Carpal Development and Morphology in Archontan Mammals

JOURNAL OF MORPHOLOGY 235:135-155 (1998)

1 2 BRIAN J. STAFFORD * AND RICHARD W. THORINGTON, JR xPhD Program in Anthropology & New York Consortium in Evolutionary Primatology, City University of New York, New York, New York ^Department ofVertebrate Zoology, Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, DC

ABSTRACT Carpal morphology and development in bats, colugos, tree shrews, murids, and sciurids were studied in order to homologize carpal elements. Prenatal coalescence of discrete cartilaginous templates with a loss of a center of ossification appears to be the most common method of reducing carpal elements in these mammals. Only bats and colugos showed postnatal ossification between discrete elements as a method of reducing carpal elements. Carpal morphology of tree shrews is more diverse than previously reported. Ptilocercus shows a highly derived carpal morphology that may be related to its relatively greater arboreality Dendrogale exhibits what is most likely the ancestral tupaiid carpal morphology. Carpal morphologies of Tupaia, Urogale, and Anathana are identical to each other. Carpal morphology differs between megachiropterans and microchiropterans. These differences may be related to different aerodynamic constraints between the suborders. The carpal morphology of microchiropterans is diverse and may reflect different adaptive regimes between microchiropteran families. Carpal morphology of the colugos shows both megachiropteran and microchiropteran characters. The function of these characters in colugos and bats (stabilization of the carpus in dorsiflexion) is proposed to be similar, although the locomotor roles may be quite different between these taxa. J. Morphol. 235:135—155, 1998. © 1998 Wiley-Liss, Inc. KEYWORDS: carpal reduction, scapholunate, hands, dermoptera, chiroptera, scanAentia, ptilocercus, peromyscus, sciuridae.

Reduction in the number of proximal and teran-paromomyid-primate clade (the Prima- intermediate carpal elements involving the tomorpha Beard, 1989, see also Beard, '93). scaphoid, lunate, and centrale is a common Similarly, fusion of the scaphoid and lunate condition among mammals. It occurs in mar- has been claimed as both a tupaiine and supials, carnivores, rodents, insectivores, scandentian character. However, there has bats, tree shrews, and dermopterans, to been some confusion over which scanden- name a few. In the case of the scaphoid and tians possess which character state (Flower, lunate, it is usually reported that the radial 1870; Lyon, '13; Clark, '26; Davis, '38; Grasse, aspect of the lunate fuses to the ulnar aspect '55; Haines, '55; Steiner, '65; Verma, '65; of the scaphoid. If the centrale is absent, it is Novacek, '80; Beard, '93; Simmons, '95). usually stated to be either lost or fused to Adult morphologies often have been errone- the distal aspect of the scaphoid (Leboucq, ously (Verma, '65) or confusingly (Davis, '38) 1899; Steiner, '22, '42, '65; Schmidt-Ehren- described, and there is no detailed descrip- berg, '42; Holmgren '52; Altner, 71). We stud- tion of carpal morphology in Urogale. ied the patterns of carpal element reduction in archontans because the composition and arrangement of elements making Up the Contract grant sponsor: New York Consortium in Evolutionary large proximal Carpal element have been Primatolo^ (BJS); contract grant sponsor: DMsion of Mam- -, mals and Dept. or Vertebrate Zoology at the National Museum ot proposed as a Synapomorphy of a chirop- Natural History, Smithsonian Institution. teran-dermopteran clade (the Volitantia II- "Correspondence to: Brian J. Stafford, who is now at the Ko-m- 1811 aoo NVwnrolr '««• S J,1JW nnrl Department of Vertebrate Zoology, Division of Mammals, NHB llger, iai± see JNOVaceK, »», Szalay7 and ggo MRC 108, National Museum of National History, Smithso- Lucas, 93, 96; Simmons, 95), Or a dermop- nian Institution, Washington, DC 20560.

C 1998 WILEY-LISS, INC. 136 B.J. STAFFORD AND R.W. THORINGTON, JR The Primatomorpha hypothesis proposes MATERIALS AND METHODS that the lunate articulates with the distal The taxa investigated in this study in- aspect of the scaphoid in the paromomyifor- clude members of the Chiroptera, Dermop- mes (usually considered to be "archaic" pri- tera, Rodentia, and Scandentia. Strepsi- mates) and that it has become fused to the rhine primates and Tarsius were also distal scaphoid in colugos (Dermoptera, examined to check specific characters involv- Cynocephalidae). Under this hypothesis, the ing the articular relationships of the cen- scaphoid has expanded ulnarly to articulate trale. The appendix provides a detailed list with the cuneiform, and the lunate has been of specimen numbers, ages, and prepara- displaced to articulate with the distal aspect tions. Specimens were obtained from the of the scaphoid. The elements remain un- National Museum of Natural History, Smith- fused in the paromomyiformes but are hy- sonian Institution (USNM), the Field Mu- pothesized to have fused into a single large seum of Natural History (FMNH), and the element, the scaphocentralolunate, in colu- Department of Zoological Research, Na- gos. Fusion of the scaphoid, centrale, and tional Zoological Park, Smithsonian Institu- lunate also has been proposed as a synapo- tion (DZR-NZP). morphy of the Volitantia (Novacek and Wyss, Four types of preparations were used for '86; Szalay and Lucas, '93, '96; Simmons, '94, this study: osteological material available at '95). Although the pattern of fusion is not USNM and from FMNH, dissections of fluid- specified in this hypothesis, it is testable. In preserved and frozen specimens at USNM tree shrews, fusion of the scaphoid and lu- and DZR-NZP, cleared and stained speci- nate also has been used as a taxonomic mens provided by USNM and DZR-NZP, and character (Novacek, '80; Beard, '93; Sim- X-rays of USNM and FMNH skins. The tree mons, '94). shrews from DZR-NZP were stained for both A central question, then, is how does one cartilage and bone (Dingerkus and Uhler, determine the homology of carpal elements? '77), whereas the Peromyscus leucopus were If an element is absent, it may have been cleared and stained for bone only (Green, either lost or fused and an examination of '52) at the New England Regional Primate the adult condition is insufficient to distin- Research Center. Other specimens in the guish between these two cases. Different USNM collections had been cleared and ontogenetic pathways can produce similar stained for bone and cartilage. Cartilagi- adult morphologies and the fusion of carpal nous templates were easily identifiable in elements should not be an assumption but all specimens. The sciurid specimens were an hypothesis to be tested against develop- not cleared and stained, but were examined mental series. grossly. The cartilages were clearly defined. The literature on carpal development in Scanning electron microscope images of se- archontans is extensive (Leboucq, 1899; lected osteological specimens were enhanced Steiner, '22, '65; Schmidt-Ehrenberg, '42; to provide black backgrounds, standard 1 Holmgren, '52; Altner, '71), but lacks taxo- mm scale bars, labels of carpal elements, nomic breadth. The carpal elements in onto- and to remove extraneous details. In no case genetic series of tree shrews, colugos, and was relevant morphology altered, obscured, bats were studied in order to determine pat- or deleted. terns and processes of carpal fusion in arch- Many different names have been applied ontan mammals. Ontogenetic series of pri- to the different carpal bones. The terminol- mates were not examined because primates ogy used in this study follows Romer ('54) as generally retain unfused carpal elements. shown in Figure 1. In the primitive mamma- Reduction of the scaphoid and lunate to a lian carpus (Fig. 1) the proximal carpal row single element also occurs independently in consists of four elements, the middle row of murids and sciurids, as evidenced by the one element, and the distal row of four ele- presence of a free lunate in Douglassiajeffer- ments (see Romer, '54; Lewis, '89). We deter- soni (Emry and Thorington, '82). To see if mined the homology of carpal cartilages and the process of reduction between these taxa bones by the morphological similarity of was the same as in archontans, a growth these structures and the commonality of series of Peromyscus leucopus and two sciu- their articular relationships. Where the num- rid specimens, were examined. ber of carpal elements was reduced, either CARPAL DEVELOPMENT IN ARCHONTAN MAMMALS 137 fusion or loss of primitive elements has occurred. Discrimination of the processes in- volved in carpal reduction is difficult because reduction of carpal elements can result Ulna / Radius from nonhomologous processes that produce similar adult conditions (Lewis, '89). These processes include the ossification between discrete cartilaginous templates, the coalescence of cartilaginous templates prior to ossification, or the failure of separate cartilaginous templates to develop. We recognized three different ways in which carpal elements fuse (columns 2—4 of Table 1). With these factors in mind, the following protocols were used to homologize carpal elements and processes of reduction. A distinct cartilage in a young animal that showed the same position and articular relationships as a primitive carpal (Fig. 1) was considered homologous with that carpal. If all the primitive carpals were present in infant animals, but fewer carpals were seen in adults, then fusion of elements was considered to have occurred during ossification. If there were fewer cartilaginous templates in postnatal animals than in the primitive condition, three possibilities exist: (1) one cartilage may have never developed; (2) it may have developed and then been lost; or (3) it Fig. 1. Hypothesized carpal morphology of an ances- may have coalesced with another cartilage tral mammal. Redrawn from Lewis ('89). C, centrale; Cu, cuneiform; L, lunate; M, magnum; Pi, pisiform; pp, prenatally If such a cartilage showed mul- prepollex; S, scaphoid; Td, trapezoid; Tm, trapezium; tiple centers of ossification, we would pre- U, unciform. sume that it was derived from more than

