodoid rodents, it inserts mostly on the acromion (Klingener, '64). In the geomyids and Ctenomys, the burrowing hystricomorph, the insertion is on the clavicle (Hill, '37). There is a similar disagreement about which insertion is primitive for rodents. Hill ('37) argues that it is the acromion and Woods ('72) argues that it is the metacromion.

M. atlantoscapularis dorsalis Origin (Fig. 4): Arises from the ventral arch of the atlas, lateral to atlantoscapularis ventralis. Atlantoscapularis dorsalis is absent in Xerus, Atlantoxerus, and Myosciu- rhomboideus anterior rus, and is very thin and narrow in Nanno- sciurus. Insertion (Fig. 3): Inserts on the scapular spine adjacent to the insertion of occipitoscapularis. The insertion is overlapped par- rhomboideus posterior tially by the insertion of occipitoscapularis in Glaucomys, Funambulus, and Spermophi- lus columbianus. In some flying squirrels (Belomys, Eoglaucomys, Petaurista, and Pteromys), where the insertion of occipitoscapularis is restricted to the vertebral border of the scapula, the insertion of atlantoscapularis dorsalis extends from the scapular Fig. 5. Dorsal view of occipitoscapularis and rhomboid musculature of Funambulus, showing the two parts spine onto the vertebral border. The inser- of rhomboid with rhomboideus posterior overlapping tions of atlantoscapularis dorsalis and occipi- rhomboideus anterior. toscapularis are inseparable in Spermophi- SQUIRREL FORELIMB MUSCLES 165 lus variegatus, Ratufa, Paraxerus, Funisciurus, rately in Neotoma and Peromyscus (Rinker, and Heliosciurus. '54), and Phodopus (Stein, '90). An achselbo- Remarks: This muscle is reported absent gen is less common in squirrels than in hys- in Aplodontia (Hill, '37; Lewis, '49), four tricomorphs, in which it has been carefully subgenera of Spermophilus (Bryant, '45), the described and discussed (Woods, '72). dipodoids (Klingener, '64), the muroids (Rinker, '54), and four genera of hystrico- M. teres major morphs (Woods, '72). Bryant reported the Origin (Fig. 3): Arises from the axillary muscle absent in the subgenus Spermophi- edge of the scapula, ventral to the caudal lus based on his examination of S. beldingi. angle, and sometimes from the caudal sur- We found it present in two other species of face of the axillary border and the adjoining this subgenus, S. columbianus and S. rich- surface of subscapularis. Its origin extends ardsonii. There appears to be a tendency for one- to two-thirds of the length of the axil- it to be lost in burrowing rodents as well as lary edge. In tree squirrels, there is a dis- in pygmy squirrels. tinct teres fossa on the axillary border of There are two hypotheses about the deri- scapula for the origin of this muscle. In vation of this muscle. Howell ('37) suggested Callosciurus and Funambulus, teres major that it was derived from the serratus sheet, originates partially from infraspinatus as because of its origin on the atlas. Woods ('72) well. argued that it was derived from the rhom- Insertion (Fig. 6): Inserts with latissimus boid sheet via the occipitoscapularis because dorsi on the medial surface of humerus, me- the two are closely associated at their inser- dial to the deltoid ridge. tions and because in Thryonomys their ori- Remarks: In the Sciuridae, a prominent gins are also adjacent. He submitted that teres major fossa is characteristic of tree Howell's hypothesis was falsified by the co- squirrels and is absent from the marmotine occurrence of atlantic slips of both the serra- and xerine ground squirrels. In contrast, tus sheet and the atlantoscapularis dorsalis Lehmann ('63) noted a prominent teres ma- in the same animal, such as we observed in jor fossa in the burrowing rodents Geomys Heliosciurus. However, this is not fatal to and Ctenomys which was lacking in the non- Howell's argument if one accepts the possibil- fossorial rodents she studied. ity of a doubling of the atlantic slip of the serratus sheet. Atlantoscapularis dorsalis oc- M. subscapularis curs in marsupials (Stein, '81), primates (Howell and Straus, '33), insectivores (Camp- Origin: Arises from the subscapular fossa, bell, '39; Reed, '51), and other orders of mam- except for its vertebral edge. mals. Therefore, the condition in Thryono- Insertion: Inserts on the lesser tuberosity mys is probably derived and irrelevant to of the humerus. the origin of this muscle in the Mammalia. Remarks: The internal structure and subdivision of this muscle (Lehmann, '63) were Latissimus-subscapular group not studied. M. latissimus dorsi Origin: This somewhat variable muscle Deltoid group commonly has a fleshy origin from the spi- M. deltoideus nous process of the posterior six thoracic Divisible into three parts: the clavodeltoid, vertebrae, a fascial origin from the first one the acromiodeltoid, and the spinodeltoid. or two lumbar vertebrae, and again a fleshy Origin (Fig. 2.): Clavodeltoid takes origin origin from the last four ribs. from the caudoventral surface of the clavicle Insertion (Fig. 6): Inserts with teres major over the lateral two-thirds of its length. It on the medial surface of the humerus, me- extends further medially in Heliosciurus, dial to the deltoid ridge. In Eoglaucomys and Eoglaucomys, and Glaucomys. It is always Funambulus, latissimus dorsi has an achsel- separable from acromiodeltoid, although bogen that inserts deep to pectoralis major their origins closely approximate one an- on the deltoid ridge. other in most genera. The origins are most Remarks: Bryant ('45) stated that the in- separated in Atlantoxerus and Glaucomys. sertions of latissimus dorsi and teres major In Spermophilus, the most superficial fibers were separate in Glaucomys. We did not find form a separate M. clavobrachialis, which this in Glaucomys or any other squirrels. In arises from the clavicle, superficial to the other rodents, the two muscles insert sepa- clavodeltoid. 166 R.W. THORINGTON ET AL.

Protoxerus Callosciurus Petaurista

pectoralis u abdominalis

Ncoracobrachialis:

m t>

Myosciurus Ratufa Atlantoxerus

Fig. 6. Medial surface of the humerus for eight squirrel genera, showing insertions of seven muscles. Scale bar = 5 mm.

