HARVARD UNIVERSITY e Library of the Museum of Comparative Zoology LOCOMOTOR MORPHOLOGY OF THE VAMPIRE BAT, DESMODUS ROTUNDUS SPECIAL PUBLICATIONS This series, published by the American Society of Mammalo- gists, has been established for papers of monographic scope con- cerned with some aspect of the biology of mammals. Correspondence concerning manuscripts to be submitted for publication in the series should be addressed to the Editor for Special Publications, Hugh H Genoways, Carnegie Museum of .Natural History, 4400 Forbes Avenue, Pittsburgh, Pennsyl- -vania 15213. Copies of special publications may be ordered from the Secre- tary-Treasurer of the Society, Duane A. Schlitter, Carnegie Museum of Natural History, 4400 Forbes Avenue, Pittsburgh, Pennsylvania 15213. Price of this issue $10.00 COMMITTEE ON SPECIAL PUBLICATIONS James N. Layne, Editor "Archbold Biological Station, Route 2, Box 180, Lake Placid, Florida 33852. J. Knox Jones, JR., Managing Editor ~The Museum, Texas Tech University Lubbock, Texas 79409 CONSULTING EDITORS FOR THIS ISSUE CLYDE JONES Don E. WILSON This publication was financed in part by a gift from David Klingener. ll LOCOMOTOR MORPHOLOGY OF THE VAMPIRE BAT, DESMODUS ROTUNDUS By J. SCOTT ALTENBACH DEPARTMENT OF BIOLOGY UNIVERSITY OF NEw MExIco ALBUQUERQUE, NEw Mexico 87131 SPECIAL PUBLICATION NO. 6 THE AMERICAN SOCIETY OF MAMMALOGISTS PUBLISHED 22 AuGustT 1979 ill MUS. COMP. ZOOL LIBRARY OCT 4 1980 HARVARD UNIVERSITY - \ (An < Library of Congress Catalog Card No. 79-53175 © 1979 by The American Society of Mammalogists FOREWORD O™ obvious objective of any functional morphological study is to determine how anatomical features operate. Far more im- portant, however, is the interpretation of the adaptive significance of those anatomical features and the role their functioning plays in the evolutionary, as well as the day-to-day, biology of an organ- ism. Although morphological features have been used widely for taxonomic purposes for centuries, only relatively recently has in- terpretation of the functional significance of morphological fea- tures been applied toward understanding the biology of organ- isms. That this is especially true of locomotor morphology is somewhat surprising, because locomotion plays such a critical role in the survival of the vast majority of heterotrophic organisms. Few, if any, groups of animals have as broad a spectrum of locomotor styles as do mammals. Certainly much of their abun- dance and general success has been a function of evolution of such diversity in locomotor mechanisms. The locomotion of bats is es- pecially interesting, because both pelvic and pectoral limbs are used in aerial as well as terrestrial locomotion. Evolutionary compromise has variously placed different bats on a spectrum between extreme limb modification for certain types of flight and modification for more efficient terrestrial locomotion. The study of a biological extreme, whether it is a community, an organism, or a functional system within an organism, can often clarify the mechanisms of operation of the average or less extreme. This is particularly true in the study of bat locomotion where the outstanding locomotor specialization, flight, is rather poorly understood. The common vampire bat (Desmodus rotundus) is an ideal candidate for locomotor morphology studies because it rep- resents an extreme in locomotor specialization. It seems logical that a flying machine can vary or be modified evolutionarily in relatively few ways and still fly. The vampire bat has seemingly approached the limit of evolutionary modification by specializing in rapid and effective terrestrial locomotion while retaining the ability to fly. A functional morphological investigation of the vampire bat as a flying machine should not only clarify the flight mechanics of oth- er, less extreme, bats, but also facilitate interpretation of the role of flight-associated morphology. Of equal interest is the study of the terrestrial locomotor modifications that make the vampire so extreme. My study of the locomotor morphology of the vampire was un- dertaken both to interpret the functional significance of its loco- motor-associated anatomy to provide another viewpoint in our bi- ological knowledge of this animal and to stimulate others to add additional interpretation of functional morphology to bat biology, as well as to the biology of other organisms. Only description of the anatomical details of the pectoral girdle and limb is included in this work. Admittedly the pelvic girdle and limb are important in locomotion in the vampire bat and show specializations for its unique locomotor mechanisms. However, I feel that the most spec- tacular of the anatomical specializations for terrestrial locomotion and certainly the most important specializations for flight are those of the pectoral limb and girdle, and I have thus focused my atten- tion on these structures. Perhaps this work will stimulate publica- tions of functional morphological data on the pelvic girdle and limb. I want to thank Terry Vaughan for his encouragement at the onset of this study. Paul Baldwin, Rowan Frandson, Thomas Bahr, and Y. Z. Abdelbaki gave encouragement, generously loaned equipment, and read the manuscript as prepared as a doctoral dissertation. Marilyn Altenbach contributed countless hours in help with surgical procedures, typing, and proofreading the manuscript. Without her assistance and encouragement this work would not have been possible. Sincere thanks are due to the per- sonnel of the U.S. Fish and Wildlife Service at the Denver Wildlife Research Center for the generous loan of living vampire bats and to Northern Arizona University for the loan of preserved speci- mens. I deeply appreciate the help of Janice Moore and Lyle Ber- ger, who read proof of the final manuscript, and want to thank James Findley, Patricia Freeman, and Michael Bogan, who criti- cally read portions of the manuscript. I also thank James N. Layne for his encouragement and his very time-consuming editorial work, and Lorene Deckert who typed the final manuscript. I would like to dedicate this monograph to my major professor, the late Robert R. Lechleitner. He was the finest teacher I have ever known and I can only hope to be a scientist of his competence and a human being of his kindness. To his family I express sincere thanks for the kindness and generosity shown to me and their encouragement of my research. Vi CONTENTS Tn s¥5 GU UN til © Ta eee a a a 1 Material seem clue tlio cl see see 5 PresenvationyandsDissectlOm=._- 22225 = 22 5 Ehotograp micikOceGunesnmss: 2.22862 e688 ee 5 lectrcomy.@ pire hn ygamee eee a a Ee ee a [Lc GCONT ANON VCS OY ae = OS ee eee eee eee 10 S Gal Gli Ow ROS(UIE CSisesete si ceemes eens eset ao) See ee eae ee Less OE 10 BSA OUI Owe OS CUT Cees seer eee Eien ote ee OIC) Soe rs eee ee 12 AV Vall Tn 6 ease eng ee nee ese ee 12 IIOP PIN geWOCOMOMOM wees arte 28 een 2 2 eee enn eset 14 (COVEN SS A I a eS ee eae 17 A fiunren pony oS eli ay @ fag erences Sa Ee ae ee 18 ontialeHbigintyHollowinrey-ay |i pss eee 31 Slows LAO LRG! OIA ONG: fe ea ee ee 4] Alighting Maneuvers on Horizontal Surfaces __-_----.--------------------- 49 Alighting Maneuvers on Vertical Surfaces ___-_-----.----------------------- 51 OS tGiamialE@}StEO) Op yi ee a Se Beh a aaa weet ee eee 52 Position lsMenmin@ logy ine sna nn Sees ee ne ed a eee eee 52 Werte lrale@o) rime ener ee ce Mee te ee Pe ON ee ee 53 SUSTAIN TT a cd tae RE Rl loo Rs ER 55 201) snes NNR NPAT ae tems eee ge Oe Re ee en 56 RectoralkGindlerandsléimb: 22 ees 56 Sat pp Ul ae re met bs OE GM AEE YN nt et eee eke 56 (Cav i cleaaeen ean nN Poe Rr emit a eee Ly a ee ee oy ae 59 TEER STEN se Speen aL a Ot tee ees ee 60 EEA CHUUSRATTC GOT eae enarnn Nae et ear eetio ome Bode eee eee Se eer 64 DAG L NON ape ee A el el ay oe a 66 LEAR VC) geese art eye a Se 68 ID) tant | eenouR vase mnie nme Caves AAP arn co ee eo See A et oe Ss aie es 69 ORE JOD, Seen et gr i et Re A nN Rea 69 JORIS LINEA G NY So ena aa ae OR 70 Functional Myology of the Pectoral Girdle and Limb -__------------------- ie Comments on Electromyographic Analysis -_-_----------------------------- 72 Miusclesml)riig ti eatomes ats mtsesee ees 1 nr sees Sah ya ae 73 DS OSE CLO DON ONS a ee 73 IVAB EO PLAS COLASS TOP Tt See ee = ee Ee ae a= 74 IMIICOTACO=CULATICLLS tara ee ee ee ee ee 75 vil Muscles of the Pectoral Girdle and Limb _______--__-____-___----____---__-_ 75 ‘rapezius Groupes 22s. eee eee eee 1 M.. clavotrapezius:, 22-2 eee ee ee ee 75 IM. aeromiotrapezius, a. -2¢ Soe oe ee ee 78 M.. SPU OMG P OZUUS joie wise ane sseeezegceseea sess ese aeaese = 2222 78 Costo=spino-scapull ate Gr Oui) eee eens ee eee ee ee 79 MOL cUatonSCOpUlach esse nan eS aeee se Sees RENEE eee eee ae See ee 79 M. serratus anterior, anterior division _______--__-__-_____________________ 79 MESS crratusiantero me OSCE Tl Ole GiyiS1O Tl === === aaa a ee ee 80 Mi. rhomobordes <2 2 2000) aes eos tae oe Se Sa 81 IMI OM OCETULEQUS ek. malate Dae SEs 22 BE Lae Sees 83 EAGISSTMALIS-SUAOS Capo Ul | clg CtsO UUp ee 83 IVE QUSSUITUUS LOT SUmes So eee ns EE eae eae eee ee ee 83 Mi teres major 2 =. Ae aN ee ee 84 MitsiLb sca Dulas, Sans aoe eee ane a ee ee 84 Deltotdt Groupe 2s. ee ee Ne ne 84 IMS Clad ode li Oud CUS ee re eae a a? oe ee 84 IVEGETOMIGUCILOLAL ISS ear. aS 2 ae area nr ne oe 85 MM spinodelioideus, woes 288 oe tras BU an on steed ees ome ea en 87 IVIGNUENESCINUNLON mts eta os nee eee Se ee eee ae ee 89 Swprascap ware Gro wpe oa eee ees ee 89 IVILE SUIS DUTLGLUUS pte os re eed SL aa See os 89 IVES tM AS PUN GUUS tae wee = 2 ee Pe a elo on 90 MCE ps" Croup, ee es es ee ee ee 90 MES CCP MOT AGI CATS telat e ial 1s) eee ee 90 IWS YEG OS aD, GRY OWN TOSCO UN TS a 90 IMI, Cine DS lent oo, CANeXUte WO vag UNS ee Ss. ae 90 EXtensOnm Groupie fethe Honea Wines = eas asa eae ene ee 93 Wily QTIAOSOP GOA OO TOONS AAES oe 93 IVIENEXECIES VCO PURIELACCLLS O11 71S eae ee eae ee 93 Miprsupiraton een aston eee ereed eomeks eek oR MES a. 95 M@extensonipollacistbrevisee: ae nis. Ltn 1a eee ES 95 IMSabductorspollicisslon ons. sees 28 ene eee 96 (MER EXTEN SOTNAV SLUNG UII DIOP TUILS ns ana a ene 97 IMIEMENL ENS OTIAUEILONUNUNCOTIETIULUT TS (=e ean ae ee 97 IVES OXLEN SOT COND UTUON TS econ tas a en ee 98 IMESEXLEMS OT ONAICIS eas nen eees IS 8 bs eed en Se ee 99 PectoralissGroupt==: 2-3 es eee 99 Mi subelaiis: Acai 20 Phe tress aio Neat td ne he 99 IME: Pectoral: nh ec Patent Hae A Slate AP eee ae ee ee 100 M. pectoralis, anterior (clavicular) division _____------------------------- 100 IMESPeCloT alsa POSte WOT (Ste TIA) GIN ISIO T= =e eae 101 Mis pectoralis audomunalts ses ee nan on nen lne atlas eae ee enn eae 102 Flexor iGroupiof the Army! suas. ee Sree ee eee 102 Mi. CONGCODYACHIOUS XA wet J8. ecw Speen eS oie 102 IVES DA COD SS UN CNT eos ne sno ee wh en es 103 IVI Di GCHAGUIS: sn a es Ss ee Ee Ie OO Pee 104 IS orr CHOU S) OE WS NOTE 00 eee ee 104 WT UGG (BENG DE DICTED Me Se a a 104 DST f OORT OO OSD NGOS as a ee 105 INS UBIO GL LOTTE OTL OS ta ne a 107 IVINS DOTICLO NL CTC Spatemeesee= seme wasen seen soo os (een ees ees ewan ae ee 108 IN lon LEO? CO GHOTLLD ARG LOUIS: 5 108 EXtensonsvoitines Mansy: cee ante Se eetS ee eee BR et 109 IVIBs TL benOSS CLUSCOTSCLE sae aee eee a Pa 109 allesour (GixoWw yey OU WAS YE MOS eee 110 INT, GERALD DONC AGT a eee ee 110 WS UAC TON ES UCU, 2 ee 110 LVIBECLALGLLCLO Ta) OLLCLS ee ees seen een rae eS a Me ois eS ee 111 PVG RRUNLLET OSS Clee ee eee ene ne UE PER hea A ee 112 IMT, GHOGIOVATGR CIVRHS GLU: ea a a ee 114 VIEROP POMCILSROROTU GUT ses eee ee eee eee een ene ee 115 IDISCUSS1@ 11 Men eE n psin E NEUE SSA ES ei ern eee SILT I? eee eA 116 Terrestrial Locomotor Behavior _..