TABLE 1. Patterns of carpal reduction in some mammals Postnatal Postnatal ossification Two centers of ossification between Prenatal ossification between Free scaphoid scaphoid coalescence of within Free scaphoid and lunate and lunate scaphoid and scapholunate centrale or lunate Taxon1 in adults cartilages lunate cartilages2 cartilage in adults and centrale Megachiroptera No3 Yes No NA No Yes Microchiroptera No Yes No NA No Yes Dermoptera No No Yes No No Yes Prosimians4 Yes NA NA NA Yes NA Rodentia Cavia No No Yes ? Yes NA Peromyscus No No ? No Yes NA Callosciurus No No ? ? Yes NA Sciurus No No ? ? Yes NA Scandentia Ptilocercus Yes NA NA NA Yes NA Dendrogale Yes NA NA NA Yes NA Tupaia No No Yes No Yes NA Urogale No ? ? ? Yes NA Anathana No ? ? ? Yes NA

1See Appendix for a detailed list of the taxa within each higher taxonomic category used here. ^Prenatal coalescence of the centrale with the scaphoid does not occur in any of the taxa studied here. 3Yes = observed condition, No = condition not present, NA = not applicable, ? = unknown. ^Pro simians = strepsirhines 4- tarsiers, a paraphyletic group. 138 B.J. STAFFORD AND R.W. THORINGTON, JR one cartilage. This latter pattern was not the cuneiform is concave radio-ulnarly, and observed in this study. However, if a carti- there is a dorsal process of the pisiform that lage of uncertain composition showed a single forms the ulnar border of the joint. This center of ossification, then it was deduced results in the ulnar styloid process being that one center of ossification has been lost. cupped radio-ulnarly between the cuneiform To distinguish between nondevelopment, and pisiform, a condition not seen in the loss, and coalescence of prenatal cartilages tupaiines. requires a series of specimens not available In the distal carpal row, the articular rela- for all of the taxa studied here (Leboucq, tionships of magnum, unciform, and cen- 1899; Holmgren, '52; Rajtova, '67; Altner, trale further make the carpus of Ptilocercus '71). unique. Proximo-radially, the magnum articulates with the centrale, but most of its RESULTS proximal articular contact is with the unci- Ptilocercus: Pen-tailed tree shrew form, which extends radially to articulate Ptilocercus (Fig. 2a) possesses four proxi- with the ulnar aspect of centrale. This radial mal carpal elements: the scaphoid, lunate, extension of the unciform isolates the mag- cuneiform, and pisiform. They also have a num from the proximal carpal row. Some large centrale. All four distal carpal ele- degree of magnum-lunate contact may be ments are present: trapezium, trapezoid, effected in certain hand positions. No devel- magnum, and unciform (see Clark, '26; opmental series of Ptilocercus was available. Haines, '55). In the proximal row, the scaphoid in Ptilo- Dendrogale: Smooth-tailed tree shrews cercus articulates with the radius proxi- Dendrogale (Fig. 2b) has four proximal mally, the lunate ulnarly, and the centrale carpal elements: scaphoid, lunate, cunei- and trapezium distally The lunate articu- form, and pisiform. They also have a large lates proximally with the radius, ulnarly centrale. All four distal carpal elements are with the cuneiform, radially with the scaph- present. oid, disto-radially with the centrale, distally In the proximal row, the scaphoid articu- with the unciform, and palmarly with the lates with the radius proximally, the lunate pisiform. The cuneiform articulates proxi- ulnarly, and a large centrale and the trape- mally with the ulna and pisiform, distally zium distally. The lunate articulates proxi- with the unciform, and radially with the mally with the radius, ulnarly with the cunei- lunate. It also may contact the centrale dur- form, radially with the scaphoid, and distally ing certain hand positions, but this is un- with the magnum. Certain hand positions clear. The articulations among cuneiform, may elicit lunate-centrale or lunate-unci- pisiform, and the ulnar styloid process are form contact, but not to any great degree. unique. The proximal articular surface of Cuneiform articulates proximally with the

Fig. 2. A: Scanning electron micrograph of the dorsal centrale; Cu, cuneiform; L, lunate; M, magnum; Pi, left carpus of USNM 121885 adult Ptilocercus lowii. B: pisiform; pp, prepollex; R, radius; S, scaphoid; Td, trap- X-ray of the right carpus of USNM 256752 adult Dendro- ezoid; Tr, trapezium; U, unciform; Ul, ulna. gale murina, image reversed. Scale bars = 1 mm. C, CARPAL DEVELOPMENT IN ARCHONTAN MAMMALS 139 ulna and pisiform, disto-radially with the trale. All four distal carpal elements are magnum, distally with the unciform, and present. radially with the lunate. The position of the In the proximal row, the scapholunate ar- pisiform is unclear from our X-rays, but there ticulates with the radius proximally, the cu- is no indication that it is similar to Ptilocer- neiform ulnarly, and the magnum, centrale, cus. and trapezium distally. Cuneiform articu- In the distal carpal row, the magnum is lates proximally with the ulna, distally with not proximo-distally truncated by the unci- the unciform, radially with the scapholu- form as it is in Ptilocercus. In Dendrogale, nate, and palmarly with the pisiform. In the magnum shows the characteristic Tupaia, the pisiform articulates with the waisted shape of tupaiine magna, and the palmar aspect of the cuneiform and the ul- unciform does not contact the centrale. With nar styloid process, and slightly with the the exception of the unfused lunate, the mor- scapholunate. It lacks the dorsal process phology and articular relationships of the seen in Ptilocercus. carpus are identical with those of Tupaia In the distal carpal row, the magnum ar- (Fig. 3), Urogale (Fig. 4a), and Anathana ticulates with the centrale on its proximo- (Fig. 4b). The specialized articular pattern radial surface and proximally with the scaph- between magnum, unciform, and centrale olunate; the unciform does not articulate seen in Ptilocercus is not present in Dendro- with the centrale. The magnum shows the gale. characteristic waisted shape of tupaiines. Figure 3a,b illustrates the process of ossi- Tupaia: Tree shrews fication in the carpus of postnatal Tupaia. Tupaia (Fig. 3) has only three proximal Distinct cartilages are present for all of the carpal elements: scapholunate, cuneiform, carpal elements except the lunate. The and pisiform. They also have a large cen- scapholunate cartilage ossifies from one cen-