The acromiodeltoid arises from the acro- the origin extends nearly to the vertebral mion, lateral to the insertion of atlantoscapu- border of the scapula. laris ventralis. Insertion (Figs. 6, 7): Clavodeltoid inserts Spinodeltoid takes origin from the ventral along the distal three-fourths of the medial half of the scapular spine to the vicinity of side of the deltoid ridge of the humerus. In the metacromion. In Atlantoxerus, Xerus, Petaurista, Atlantoxerus, Myosciurus, Callosciurus, Funambulus, Myosciurus, Eo- Ratufa, and Funambulus, the insertion of glaucomys, and Glaucomys, it also origi- clavodeltoid extends to the proximal end of nates slightly from the surface of the infra- the humerus. In all genera except Atlan- spinatus. In Myosciurus and Nannosciurus, toxerus, spinodeltoid fuses with acromiodel- SQUIRREL FORELIMB MUSCLES 167

Atlantoxerus Spermophilus

Fig. 7. Deltoid musculature of Atlantoxerus and Spermophilus, showing the special clavobrachialis, found in the marmotine ground squirrels Spermophilus, Cynomys, and Marmota, but not in the African xerine ground squirrels Atlantoxerus and Xerus. Scale bar = 5 mm.

toid, which then inserts on the lateral side of origin of the long head of triceps extends the deltoid ridge. In Atlantoxerus, the spi- further from the glenoid than does the origin nodeltoid inserts tendinously, separate from of the teres minor. The opposite is true in the acromiodeltoid. In Myosciurus, Pe- Spermophilus columbianus, in the flying taurista, and Funambulus, this insertion ex- squirrels Glaucomys and Belomys, and espe- tends to the top of the humerus. In most cially in Petaurista. genera, the insertion of acromiodeltoid is Insertion: Inserts on the distal surface of relatively thin, but in Atlantoxerus, Pe- greater tuberosity of the humerus, distal to taurista, Eoglaucomys, Glaucomys, and the insertion of the infraspinatus muscle. In Ratufa, the insertion is thick. In Spermophi- Ratufa, and to a greater degree in Petaurista, lus, the clavobrachialis inserts with brachia- the insertion is elongated, rather than circu- lis on the proximal end of the ulna. lar. Remarks: In squirrels, a clavobrachialis, Remarks: In many squirrels this muscle is innervated by the axillary nerve, occurs in minuscule and therefore is not easily differ- Spermophilus, Cynomys, and Marmota, but entiated from the infraspinatus. is absent in other members of this tribe: Ammospermophilus, Tamias, and Sciurot- Suprascapular group amias (Parsons, 1894; Brizzee, '41; Bryant, M. infraspinatus '45). In the hystricomorphs Cavia and Dasy- Origin: Arises from the infraspinous fossa procta, the clavodeltoid inserts distally on of the scapula. the humerus, but this is very different from Insertion: Inserts on the greater tuberos- the clavobrachialis of Spermophilus, which ity of the humerus, between the insertions of crosses the elbow joint and inserts on the ulna. supraspinatus and teres minor. Remarks: Differences in the relative sizes M. teres minor of the infraspinatus and supraspinatus Origin (Fig. 3): Arises from the axillary muscles and their fossae vary among gen- surface of the scapula adjacent to the gle- era, but this variation is better studied in a noid process, superficial to the origin of the series of scapulae than in dissections (e.g., long head of triceps. In most genera, the Swidersky, '93). 168 R.W. THORINGTON ET AL. M. supraspinatus nous or aponeurotic origin of the lateral head, Origin: Arises from the supraspinous fossa common in squirrels, is found in most other of the scapula. rodents, also. Insertion: Inserts on the greater tuberos- M.anconeus ity of the humerus, proximal to the insertion of infraspinatus. Origin: Arises from the posterior surface of the lateral epicondylar ridge of the humerus. Triceps group Insertion (Fig. 9): Inserts on the lateral M. triceps brachii surface of the olecranon process of the ulna Origin (Fig. 3): The long head arises from and extends distal to the semilunar notch. the axillary border of the scapula adjacent to Remarks: The most distal fibers pass on the glenoid fossa, deep to the origin of teres the flexor side of the elbow joint when the minor. In Funambulus, the origin of the long arm is flexed. Only when the elbow is partly head has shifted away from the glenoid. extended could they act to further extend In most squirrels, the lateral head arises the arm. aponeurotically distal to the insertion of teres minor, along the lateral surface of the del- M. dorsoepitrochlearis toid ridge, adjacent to the insertion of del- Origin: Arises from both teres major and toid. It extends distally to the crest of the latissimus dorsi near their common inser- deltoid ridge in Myosciurus, Protoxerus, He- tion on the humerus. liosciurus, and Funambulus, while in Funis- Insertion (Fig. 10): Inserts on the medial ciurus and Ratufa, the origin barely extends side of the proximal end of the ulna. In to the deltoid ridge. The condition in the Atlantoxerus and Xerus, the dorsoepitrochle- other genera is intermediate. In some flying aris inserts on the dense connective tissue squirrels (Belomys, Eoglaucomys, and Ptero- on the medial side of the elbow, overlying mys), the lateral head has a fleshy origin flexor carpi ulnaris. In Protoxerus, there is distal to the insertion of teres minor. This an additional insertion on the superficial contrasts with the strictly tendinous origin surface of anconeus. in Glaucomys and Hylopetes. In Petaurista, Remarks: The usual origin of this muscle the fleshy origin covers a larger area on the in squirrels is from both teres major and lateral surface of the humerus and extends latissimus dorsi. Bryant ('45) reports an ori- onto the proximal third of the posterior sur- gin, in some species of Spermophilus, from face of the humerus. the teres major and the scapula, but not In most squirrels, the medial head of tri- from latissimus dorsi. In contrast, the muscle ceps arises extensively from the posterior takes origin almost exclusively from the latis- surface of the humerus, from a point be- simus dorsi in hystricomorphs (Woods, '72). tween the head and the lesser tuberosity to a Howell ('37) and Cheng ('55) consider this point only slightly proximal to the medial muscle to be derived from the latissimus epicondyle. In Petaurista, the origin of the dorsi, in spite of its innervation by the radial medial head is restricted to the distal two- nerve. Therefore, Woods ('72) suggests that thirds of the humerus. In Funambulus, the the origin from the latissimus dorsi is primi- medial head is divided into superficial and tive. Origin from the teres major is com- deep parts by the radial nerve. monly found in other rodents as well as Insertion (Figs. 8, 9): The long head and squirrels. the medial head insert on the distal tip of the olecranon. The lateral head inserts on the Extensor group of the forearm olecranon with the long head, and along the M. brachioradialis lateral surface of the ulna to a point slightly Origin: Arises from the anterior surface of distal to the semilunar notch. In Petaurista, the lateral epicondylar ridge of the hu- the insertion of the lateral head is restricted merus, proximal to extensor carpi radialis to the distal end of the olecranon process. longus. Remarks: The separation of the medial Insertion (Fig. 9): Inserts tendinously on head into superficial and deep parts is rare the distal end of the radius. In Petaurista, in squirrels, but is seen in nine genera of the tendinous insertion is elongated over the hystricomorph rodents (Woods, '72). A tendi- distal one-third of the radius. In Ratufa in- SQUIRREL FORELIMB MUSCLES 169