-_-------_-_____----_---------------------- 116 Flight and Aerodynamic Considerations _______----------------------------- 119 AmatomicaliGonsideratioms) sess se eee 124 SUR TUTE a a 129 Ei tenatumes Cite cli wets ce cn eee ene in See ae eee ee eae ae Te Pee 132 Vinay Wee Sen Ok 2 eS ak aS Ne ee ee ner ee 135 1x My study of the locomotor morphology of the vampire was un- dertaken both to interpret the functional significance of its loco- motor-associated anatomy to provide another viewpoint in our bi- ological knowledge of this animal and to stimulate others to add additional interpretation of functional morphology to bat biology, as well as to the biology of other organisms. Only description of the anatomical details of the pectoral girdle and limb is included in this work. Admittedly the pelvic girdle and limb are important in locomotion in the vampire bat and show specializations for its unique locomotor mechanisms. However, I feel that the most spec- tacular of the anatomical specializations for terrestrial locomotion and certainly the most important specializations for flight are those of the pectoral limb and girdle, and I have thus focused my atten- tion on these structures. Perhaps this work will stimulate publica- tions of functional morphological data on the pelvic girdle and limb. I want to thank Terry Vaughan for his encouragement at the onset of this study. Paul Baldwin, Rowan Frandson, Thomas Bahr, and Y. Z. Abdelbaki gave encouragement, generously loaned equipment, and read the manuscript as prepared as a doctoral dissertation. Marilyn Altenbach contributed countless hours in help with surgical procedures, typing, and proofreading the manuscript. Without her assistance and encouragement this work would not have been possible. Sincere thanks are due to the per- sonnel of the U.S. Fish and Wildlife Service at the Denver Wildlife Research Center for the generous loan of living vampire bats and to Northern Arizona University for the loan of preserved speci- mens. I deeply appreciate the help of Janice Moore and Lyle Ber- ger, who read proof of the final manuscript, and want to thank James Findley, Patricia Freeman, and Michael Bogan, who criti- cally read portions of the manuscript. I also thank James N. Layne for his encouragement and his very time-consuming editorial work, and Lorene Deckert who typed the final manuscript. I would like to dedicate this monograph to my major professor, the late Robert R. Lechleitner. He was the finest teacher I have ever known and I can only hope to be a scientist of his competence and a human being of his kindness. To his family I express sincere thanks for the kindness and generosity shown to me and their encouragement of my research. vi CONTENTS EhotocrapiicuProcedunies)ssts:2- se 288 ee LE CEROMIY.O Cura lnyy aan ene ee a el a NES OTN OU a emer a an Pe I pee te eae Sar oe Sa S tala Gin pg ROSEN ES esse = wae ees A Ee en ee [RIBVOSR TER LOREM ec Se ee cae ee ee ee eee \AV EU 2 ae eee ea eee eee LO PPI GelUOCOMOLO Mie es eee eee ee eee ne ane ee SS (Ca OT Se at eee ee ee nee ee eee ae S)trmpimeg Ss chavo tee ne ne ee ere eee eee ee ee intial nh oh tahollowimg: a) [UMP sssesssee see eee eee STOWBHO Tawa aly ton Gewese aoe tes oe ee see eo a Alighting Maneuvers on Horizontal Surfaces _____---_--------------------- Alighting Maneuvers on Vertical Surfaces ___---__-------------------------- Ost@halitiall@Stel O Owienee seat a alse ee os eee eee ee OSitiOnalMNETIMINOG Op Vets eee sea nent See Sees ae eee eee ie Tce bTralg@.@ lNrrnnteee 2 oe oe ee iee seen eee ae Se et ae ee SCA 1 eee mn ee RA EyaI TREE SURE ct A 2 EEK oS oe Se eS a (6 avr cel eee eprint eu DOH re DU ge reece ee reece Fe ea en See LSS LIN IG a Functional Myology of the Pectoral Girdle and Limb -_-------------------- Comments on Electromyographic Analysis -___------------------------------ IA UISE] Esme ENT SHE sis cls fy een ne tne ee ee eee IES QLEEE TOTO DON TCM NS ee So eae IRL, (BIRO DOWTAN SOAS SOROY DTTOIS a ES IVES CONOCO=CULATIOUS a a ee ee eee vil Muscles of the Pectoral Girdle and Limb ________---___________---------_--- aPRApezius Group Cees se eee es ee ee a Mi Clavotna pezitis, 2. oaks sees. ne ee eee IMIS GCNOMLOLNG POZU tS; eek = sere wes ee ene eee a = De ne IME. SPIN OUNGP CZAUS) Sas ees eee Se eee ne Costo-spino-scapulan Grou) eee ee ee ee SLeUAtOT: SCA Pt dep we em renee sinus. =e teinne Niven bes SN Tone ona ae ee . serratus anterior, anterior division ______----------____________________ MISENTALUSANTER On mp OStETI Ol GIVIS1@ t==a=a= aes saan e naan enn eee C57) LONODOLA CTS) mance & iene ee eae Tees Se Es ee ae EF OMLOCENULCCUIS pe ace rm ara ae Ee ks Oe os Le ticermnms-gunl oseayonl eve (CRON) ae IVER alassimpssd Ons te een ae ee nL 20 IME COn eSNG] OF eet Se Se 2 See a eee Missubscapulans aoe Seer ic Dh Nee ee ee Deltordi Group sees) eee en ee ee Mir clavodeltotdeus( <2 oven te eee owe se SSSS55 IMicspivodeltordeus, ©. 229 2 ae) Vso 1 YA eee eee ae IVES UETESMIMUNON Base ante eee oe ee ce hae Suprascapullarm Groups 22. °- 23 8 ee ee ee Mise SUPTOSPINGUUS, 9 ne: Sa 8 ser oe ce nee ee 1 MEU NOS PIN GLUS ae oP ne ee Se ee ne IPHICEP SKC TOUP w= mes te ok ee 2 ee IMITETUC EP HOTAGHU NGAP Ut Ave Talis yee eames een a nae eee a IDES TG DS (CanOLEA Ye, CANONUAG, TANS NEV NS IG, WOE DS (eG, CRYO WUIE MOVES oct e Se Mec sed hada Extensor Grouprotstne Rone apie ssa wake ns se ee eee ae 5 GCOS COG TD TCU ALES WRADS oe CXLENSOTACON PI BALAI OT CALS, me see men en a ee ee SUP INGO eee = sake eat mre eeeee. S80 EE ee Ae wextenson pollicis bncuist =e = 529 _.-8 2) ee oe = LUD R OG? | DONG UD LOS ee CHLETISON A CISTI GUAT IOP TUES eas ers a eee eae oe ee BTRAISORP CNS MOTOUID COMP COONS, ae re DEXLENSOT COND DN ULLIVANES, han 2 a aera rea So nee oe oe CRLCNSOWMILAICL Serene ek tae aa nae 2k Ne eee Pectoralis(Groupiets 2s ook e ki be Ao ee ee IM. SUDGLG UUs | Bane iBB Boos > oiBoms is Beinn oii Ley Bee eh a ae IM PeClovauis. flexion basal pad distal pad Soest ; 4s? " propatagium entetion dactylopatagium Uae nS Vv Sie posterior antero- . posters \ lateral p 7 medial \ brachium 1 thigh medial lateral 2 1 shank | 2 hi : plagiopatagium eniropatagium Fic. 24. Ventral view of Desmodus with parts of the flight membranes and po- sitional terms relative to the arm, hand, and pelvic limb: I-V are metacarpals of corresponding digits and 1-4 are phalangeal elements; superscript “c” indicates the phalanx is cartilaginous. The right wing is folded as in terrestrial locomotion and the left wing is extended as in mid-downstroke of forward flight. ventral and the opposite side dorsal. Movements in the plane of the wing membranes are termed either tibial or fibular. Digit V is located on the medial side of the foot and digit I on the lateral side. Vertebral Column Desmodus has seven cervical, 12 thoracic, six lumbar, five sacral, and no caudal vertebrae. Only the most significant features of the vertebrae are described below. Cervical vertebrae.—The atlas and axis allow extreme lateral and vertical mobility of the skull, which is advantageous for making incisions in a host animal prior to feeding. The remainder of the cervical vertebrae are relatively short and broad and have well- developed transverse processes. These processes have a broad, flange-like projection ventrally and a thin posterodorsal projection that serves for the origin of the four slips of the M. levator scapulae on the last four vertebrae. Thoracic vertebrae.—Anteriorly the vertebrae are relatively short 54 Spec. Publ. Amer. Soc. Mamm. 6 articular facet for clavicle ventral process lateral process 1st costal cart. manubrium : posterior process body xiphoid process Fic. 25. Sternum and first costal cartilages of Desmodus. A, ventral aspect; B, lateral aspect. and wide, and become increasingly longer and narrower poste- riorly. The articulations between these vertebrae are similar to those of Macrotus as described by Vaughan (1959), but are more rigid, and the vertebral elements are closer together, providing a sturdy chain of bone. A solid, tubercle-like, spinous process projects 1 mm dorsally from the mid-dorsal portion of the vertebral arch of the first tho- racic vertebra. Bordered laterally by ridges that give rise to thin projections extending posteriorly beyond the border of the ver- tebra, it serves for the point of origin of the thickest portion of the trapezius muscles. The spinous processes of the next two vertebrae are represented by slight mid-dorsal elevations bounded laterally by prominent, posteriorly projecting ridges similar to those de- scribed on the first thoracic vertebra. On more posterior vertebrae, these ridges converge toward the midline and at the fifth thoracic vertebra, fuse medially to form a mid-dorsal ridge approximately 0.5 mm wide. On the sixth and successive vertebrae these ridges widen posteriorly to form a triangular dorsal prominence. The apex of the prominence on the last thoracic vertebra is directed anteriorly and is 1.2 mm in width at the posterior margin of the vertebra. Lumbar vertebrae.—The mid-dorsal spinous processes are more Altenbach—V ampire Locomotor Morphology 55 pronounced on the lumbar vertebrae. They become arrowhead- shaped, and the anterior point of one vertebra projects into a pos- terior indentation on the one before it. The spinous processes on the third, fourth, and fifth lumbar vertebrae are extremely high, and those of the fourth and fifth are low anteriorly and project strongly upward and backward. The centrum of the last lumbar vertebra is fused with the centrum of the first sacral vertebra and its transverse processes articulate laterally with the medial borders of the ilia. Sacral vertebrae. —These are completely fused to each other and laterally to the medial aspect of the ilia. The fused vertebrae taper posteriorly into a laterally compressed rod of bone that arches posterodorsally for almost the length of the pelvic girdle. The pos- teroventral margins of the fused vertebrae are fused to the ischia immediately dorsal to the ischial tuberosities. Sternum In Desmodus, the sternum is composed of three distinct parts— manubrium, body, and xiphoid process—joined by thin cartilagi- nous discs. The manubrium has a laterally compressed and slightly anteriorly directed ventral process (Fig. 25A—B). Lateral processes project about 15 degrees dorsally and swing slightly anteriorly to enlarged distal ends, which have an anterolaterally and slightly dorsally oriented articular surface for the clavicle and a laterally directed articular surface for the first costal cartilage (Fig. 25A—B). A posterior process, approximately 2.5 mm long and triangular in cross-section, has a ventral apex that forms a thin ridge continuous anteriorly with the posterior edge of the ventral process. The ar- ticular facets of the costal cartilages of the second pair of ribs are located on the posterolateral surfaces of the posterior process. The elongate body of the sternum is about 8 mm in length. It is roughly triangular in cross-section, slightly rounded dorsally, and, unlike many phyllostomatid bats, has no enlarged midventral keel. Articular facets for the costal cartilages of ribs three through six are arranged along the lateral borders at progressively shorter intervals (Fig. 25A—B). The xiphoid process is slightly less than half the length of the body and is almost square in cross section in its anterior region. 