Fig. 3. Postnatal carpal development and morphology in Tupaia. A: Dorsal left carpus of NZP 109835 4-day-old Tupaia tana. B: Dorsal left carpus of NZP 109835 4-day-old Tupaia tana. C: Dorsal right carpus of USNM 396666 adult Tupaia minor, image reversed. Scale bars = 1 mm. C, centrale; Cu, cuneiform; M, magnum; P, pisiform; pp, prepollex; R, radius; SL, scapholunate; Td, trapezoid; Tr, trapezium; U, unciform; Ul, ulna. 140 B.J. STAFFORD AND R.W. THORINGTON, JR ter that appears radially and proceeds ul- portion that contacts the trapezoid is dor- narly. sally oriented. The proximal surface of the cuneiform is concave dorso-ventrally for ar- Urogale: Philippine tree shrew ticulation with the remnant of the ulnar The carpus of Urogale (Fig. 4a) is indistin- styloid process that is fused to the radius. guishable from that of Tupaia. It has three The pisiform articulates with the palmar proximal carpal elements: scapholunate, cu- portion of the cuneiform and the ulnar sty- neiform, and pisiform, and a large centrale. loid process, not with the ulnar side of the All four distal carpal elements are present. process. The ulnar styloid process articu- No developmental series of Urogale was lates with the ulnar aspect of the cuneiform, available. projecting past its proximal border. In the distal row, the trapezium is large Anathana: Indian tree shrew and quadrangular, and possesses a small The carpus of Anathana (Fig. 4b) is also proximal process that overrides the dorsal indistinguishable from that of Tupaia. It has surface of the scaphoid portion of the scapho- three proximal carpal elements: scapholu- centralolunate. The scaphocentralolunate- nate, cuneiform, and pisiform, and a large trapezoid articular surface of the scaphocen- centrale. All four distal carpal elements are tralolunate is also exposed dorsally This present. No developmental series of allows the trapezoid to dorsally override the Anathana was available. centrale portion of the scaphocentralolunate. Dermoptera: Colugos or "flying lemurs" We found no evidence of a separate lunate The colugos (Fig. 5) also have three proxi- cartilage in either fetal or postnatal colugos mal carpal elements: scaphocentralolunate, (see Appendix, Fig. 5a,b,d,e). Our series of cuneiform, and pisiform. All four distal car- specimens (USNM 144374, to USNM pal elements are present. 197203, to USNM 317118 and 578084) shows In the proximal row, the large scaphocen- that ossification is complete within the centralolunate articulates with the radius and trale and scapholunate cartilages while fu- ulna proximally, the cuneiform ulnarly, and sion between them is incomplete. Fusion the trapezium, trapezoid, magnum, and un- between them progresses ulnar to radial. ciform distally. The scapholunate portion of the scaphocentralolunate articulates proxi- Chiroptera: Bats mally with the radius, ulnarly with the cunei- The bats (Figs. 6, 7) also have three ele- form, and palmarly with the pisiform. The ments in the proximal carpal row: large centrale portion of this element articulates scaphocentralolunate, cuneiform, and pisi- with all of the distal carpals and the cuneiform. All four distal carpal elements are form. The articular surface of the centrale present. The position of the pisiform is

Fig. 4. A: X-ray of the left carpus of USNM 292293 Urogale everetti. B: X-ray of the right carpus of FMNH 91265 Anathana ellioti, image reversed. Scale bars = 1 mm. Abbreviations as in Figure 3. CARPAL DEVELOPMENT IN ARCHONTAN MAMMALS

6%3Q

Fig. 5. Carpal development and morphology in colu- tus. E: Dorsal left carpus of USNM 144374 fetal Galeop- gos. A: Dorsal right carpus (reversed) of fetal Cynocepha- terus variegatus. F: Dorsal left scaphocentralolunate of lus volans, redrawn from Holmgren ('52). B: Dorsal left USNM 317118 adult Galeopterus variegatus. Scale carpus of fetal Cynocephalus volans, redrawn from bars = 1 mm. Cu, cuneiform; M, magnum; Pi, pisiform; Holmgren ('52). C: Dorsal right carpus (reversed) of pp, prepollex; R, radius; SCL, scaphocentralolunate; Td, USNM 578084 adult Cynocephalus volans. D: Dorsal trapezoid; Tr, trapezium; U, unciform; Ul, ulna. left carpus of USNM 144374 fetal Galeopterus variega-

greatly modified and articulates with the orders in the articular relationships of the palmar aspect of the magnum (Norberg, '70, carpals. '72; Vaughan and Bateman, '70; Altenbach, In the Megachiroptera (Fig. 6), the scapho- '79). There are differences between the sub- centralolunate is large and articulates with 142 B.J. STAFFORD AND R.W. THORINGTON, JR

Fig. 6. Carpal development and morphology in mega- adult Hypsignathus monstrosus. Scale bars = 1 mm. LI, chiropterans. A: Dorsal right scaphocentralolunate (re- dorsal component of lunate (centralia 3 of Holmgren, versed) of USNM 448865 juvenile Hypsignathus monstro- '52); L2, palmar component of lunate (lunate of Hol- sus. B: Dorsal right carpus (reversed) of USNM 543166 mgren, '52). Other abbreviations as in Figure 5.

the radius proximally. It is expanded ulnarly The trapezium dorsally overrides the and interposes between the radioulnar ar- scaphoid when the wrist is dorsiflexed, but ticular surface and the reduced cuneiform. there is no trapezial-scaphoid locking mech- The cuneiform articulates with the palmar anism in most microchiropterans. In the Em- radioulnar articular surface when the car- ballonuridae, Nycteridae, Noctilionidae, pus is flexed. The styloid process of the ulna Mormoopidae, Phyllostomidae, Vespertilioni- extends distal to the scaphocentralolunate dae, and Natalidae, a proximal process of and articulates with the ulnar aspect of the the trapezoid, rather than the trapezium, cuneiform as it does in colugos. Distally, the articulates with a shallow groove on the scaphoid tubercle articulates with the base dorsal surface of the centrale portion of the of metacarpal I. Radial to the line of fusion scaphocentralolunate. between the scaphoid and centrale, there is Artibeus jamaicensis (Fig. 7b) is a good a deep pit on the scaphoid for articulation example of this most common microchirop- with a process of the trapezium. The base of teran condition. There is a high degree of metacarpal II is wedged between the trape- variability in the development and projec- zium and magnum radio-ulnarly, and articu- tion of the radial ridge of the centrale groove lates with the trapezoid at its base. This into the distal carpal row between these pattern is similar to that seen in the colugos, families. However, in all of these families tree shrews, squirrels, and mice examined. the centrale ridge is wedged between the In microchiropterans (Fig. 7), the articu- trapezium and the trapezoid. lar relationships of the carpal elements are In the Furipteridae (Fig. 7c), there is a generally similar to the megachiropterans, reduced trapezoidal process and a trapezial but the articulation of the scaphoid tubercle with the base of metacarpal I is reduced. The scaphoid tubercle forms part of a cup within which the base of metacarpal I fits when it is Fig. 7. Carpal development and morphology in micro- abducted. The cuneiform is relatively larger chiropterans. A: Dorsal left carpus of USNM 103405 in most Microchiroptera than in the Megachi- juvenile Phyllonycteris poeyi. B: Dorsal left carpus of roptera and may extend proximal to the USNM 362098 adult Artibeus jamaicensis. C: Dorsal left carpus of USNM 549510 adult Furipterus horrens. D: ulnar styloid process. This proximal exten- Dorsal right carpus (reversed) of USNM 519701 adult sion provides part of a grooved passage for Thyroptera tricolor. E: Dorsal right carpus (reversed) of the tendon of M. extensor carpi ulnaris. The USNM 577065 adult Myzopoda aurita. F: Dorsal right ulnar styloid process does not extend disto- carpus (reversed) of USNM 437362 adult Otomops martiensseni. G: Dorsal left carpus of USNM 573474 adult ulnar to the cuneiform. In all microchiropter- Megaderma spasma. H: Dorsal right carpus (reversed) ans, the base of metacarpal II is wedged of USNM 548605 adult Rhinolophus inops. Scale bars = between the trapezoid and magnum. 1 mm. Abbreviations as in Figure 5. k^m ^W * 3