Petaurista Eoglaucomys Glaucomys R) -^•lateral head of triceps Q

•brachialis \W\

Funisciurus Callosciurus Heliosciurus

Fig. 8. Lateral view of the humerus for six genera of squirrels, demonstrating the variation in the origin of the lateral head of triceps. Scale bar = 5 mm.

dica, but not in other species of Ratufa, the McEvoy, '82), Castor (Parsons, 1894), geomy- insertion is fleshy, rather than tendinous, ids (Hill, '37), and some muroids (Rinker, '54). and extends over the distal one-fourth of the radius. M. extensor carpi radialis longus Remarks: Although universally present in squirrels, this muscle is commonly lost in Origin (Fig. 9): Arises from the anterior other rodents. It is absent in Aplodontia surface of the lateral epicondylar ridge of (Hill, '37; Lewis, '49), all hystricomorphs ex- the humerus, between brachioradialis and cept Erethizon and Coendou (Woods, '72; extensor carpi radialis brevis. 170 R.W. THORINGTON ET AL.

extensor carpi radialis / II M |on3us>•'' J~ brachioradialis " ° El W.\ brevis V ggjj| abductor pollicis longus \ A W\ brachioradialis X .'•;py .a-iconeus [^]

Xerus rutilus

Fig. 9. Extensor surface of the forearm (radius, ulna, and distal end of humerus) of ten genera of squirrels, showing the origins of seven muscles and the insertions of brachioradialis, supinator, anconeus, and triceps. Scale bar = 5 mm.

Insertion: Inserts on the proximal end of M. supinator the second metacarpal. Remarks: In sciurids, this is always larger Origin (Fig. 9): Arises from the anterior than extensor carpi radialis brevis. In the portion of the lateral epicondyle of the hu- hystricomorphs Myocastor and Thryonomys, merus. geomyids, and others, the reverse is true Insertion (Fig. 9): Inserts on the lateral (Hill, '37; Woods, 72). surface of the proximal half of the radius. At its proximal end, the insertion also wraps around to the medial surface of the radius. M. extensor carpi radialis brevis In Callosciurus and Spermophilus, supina- Origin (Fig. 9): Arises from the anterior tor inserts on more than half the length of surface of the lateral epicondylar ridge of the radial shaft. the humerus, distal to extensor carpi radia- Remarks: In squirrels, a sesamoid bone lis longus. does not occur in the tendon of origin of the Insertion: Inserts on the proximal end of supinator. Such a sesamoid is found in other the third metacarpal. rodents: geomyids (Hill, '37), cricetines SQUIRREL FORELIMB MUSCLES 171

Funisciurus anerythrus i 1

Fig. 9. (Continued.)

(Rinker, '54), and microtines (Stein, '86), but Remarks: In sciurids, the tendon varies not in dipodoids (Stein, '90). from a single broad insertion on both the first metacarpal and the falciform to a dis- M. abductor pollicis longus tinctly bifurcated tendon. Bryant ('45) re- Origin (Fig. 9): Arises linearly from the ported the absence of the insertion on the lateral surface of the ulna, from the lateral falciform in Sciurus, Tamiasciurus, and surface of the radius, and from the interosse- Glaucomys. We observed a falciform inser- ous membrane. The ulnar origin begins near tion in all specimens we dissected. In flying the elbow joint and continues distally two- squirrels, the falciform is connected by a thirds of the way down the shaft. The radial ligament to the styliform cartilage by means origin begins at the radial head and extends of which the abductor has the important distally halfway down the shaft. In all gen- function of extending the wingtip (Thoring- era except for Myosciurus, Petaurista, Glau- ton et al., in press). Therefore, reports of the comys, and Atlantoxerus, the ulnar origin is absence of a falciform insertion in flying much longer than the radial origin. squirrels should be viewed as dubious. Insertion: Inserts via a bifurcated tendon In seven genera of hystricomorphs, the on the radial side of the first metacarpal and muscle is described as having two distinct on the falciform. In Ratufa and Funambu- tendons. In dipodoids and some muroids, lus, there is only one broad tendon, which Rinker ('54) and Klingener ('64) considered inserts across the two bones. it to be two separate muscles, using the 172 R.W. THORINGTON ET AL.

\M\ epitrochleoanconeus flexor digitorum profundus hj

pronator quadratus ^

Xerus rutilus

Fig. 10. Flexor surface of the forearm (radius, ulna, tus, and the insertions of epitrocleo-anconeus, dorsoepitro- and distal end of humerus) of ten genera of squirrels, clearis, brachialis, biceps, pronator teres, and pronator showing the origins of epitrochleo-anconeus, flexor carpi quadratus. Scale bar = 5 mm. ulnaris, flexor digitorum profundus, and pronator quadra- name M. extensor pollicis brevis for the part two tendons to digit 3. In Eoglaucomys, the that inserted on the falciform. Woods ('72) tendon to digit 2 arises from a separate head argued that it was not the extensor, but of the muscle. rather a subdivided abductor. The difference between the two hypotheses is moot, be- M. extensor indicis cause the extensor pollicis brevis is a de- Origin (Fig. 9): Arises from the lateral rived feature in primates, found in Homo surface of the ulna toward the distal end of and Gorilla (Howell and Straus, '33). There- the bone. The origin is distal to the origin of fore, the subdivision of the abductor pollicis abductor pollicis longus in all genera except in rodents, no matter what it is called, is Atlantoxerus, Sciurus, and Spermophilus co- independent of the evolution of the extensor lumbianus. pollicis brevis in primates. Insertion: Inserts on digit 2. In Ratufa, Protoxerus, Heliosciurus, Callosciurus, M. extensor digitorum communis Paraxerus, Funisciurus, and Spermophilus Origin: Arises from the proximal surface columbianus, there was an additional inser- of the lateral epicondyle of the humerus. tion on digit 1. Insertion: Inserts on digits 2•5. In Xerus, Remarks: The insertion on the pollex was Atlantoxerus, Ratufa, Sciurus, Callosciurus, not observed by Hill ('37) or Bryant ('45) in Funisciurus, and Spermophilus, there are nearctic sciurids, but it was present in speci- SQUIRREL FORELIMB MUSCLES 173