56 Spec. Publ. Amer. Soc. Mamm. 6 The costal cartilages of the seventh pair of ribs articulate on the anterolateral aspects of the xiphoid process. Posteriorly the x1- phoid process becomes dorsoventrally flattened and terminates in an expanded flange. Ribs The rib cage is about 1.4 times as broad and 1.1 times as deep as it is long. In one specimen, it was about 5 mm deep and 13.5 mm wide at its anterior end, and was expanded posteriorly to a depth of about 18 mm and breadth of 26 mm. The first rib is strongly thickened anteroposteriorly as described by Vaughan (1959, 1970b) for other species of bats. A stout tu- bercle is found on the dorsal aspect immediately distal to the tu- berculum. The rib arches gently dorsad and terminates in an ex- panded tip, which articulates with the thick, first costal cartilage. The costal cartilage is parallelogram-shaped and articulates on its dorsal surface with the first rib and on its medial surface with the lateral process on the manubrium. Inasmuch as the remaining cos- tal cartilages of the sternal ribs are thin, the first costal cartilages provide much of the support of the sternum and reinforce it against the powerful dorsolateral pull of the sternal M. pectoralis. The second and third ribs are anteroposteriorly flattened, but cau- dally the ribs become dorsoventrally and laterally flattened. Rib seven is the last sternal rib, and the costal cartilage of rib eight connects with its costal cartilage. The cartilage of rib nine attaches to the costal cartilage of rib eight, but the cartilage of rib 10 con- nects directly with rib nine and the cartilage of rib 11 connects to rib 10. The twelfth rib is normally less than a millimeter long and has poorly defined distal connection. Pectoral Girdle and Limb Scapula (Fig. 26).—Viewed dorsally, the scapula is roughly elip- tical posteriorly, truncate anteriorly, and about 41 per cent as wide as it is long. The glenoid fossa is directed slightly craniolaterally. The articular surface is anteroposteriorly elongated and is twice as high posteriorly as anteriorly. The posterior half of the fossa is deeply concave and strongly reinforced posteriorly by the expand- Altenbach—V ampire Locomotor Morphology 57 coracoid process coracoid proc. acromion process scapular flange connective tissue brace supraspinous fossa spine humerus anteromedial facet intermediate facet posterolateral facet glenoid fossa om lateral border——_{_| supraglenoid tuberosity scapular flange coracoid process Fic. 26. Scapula and proximal portion of humerus of Desmodus: Ventral view of right humerus (A) and scapula (B); dorsal view of right humerus (D) and scapula (C); anterior view of right scapula (E). ed lateral scapular border. Paired infraglenoid tuberosities are sit- uated immediately posterior to the fossa and serve as points of origin for slips of the long head of the M. triceps brachu. The thick lateral scapular border slopes gently posteromedially and becomes progressively thinner toward the rounded posterior margin. The medial border, which is not as thick as the lateral border, is nearly parallel with the long axis of the body. Anteriorly, the medial bor- der is thickened dorsoventrally and curves laterally to form the scapular flange. Lateral to the flange, the anterior scapular border is concave for about 2 mm, and then becomes thickened and di- rected anteriorly to form the projection that is the base of the coracoid process. Laterally, the thickened anterior process bears a small supraglenoid tuberosity that lies immediately anterior to the glenoid fossa. The anteroposteriorly flattened coracoid process extends ven- trally from the thickened anterior projection of the scapula, medial to the supraglenoid tuberosity, and then curves laterally and slight- ly posteriorly. The tip of the coracoid process is expanded and lies below and slightly lateral to the middle of the glenoid fossa. The dorsal surface of the scapula is transected by the scapular 58 Spec. Publ. Amer. Soc. Mamm. 6 scapula clavicle XY a humerus manubrium Fic. 27. Diagrammatic frontal view of the pectoral girdle of Desmodus: A, right clavicle and scapula tipped ventrally and right humerus fully adducted as might occur at the end of a jump; B, position of left clavicle, scapula and humerus at the start of a jump or downstroke. The lateral scapular border is tipped upward and the humerus is locked dorsally with the scapular border. spine, which runs from the medial border anterolaterally toward the posterior half of the glenoid fossa. Quite low medially, the spine becomes progressively higher laterally and, about 4 mm from the glenoid fossa, curves sharply cranially and dorsally to the anteroposteriorly flattened acromion process. The distal 3 mm of the acromion process is thickened and strongly anteroventrally curved so that it lies medial to, and above, the glenoid fossa. The lateral border of the acromion process arises about a millimeter medial to the highest point of the glenoid fossa. A strong band of connective tissue runs from the dorsolateral aspect of the flange to the medial surface of the expanded tip of the acromion process, and helps brace the latter against the pull of the abductors and supinators of the humerus. The anteroposterior flattening of the process and the increased height of the scapular spine also aid in resisting these forces. In Desmodus, the supraspinous fossa is smaller relative to the Altenbach—V ampire Locomotor Morphology 59 infraspinous fossa than in some of the closely related phyllostom- atids. A thickened ridge extending from the base of the acromion process to the anteromedial edge of the posterior border separates the large anteromedial facet from the small and nearly vertically oriented intermediate facet. Another thickening separates the in- termediate facet from the nearly horizontally-oriented postero- lateral facet. The vertical orientation of the intermediate facet pro- vides a solid surface for muscular attachment and reduces the relative width of the entire facet. This suggests that the muscle mass that originates there, the M. infraspinatus, is suited for pow- erful contraction in a limited direction. Posteriorly the scapula ter- minates in a cartilaginous extension typical of many other bats. Clavicle (Fig. 27)—The proximal articular surface is greatly en- larged, rather ovoid, and elongate laterally. Within 2 mm of the articular surface, its diameter constricts to about a millimeter. At this point the clavicle is nearly circular in cross-section, but becomes laterally compressed distally. In specimens preserved with the wing folded in the typical pos- ture seen in hanging, the long axes of the proximal half of the clavicles are oriented about 20 degrees anterolateral and about 30 degrees anterodorsal to the long axis of the body. From their prox- imal articulations, the clavicles curve gently posterodorsally and, over the proximal 80 per cent of their length, become increasingly deeper (anteroposteriorly) in cross-section. The distal 20 per cent of each clavicle is curved sharply posteriorly, and the slightly ex- panded distal tip is displaced about 3 mm posterior to the long axis of the proximal shaft. The ventrolateral aspect of the distal 1.5 mm of the clavicle is bound by tough connective tissue to the ventromedial surface of the anterior tip of the scapula. The articular surface is elongate and nearly horizontal, a configuration that permits the scapula to tilt about its long axis relative to the clavicle. Angular displacement of the long axis of the scapula is limited to only a few degrees by the articulation. However, when the lateral scapular border is rocked strongly ventrally, the articulation allows the long axis of the scapula to be inclined upward posteriorly between 10 and 15 degrees. This suggests that the anterior end of the scapula is com- monly tipped ventrally when the lateral scapular border is tipped ventrally, as in a jumping maneuver or in certain terrestrial feeding postures. This helps explain the apparent depression of the shoul- 60 Spec. Publ. Amer. Soc. Mamm. 6 der joint during these movements. The curvature of the posterior surface of the clavicle, adjacent to its distal tip, perfectly matches the curvature of the coracoid process, and allows the coracoid pro- cess to swing behind the clavicle (Fig. 27A). The scapula can be rotated about its long axis to position the coracoid process directly behind the clavicle. When the clavicle is inclined a normal 40 de- grees above horizontal (viewed frontally), this rotation of the scap- ula orients the short scapular axis vertically, thus directing the glenoid fossa ventrally. This is the most striking feature of the pectoral girdle osteology of Desmodus and is partly responsible for the high quadrupedal stance and remarkable jumping ability of the species, as it allows the humerus to be directed completely ventrally. At the clavo-scapular articulation, the surfaces of both the clav- icle and scapula are bordered dorsally by nearly vertical bony sur- faces that limit upward rotation of the lateral scapular border. When the short axis of the scapula is within a few degrees of being parallel to the long frontal axis of the clavicle, following upward rotation of the lateral scapular border (Fig. 27B), the supra-arti- cular surfaces meet and stop further rotation. Rotational forces applied to the scapula are thus transferred to the clavicle. A strong connective tissue band runs from the middle anterior surface of the clavicle to the middle of the coracoid process and aids 1n stop- ping the upward lateral rotation of the scapula. The articulation of clavicle and scapula allows rotation of the short axis of the scap- ula through an arc of fully 120 degrees. Humerus (Figs. 26—28).