Figure 7 144 B.J. STAFFORD AND R.W. THORINGTON, JR process that articulates with a scaphoid Rodentia: Rodents groove. The trapezium overrides the trap- The carpus of Peromyscus leucopus (Fig. ezoid to articulate with the magnum dor- 8) has three elements in the proximal carpal sally. In the Thyropteridae (Fig. 7d), there is row: scapholunate, cuneiform, and pisiform. an ulnar expansion of the trapezium over The centrale is present and unfused. All four the radial ridge of the centrale groove. There- distal carpal elements are present. The fore, the trapezium articulates in the cen- scapholunate articulates proximally with the trale groove with the trapezoid. Here also, radius and ulnarly with the cuneiform. Dis- the trapezium overrides the trapezoid to the tally, it articulates with the base of metacar- extent that it now articulates with the mag- pal I, with the trapezium, trapezoid, cen- num. In both of these families, the trapezoid trale, magnum, and unciform, and palmarly maintains contact with the centrale groove. with the pisiform. The pisiform has a slight In the Myzopodidae and Molossidae (Fig. dorsal extension, but this is not nearly as 7e,f), the trapezium has expanded ulnarly to extensive as in Ptilocercus, and it does not articulate with the centrale groove and com- cup the ulnar styloid process. The base of metacarpal V may articulate with the cunei- pletely exclude the trapezoid from contact form in extreme ulnar deviation or digital with the proximal carpal row dorsally In abduction. these taxa, there is trapezium-magnum con- Peromyscus has a single cartilaginous tem- tact proximally, but not dorsally. This ar- plate for the large proximal carpal element rangement results in a trapezium-centrale postnatally (Fig. 8a,b) and ossification is com- locking mechanism with little or no contribu- plete by about 10 days after birth. Ossifica- tion from the trapezoid. tion of the single cartilage begins in the In the Megadermatidae (Fig. 7g), there is radial portion of the cartilage and proceeds no centrale groove, but there is a well- ulnarly. There was no evidence of a separate developed centrale tubercle. This tubercle cartilage or center of ossification for the lu- projects distally and is wedged between the nate. trapezium and the trapezoid. The Rhinolo- Squirrels (Fig. 9) also have three proximal phidae (Fig. 7h) and Rhinopomatidae show carpal elements: scapholunate, cuneiform, a similar condition, but here the centrale and pisiform, and a free centrale. All four tubercle is smaller then in megadermatids distal carpal elements are present. The ar- and does not project between the trapezium ticular relationships of the proximal carpal and the trapezoid. Instead, the tubercle fits elements are generally similar to Peromys- against the deeply concave surface of the cus leucopus. Wrist dissections of one young trapezium. Both the rhinolophids and rhi- Callosciurus finlaysoni, and one young Sciu- nopomatids also lack a centrale groove. rus carolinensis showed a large cartilage element in the proximal carpal row that had In all the bats examined, the scaphocen- the same shape and articular relationships tralolunate forms from the fusion of the as the adult element. There is no evidence scaphoid, lunate, and centrale postnatally for a separate lunate cartilage at either about after the onset of ossification in these carti- 7 or about 21 days of age. lages. However, the patterns differ between megachiropterans and microchiropterans. In DISCUSSION microchiropterans the scaphoid and lunate fuse medio-laterally and the centrale fuses The literature on tupaiine anatomy to the distal aspect of the scaphoid radial to (Flower, 1885; Lyon, '13; Davis, '38; Hol- mgren, '52; Haines, '55; Verma, '65; Altner, the scapho-lunate border (Fig. 7a). In mega- '71) generally agrees that the Tupaiinae have chiropterans (Fig. 6a), the centrale is inter- a fused scaphoid and lunate. Steiner ('65) posed between the scaphoid and lunate and and Altner ('71) illustrate a separate lunate articulates with the radius proximally. In cartilage in fetal Tupaia glis, which coa- Hypsignathus monstrosus and Pteropus per- lesces into a single large proximal carpal sonatus, the centrale separates the scaphoid prenatally Holmgren ('52) agrees with this from the lunate dorsally. In a juvenile speci- interpretation but shows the proximal half men of Hypsignathus, the lunate is com- of the magnum to be composed of centrale 3. posed of two distinct elements (Fig. 6a), the This interpretation agrees with the illustra- more dorsal of which may be the remnant of tions in Steiner ('65) and Altner ('71), al- the 3rd centralia (Holmgren, '52). though these authors do not name this ele- CARPAL DEVELOPMENT IN ARCHONTAN MAMMALS 145

Fig. 8. Carpal development and morphology in Peromyscus. A: Dorsal left carpus of P18 H a 4-day- old Peromyscus leucopus. B: Dorsal left carpus of P18 H a 4-day-old Peromyscus leucopus. C: Dorsal right carpus (reversed) of USNM 398163 adult Peromys- cus leucopus. Scale bars = 1 mm. C, centrale; Cu, cuneiform; M, magnum; Pi, pisiform; pp, prepollex; R, radius; SL, scapholunate; Td, trapezoid; Tr, trapezium; U, unciform; Ul, ulna. merit. In this study, no evidence of a center of gale, or Anathana, but there is in Ptilocercus ossification for the lunate in Tupaia was andDendrogale. Therefore, scapholunate fu- found, nor were multiple centers of ossifica- sion is neither a tupaiid nor a tupaiine char- tion observed in the magnum (Table 1). This acter. Davis ('38, p. 386) does note a free suggests that the loss of an ossification cen- lunate for Dendrogale, but contradicts him- ter is not evidence for the loss of an element. self when he says "The scaphoid and lunar Verma ('65) reports that in Anathana are separate, instead of being fused into a wroughtoni not only are the scaphoid and single bone as they are in Tupaia," but later lunate fused, but so are the trapezium and that "In keeping with the fused condition of trapezoid, the unciform and magnum, and the scaphoid and lunar in Dendrogale the that the centrale has been lost. This bizarre magnum articulates with the lunar, rather combination of fusions was not observed in than with the cuneiform." He also claims the specimen studied here, which showed that "The carpus is strikingly similar to that the same carpal morphology as Tupaia and of Ptilocercus." No especially striking simi- Urogale. larities were found in this study between In spite of the general agreement on tupai- Dendrogale and Ptilocercus. With the excep- ine carpal morphology, Novacek ('80) claims tion of the free lunate, the carpus of Dendro- the Tupaiidae retain an unfused lunate (pp. gale is very similar to that of Tupaia, Uro- 78-79, fig. 23 and table 5, character #11). gale, and Anathana. Simmons ('95) correctly codes this character Le Gros Clark ('26, p. 1207) notes none of as polymorphic for the family, but does not the characters that we found in Ptilocercus. discuss its distribution within tree shrews. He says of the lunate that "On its distal There is no separate lunate in Tupaia, Uro- aspect it has a narrow facet for articulation 146 B.J. STAFFORD AND R.W. THORINGTON, JR