Fig. 10. (Continued)

mens of Sciurus carolinensis dissected by serts on digits 3 and 4 is completely separate Woods ('72). Our dissections demonstrate from the belly that inserts on digit 5. that it is common in sciurids as a bifurcation Remarks: The frequent insertion of this of the tendon to the index finger. Woods ('72) muscle into digit 3 suggests that the exten- found it in ten genera of hystricomorphs, sor digiti tertii has been incorporated into and in one of these, Mesomys, there was a the extensor digiti quinti, as suggested by completely separate tendon to the pollex. Klingener ('64). Hill ('37) suggested that the extensor pollicis brevis has been incorporated into the exten- M. extensor carpi ulnaris sor indicis, but this interpretation assumes Origin: Arises from the distal end of the that the extensor pollicis brevis of humans is lateral epicondyle of the humerus. primitive for rodents, which it surely is not. Insertion: Inserts on the proximal end of the fifth metacarpal. M. extensor digiti quinti proprius Origin: Arises from the lateral epicondyle Flexor system of the humerus and is inseparable from the Pectoral group origin of the extensor digitorum communis, M. pectoralis major (ectopectoralis of Hill, '37) except in Spermophilus columbianus. Origin: Arises from the sternebrae, from Insertion: Inserts on digits 3•5. In Xerus, the manubrium to the xiphisternum in all Atlantoxerus, Ratufa, Sciurus, Callosciurus, genera. Heliosciurus, and Spermophilus, the inser- Insertion (Fig. 6): Inserts on the deltoid tion is restricted to digits 4 and 5. In Ratufa ridge of the humerus, deep to the insertion and Eoglaucomys, the muscle belly that in- of clavodeltoid, usually along the distal three- 174 R.W. THORINGTON ET AL. fourths of the ridge. In Petaurista and Fu- The proximal end of the insertion is most nambulus, the insertion of pectoralis major extensive in Funambulus, Petaurista, and extends to the proximal end of the humerus. Eoglaucomys, where both insert on the proxi- Remarks: The origin of a few fibers from mal end of the humerus; in Petaurista and the clavicle was reported in Tamias and Eoglaucomys, the insertion continues onto Glaucomys (Bryant, '45) and in Aplodontia the coracoid process of the scapula. The inser- (Lewis, '49). tion does not extend onto the deltoid ridge in Callosciurus, Paraxerus, Myosciurus, and M. pectoralis minor Funisciurus. The insertion of pectoralis ab- Origin: Takes origin deep to the pectoralis dominalis extends onto the deltoid ridge in major, commonly from sternebrae 2•5 and Sciurus, Protoxerus, and Heliosciurus, and the sternal ends of costal cartilages 2•4, and is most extensive in Atlantoxerus and Fu- sometimes 5. There is some variation in the nambulus. In Glaucomys, the insertion is extent of the origin. It has shifted slightly restricted to the proximal end of the hu- caudally in Heliosciurus, Protoxerus, and merus, just distal to the insertion of supra- Spermophilus, in which it did not take origin spinatus. from sternebra 2 or costal cartilage 2. In Remarks: We found the insertion to ex- Atlantoxerus, the origin extended from ster- tend further distally on the humerus in some nebra 2 to the xiphisternum. genera than was reported by Bryant ('45) for Insertion (Fig. 6): Inserts on the deltoid nearctic sciurids. If the insertion on the ridge of the humerus, deep to the insertion shoulder capsule is the primitive condition of pectoralis major. It extends to the distal for rodents (Woods, '72), then the more distal end of the pectoralis major insertion in one insertion in Atlantoxerus and Funambulus flying squirrel (Petaurista), but not the oth- is derived. ers; in three tree squirrels (Ratufa, Paraxerus, and Callosciurus), but not the M. entopectoralis profundus other tree squirrels; and in one ground squir- Origin: Arises as a thin membranous sheet rel (Atlantoxerus), but not the others (Xerus from 2 to 4 costal cartilages (between carti- and Spermophilus). The proximal end of the lages 2 and 5) and adjoining sternebrae. insertion extends to the proximal end of the Insertion: Inserts on the first rib, lateral humerus, distal to the insertion of supraspi- to the origin of the subclavius. natus, in all genera except Protoxerus. The insertion continues onto the coracoid pro- M. cutaneus maximus cess of the scapula in the large flying squirrels, Petaurista and Eoglaucomys. In Myo- Origin: Arises from the skin over the tho- sciurus and Glaucomys, the insertion is racic and lumbar regions. restricted to the proximal end of the hu- Insertion: Inserts on the shoulder joint merus, near the insertion of supraspinatus. (anterior fibers) and further down on the The insertion is short and is proximal to and humerus deep to pectoralis major, usually aligned with the insertion of pectoralis ma- with pectoralis minor, pectoralis abdomina- jor in Xerus. In Callosciurus, pectoralis mi- lis, and latissimus dorsi. In Myosciurus, it nor splits into two slips, the dorsal slip insert- inserts independently on the humeral head. ing just distal to supraspinatus insertion In Petaurista, cutaneus maximus inserts in- and the ventral slip inserting further dis- dependently as well, but its insertion ex- tally on the deltoid ridge. tends onto the coracoid of the scapula. In Remarks: In other rodents, insertion on Eoglaucomys, cutaneus maximus inserts the coracoid process is common (Parsons, only on the coracoid process. 1896; Rinker, '54). An insertion onto the Remarks: The derived condition of this clavicle, as seen in many hystricomorphs muscle in the gliding membrane of flying (Woods, '72), was not found in any sciurids. squirrels was not examined. See Johnson- Murray ('77). M. pectoralis abdominalis Origin: Arises from abdominal facia, cau- M. subclavius dal to the xiphisternum. It is most extensive Origin: Arises from the proximal end of in Funambulus. It has a very narrow origin the first costal cartilage. in Petaurista. Insertion (Figs. 2, 11): Inserts on the dor- Insertion (Fig. 6): Inserts on the proximal sal surface of the distal half of the clavicle. end of the medial side of the deltoid ridge. The insertion of subclavius extends to the SQUIRREL FORELIMB MUSCLES 175