—This bone is relatively stocky in Desmo- dus; the greatest diameter of the middle diaphysis is about 5.4 per cent of the length. The head is directed posterior to the proximal end of the shaft. Anterior to the head is a deep depression (Fig. 28E) into which the supraglenoid tuberosity fits when the humerus is extended anteriorly. The greater tuberosity extends postero- dorsally and medially from the medial end of the shaft. The ridge of bone that runs between the tuberosity and the dorsal aspect of the head articulates with the dorsal border of the glenoid fossa to stop abduction of the humerus (Fig. 27B). Anteriorly, the greater tuberosity gives way to a ridge that projects anteroventrally to meet the medial end of the pectoral ridge. The lesser tuberosity projects posteroventrally and medially from the medial end of the shaft, and is continuous laterally with a low midventral ridge that extends Altenbach—V ampire Locomotor Morphology 61 pectoral ridge A dorsal epicondyle spinous process P dorsal epicondyle greater tuberosity pectoral ridge capitulum trochlea spinous process lesser tuberosity cap. troch. spin. proc. a cap. troch. spin. proc. H lesser tuberosity Fic. 28. Humerus of Desmodus: A, dorsal view; B, ventral view; C, anterior view of proximal end; D, posterior view of proximal end; E, medial view of proximal end; F, anterior view of distal end; G, posterior view of distal end; H, lateral view of distal end. 62 Spec. Publ. Amer. Soc. Mamm. 6 for several millimeters along the shaft and ends in a small tubercle about 6.5 mm distal to the tip. A ridge runs anterodorsally from the lesser tuberosity to the ventromedial base of the pectoral ridge. The importance of the rotative forces applied by the muscles that insert on the greater and lesser tuberosities is reflected by the ridges that run from their bases anteriorly to the medial end of the pectoral ridge. The pectoral ridge projects anteriorly about a millimeter from the middle of the proximal end of the shaft, beginning adjacent to the head, and continues distally for about 8 or 9 mm. The ridge is divided in its middle part into two ridges, one below the other, but it becomes quite thin about 2.5 mm distal to that point and is thin for the remainder of its length. For the first one-fourth of its length, the shaft is quite straight and roughly circular in cross section except for the pectoral ridge. The distal three-fourths of the shaft is strongly bowed posteriorly and compressed anteroposteriorly. The anterior aspect of the dis- tal half is slightly concave. These structural features apparently strengthen the distal shaft against the torque and strong upward forces encountered in the wingbeat cycle and terrestrial locomo- tion. The bowing of the distal three-fourths accomodates the prominent forearm musculature when the forearm is strongly flexed toward the humerus during terrestrial locomotion. The locking mechanism between the humerus and scapula of other bats described by Vaughan (1959) and others is quite evident in Desmodus and limits adduction and abduction to about 30 de- grees above and below the short axis of the scapula (Fig. 27). How- ever, the depression anterior to the head of the humerus is suffi- ciently deep, and the supraglenoid tuberosity is sufficiently small and anteriorly positioned, that the humerus can be extended to within 30 degrees of the long axis of the lateral scapular border before being stopped by this locking mechanism. Anterior exten- sion of the humerus is necessary for alighting on a horizontal sur- face (Fig. 23), a backward jump (Fig. 12), and climbing on a vertical surface (Fig. 6). —> Fic. 29. Right radius and ulna of Desmodus. A, dorsal view; B, ventral view; C, anteromedial view of proximal end; D, ventral view of proximal end; E, dorsal view of proximal end. Altenbach—Vampire Locomotor Morphology sesamoid for triceps tendon ulna radius radius ulna radius Cc flexor fossa for biceps tendon radius 64 Spec. Publ. Amer. Soc. Mamm. 6 The distal articular surfaces formed by the capitulum and the trochlea are displaced anteriorly and slightly dorsally to the axis of the shaft (Fig. 23F—H). The groove separating the two inclined surfaces of the capitulum is rather shallowly concave, whereas the groove separating the capitulum from the ventral trochlea 1s deep- er and rather V-shaped in section. The prominent ventral flange of the trochlea continues to the posterior side of the epiphysis, where the groove above it is broadened and bordered above by the ridgelike, posterior continuation of the dorsal side of the ca- pitulum. The ulna and the elongate sesamoid of the M. triceps brachu tendon (Fig. 29A—B) run into this groove as the forearm is extended. The epicondyle above the capitulum is indented (Fig. 28A), and the M. supinator arises from the center of this indenta- tion. Proximally, a small ridge runs posteromedially to the shaft and serves for the point of origin of the M. extensor carpi radialis longus and M. extensor carpi radialis brevis. Ventrally, the epicondyle (medial epicondyle) extends slightly more than 2 mm to form a spinous process (Fig. 28B, 28F-G). The tip of this process is located directly below the center of rotation of the radius; thus, flexion and extension of the radius do not affect the length of the muscles that originate on the spinous process. Radius and ulna (Fig. 29)—The radius is about 1.6 times the length of the humerus and over its proximal half curves strongly posteriorly and ventrally (Fig. 29A—B). The proximal articular sur- face is directed anteromedially and has a central concavity that is bordered dorsally and ventrally by low ridges and adjacent flat- tened areas (Fig. 29B—D). The rounded ventral part of the capit- ulum fits into the central concavity, and the inclined dorsal portion of the capitulum and the ventral trochlea articulate with the nar- row flattened surfaces above and below the concavity. The con- cavity is in line with the axis of the shaft and is bordered ventrally by a flange that makes up the ventral articular surface. A promi- nent ridge of bone extends from the anterior border of this sur- face, at the level of the bottom of the concavity, laterally for about 5 mm (Fig. 29B, 29D). Posterior to this ridge is a flattened, pos- terodorsally inclined surface that ends in a deep groove (the flexor fossa) on the posterior face of the radius. The tendons of the M. biceps brachi and M. brachialis run ventrally over the ridge imme- diately distal to the ventral flange and insert into the flexor fossa. Thus, contraction of these muscles exerts both a flexive force to Altenbach—V ampire Locomotor Morphology 65 the forearm and a powerful supinating force to the entire arm, as the articulation of the humerus and radius severely limits any movement except flexion and extension. The thickened proximal end of the ulna is positioned posterior to the ventral half of the proximal articular surface of the radius and projects 1.5 mm beyond its proximal tip (Fig. 29A, 29D). A vertical groove on the anterior surface of the ulna articulates with a ridge on the posterior surface of the radius about 1.5 mm distal to its end. A groove distal to the ridge on the radius accepts a ridge on the ulna. This tongue-in-groove mechanism stabilizes the ulna against the medial pull of the M. triceps brachi. Distal to the thick- ened proximal articular area, the shaft of the ulna is thin and concave anteriorly. The ulna is fused distally to the posterodorsal surface of the radius at about the middle of the radial shaft. The rigid fusion distally and strong articulation proximally suggest that the ulna is important in bracing the radius against forces directed toward its long axis during terrestrial locomotion or jumping. It also affords a rigid structure for muscle attachment. Distal to the fusion of the ulna and radius, a thin ridge runs along the postero- dorsal surface of the radius to within 5 mm of its distal end. The ridge is the same thickness and width as the ulna before its fusion to the radius. Although no embryologic evidence is available, this ridge may represent the distal end of the fused ulna. The concave underside of this ridge serves for muscle attachment. Distal to the fusion of the ulna with the radius, the radius is diamond-shaped in cross section. The broad, anterodorsal surface of the distal 2 or 3 mm is divided by bony ridges into grooves for the tendons of several of the forearm muscles (Figs. 30-31). Anteroventrally, two ridges of bone make a deep channel for the M. abductor pollicis longus. The large, posterodorsal ridge bordering this channel is the anteroventral edge of a pair of channels divided by a small median ridge. The lower channel accommodates the M. extensor carpi ra- dials longus and the upper accommodates the M. extensor carpi ra- dialis brevis. Posterodorsally, a broad flat surface separates these channels to form a prominent posteriorly-projecting flange at the distal tip of the radius. This flange is the dorsal edge of a channel bordered ventrally by a median projection of the cuneiform. The tendons of the M. extensor pollicis brevis, M. extensor digitorum com- munis to digits III and IV, and the M. extensor indicis run through this channel. On the posterior surface of the radius medial to this 66 Spec. Publ. Amer. Soc. Mamm. 6 trapezoid lunar 2 trapezium 1 scaphoid (FEB pe sslD radius magnum \ rite. MN unciform ¥ (: . [~ tt cuneiform ‘ vi Vv Fic. 30. Dorsal view of the right carpus and first digit of Desmodus. channel is a large backward-projecting flange of bone that supports the tendons ventrally and functions as a posterior extension of the ventral aspect of the channel described above. This flange on the radius also forms a shelf for the tendon of the M. extensor digiti quinti proprius to digit V and the tendon of the M. extensor carpi ulnaris. The tendons are bound to this shelf of bone by-a tough ligamentous band, which runs from the posterior tip of the shelf to the posterior tip of the cuneiform. The exceptional investment of the distal portion of the radius with grooves and ridges of bone to confine tendons reflects the great forces placed upon the ten- dons, and thus elements in the hand, during terrestrial locomotion, jumping, and initial flight. The distal articular surface of the radius is deeply concave and directed posterolaterally from the long axis of the shaft. The pos- teroventral surface of the border of the articular surface bears a prominent lateral projection, which interlocks with the deep notch in the posterior aspect of the lunar. The edge of the articular surface posterodorsal to the projection forms a ridge that serves to hold the lunar in position. Anteroventrally, the projection con- tinues as a ridge of bone that confines the lunar ventrally and helps limit it to movement on only one plane. Manus (Figs. 30-31).