Fig. 9. Dorsal right carpus (reversed) of USNM 396202 adult Sciurus carolinensis. Scale bar = 1 mm. C, centrale; Cu, cuneiform; M, magnum; Pi, pisiform; pp, prepollex; R, radius; SL, scapholunate; Td, trapezoid; Tr, trapezium; U, unciform; Ul, ulna. with the os magnum.", and that the mag- primates (Godinot and Beard, '93). It is also num ". . . has an attenuated head, com- present in Tarsius bancanus. In the pro sim- pressed laterally, which projects proximally ian primates, the centrale extends ulnarly to to reach and articulate with the lunate." contact the unciform, but this contact is re- However, his figure 15 (p. 1207) shows exten- stricted entirely to the dorsal aspect of the sive lunate-magnum contact, and no appar- carpus. Magnum-lunate contact is main- ent attenuation of the magnum. He makes tained palmarly through a distal extension no special note of any unusual characteris- of the lunate, although the degree of this tics of the unciform, or of the cuneiform- contact probably varies with hand position. pisiform-ulna complex. In fact, the condition In Ptilocercus, however, it is the unciform that Le Gros Clark figures for Ptilocercus is that is expanded radially and contact be- what was observed in this study for Dendro- tween the magnum and the proximal carpal gale. row is completely lost. The articular patterns between the cunei- The differences in carpal morphology be- form, pisiform, and ulna in Ptilocercus are tween Ptilocercus and the other tree shrews derived, as are the centrale, magnum, and are difficult to interpret due to the lack of unciform articulations. In Ptilocercus, the information on tree shrew locomotion. Most centrale has expanded ulnarly, articulating of what is available is very general in nature with the lunate proximally and almost con- (see Banks, '31; Wharton, '50; Davis, '62; tacting the cuneiform. Also, the unciform Vandenbergh, '63; Lim, '67; but also Bishop, has expanded radially to contact the ulnar '64; and Jenkins, '74 for more detailed treat- aspect of the centrale. The combination of ments). The results of this study suggest these conditions prevents the magnum from that the differences between Ptilocercus and contacting the proximal carpal row. X-rays the other tree shrews relate to differences in show that the separation of magnum and the degrees of ulnar deviation of the manus, lunate is maintained when the carpus is in to differences in digital abduction, and to both radial and ulnar deviation. However, differences in the functional axes of the ma- one of the specimens examined (USNM nus. Louise Emmons (pers. comm.) notes 481105) showed a slight degree of magnum- that Ptilocercus are more arboreal than other lunate contact palmarly in the left manus. sympatric tree shrews in Borneo (see also There was no magnum-lunate contact in the Payne et al., '85; Corbet and Hill, '92) and right manus. A similar condition of reduced that they spend relatively more time on large magnum contact with the proximal carpal vertical supports. She has observed that row has been noted in living strep sir hine when descending tree trunks head first, CARPAL DEVELOPMENT IN ARCHONTAN MAMMALS 147 Ptilocercus maximally abducts and pronates proximal carpal element of colugos be com- the upper extremities in order to grasp the posed of a fused scaphoid, centrale, and lu- tree trunk. This position produces ulnar de- nate and that the lunate be displaced distal viation of the manus. The derived nature of to the scaphoid. In the colugos, the cunei- the cuneiform-pisiform-ulnar complex in form has developed distinct proximal and Ptilocercus (Fig. 2a) would resist dislocation distal articular facets on its radial aspect. of the carpus ulnarly in this position because Beard ('89, '93) proposes that the proximal the cuneiform and pisiform are effectively facet articulates with the scaphoid portion wrapped around the ulnar styloid process. and the distal one articulates with the lu- The interposition of the pisiform between nate portion of the scaphocentralolunate the cuneiform and the ulnar styloid process (Fig. 5c). This hypothesis parallels Beard's would also provide an effective stop to ulnar interpretation of the carpals of the plesiad- deviation of the manus. This arrangement apid Nannodectes intermedius (USNM would stabilize the ulna as the antebra- 442229). This specimen includes a scaphoid chium pivots over the manus. Ptilocercus and a purported lunate, but not a cuneiform. appear to use a supinated and ulnarly devi- The scaphoid does appear to have two dis- ated manus with highly abducted digits to tinct articular facets on its distal face, but grasp supports (see figures in Le Gros Clark, most of this surface is broken. Beard ('89, '26; Napier and Napier, '67; Nowak, '88). The '93) also reports on Plesiadapis tricuspidens cuneiform-pisiform complex would therefore (MNHM R 5320) and Phenacolemur sp. resist forces generated during plantar flex- (USGS 17847) that have cuneiforms but lack ion of the manus (see Godinot and Beard, scaphoid and lunate bones. The cuneiform '93; Preuschoft et al., '93; but also Hamrick, bones show two articular facets on their '97). radial sides. Beard proposes that the more Photographs also show that Ptilocercus proximal facet is for articulation with the spread their digits widely when grasping a ulnarly expanded scaphoid and the more branch. This position would provide a fixed distal is for articulation with a distally dis- pivot point for the antebrachium. Photo- placed lunate. Combining these observa- graphs of tupaiine tree shrews do not show tions and interpretations, Beard proposes the same manual positioning as Ptilocercus that a distally displaced lunate is present in (i.e., a supinated, ulnarly deviated manus, all the taxa just mentioned. However, it with splayed digits). Although Jenkins ('74) seems just as likely that the proximal facet notes that in Tupaia the deviation between in these specimens could articulate with ei- digits I and V may be as large as 150°, ther the scaphoid or the lunate while the Bishop's ('64, table 2, fig. 12) data indicate distal facet could articulate with either the much less digital divergence. In Tupaia, Uro- centrale, magnum, or unciform. Radial cunei- gale, and Anathana, fusion of the lunate form-centrale contact occurs in Ptilocercus would provide stability and prevent the con- (Fig. 2a), cuneiform-magnum contact in Den- centration of stresses at the radiocarpal joint drogale (Fig. 2b), and cuneiform-unciform at the articulation between the scaphoid and contact in the Chiroptera (Figs. 6, 7). These lunate. This fusion and stability may be findings contradict Beard's proposal ('93, p. related to the different degrees of manual 137) that the cuneiform only contacts the mobility in the more terrestrial Tupaia, Uro- lunate radially in tree shrews, bats, and gale, and Anathana compared to Ptilocercus. primates. Furthermore, Beard's taxonomic Likewise, the free lunate in Dendrogale may assignment of the fossil specimens has been also reflect extensive manual mobility. The seriously questioned (Krause, '91). Regard- radial expansion of the unciform in Ptilocer- less, the proposition that the colugo has a cus also suggests a pattern of force transmis- distally displaced lunate, like that proposed sion in which forces from digits IV and V are for the fossils, is a testable hypothesis. directed more radially as compared to the Prenatally (Fig. 5d,e) the colugo examined pattern in other tree shrews. However, these in this study had a large proximal cartilage hypotheses are difficult to evaluate without and a large intermediate cartilage. Postna- detailed kinematic and behavioral data. tally (Fig. 5f), fusion between these carti- The Primatomorpha hypothesis proposes lages proceeds after the onset of ossification that the positioning of carpal elements in within the cartilages (Table 1). There is no colugos and "archaic" primates is homolo- evidence for the existence of a separate lu- gous. This hypothesis requires that the large nate cartilage in colugos, but Tupaia still 148 B.J. STAFFORD AND R.W. THORINGTON, JR retain a distinct lunate cartilage (Steiner, a distally displaced lunate because there is '65) at a comparable stage of development to no separate lunate cartilage in the fetal the youngest colugo (USNM 144374) studied colugo (USNM 144374), the juvenile colugos here. However, Holmgren ('52, fig. 33, our (USNM 197203 and 143326) do not show a Fig. 5b) shows a lunate cartilage fused to the similar defect, and this defect is not present ulnar side of the scaphoid cartilage in Cyno- in the right scaphocentrale of USNM 317118. cephalus volans. This scapholunate element Consequently, this defect was interpreted as has already coalesced with a distal element a postmortem crack in the centrale portion composed of the cartilages of centralia 3 and of the scaphocentralolunate of this speci- 4. Unfortunately, Holmgren's figure 32 (our men. Fig. 5a) upon which this interpretation rests Fusion of the scaphoid, centrale, and lu- is difficult to interpret. This figure shows the nate also has been used as a taxonomic lunate cartilage separated from the scaph- character of the Chiroptera (Flower, 1885; oid cartilage along an oblique line. It also Grasse, '55; Jepsen, '66, '70; Walton and shows lunate-radius contact and extensive Walton, '70) and the Volitantia (Novacek, lunate-cuneiform contact. However, there is '80; Szalay and Lucas, '93, '96; Simmons, '94, no cartilage visible for centralia 3. '95). Although the consensus now seems to In colugos, it appears that the large proxi- be that the scaphoid, lunate, and centrale mal cartilage is the scapholunate, that the are fused in bats (Novacek, '80; Beard, '89; lunate cartilage coalesces with the scaphoid Szalay and Lucas, '93, '96; Simmons, '94, cartilage on its ulnar, not distal, aspect, and '95), the pattern of fusion in these hypoth- that the large intermediate cartilage is the eses has not been specified. Most studies centrale. The developmental series exam- (Flower, 1885; Allen, 1893; Grasse, '55; Jep- ined here (from USNM 144374, to USNM sen, '66, '70; Walton and Walton, '70; Szalay 197203 and 143326, to USNM 578084) shows and Lucas, '93, '96; Simmons, '94, '95) only that ossification is complete within the cen- mention that the bones fuse and seem to rely trale and scapholunate cartilages, whereas on each other for authority. For example, fusion between these elements is still incom- Flower (1885) and Grasse ('55) have been plete. This pattern of carpal fusion is a com- often cited as authorities on the fusion of bination of the processes seen in bats and carpal elements in bats. However, Flower tree shrews. Interestingly, the cleared and (1870, p. 290) only notes that "In the carpus stained colugo specimen (USNM 144374, Fig. the scaphoid and lunar are united, and in 5d,e) shows complete separation between some genera (as Pteropus) the cuneiform is the scapholunate and centrale cartilages joined with them, so that the proximal bone even though it is significantly older than the contains but a single bone. There is no cen- specimen reported by Holmgren ('52). This trale. The pisiform is very small"; and Grasse difference may reflect a high degree of vari- ('55, p. 1748) cites Leboucq "D'apres Leb- ability in the process of carpal reduction in oucq (1899), le centrale au cours de la vie colugos. Clearing and staining further speci- embryonnaire se fusionne rait avec le scapho- mens would resolve these questions, but ap- semilunaire." It appears that Leboucq (1899), propriate specimens are not available at this Schmidt-Ehrenberg ('42), and Holmgren ('52) time. Complete ossification within the scaph- are the primary sources of data on carpal olunate and centrale cartilages prior to ossi- fusion in bats. They show that the scaphoid fication between these elements is docu- and lunate fuse mediolaterally, whereas the mented in several colugo specimens, centrale fuses to the distal aspect of the supporting our hypothesis of the homology scaphoid. This study confirms that the pat- of these elements. No evidence to support terns described by Leboucq (1899) for Vesper- the homology of carpal elements as proposed tilio murinus, by Schmidt-Ehrenberg ('42) by Beard ('89, '93) was found. One adult for Molossus, and by Holmgren ('52) for Pip- colugo (USNM 317118) does present a defect istrellus ceylonicus and Hipposideros sp. are in the distal face of the centrale. This speci- also found in five other genera of microchi- men, although an adult based on complete ropterans (see Appendix). Fusion of the fusion of all other cranial and postcranial scaphoid, centrale, and lunate postnatally sutures and epiphyses, shows incomplete after intracartilage ossification has com- fusion proximodistally between the centrale menced is a valid chiropteran character and scaphoid. This defect was not inter- (Table 1). No evidence of postnatal scaphoid- preted as a suture between the centrale and lunate fusion was found in any other taxa CARPAL DEVELOPMENT IN ARCHONTAN MAMMALS 149 examined, most notably in colugos. How- mobility of the pollex and thereby the lead- ever, the colugos do show postnatal fusion ing edge of the wing between megachiropter- between the centrale and scapholunate after ans and microchiropterans. The differences intracartilaginous ossification is complete. in carpal-metacarpal II articulations may This process may be homologous between also reflect these factors and be functionally bats and colugos. linked to the repositioned locking mecha- The patterns of carpal fusion and articula- nisms. In microchiropterans the second tion between the two chiropteran suborders, metacarpal is wedged between the trapezoid however, are difficult to assess and require and magnum and has less contact with the more detailed study. Different patterns of trapezium. This arrangement would still pro- force transmission related to aerodynamic vide a rigid leading edge to the distal wing parameters, wing kinematics, or