Callosciurus Ratufa

Fig. 11. Cranial view of clavicle and scapula, showing the insertion of subclavius in Callosciurus, as it is in most squirrels, and the insertion extending onto the supraspinatus muscle of the scapula in Ratufa. Scale bar = 5 mm. distal end of clavicle in most genera. It does chialis begins near the peak of deltoid ridge not extend quite to the distal end in Sciurus, in Sciurus, Protoxerus, Heliosciurus, Atlan- Heliosciurus, Funisciurus, Myosciurus, Sper- toxerus, Ratufa, Petaurista, Eoglaucomys, mophilus, and Atlantoxerus. In Ratufa, the Glaucomys, Spermophilus columbianus, and insertion extends onto the surface of the Paraxerus. In Myosciurus, Callosciurus, Xe- supraspinatus muscle of the scapula. rus, Spermophilus variegatus, Funambulus, Remarks: In hystricomorphs (Woods, '72), and Funisciurus, the insertion begins distal bathyergids (Parsons, 1896), and other mam- to the deltoid ridge. mals, there is a scapuloclavicularis muscle Remarks: The short head has been found which originates on the clavicle and inserts in all genera of squirrels studied, in Aplodon- on the scapular spine or vertebral border. tia and in the geomyids (Hill, '37), heteromy- This is superficially similar to the scapular ids (Howell, '32), dipodoids (Klingener, '64), insertion of subclavius in Ratufa, but the and some muroids (Rinker, '54). The distal origins and insertions are different. Thus, insertion in sciurids, Aplodontia (Hill, '37; the morphology in Ratufa is probably inde- Lewis, '49), and most myomorphs (Parsons, pendently derived from the scapuloclavicula- 1896) reputedly includes the middle and long ris of other rodents. heads described by Wood (1867), although it is not clear how to distinguish this condition Flexor group of the arm from an extended middle head. M. coracobrachialis Origin: Arises from the coracoid process. M. biceps brachii Insertion (Fig. 6): Short head inserts on Origin: The long head originates from the the medial surface of the humerus slightly supraglenoid tuberosity. The short head distal to the greater tuberosity The linear originates from the coracoid process. insertion is perpendicular to the insertion of Insertion (Fig. 10): Inserts on the bicipital teres major. Atlantoxerus, Glaucomys, and tuberosity on the radius, distal to or slightly Ratufa have a more dot-like insertion. In overlapping the insertion of brachialis on Petaurista, the short head has two points of the ulna. The short head merges into and insertion, adjacent to each other. The long inserts with the long head. head inserts on the distal half of the medial Remarks: In sciurids, the short head of surface of the humerus and on the medial biceps is usually present, but has been re- epicondylar ridge. The insertion of coracobra- ported absent in Sciurus vulgaris (Hoff- 176 R.W. THORINGTON ET AL. mann and Weyenbergh, 1870) and in Sper- tilage. This latter is the tendon of the pal- mophilus variegatus and S. beecheyi (Bryant, maris longus (Thorington et al., '97a). In '45). The biceps always inserts on the radius flying squirrels, the flexor carpi ulnaris (Parsons, 1894; Alezais, 1900; Hill, '37; serves the additional function of retracting Brizzee, '41; Bryant, '45). In other rodents, the wing tip when the animals are not glid- the short head of biceps is absent in some ing (Thorington et al., '97a). In other ro- hystricognaths and Castor (Parsons, 1894), dents, the epicondylar head is absent in geo- Zapus and Jaculus (Klingener, '64), and Alac- myids (Hill, '37), Oryzomys (Rinker, '54), taga (Howell, '32). Insertion on both radius dipodoids (Klingener, '64), microtines (Stein, and ulna, or just on ulna, is common (Par- '86), and heteromyids (Ryan, '89). sons, 1894; Alezais, 1900; Hill, '37; Rinker, '54; Klingener, '64; Ryan, '89). M. palmaris longus Origin: Arises from the medial epicondyle M. brachialis of the humerus with flexor digitorum subli- Origin: Arises extensively as a single head mis. It is completely separable from the flexor from the lateral surface of the humerus dis- in Spermophilus columbianus, Callosciurus, tal to the origin of the lateral head of triceps. Funisciurus, Paraxerus, and Sciurus. Distal to the deltoid ridge, the origin extends Insertion: Inserts on the palmar facia of more medially, adjoining the insertion of the the hand. In flying squirrels, it also inserts coracobrachialis. on the styliform cartilage. In Petaurista, a Insertion (Fig. 8): Inserts on the ulna dis- broad tendon separates into two parts before tal to the coronoid process. inserting on the palmar fascia. Remarks: The recognition of a small me- Remarks: In other mammals, this muscle dial head of brachialis, seen in other rodents is usually innervated by the median nerve. (Parsons, 1894; Hill, '37; Rinker, '54; Klinge- In sciurids and hystricomorphs, it is inner- ner, '64; Woods, '72), does not seem war- vated by the ulnar nerve (Woods, '72). ranted for squirrels. Parsons (1894) described the two heads in sciurids as "so M. flexor carpi radialis closely blended as to be indistinguishable," Origin: Arises from the medial epicondyle and Bryant ('45) remarked that brachialis of the humerus, distal to the origin of prona- "has two incompletely separated heads." tor teres, either separately or with the other flexor muscles. It is completely separate in Flexor group of the forearm Spermophilus columbianus, Heliosciurus, M. epitrochleo-anconeus Paraxerus, Callosciurus, and Funisciurus. Origin (Fig. 10): Arises from the extensor Insertion: Inserts on the base of the sec- side of the medial epicondyle of the hu- ond metacarpal. merus. Petaurista has a more extensive origin that includes the epicondylar ridge. M. pronator teres Insertion: Inserts on the medial surface of Origin: Arises from the proximal portion the olecranon process deep to the dorsoepi- of medial epicondyle of the humerus, sepa- trochlearis. rate from the other forearm flexors in all genera except Eoglaucomys. M. flexor carpi ulnaris Insertion (Fig. 10): Inserts on the medial Origin (Fig. 10): Arises from the base of surface of the radius, over approximately the medial epicondyle of the humerus, ei- the middle third of the bone. Pronator teres ther on its own or in common with the other inserts more distally in Eoglaucomys, Cal- forearm flexors, and from the medial surface losciurus, andXerus. The length of the inser- of the olecranon, deep to the insertion of tion varies. Spermophilus, Ratufa, Funam- dorsoepitrochlearis. bulus, Sciurus, Protoxerus, Eoglaucomys, Insertion: Inserts on the distal tip of the and Glaucomys have relatively long inser- pisiform bone. In the flying squirrels, flexor tions, but the insertion is relatively short in carpi ulnaris inserts both on the pisiform the other genera. In Glaucomys and Ratufa, and on the styliform cartilage. the proximal portion of the insertion curves Remarks: In squirrels, the epicondylar medially toward the insertion of biceps. head is almost always present, but has been reported absent in Spermophilus (Parsons, M. flexor digitorum sublimis 1894). Gupta ('66) and Johnson-Murray ('77) Origin: Arises from the medial epicondyle described two tendons of insertion in flying of the humerus, between the condyloradial squirrels, one inserting on the styliform car- and central heads of flexor digitorum profun- SQUIRREL FORELIMB MUSCLES 177 dus, either separately or in common with the digit 1 was absent in Myosciurus, Sciurus, other forearm flexors. It arises separately in Callosciurus, and Petaurista. Spermophilus columbianus, Callosciurus, Remarks: The innervation of this muscle Paraxerus, and Funisciurus. is also variable. Innervation of the ulnar Insertion: Inserts on digits 2•5. The ten- head by the ulnar nerve, and the other heads don to each digit is perforated by the corre- by the median nerve, is probably most com- sponding tendon of the flexor digitorum pro- mon, as in other rodents (Hill, '37), but we fundus. It divides over the distal end of the observed innervation of the two condylar metacarpal and reunites deep to the profun- heads by both median and ulnar nerves in dus tendon over the first phalanx. Each in- two specimens of Glaucomys, and of the con- serts as a single broad tendon on the palmar dyloradial head in Funisciurus. surface of the base of the second phalanx. The tendon to digit 1 was not found by Remarks: Contrary to the normal innerva- Parsons (1894) in Callosciurus or Pteromys, tion by the median nerve in other mammals, and by Alezais (1900) in Marmota. It was this muscle is commonly innervated by the found in Sciurus by Alezais (1900). Bryant ulnar nerve in squirrels. We found only ul- ('45) found it in all of his specimens, includ- nar innervation hiXerus, Protoxerus, Ratufa, ing Sciurus and Marmota. and Petaurista, and Woods ('72) found it in M. pronator quadratus Sciurus and Eutamias. We found only median innervation in Funisciurus and Glauco- Origin (Fig. 10): Arises from the medial mys and in two specimens of Callosciurus. surface of the ulna near its distal end. We found both median and ulnar innerva- Insertion (Fig. 10): Inserts on the medial tion in one specimen of Callosciurus. Thus surface of the radius near its distal end. In ulnar innervation of the flexor digitorum Callosciurus, Spermophilus, Paraxerus, sublimis has been observed in both subfami- Sciurus, Atlantoxerus, and Xerus, the origin lies and five of the seven tribes of the Sciuri- is more extensive than the insertion. nae, and median innervation in flying squir- Remarks: This muscle is absent in the rels and two tribes of the Sciurinae. The pygmy squirrels Nannosciurus and Myosciu- insertion of this muscle is commonly re- rus and in the smaller flying squirrels Glau- stricted to digits 2•4 in other rodents (Par- comys, Pteromys, and Hylopetes. In the larger sons, 1894; Rinker, '54; Klingener, '64; Stein, flying squirrels Petaurista, Eupetaurus, Eo- '86; Ryan, '89). glaucomys, and Belomys, it is a narrow, thin, interosseus muscle, in contrast to the robust M. flexor digitorum profundus pronator quadratus of tree and ground squirrels. Origin: Arises by four heads. The condyloradial head arises from the posterior portion Miscellaneous muscles of the medial epicondyle of the humerus, M. omohyoid anterior to the origin of epitrochleo-anco- Origin: Arises from the ventral portion of neus. The central head arises from the ante- the cranial border of the scapula, in the rior portion of the medial epicondyle, deep to cranial notch. the other forearm flexors. These two heads Insertion: Inserts on the hyoid. arise separately in Spermophilus columbianus, Paraxerus, Funisciurus, and Callosciu- Lateral retractor of pouch rus. Only the central head is separate in We found this muscle present in Spermophi- Sciurus. In other genera, these arise in com- lus and Sciurotamias. mon with the other forearm flexors. The Origin: Arises from the metacromion of radial head arises from the medial surface of the scapula, between the insertion of trape- the radius, deep to the insertion of pronator zius and atlantoscapularis ventralis and the teres. The ulnar head arises from the medial origin of spinodeltoid. surface of the ulna, deep to the origin of Insertion: Inserts on the cheek pouch in flexor carpi ulnaris. Spermophilus and Sciurotamias. There is a Insertion: All four heads converge to a similar muscle taking origin on the scapula single tendon in the carpal tunnel and di- and inserting on the cheek in Heliosciurus, verge into four tendons at the level of the Callosciurus, and Funambulus, although metacarpals. These tendons insert on the these squirrels lack cheek pouches. terminal phalanges of digits 2 through 5. Remarks: Bryant ('45) found this muscle The tendon to digit 2 commonly bifurcates in Spermophilus, Cynomys, Ammosper- and sends a branch to digit 1. This tendon to mophilus, and Tamias, but not in Marmota. 178 R.W. THORINGTON ET AL. The lateral retractor of the cheek pouch in traditionally, but probably incorrectly, allo- squirrels is formed of facial musculature. In cated to the same tribe as the African squir- hamsters, it is derived from the auricular rels Funisciurus, Paraxerus, and Myosciu- slip of the trapezius muscle. In geomyids rus. Like chipmunks, they are active both on and heteromyids, both facial musculature the ground and in trees. Ratufa, the giant and trapezius muscle contribute to the lat- tree squirrels of Southeast Asia, are highly eral retractor (Hill, '35; Priddy and Brodie, arboreal and seldom come to the ground '48; Klingener, '64, '70). The presence of an (MacKinnon, '78; Payne, '80; Thorington and auricular portion of trapezius in Marmota Cifelli, '90). Callosciurus, also of Southeast and Xerus suggests that another form of Asia, are usually highly arboreal, but the cheek retractor could readily have evolved species we studied, C. notatus, frequently in sciurids. comes to the ground like North American tree squirrels of the genus Sciurus (MacKin- DISCUSSION non, '78; Payne, '80). The six genera of flying Our