—The lunar is the largest of the eight car- pals and is elongate parallel to the long axis of the distal articular surface of the radius. The body of the lunar is offset posteroven- trally to the long axis of the shaft and bound to the shaft by heavy ligaments on the posterodorsal surface. On the posteromedial as- pect of the lunar is a deep groove that interlocks medially with the Altenbach—V ampire Locomotor Morphology 67 2 lunar Se ; trapezium scaphoid Ppisiform radius TT cuneiform Fic. 31. Ventral view of the right carpus and first digit of Desmodus. distal projection on the posteroventral side of the articular surface of the radius and limits flexion of the lunar. The cuneiform is tightly bound to the radius posterodorsally to the lunar and bears a posteromedial projection that forms the ventral half of the deep channel described above. The posterior tip of this projection curves strongly dorsally, making the channel almost tubular (Fig. 30). A cylindrical anteroventral projection of the lunar bears a smooth surface anteriorly on which the small ovoid scaphoid rests. A deep circular groove separates the projection posterodorsally from an expanded circular ridge perpendicular to the long axis of the lunar. This groove accommodates a prominent anteromedial projection from the flattened trapezium and stabilizes it as the carpus is flexed and extended. The anterodorsal surface of the lunar posterior to the lateral ridge is saddle-shaped and accom- modates an anteromedial projection of the small trapezoid that projects from beneath the overlying trapezium. The lateral artic- ular surfaces of the lunar limit the movements of the trapezium, trapezoid, magnum, and cuneiform to a single plane, that of lateral extension and medial flexion. Distally, the cuneiform projects anteroventrally parallel to the long axis of the lunar and forms a broad articular surface that contacts the posteromedial aspect of the cuneiform. The trapezoid, which rides against the posterodorsal surface of the ridge on the lunar, serves as a spacer between the trapezium and the adjacent 68 Spec. Publ. Amer. Soc. Mamm. 6 magnum. The magnum bears a prominent posteroventrally-di- rected spine beneath the rounded articular surface, which slides against the deep lateral depression of the lunar. As the magnum is flexed, this spine locks against the posterior surface of the lunar. Distal to its articulation with the lunar and the cuneiform, the unciform is expanded and bears on its posterior surface a deep groove bordered above and below by slightly convex articular sur- faces. The long axis of the groove is inclined medially, slightly above the long axis of the radius, and accommodates the fingerlike projection on the proximal end of metacarpal IV. The surfaces above and below the groove accommodate proximal portions of metacarpals IV and V, respectively. Distally, the arrangement of the trapezium, trapezoid, magnum, and cuneiform produces deep notches on the posterolateral surface of the carpus, which receive the proximal processes of metacarpals II and III. The long axis of the rodlike pisiform is oriented obliquely across the posterior surface of the carpus from the medial projection of the trapezium adjacent to its articulation with the lunar postero- dorsally to the posteromedial tip of the cuneiform. Heavy liga- ments bind the pisiform to the posteromedial tip of the cuneiform, the posteromedial surface of the magnum, and the medial tip of the trapezium. A large tubercle projects from the posterior surface of the pisiform immediately ventrad to its dorsal tip, which is flat- tened into a smooth articular surface. This dorsal articular surface meets the flattened and slightly ovoid ventral surface of the prox- imal tip of metacarpal V. The articular facet on the metacarpal is oriented ventral and perpendicular to the slightly concave proxi- mal articular facet that contacts the cuneiform. Digit I (Figs. 30-31).—The proximal articular surface of the first metacarpal slopes anterolaterally from its ventral ligamentous at- tachment to the broad, flattened, distal surface of the trapezium, which slopes anteromedially. The articulation allows considerable freedom of movement, and the first metacarpal can be adducted or abducted through an angle of about 130 degrees. The first metacarpal is the thickest of the metacarpals and about 7 mm long, longer than the entire pollux of most other microchiropteran bats. Its thickness reflects the forces it bears in terrestrial locomotion and jumping. The distal articular surface is rounded, allowing movement of the first phalanx in almost any plane. The proximal articular surface of the first phalanx is deeply concave to accom- Altenbach—V ampire Locomotor Morphology 69 modate the rounded articular surface of the metacarpal, and the hingelike distal articular surface limits movement of the short sec- ond phalanx (which bears a recurved claw), to flexion and exten- sion. Digit IT (Figs. 30-31).—The proximal end of the second meta- carpal is vertically expanded and compressed anteroposteriorly into a rounded flange, which articulates in the groove between the trapezium and the magnum. The anterior tip of the flange rests against the posterolateral tip of the trapezoid. Distally, there is a ventral tubercle that articulates with the proximal part of meta- carpal III. Two millimeters distal to this tubercle there is a small posterodorsal saddle, bordered distally by a tubercle, into which articulates the large, anterodorsal tubercle of metacarpal III. This is the spacer described by Vaughan and Bateman (1970) that main- tains the spread of the second and third metacarpals in bats with a large dactylopatagium minus. Because Desmodus does not have a large dactylopatagium minus, this tubercle is quite small. The second metacarpal is approximately 81 per cent of the length of metacarpals III through V. Its distal articular surface and the proximal articular surface of the first phalanx are ex- panded, flattened, and nearly perpendicular to the long axis of the digit. Firm ligamentous binding of the joint limits movement and stabilizes the leading edge of the chiropatagium. The second pha- lanx is cartilaginous and serves only as a connection between the second and third digits to stabilize the leading edge of the chiro- patagium. Digit IIT (Figs. 30-31).—Medially the metacarpal is enlarged and flattened into a vertically-oriented flange similar to, but larger than, the flange of metacarpal II. The flange fits into a shallow curved depression on the posterior surface of the magnum and is bordered posteriorly by the concave, flattened anterolateral por- tion of the distal part of the cuneiform. There is a prominent depression on its posterior surface that accommodates an ante- riorly-directed process on the anteroventral aspect of the proximal tip of metacarpal IV. The distal articular surface of metacarpal III is expanded to one and a half times the diameter of the distal shaft and, along with the proximal articular surface of the basal phalanx, is perpendicular to the long axis of the shaft. The long axis of the shaft of the basal phalanx is offset dorsally and in line with the dorsal aspect of the shaft of the metacarpal. The metacarpopha- 70 Spec. Publ. Amer. Soc. Mamm. 6 langeal joint allows limited movement in any direction, but liga- mentous binding limits upward deflection. Much of the stability of this joint is provided by medially directed forces imparted by the tendons inserting on the first phalanx. Compression of the shaft forms a ventral notch proximal to the distal articular surface. The trochlealike articular surface bears a shallow vertical groove on its dorsal and distal surface. The proximal articular surface of the second phalanx is deeply concave and bears a dorsomedian process that curves strongly proximad to articulate dorsally with the groove of the distal surface of phalanx one. Lateral processes of phalanx two articulate medially with the lateral edges of the trochlea of the first phalanx and limit the movement of this joint to a vertical plane. The second phalanx can be deflected about 30 degrees above the long axis of the metacarpal and first phalanx, but this movement is then stopped by the dorsomedian process of the sec- ond phalanx. Ventral flexion through an arc of more than 90 degrees is possible as the ventral aspect of the articular surface of phalanx two fits into the notch proximal to the distal tip of the first phalanx. The second interphalangeal joint is flattened and similar to the metacarpophalangeal joint. All but ventromedial flexion is restricted by a firm ligamentous binding. Digits IV and V (Figs. 30-31).—From the anterolateral aspect of the proximal articular surface of metacarpal IV, a spine projects anteriad to fit into the depression on metacarpal III. This serves as a center of rotation that allows upward deflection of the fourth metacarpal. However, if the hand is extended, a flange on the anterodorsal edge of metacarpal IV slides into the posteriorly- turned dorsal edge of the articular flange of metacarpal III and stops this movement. This effectively braces the fourth metacarpal against upward displacement from the forces of the airstream as the extended wing is adducted. A posteromedially directed fin- gerlike projection of the proximal articular surface of metacarpal IV articulates with the groove in the distal surface of the cunei- form. The depression dorsal to the projection fits over the convex surface above the groove on the cuneiform. This arrangement prevents any rotation of the shaft, which would reduce the effec- tiveness of the dorsal bracing previously described. The proximal surface of metacarpal V bears a central notch that fits against the fingerlike posteromedial projection of the fourth metacarpal. Dorsally, a projection of the fifth metacarpal fits into Altenbach—V ampire Locomotor Morphology 71 a depression on the posteromedial and dorsal aspect of the fourth metacarpal and prevents upward deflection of the fifth metacarpal when the wing is extended and forced downward against the air- stream. The ventromedial surface bears a tubercle that projects antero- laterally and fits into a groove on the posteromedial and ventral part of metacarpal IV. Strong tendinous binding here further braces the fifth metacarpal against upward deflection by the air stream. Medial to the central notch, a flat articular surface curves posteriorly and articulates with the flattened distal surface of the cuneiform below the groove that accommodates the fingerlike pro- jection on metacarpal IV. The distal articular surfaces of the fourth and fifth metacarpals are similar to that of the third, but typically slope proximally on their ventral edge, allowing ventral flexion of the first phalanges through an arc of more than 90 degrees as the wing is folded. The proximal articular surfaces of the first pha- langes of digits III and IV are flattened and similar to that of the first phalanx of digit III. The first interphalangeal articulations of digits IV and V are similar to the first interphalangeal articulation of digit III. Digits IV and V have similar dorsomedial