nonaerial by stabilizing the second digit. At the same locomotion may be factors in the differences time, it may provide greater mobility of the between megachiropterans and microchirop- trapezium and metacarpal I, which would terans. In particular, the development of the provide greater mobility of the leading edge trapezial-scaphoid locking mechanism in of the wing. This mobility could enhance megachiropterans vs. a trapezoidal-centrale control and maneuverability in microchirop- locking mechanism in most microchiropter- terans and be related to the more acrobatic ans may reflect different functional require- nature of microchiropteran flight (i.e., somer- ments between the two suborders. saulting during landing, catching insects "on In the megachiropterans, the trapezium the wing," etc.). has a large process. This process dorsally Most microchiropteran families possess overrides the scaphoid and fits into a deep the locking mechanism illustrated by Phyll- pit on the dorsal scaphocentralolunate that onycteris poeyi and Artibeusjamaicensis (Fig. is radial to the line of scaphoid-centrale fu- 7a,b). Both the trapezium and trapezoid dor- sion (Fig. 6a). This trapezial process is bound sally overriding the scaphocentralolunate to the scaphocentrale pit by a strong liga- characterize this mechanism. The trape- ment. Engagement of the process and pit zium dorsally overrides the trapezoid and would stabilize and lock these carpals dur- articulates with the radial lip of the centrale ing dorsiflexion. In megachiropterans the second metacarpal has a large area of articu- groove and with the scaphoid portion of the lation with the trapezium, and this would scaphocentralolunate when dorsifiexed. provide support to the leading edge of the However, it is the proximal process of the wing in flight by resisting dorsiflexion of the trapezoid that articulates with the centrale second metacarpal. Norberg ('70, '72) dis- groove and provides stabilization during dor- cusses the benefits of leading edge rigidity in siflexion. The height of the radial lip of the detail. Megachiropterans also use the pollex groove varies among families. This lip is in suspensory positional behaviors associ- usually high and sharp, but it can also be ated with feeding and roosting. The locking low and rounded and more closely resemble mechanism and its strong ligamentous con- the tubercle seen in the megadermatids and nection may serve to anchor the trapezium rhinolophids. during suspensory positional behaviors The Molossidae (Fig. 7f) are characterized where the pollex is dorsifiexed. The locking by just such low and rounded centrale borders. mechanism would probably not be com- In this family, the trapezium has expanded pletely engaged during these behaviors be- ulnarly and reduces trapezoid contact with the cause digits II-V are flexed against the fore- centrale portion of the scaphocentralolunate arm, but the high radial border of the pit (Molossus and Tadarida, for example). In would prevent the process from dislocating other genera (Otomops), the trapezoid does radially under tension (see Jenkins, '81, fig- not contact the scaphocentralolunate. ures 5 and 7, that show the separation of The Myzopodidae (Fig. 7e) show a condi- carpal elements during suspensory locomotion similar to that seen in the molossids. tion in spider monkeys and gibbons). Here, the trapezoid still maintains some con- In most microchiropterans, the locking tact with the dorsal centrale, but the trape- mechanism is located between the trapezoid zium also has a large degree of articulation and the centrale portion of the scaphocen- with the dorsal aspect of the centrale. In this tralolunate (Fig. 7). This repositioning of the condition there is no apparent radial lip to locking mechanism may reflect differential the centrale groove. The Furipteridae (Fig. 150 B.J. STAFFORD AND R.W. THORINGTON, JR 7c) exhibit still a different condition whereby same one described here that articulates the carpus shows both trapezial-scaphoid with the centrale groove. Norberg notes that and trapezoidal-centrale locking mecha- this arrangement would act to prevent radio- nisms. ulnar movements of the carpus, but does not The Rhinopomatidae and Rhinolophidae discuss any restriction of dorsiflexion. She (Fig. 7h) also have low rounded centrale describes no locking mechanism for megachi- tubercles, but are characterized by having ropterans (Norberg, '72). no dorsal overlap of the scaphocentralolu- Because little is known about the kinemat- nate by any of the distal carpals. These ics of the carpus and nonaerial locomotion in families also lack the centrale groove and bats, functional hypotheses are difficult to instead have a transverse (radio-ulnar) ridge evaluate. Altringham ('96, p. 17, citing Petti- across the distal surface of the scaphocen- grew et al., '89) claims that in microchiropter- tralolunate. These two families do not show ans the ". . . thumb and forefinger have mini- any obvious dorsal locking mechanism. mal independent mobility . . ." while the The Megadermatidae (Fig. 7g) exhibit a megachiropterans have an ". . . opposable condition similar to that present in the rhi- thumb and mobile forefinger. ..." However, nopomatids and rhinolophids. Megaderma- Pettigrew et al. ('89, p. 492) cite Leen and tids also show no dorsal overlap of the Novick ('69) as the source of this observa- scaphocentralolunate by the distal carpals, tion. Leen and Novick ('69, p. 34) simply but there is a large centrale tubercle that state that in "All living bats. . . . The thumb projects into the distal carpal row dorsally. bears a claw and is not much modified from This distal projection is tightly cupped be- the typical mammalian form though it may, tween the trapezium and trapezoid radio- as in flying foxes, be rather elongate. The ulnarly and palmarly. Although very differ- thumb, like that of primates, is also excep- ent from any other chiropteran pattern, this tionally mobile." This description does not pattern would also provide a dorsal locking contradict the morphological evidence of this mechanism. study that suggests the microchiropterans The conditions seen in the Furipteridae, have a more mobile pollex. Thyropteridae, Myzopodidae, and Molossi- Detailed studies of the kinematics of the dae may be modifications of the pattern pre- chiropteran carpus are needed to fully under- sent in Artibeus jamaicensis and most other stand the function and role of the morpho- microchiropterans. Because a portion of the logical differences between the two subor- centrale is wedged between the trapezium ders. Similar studies on bat and colugo and trapezoid, the megadermatid condition kinematics are also required if we are to is most similar to the common microchirop- evaluate the striking phenetic similarity be- teran condition. The condition seen in the tween the scaphocentralolunates in these rhinolophids and rhinopomatids seems more taxa. divergent. Although not well developed, the colugos Although the development of these lock- possess a trapezial-scaphoid locking mecha- ing mechanism could be related to body size nism. Similarly, the trapezoid articulation in microchiropterans, there are insufficient with the centrale portion of the scaphocen- data to support the concept that the reposi- tralolunate is oriented dorsally, although tioning of the locking mechanism between there is no hint of a centrale groove. These megachiropterans and microchiropterans is characters provide a close-packed and stable size related. Small Megachiroptera (i.e., Mi- articulation for the trapezium and trapezoid cropterus pusillus) have well-developed tra- (and thereby for metacarpals I and II) in pezial-scaphoid locking mechanisms. The dorsiflexion. The significance of this locking vampire bat Desmodus rotundas uses the complex may relate to the reduction in in- pollex extensively in locomotion (Altenbach, duced drag imparted by a dorsiflexed wing- '79), as do many microchiropterans, but only tip (Thorington et al., '98). In any case, the the Furipteridae (Fig. 7c) show anything colugo morphology represents a reasonable resembling a trapezial locking mechanism. analogue for a chiropteran ancestor. The Norberg ('70) describes a proximal process of similarity in the function of these characters the trapezoid in Plecotus auritus as being (i.e., to stabilize the carpus in dorsiflexion) is ". . . wedged between the lunar, the trape- significant, but whether or not the biological zium, and the magnum . . ." (lunar = scapho- role (sensu Bock and von Whalert, '65) of the centralolunate). This process may be the colugo carpus represents a reasonable ana- CARPAL DEVELOPMENT IN ARCHONTAN MAMMALS 151 logue for a preflapping bat is difficult to articular relationships of the carpals in each evaluate. suborder. These unique features may reflect The exact homology of the large proximal different functional-adaptive regimes. Be- carpal element in Peromyscus and in Sciu- cause of the different processes producing rus is unclear. A free lunate is found in some scaphocentralolunate fusion in colugos and rodents (Bathyergus, Ctenodactylus), and in bats, we cannot unequivocally support the the fossil tree squirrel Douglassia (Emry hypothesis of scaphocentralolunate homol- and Thorington, '82), indicating that reduc- ogy among colugos and bats. Nevertheless, tion of proximal carpal elements is conver- similarities in the articular relationships of gent between rodent families. The different the carpus and in proposed functional-adap- morphology of the scapholunate in sciurids tive scenarios suggest a common evolution- and murids also hints at convergence. In the ary origin of this character complex in colu- Sciurinae, the large proximal carpal ele- gos and bats. ment is universally referred to as a scapholu- Prenatal coalescence of cartilages concomi- nate (Bryant, '45; Gupta, '66; Emry and Thor- tant with the loss of a center of ossification ington, '82, '84; Thorington, '84), although a appears to be the most common pattern of separate lunate element has been demon- carpal reduction in these mammals. The bats strated only uiFunambulus (Holmgren, '52). and colugos deviate from this pattern in The scaphoid and lunate cartilages do coa- exhibiting postnatal fusion between ele- lesce prenatally in Cavia (Schmidt-Ehren- ments. This deviation of colugos and bats berg, '42; Holmgren, '52; Rajtova, '67), and may be a significant difference with phyloge- Mus (Muridae) (Holmgren, '52). Therefore, netic implications. More detailed studies on it appears that the proximal carpal element colugo and chiropteran positional behavior in Peromyscus and Sciurus is likely a scaph- and functional morphology are needed. De- olunate. tailed descriptions of the kinematics of the carpus during aerial and nonaerial behav- CONCLUSIONS iors are needed as well. Ptilocercus and Dendrogale retain a free lunate, whereas in Tupaia, the scaphoid and ACKNOWLEDGMENTS lunate cartilages coalesce prenatally and os- We thank Karolyn Darrow who produced sify from a single center. Adult Urogale and the drawings of the cleared and stained speci- Anathana have the same morphology as mens, cleaned up the SEM images, and de- Tupaia, and the process of carpal reduction signed the layout of the plates. The scanning is also assumed to be the same. Ptilocercus electron micrographs were taken in the Scan- exhibit a derived carpal morphology, which ning Electron Microscope Laboratory, Na- may be related to a greater reliance on ab- tional Museum of Natural History, Smithso- ducted digits and ulnarly deviated hand pos- nian Institution. Walter R. Brown provided tures as compared to Tupaia, Urogale, and the training and expertise needed to pro- Anathana. The results of this study suggest duce images of uncoated material, and Su- that the carpal morphology of Dendrogale, sann G. Braden developed all of the nega- not Ptilocercus, best represents the ances- tives of these images. Kenneth Tighe of the tral scandentian condition. Division of Reptiles and Amphibians, Na- The large proximal carpal element in colu- tional Museum of Natural History, Smithso- gos and bats is a scaphocentralolunate. Both nian Institution cleared and stained our fe- colugos and bats show postnatal ossification tal colugo. Louise Emmons of the Division of between discrete carpal elements. However, Mammals at the National Museum of Natu- colugos but not bats show the prenatal coa- ral History provided valuable insight into lescence of the scaphoid and lunate carti- the behavior of wild tree shrews. Larry lages seen in most other mammals. No evi- Heaney of the Field Museum of Natural dence was found to support Beard's ('93) History was kind enough to loan us several contention that the lunate fuses to the distal of the specimens used in this study. The surface of the scaphoid in colugos. Department of Zoological Research at the The large proximal carpal element in Chi- National Zolological Park, Smithsonian In- roptera is a scaphocentralolunate, the dis- stitution provided the tree shrews for clear- crete elements of which fuse postnatally af- ing and staining. B.J.S. was supported by a ter the onset of ossification. 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Appendix. Specimens Examined in this Study Number and Ages1 of Taxon specimens examined Preparations2 Chiroptera MEGACHIROPTERA Pteropodidae Acerodon jubatus 3A SK Cynopterus brachyotis 3A SK Dobsonia crenulata 3A SK Eidolon helvum 3A SK Eonycteris spelaea 3A SK Epomops franquenti 3A SK Haplonycteris fisheri 3A SK Hypsignathus monstrosus 1J, 8A SK Macroglossus minimus 3A SK Melonycteris melanops 3A SK Micropterus pusillus 3A SK Nyctimene albiventer 3A SK Otopterus cartilagonodus 3A SK Ptenochirus jagori 3A SK Pteropus alecto 3A SK Pteropus conspicillatus 3J SK Pteropus dasymallus 1J, 3A AL, SK Pteropus personatus 1J SK Pteropus vampyrus 2A SK Rousettus amplexicaudatus 6A SK Rousettus madagascarensis 3A SK Syconycteris australis 3A SK 154 B.J. STAFFORD AND R.W. THORINGTON, JR