goal in this study was to locate de- squirrels we dissected include Petaurista, rived myological features of phylogenetic or the giant flying squirrels of Southern Asia; functional significance. Forelimb muscula- Eoglaucomys, the large Himalayan flying ture alone is an inadequate base for a phylo- squirrels; Belomys and Hylopetes, smaller genetic analysis, but it is clear that some of flying squirrels of Southern Asia; Pteromys, the myological differences we describe have the northern flying squirrels of Eurasia; and important phylogenetic implications. An ad- Glaucomys, the North American flying squir- equate understanding of how muscles func- rels. In addition, we examined a few muscles tion during locomotion requires a great deal in a forearm of the large wooly flying squir- of information not currently available for rel, Eupetaurus cinereus, and one specimen squirrels. These include differences in muscle of the Chinese rock squirrel, Sciurotamias masses, distributions of slow and fast twitch davidianus. muscle fibers, differences in recruitment pat- Arboreality is presumed to be primitive terns, etc. (Jenkins and Weijs, '79; Arm- for the Sciuridae because the earliest fossil strong, '81; Fleagle, '82; Stalheim-Smith, '84; squirrel, Douglassia jeffersoni, has so many Larson, '93). However, even if we had all of features of an arboreal squirrel (Emry and this information for squirrels, it would be Thorington, '82). Accordingly, it is likely that difficult to interpret it in view of the diverse the forelimb anatomy of tree squirrels is locomotor behaviors of these animals, which primitive for the family. The similarity of include walking, bounding on horizontal to musculature among tree squirrels in five vertical surfaces, digging, leaping, gliding, tribes of the Sciurinae is in keeping with landing, and head-first descent of vertical this assumption. Only in the Ratufini is there surfaces. Nonetheless, comparative anatomy a noteworthy derived myological feature, the provides data for initial hypotheses about insertion of the subclavius on the supraspi- the functional differences between animals, natus muscle in addition to the insertion on and it seems appropriate to speculate on the the clavicle (Fig. 11). This muscle stabilizes biological significance of the data presented. the distal end of the clavicle, which serves as The 19 genera of squirrels we selected for a strut for positioning the shoulder joint. morphological comparison are geographi- The extended insertion of the subclavius cally and ecologically diverse. The two gen- presumably strengthens this role. The divi- era of pygmy tree squirrels, Myosciurus of sion of the rhomboid (Figs. 1, 3, 5) into Africa and Nannosciurus of Southeast Asia, anterior and posterior sections occurs in Fu- occupy the bark gleaner niche (Emmons, nambulus and Heliosciurus gambianus, '80). Atlantoxerus and Xerus are genera of which are not closely related to one another. African ground squirrels. Like many of the Functional reasons for this morphology are North American ground squirrels, Sper- unclear. There are other differences among mophilus, they live in burrows, but also climb the tree squirrels in the relative positions of readily (Herzig-Straschil, '78; Herzig-Stra- origins and insertions of muscles, but these schil and Herzig, '89; O'Shea, '91). The two are subtle and do not distinguish any of the tribes of African tree squirrels are repre- tribes from each other. The scansorial and sented by the highly arboreal Protoxerus arboreal locomotion of tree squirrels in all and Heliosciurus, and by the less arboreal five tribes is accomplished with the same members of the genera Funisciurus and basic arrangement of forelimb muscles. One Paraxerus (Kingdon, '74; Emmons, '80). Fu- feature shared by all tree squirrels, but not nambulus, the Indian striped squirrels, are by other sciurids, is a well-developed teres SQUIRREL FORELIMB MUSCLES 179 major fossa at the posterior angle of the deltoid, to flex the elbow in support of the scapula (Fig. 3). The teres major functions in normal function of the brachialis. These retrofiexion of the shoulder•decreasing the muscles flex the elbow without causing supi- angle between the humerus and the axillary nation of the forearm, in contrast with the border of the scapula. In terrestrial locomo- biceps, which causes both flexion and supination, retrofiexion occurs during the support tion. In comparing Sciurus and Cynomys, phase as the forelimb is retracted, but the Stalheim-Smith ('84) noted that the biceps weight of the animal probably contributes to of Sciurus generated more than twice the this movement and little force is required by torque as that of Cynomys. Tree climbing the teres major. In a climbing animal, how- probably requires both strong elbow flexion ever, gravity works against retrofiexion and and forearm supination, while digging may the teres major must overcome it (Jenkins require flexion without supination. The at- and Weijs, '79). This may explain why tree lantoscapularis dorsalis is lost repeatedly in squirrels have the enlarged fossa and why the xerine ground squirrels, and in four sub- Stalheim-Smith ('84) found that the tree genera of the marmotine genus Spermophi- squirrel Sciurus niger has a much stronger lus. It is not clear to us why this muscle teres major than does the prairie dog Cyno- would be lost in burrowing squirrels. It would mys gunnisoni. appear to function as a rotator of the scapula, Pygmy tree squirrels are bark gleaners a movement that may be more effectively and forage on large tree trunks with their accomplished by the occipitoscapularis in limbs placed far more laterally than is seen these animals. in larger tree squirrels. The limbs are elon- Flying squirrels exhibit a number of de- gated, particularly the forearm, and the rived myological features. The trapezius thumb is reduced or absent (Anthony and lacks a cranial origin and, in association Tate, '35; Emmons, '79; Thorington and Thor- with this, the insertion of the cleido-occipita- ington, '89). The atlantoscapularis dorsalis lis on the nuchal line is more extensive than (Fig. 3) is lost in Myosciurus and is greatly in other squirrels (Fig. 1). The cranial fibers reduced in Nannosciurus. This muscle func- of trapezius in tree squirrels probably functions to rotate the scapula during retraction tion both to assist in head movements and in of the limb, but it may be in a poor position protraction of the shoulder joint. The absence of