projections on the proximal articular surfaces of the second phalanges, which, unlike the less restrictive arrangement seen at the first interphalangeal joint of digit III, limit upward deflection of the second phalanges to a position parallel to the long axis of the basal phalanges. As the metacarpophalangeal joints allow considerable upward deflection, there is little need for additional deflection at the interphalangeal joints. However, ventral flexion through an arc of more than 100 degrees is permitted to facilitate folding of the wing. Lateral move- ments of the distal phalanges of digits IV and V are limited by ligamentous binding, which holds the second phalanges by their lateral articular surfaces against the distal articular surface of the basal phalanges, and by proximolateral projections, which articu- late with the distolateral surfaces of the basal phalanges. FUNCTIONAL MYOLOGY OF THE PECTORAL GIRDLE AND LIMB N the following descriptions I follow the system of muscle ter- I minology used by Vaughan (1959) who, in turn, followed those of Hill (1937) and Rinker (1954). However, I have used the same positional terms as in the previous section on osteology. Thus, the body, arm, and hand are described as in forward flight with the wing fully extended in mid downstroke. Comments on Electromyographic Analysis Without implant of a tension transducer in series with the in- sertional tendon of a specific muscle, there is no way of determin- ing the exact amount of tension that a muscle exerts on its insertion and origin or the temporal distribution of that tension in normal movements. However, electromyography provides useful information about both parameters if the electromyographic record is accurately in- terpreted. Bigland and Lippold (1954) and Bergstrom (1959) have demonstrated that tension varies directly with the integrated po- tential changes and that spikes of an electromyogram can be used to estimate the relative tension generated by a given muscle. Bas- majian (1962) suggested that the number of spikes, the degree of their superimposition, and their relative height and type, are im- portant factors in analysis of muscular function through an elec- tromyogram. He stated: “Experience has shown that the easiest, and in most cases, most reliable evaluation is by the trained ob- server's visual evaluation of results colored by his knowledge of the technique involved.” I have made no attempt to precisely quan- tify the data, but have discussed it in such relative terms as “no contraction,” “slight contraction,” or “strong contraction.” Until electromyographic data are available for all the major muscles of a particular part of the girdle or limb, or the exact force produced can be determined from implanted tension transducers, any at- tempt at a more precise quantification easily could be misleading. Electromyographic data, however, do allow more accurate anal- ysis of the function of many muscles than heretofore has been 72 Altenbach—V ampire Locomotor Morphology 73 possible. All of the literature on the function of muscles in bats is centered around predictions about the role of a given muscle based on strictly positional criteria. Although reasonably reliable conclu- sions can be drawn from positional relationships, they can be nicely supplemented and clarified by electromyographic data. The temporal lag between myopotential changes and force gen- erated by a muscle, which is a function of the time between de- polarization and shortening of the fibers and the time required to stretch the elastic components of the muscle, probably varies be- tween muscles in Desmodus. For the coracoid head of the M. biceps brachu, this delay was experimentally determined to be approxi- mately 10 milliseconds. A tension transducer was attached to the insertional tendon of this muscle and the electromyogram from the muscle and output from the transducer were recorded simul- taneously with the high-speed camera. Restraints of time and avail- ability of additional living specimens for these experiments pre- vented doing this with other muscles. When such data are available, the electromyographs might be interpreted differently. However, as presently interpreted, they provide considerable insight about the function of muscles in the pectoral girdle and limb. The points on the electromyographic traces in Figs. 32-33, and 35-41 coincide temporally with corresponding drawings of the lo- comotor behavior. Both the electromyogram and drawings are la- beled with upper case letters. The probable time of muscular con- traction, represented by a solid line, is displaced to the right along the horizontal axis of the electromyogram, a distance correspond- ing to 10 milliseconds. A scale indicating the magnitude of the potential changes on the vertical axis and time on the horizontal axis 1s included in each figure. Muscles Unique to Bats M. occipito-pollicalis (Figs. 42, 44).—The anatomical modification of this muscle in Desmodus seems quite different from that in other bats (Macalister, 1872; Humphry, 1869; Vaughan, 1959; Norberg, 19706). There is considerable variability between species in the relative length of the fleshy belly distal to its origin on the cranium, and in some bats, such as Plecotus auritus (Norberg, 1970b) and Pteropus edwardsi (Humphry, 1869), there is a second, distal belly. 74 Spec. Publ. Amer. Soc. Mamm. 6 However, descriptions of this distal belly indicate it is relatively fusiform and originates almost entirely on the rather compact in- sertional tendon of the proximal belly, which runs along the lead- ing edge of the propatagium (Fig. 24). In Desmodus, the proximal belly inserts rather diffusely into the proximal propatagium. A broad, flat belly originates from fibers in the anterior half of the propatagium anterior to the radius, about one-third the distance toward its distal tip, and from some of the small insertional tendons of the proximal belly. Schumacher (1932) described a M. propa- tagialis proprius in Pteropus that was innervated by nerves of the cranial portion of the brachial plexus, whereas Macalister (1872) found the proximal belly in three other genera to be innervated by the spinal accessory nerve. I was unable to trace the innervation of either muscle, but on strictly positional criteria, I designate the proximal belly as M. occipito-pollicals and the distal belly as M. propatagials proprius. Origin is primarily on connective tissue lateral to the midline from the posterior tip of the saggittal crest and down the supraoc- cipital for 2 mm. A distal slip originates from fibers of the clavicular M. pectoralis. Insertion is by a finely branched tendon onto the connective tissue fibers of the propatagium at the level of the base of the forearm. In contrast to the condition in most other bats, the M. occipito- pollicalis tenses the propatagium directly by drawing its elastic fi- bers anteromediad. As in other bats, it depresses and tightens the leading edge of the propatagium. Contraction of the fibers of the clavicular M. pectoralis, which insert on this muscle, draws the me- dial half of the propatagium strongly ventrad and increases the camber of the medial portion of the wing. M. propatagialis proprius (Fig. 46)—The origin is from the fibers in the anterior half of the middle propatagium and on some of the insertional fibers of the M. occipito-pollicalis. Insertion is by an apo- neurosis over the medial aspect of metacarpal I, a thin tendon to an aponeurosis over the metacarpophalangeal joint of digit I, and a tendon on the middle of the anterior surface of the first phalanx of digit IT. This muscle is not effective in moving the digits, but uses them as a fulcrum to tense the propatagium. The vertical orientation of the wing during the first half of the upstroke and its position an- terior to the body may have necessitated the development of this Altenbach—V ampire Locomotor Morphology 75 muscle. When the wing is highly flexed in this phase of the up- stroke, contraction of the M. occipito-pollicahs would have only lim- ited effect if it inserted on the hand. However, tension from both proximal and distal sides of the propatagium, directed against the fibers posterior to the leading edge, is effective in reinforcing it for a firm airfoil. Contraction of both muscles at the start of the coasting phase of the jump would keep the propatagium oriented ahead of the arm and somewhat reduce its area and drag. This muscle also serves to help brace the leading edge of the medial wing as it is deeply pronated for thrust production in the down- strokes during accelerating flight. M. coraco-cutaneus (Fig. 44).—Origin is on the medial aspect of the tip of the coracoid process of the scapula. The belly gives rise to a second belly about 5 mm distal to the origin on the coracoid process, and both bellies insert onto elastic fibers in the plagiopa- tagium posterior to the brachium and proximal one-fourth of the forearm. When the wing is adducted in the downstroke, contraction helps reinforce the plagiopatagium and reduce billowing from the force of the air stream. In the first half of the upstroke, when the distal half of the wing is oriented vertically and raised anterior to the body (Fig. 20), contraction of this muscle and pull from the hind limbs probably help maintain tension on the plagiopatagium to reduce its surface area and minimize drag. Muscles of the Pectoral Girdle and Limb Trapezius Group M. clavotrapezius (Fig. 42).