Appendix. Specimens Examined in this Study (continued) Number and Ages1 of Taxon specimens examined Preparations2 MICROCHIROPTERA Rhinopomatidae Rhinopoma muscatellum 6A SK Emballonuridae Emballonura semicaudata 6A SK Saccopteryx bilineata 5A SK Taphozous georgianus 1A SK Nycteridae Nycteris arge 1A SK Megadermatidae Lavia frons 1A SK Macroderma gigas 2A SK Megaderma spasma 5A SK Rhinolophidae Hipposideros armiger 4A SK Rhinolophus inops 6A SK Triaenops rufus 2A SK Noctilionidae Noctilio leporinus 6A SK Mormoopidae Mormoops megalophylla 6A SK Pteronotus davyi 4A SK Phyllostomidae Artibeus jamacensis 1J, 6A CS, SK Desmodus rotundus 6A SK Erophylla sezekorni 2J, 6A CS, SK Phyllonycteris poeyi 4J, 3A CS, SK Phyllostomus hastatus 6A SK Uroderma bilobatum 1J, 6A CS, SK Natalidae Natalus stramineus 6A SK Furipteridae Furipterus horrens 4A SK Thyropteridae Thyroptera tricolor 2A SK Myzopodidae Myzopoda aurita 1A SK Vespertilionidae Antrozous dubiaquercus 5A SK Miniopterus minor 6A SK Scotophilus kuhlii 6A SK Molossidae Molossus molossus 7A SK Molossus obscurus 1A SK Otomops martiensseni 3A SK Promops sp. 1J CS Tadarida condylura 6A SK Dermoptera Cynocephalidae3 Cynocephalus volans 4A SK Galeopterus variegatus IF, 2J, 4A CS, AL, and SK Primates Cheirogaleidae Cheirogaleus major 1A SK Daubentoniidae Daubentonia madagascarensis 1A SK Galagidae Otolemur crassicaudatus 6A SK Lemuridae Eulemur fulvus 1A SK Eulemur macacao 1A SK Eulemur mongoz 2A SK Hapalemur griseus 3A SK Lemur catta 1A SK Lorisidae Nycticebus coucang 4A SK Perodicticus potto 1A SK CARPAL DEVELOPMENT IN ARCHONTAN MAMMALS 155