these fibers in flying squirrels does to effect this when the limbs are held later- not greatly affect the protraction of the ally. The spinodeltoid is extensive in pygmy scapula, but it does eliminate the use of the squirrels and probably plays a major role in trapezius in cranial movement. The more retrofiexion of the shoulder joint. Pronator extensive insertion of the cleido-occipitalis quadratus (Fig. 10) is lost in these two ani- in flying squirrels presumably assumes this mals, correlating with the elongation of the function. Occipitoscapularis has a restricted forearm and presumably with a reduction in lateral origin on the nuchal line and tends to the amount of pronation and supination at insert on the vertebral border and not on the the wrist. spine of the scapula. The insertion of atlanto- Terrestrial locomotion takes several forms scapularis dorsalis extends to or onto the within the Sciurinae. Cursorial terrestrial vertebral border of the scapula (Fig. 3). Both squirrels (Rheithrosciurus andEpixerus) and these muscles are positioned to have better the terrestrial Asiatic squirrel Rhinosciurus leverage than in tree squirrels for rotating were not included in this study because of the scapula during retraction of the limb. In the unavailability of specimens. The two larger flying squirrels, the lateral head of tribes of burrowing ground squirrels, Xerini triceps has a muscular origin, and in the and Marmotini, were included. These ani- giant flying squirrel Petaurista, it has an mals both climb less and dig more than do extensive muscular origin, contrasting with tree squirrels. A distinctive derived muscle the tendinous origin in other squirrels (Fig. in the Marmotini is the superficial layer of 8). As a result of this, there appears to be an the clavodeltoid, which inserts on the ulna increase in the number of long muscle fibers and forms a clavobrachialis (Fig. 7). This is in these flying squirrels. A very important found only in some genera (Marmota, Sper- aspect of flying squirrel locomotion is safe mophilus, and Cynomys) forming a single landing after a glide. The triceps absorbs the clade of the Marmotini (Bryant, '45), and is impact, and the lateral head may play a absent in others {Tamias, Sciurotamias, and special role in this if it is composed of fast Ammospermophilus). This muscle has a com- twitch fibers, as in other mammals (Arm- pletely different function from the rest of the strong, '81). The radial and ulnar heads of 180 R.W. THORINGTON ET AL. the forearm flexors have more restricted ori- other closely related species of Spermophi- gins than usual for squirrels, reflecting the lus. How does the absence of this muscle elongation of the radius and ulna for gliding, affect scapular rotation? Does the absence of and the pronator quadratus is greatly re- pronator quadratus in pygmy tree squirrels duced or absent. Flying squirrels exhibit reflect a difference in how they pronate and greatly reduced mobility between the distal supinate their forearms, as it does in flying ends of radius and ulna, yet they pronate squirrels? We conclude this study with more and supinate their forearms readily. Prona- questions, but more focused questions than tion and supination occur at the elbow and before, about the functional anatomy of these are effected by pronator teres and supinator interesting animals. muscles, thereby reducing the function of the pronator quadratus (Thorington, '84). ACKNOWLEDGMENTS The flying squirrels are characterized by the We thank Lawrence R. Heaney and derived morphology of the abductor pollicis, William Stanley of the Field Museum of the flexor carpi ulnaris, and the palmaris Natural History (FMNH), Eric Yensen of the longus, associated with the extension and O.J. Smith Museum of Natural History at retraction of the styliform cartilage and the Albertson College of Idaho (OJSMNH), and wing tip of the plagiopatagium (Thorington Duane Schlitter and Suzanne McLaren of et al., in press). the Carnegie Museum (CM) for the loan of Derived features of forelimb musculature specimens. Peter Zahler provided us with in squirrels may characterize groups of gen- the Eupetaurus forelimb. Advice and com- era or tribes, like the clavobrachialis (Fig. 7) ments on the manuscript were provided by and the scapular insertion of subclavius (Fig. Robert Hoffmann and Brian Stafford. Fund- 11), or they may evolve independently in ing for A.D.K.B. was provided by the Re- several tribes, like the loss of the atlanto- search Training Program and the Minority scapularis dorsalis. No derived myological Internship Program of the Smithsonian In- features of the forelimb appear to be synapo- stitution. morphies of two or more tribes. 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APPENDIX. Specimens dissected Family Sciuridae Subfamily Sciurinae: Tree, ground, and pygmy squirrels Tribe Ratufini: Indo-Malayan giant squirrels Ratufa affinis: USNM 522980 Ratufa bicolor: USNM 546334 Ratufa indica: USNM 548661 Tribe Protoxerini: African giant and sun squirrels Protoxerus stangeri: USNM 481817, 481821 Heliosciurus gambianus: USNM 381419, 481830 Heliosciurus rufobrachium: USNM 463538, 463544, 463545, 541537 Tribe Funambulini: Indian and African tree and pygmy squirrels Subtribe Funambulina: Indian striped squirrels Funambulus palmarum: USNM 448821, 448824 Subtribe Funisciurina: African striped squirrels and tree squirrels Funisciurus anerythrus: USNM 463536 Paraxerus ochraceus: USNM 251930 Paraxerus palliatus: USNM 548034 Subtribe Myosciurina: African pygmy squirrels Myosciurus pumilio: USNM 514360, 220760 Tribe Callosciurini: Oriental squirrels Callosciurus notatus: USNM 521141, USNM uncatalogued (IMR 84702, 86338, 86351) Nannosciurus melanotis: USNM 154407 Tribe Sciurini: Holarctic and neotropical tree and pygmy squirrels Sciurus carolinensis: USNM 396002, 497249, 497250, 522976 Tribe Marmotini: Holarctic ground squirrels Spermophilus columbianus: OJSMNH uncatalogued (EY821) Spermophilus richardsonii: USNM 398236 Spermophilus variegatus: OJSMNH 414 Sciurotamias davidianus: USNM 541398 Tribe Xerini: African ground squirrels Xerus rutilus: CM 86231 Atlantoxerus getulus: USNM 477053, 477054 Subfamily Pteromyinae: Flying squirrels Belomys pearsoni: USNM 359595 Eoglaucomys fimbriatus: FMNH 140501 Eupetaurus cinereus: USNM uncatalogued forelimb Glaucomys volans: USNM 457978, 457979 Hylopetes spadiceus: USNM uncatalogued (IMR 89902, 89799) Petaurista philippensis: USNM 334352, 334359 Pteromys volans: USNM 547926