—This muscle has its origin on a tough tendinous sheet bound to the anterior tip of the dorsal process on the first thoracic vertebra and to a dorsal tubercle on the first rib. It inserts over the dorsal surface of the clavicle, beginning about 9 mm distal to its proximal tip and continuing to within 2 or 3 mm of its distal tip. In contrast to the condition in many other species of bats, the clavotrapezius is separate from the acromiotrapezius. It is much larger than the anterior portion of the united clavotrapezius and acromiotrapezius, which insert on the clavicle of other species. Contraction pulls the distal end of the clavicle, and thus the an- terior end of the scapula, dorsomedially. The relatively free artic- 76 Spec. Publ. Amer. Soc. Mamm. 6 w @ © 2 mv | Ais Ri eee ees 20 msec A B Cc D) fe F Fic. 32. Electromyogram of right M. clavotrapezius of Desmodus and correspond- ing locomotor behavior. The contraction of the muscle occurs slightly after the electrical event and is shown as a solid line above the electromyographic recording. Corresponding locomotor stages and portions of the electromyogram are indicated by the same letters. ulation of the scapula and clavicle of Desmodus requires that the clavicle be firmly braced to provide a solid fulcrum on which the scapula can rock about its long axis, as described in other species of bats by Vaughan (1959). However, more importantly, the an- terior tip of the scapula, and thus the shoulder joint, can be pulled dorsomediad by this muscle. This movement is important in Des- modus to position the wing prior to the first downstroke after a jump. The shoulder is pulled ventrad during the jump and must be positioned dorsally to give the ventral flight musculature a good mechanical advantage on the downstroke. Electromyographic data illustrate that the contraction of this muscle probably occurs during the powered phase of the jump to stabilize the clavicle. Assuming a 10 millisecond temporal lag between the myopotential changes and the generation of force by the muscle, power should be applied roughly from before B, through C, and nearly to D in Fig. 32. The contraction could certainly be overpowered by the M. subclavius during any of the powered phase of the jump, although the qui- escence before and after D indicates probable shoulder joint depression late in the jump. The jump on which electromyograph- ic data are available did not lead to flight (the bat landed on the side of the flight chamber after the jump). Thus, the flick and subsequent first downstroke do not occur and the contraction to Altenbach—V ampire Locomotor Morphology 77 Ba eB AW PAS BH ie Sy, io > M N O Pp Q » ino 2mv R Ss Es 20 msec EE i eealek cle ele battee? fee dees A ek Co et ee ee ea A Baa D CE F G H I J K L M N O P Q R Fic. 33. Electromyogram of right M. spinotrapezius of Desmodus and correspond- ing locomotor behavior. The contraction of the muscle occurs slightly after the electrical event and is shown as a solid line above the electromyographic recording. Corresponding locomotor stages and portions of the electromyogram are indicated by the same letters. 78 Spec. Publ. Amer. Soc. Mamm. 6 raise the clavicle and shoulder from the adducted position is not seen. A short burst of activity after the powered phase of the jump might be the beginning of such a contraction. M. acromiotrapezus (Fig. 42).—The origin is on the dorsal midline from the posterior tip of the tubercle on the first thoracic vertebra to the posterior tip of the fifth thoracic vertebra. Insertion is onto the tendon of origin of the M. acromiodeltoideus from a point about half a millimeter anterior to the tip of the acromial process and posteriorly for 7.5 mm along the lateral aspect of the acromial process and scapular spine. The anterior portion of the acromiotrapezius, which inserts on the enlarged area of the acromion process, is three times as thick as any portion posterior to it. The combined clavotrapezius and acromiotrapezius is thicker anteriorly in many other bats (Vaughan, 1959; Norberg, 1970b), but the thickened anterior por- tion is usually considered the M. clavotrapezius. In Desmodus, the thick anterior portion is suited to powerfully tip the acromial pro- cess mediad and thus the medial scapular border ventrad, inde- pendent of movement of the clavicle. As Vaughan (1959) noted, this action can initiate abduction of the humerus when the latter is locked with the ventral scapular border. In addition, this muscle probably helps steady the scapula when the bat is moving on the ground and the lateral scapular border is tipped strongly ventrally. M. spinotrapezius (Fig. 42) —Origin is on the dorsal midline from the eighth thoracic vertebra to the posterior tip of the second lum- bar vertebra. Insertion is from the dorsolateral aspect of the thick- ening at the junction of the spine and medial scapular border to a point about 5 mm anterior. As in other bats (Vaughan, 1959; Norberg, 19706), this muscle is situated to exert a strong posterior pull on the medial scapular border. This is important, because the fulcrum of scapular motion is the anterior articulation with the clavicle. A posterior anchor is necessary if the muscles applying ventral force to the medial and lateral scapular borders are to be effective in rocking the scapula and the wing when the humerus and scapular border are locked. Assuming a 10 millisecond temporal delay, electromyographic data illustrate continuous, probably moderate, contraction during the jump and quiescence at its end (Fig. 33A—F). Activity during the coasting phase may reflect initial limb abduction and scapular sta- bilization (Fig. 33G—J), but it is much better positioned for the Altenbach—V ampire Locomotor Morphology 79 latter. However, the relatively great activity around G suggests this muscle may be important in reorienting the scapula after its lateral border is so highly depressed during the jump. The posteriorly elongate scapula in this species is a feature that aids scapular sta- bilization by the M. spinotrapezius during movements in flight and terrestrial locomotion. Function in the former role is suggested by nearly continuous activity during the next two wingbeats (Fig. 33K-R). Costo-spino-scapular Group M. levator scapulae (Fig. 42).—The origin of this muscle is by four slips onto the dorsal projections of the transverse processes of the fourth through seventh cervical vertebrae. Insertion is on the me- dial scapular border, beginning about 5 mm posterior to the an- terior tip of the scapular flange and continuing posteriorly to the junction of the spine and medial border. As in other bats (Vaughan, 1959; Norberg, 1970b), this muscle tips the medial scapula border ventrad and, along with the M. acromiotrapezius and the anterior division of the M. serratus anterior, can brace the scapula or aid in the upstroke. The deep, ventral arch of the cervical vertebrae and the relatively high position of the scapula separate the origin and insertion of this muscle more than in most bats and allow it to exert nearly constant force, ir- respective of the position of the scapula. _ M. serratus anterior, anterior division (Figs. 42, 45).—The origin of the muscle is by two large bellies: one from the anterior face of the first rib adjacent to its articulation with the first costal cartilage, and the other by a slip from a tubercle lateral to the transverse foramen of the sixth cervical vertebra and a slip from a tubercle ventral to the dorsal projection on the transverse process of the seventh cervical vertebra. Insertion is onto the medial scapular border from the anterior tip of the flange posteriorly to within about 4 to 5 mm of the junction of the spine and medial border. The anterior portion of the serratus, anterior division, is thick; the posterior portion is thin and membranous. Thus, most of the contractile force is exerted on the enlarged scapular flange and tilts the medial border ventrad. Along with the M. levator scapulae, M. acromiotrapezius, and M. rhomboideus, this muscle aids in abduc- tion of the arm when the humerus is locked ventrally with the 80 Spec. Publ. Amer. Soc. Mamm. 6 ‘\ humerus scapula M. subclavius . serratus anterior post. div. M. pectoralis sternal div. Fic. 34. Diagram of anterior view of the rib cage, pectoral girdle, and proximal end of the humerus of Desmodus showing primary adductive forces during the powered phase of a jump or during the downstroke in initial flight following a jump. The humerus is dorsally locked with the scapular border. lateral scapular border and probably steadies the scapula during jumping behavior and terrestrial locomotion. M. serratus anterior, posterior division (Figs. 34, 42, 44-45) —The origin extends from the lateral aspect of the first costal cartilage in a line along the junctions of the second through sixth ribs and their costal cartilages, then dorsally along the costal cartilages of ribs seven and eight to the level of the junction of rib eight and its costal cartilage. Insertion is on the lateral and ventral aspect of the lateral scapular border, from the posterior tip of the posterior cartilaginous extension anteriorly to within about 3 mm of the glenoid fossa. As in other bats (Macalister, 1872; Vaughan, 1959; Norberg, Altenbach—V ampire Locomotor Morphology 81 1970b), the posterior division of the serratus is massive. When the humerus is locked with the dorsal scapular border, this muscle can adduct the brachium, as in the first portion of the downstroke or in much of the powered phase of the jump (Fig. 34). A tremendous amount of power is required in the jump to accelerate the bat upward with a heavy load of blood. This muscle is probably able to assist the sternal M. pectoralis in this movement through an arc of more than 130 degrees. The posterior division of the M. serratus anterior also is vital in the first of the downstroke where it assists the M. pectoralis in ad- ducting the extended wing, as described by Vaughan (1959) in other bats. Following a jump, air speed is low and the first few wingbeats must rapidly accelerate the bat. By functioning simul- taneously in the first half of the downstroke, the posterior division of the M. serratus anterior and the M. pectoralis supply maximal power to the wing when it is configured to provide both thrust and lift. During faster and more efficient flight, a division of labor, suggested by Vaughan (1959) for other species of bats, between the M. serratus anterior, M. pectoralis, and M. subscapularis may occur and the muscles may not contract simultaneously. During terrestrial locomotion, forces acting on the pectoral limb are transferred to the lateral scapular border by the humerus. During locomotion with the body extremely elevated, as seen in terrestrial feeding behavior, this muscle tips the short axis of the scapula nearly vertically, thus directing the forces acting against the pectoral limbs directly upward against the scapula, with little or no rotational component. The M. serratus anterior and the clav- icle thus act as a sling to support the body. M. rhomboideus (Fig. 42)—The origin is a large belly from tho- racic vertebrae one through six; a small anterior slip on the ten- dinous sheet that is the origin of the M. clavotrapezius; and a third slip on the dorsal spinal musculature adjacent the first thoracic vertebra. Insertion is on the ventral and medial aspect of the pos- terior cartilaginous extension of the scapula and anteriad along the medial scapular border to its junction with the scapular spine. Thin anteriorly, the rhomboideus becomes thick posteriorly in the region of its insertion on the posterior cartilaginous extension of the scapula. This suggests the major function is to shift the scapula anteriad and tilt its medial border ventrad. As in other bats (Vaughan, 1959; Norberg, 19706), this muscle functions with 82 Spec. Publ. Amer. Soc. Mamm. 6 Q R Ss Vv U 20msec Fic. 35. Electromyogram of right M. latissimus dorsi of Desmodus and corre- sponding locomotor behavior. The contraction of the muscle occurs slightly after the electrical event and is shown as a solid line above the electromyographic re- cording. Corresponding locomotor stages and portions of the electromyogram are indicated by the same letters. Altenbach—V ampire Locomotor Morphology 83 the M. acromiotrapezius, M. levator scapulae, and the anterior division of the M. serratus anterior to power the initial abduction of the arm or to steady the scapula when contracting against the antagonistic posterior division of the M. serratus anterior. Anteroposterior move- ments of the scapula probably aid in balancing the bat over the line of force exerted by the pectoral limbs during a jump and in stabilizing the shoulder girdle during turning maneuvers (Fig. 18). M. omocervicalis (Fig. 42).