Appendix. Specimens Examined in this Study (continued) Number and Ages1 of Taxon specimens examined Preparations2 Primates (continued) Megaladapidae Lepilemur mustelinus 1A SK Tarsiidae Tarsius bancanus 3A SK Rodentia Muridae Peromyscus leucopus 9J, 6A CS, SK Sciuridae Callosciurus finlaysonii 1J, 2A AL, SK Sciurus carolinensis 1J, 6A AL, SK Scandentia Ptilocercinae3 Ptilocercus lowii 1J, 4A SK, X-ray Tupaiinae3 Anathana ellioti 1A X-ray Dendrogale melanura 2A X-ray Dendrogale murina 1J X-ray Tupaia chinensis 4J CS Tupaia glis 6A SK Tupaia gracilis 1A SK Tupaia minor 1J, 6A CS Tupaia montana 1A SK Tupaia tana 2J, 6A CS Urogale everetti 2A X-ray *A = adult, all epiphyses fused and adult dentition fully erupted. J = juvenile, postnatal, but epiphyses unfused and/or adult dentition not fully erupted. F = fetus, prenatal. 2AL = alcohol preserved specimens used for identifying cartilages via gross dissection. CS = cleared and stained specimens. SK = skeletal material. X-ray = x-rays of museum skins. ^Because our interpretation of the morphology of these taxa differs from that in the literature, we list ages and specimen numbers. Cynocephalidae: Cynocephalus volans, FMNH 56442 (A), FMNH 61032 (A), USNM 144662 (A), USNM 578084 (A); Galeopterus variegatus, USNM 144374 (F), USNM 143326 (J), USNM 197203 (J), USNM 49470 (A), USNM 49640 (A), USNM 49693 (A), USNM 317118 (A). Ptilocercinae; Ptilocercus lowii, USNM 121885 (A). Tupaiinae: Anathana ellioti, FMNH 91265 (A); Dendrogale melanura, USNM 292544 (A), USNM 300913 (A); Dendrogale murina, USNM 256752 (A); Tupaia chinensis, USNM 399596 (5 days), USNM 399594 (11 days), USNM (#116)" (15 days), USNM 399591 (20 days); Tupaia glis, USNM 320721 (A), USNM 396665 (A), USNM 396666 (A), USNM 396673 (A), USNM 397663 (A), USNM 535137 (A); Tupaia gracilis, USNM 578656 (A); Tupaia minor, NZP 110705 (32 days), USNM 396668 (A), USNM 396669 (A), USNM 396670 (A), USNM 548410 (A), USNM 574130 (A); Tupaia montana, USNM 449964 (A); Tupaia tana, NZP 109835 (4 days), NZP 109834 (11 days), USNM 396661 (A), USNM 396663 (A), USNM 449968 (A), USNM 449969 (A), USNM 574901 (A), USNM 579556 (A); Urogale everettii, USNM 292292 (A), USNM 292293 (A). 4Uncatalogued USNM specimen.