—Origin is on the ventral arch of the atlas. Insertion is onto the dorsal border of the clavicle and half a millimeter of the adjacent M. subclavius, 7 mm distal to the sternal articulation of the clavicle. The omocervicalis probably aids in the movement of the head. Insertion on the central clavicle instead of the acromial process (as in many other bats) is indicative of the great motility of the head in this species. Latissimus-subscapular Group M. latissimus dorsi (Fig. 42).—Origin is on the dorsal midline from the posterior tip of thoracic vertebra nine to the anterior tip of lumbar vertebra three. Insertion is in common with the M. teres major on the low ridge on the ventral aspect of the humerus be- ginning about 3.5 mm distal to the tip of the lesser tuberosity. The latissimus dorsi and the teres major are well suited to pro- nate the humerus and thus the entire arm, as well as to flex and abduct the humerus. These movements are important in terrestrial locomotion when the pectoral limbs are pulled posteriad and pro- nated in the power stroke. Figure 35 illustrates the function of this muscle during a jump into flight and the initial two wingbeats. A 10 millisecond temporal delay between myopotential changes and contraction is assumed. Contraction begins at the onset of the coasting phase (Fig. 35E) and probably helps abduct the wing. During the early part of the initial flick (Fig. 35H), contraction helps pronate the arm to drive the digits upward and backward against the airstream and help position the wing for the first down- stroke. Slight electrical activity indicates weak contractions during the downstroke that perhaps help stabilize the angle of attack and may reinforce the strong pronation of the wing. After flexion and supination of the arm in the first of the upstroke, sudden con- traction helps pronate and abduct the arm early in the flick phase (Fig. 35L to between M and N). This myopotential burst indicates 84 Spec. Publ. Amer. Soc. Mamm. 6 strong, perhaps maximal, contractive force during this movement. Feeble contractions again occur periodically during the down- stroke, perhaps for fine control of wing orientation, and a strong contraction occurs early in the flick phase (Fig. 35R to between S and T). M. teres major (Fig. 42).—Origin is on the lateral scapular border from the level of the junction of the spine and medial border to within about a millimeter of the posterior tip. Insertion is with the M. latissimus dorsi on the ventral aspect of the humerus distal to the lesser tuberosity. The function of the teres major is essentially similar to that of the M. latissimus dorsi, except that it is not suited to abduct the humerus. It probably functions primarily in the flick phase of the upstroke in flight, in terrestrial locomotion, and in climbing. M. subscapularis (Fig. 45).—Origin is on the ventral aspect of the scapula and posterior cartilaginous extension to within 2 mm of the base of the coracoid process and within 2 mm of the posterior edge of the glenoid fossa. Insertion is onto the posterior and me- dial aspect of the tip of the lesser tuberosity of the humerus. Although no electromyographic data are available, the subscap- ularis almost certainly functions to adduct the humerus after it is unlocked from the dorsal scapular border in the last of the down- stroke in forward flight, as described by Vaughan (1959). In an alighting maneuver (Fig. 23), the subscapularis, along with the cla- vicular M. pectoralis, extends and adducts the humerus prior to contact of the substrate by the forelimbs and probably helps cush- ion the impact by contraction as the humerus is forced upward and backward. Deltoid Group M. clavodeltoideus (Figs. 42, 44) —Origin of a large belly is from the anterodorsal aspect of the clavicle for about 9 mm beginning approximately 2.5 mm from its distal tip; and a small belly, deep to the first, from about 2 mm of the anteroventral surface of the clavicle in the region of the sharp posterior curve of the clavicle before its articulation from the scapula. Insertion of the larger belly is onto the anterior aspect of the expanded proximal tip of the pectoral ridge and laterally for 9 mm. The second belly inserts onto the dorsomedial aspect of the proximal end of the pectoral Altenbach—V ampire Locomotor Morphology 85 ridge and onto a ridge on the anterior base of the greater tuber- osity. Both bellies are clearly separate from the clavicular portion of the M. pectoralis. The clavodeltoideus powers the forward, recovery stroke of the brachium during terrestrial locomotion and the thrusting stroke of the brachium during backward climbing. It is probably aided in this movement by the clavicular M. pectoralis and somewhat by the M. subscapularis. Its clear separation from the clavicular M. pectorahs suggests that the clavodeltoideus is impor- tant in powering the complex movements of terrestrial locomotion and climbing. The clavodeltoideus cannot assist in adduction of the brachium during the powered phase of the jump or in the downstroke of forward flight, but it is important in controlling the angle through which adduction progresses. Steady contraction during a down- stroke would direct the stroke strongly forward. In a braking ma- neuver, this muscle functions to anteriorly brace the wing as it remains extended at a high angle of attack. M. acromiodeltoideus (Fig. 42).—The origin is on the tendon of insertion of the M. acromiotrapezius at a point anterior to the acro- mion process and extending for 6 mm along the lateral aspect of the acromion process and scapular spine. Insertion is on the an- terior 2 mm of the dorsal aspect of the pectoral ridge beginning 5 mm distal to the tip of the greater tuberosity and continuing lateral for 11 mm. The acromiodeltoideus is situated to abduct, slightly flex, and impart a strong supinating force to the humerus. The relatively long scapula, along with bracing supplied by the M. spinotrapezius, provides a stable origin for the muscle to supinate the brachium and thus raise the wing when the forearm is flexed toward the brachium, as occurs at the beginning of the upstroke. An electro- myographic record during a jump and initial flight indicates a relatively long contraction during the adduction of the brachium (Fig. 36D-G). This seems surprising, but possibly the acromiodel- toideus stabilizes the dorsal locking of the scapula and humerus throughout the entire powered phase of the jump, thus suggesting that the humerus is not adducted relative to the scapula during even the last of the jump. The posterior division of the M. serratus anterior and the sternal M. pectoralis thus would supply the power for the entire adduction of the brachium. The relatively free ar- 86 = Spec. Publ. Amer. Soc. Mamm. 6 OA Ne eK eS BR Sr ° A D 20 msec SSS rans May, un AW ty a AV Den a cae ees TOT VY, i] I I ! | | 1 ! I I l I 1 I I I I A B Cc D E F G H I J K E M N O P Q Fic. 36. Electromyogram of right M. acromiodeltoideus of Desmodus and corre- sponding locomotor behavior. The contraction of the muscle occurs slightly after the electrical event and is shown as a solid line above the electromyographic re- cording. Corresponding locomotor stages and portions of the electromyogram are indicated by the same letters. Altenbach—V ampire Locomotor Morphology 87 ticulation of the scapula and clavicle allows the two largest muscles in the bat to power the adduction of the brachium during the jump. The M. subscapularis apparently does not aid the adduction during the jump as perhaps it does in the downstroke of forward flight, as Vaughan (1959) suggested for other bats. However, the electromyographic data provide no evidence that the M. subscap- ularis does not overpower the deltoid group and adduct the hu- merus relative to the scapula at the very last of the powered phase of the jump. Contraction of the M. acromiodeltoideus probably continues dur- ing the first part of the coasting phase of the jump, or until the initiation of the flick phase (Fig. 36, between G and H). Activity depicted at Fig. 361 suggests the muscle again stabilizes the dorsal locking of scapula and humerus prior to the downstroke. Only slight activity is apparent in the first downstroke, but contraction again occurs at the last of the downstroke and onset of the up- stroke, and continues to the initiation of the flick phase (Fig. 36, K to between L and M). Contraction at the end of the upstroke again indicates stabilization of dorsal locking of scapula and hu- merus. The muscle probably functions to supinate and abduct the brachium during the very last of the downstroke and first half of the upstroke. Final positioning of the brachium prior to the down- stroke appears to be the function of the M. latissimus dorsi and M. teres major. M. spinodeltoideus (Fig. 42).—Origin is by a tendinous raphe over the scapular spine and then along the dorsal aspect of the thick- ened medial scapular border to its posterior tip. Insertion is by a flat tendon posterior to the proximal 2.5 mm of the insertion of the M. acromiodeltoideus. The spinodeltoideus is relatively thin and situated to slightly abduct, flex, and supinate the humerus. An electromyographic re- cording during a jump into flight (Fig. 37) illustrates contractions similar to those of the M. acromiodeltoideus (Fig. 36). Initially, there is a contraction that, along with the other deltoid muscles, probably stabilizes the locking of the humerus and dorsal scapular border. The contraction continues during the powered phase of the jump, but becomes less intense over the last half of the adduction of the brachium (Fig. 37F). At the beginning of the coasting phase (Fig. 37G), contraction aids the supination and perhaps the abduction of the brachium. In the flick phase, slight contraction apparently 88 Spec. Publ. Amer. Soc. Mamm. 6 20msec eee tc, Sa ne atte ‘ pir fee suet ght — Apa or yy ! I ! | I ! ! ! I ! ! | | | I | | I AY Bac D CE Ei GOW Sheed) cK SB Me ENS £0 P Q R Fic. 37. Electromyogram of right M. spinodeltoideus of Desmodus and corre- sponding locomotor behavior. The contraction of the muscle occurs slightly after the electrical event and is shown as a solid line above the electromyographic re- cording. Corresponding locomotor stages and portions of the electromyogram are indicated by the same letters. Altenbach—V ampire Locomotor Morphology 89 helps pull the brachium mediad prior to the downstroke (Fig. 37I- J). The supinating force imparted by this contraction is probably offset by the pronating force of the M. latissrmus dorsi, M. teres major, and M. pectoralis. With the wing at the level of midbody, another contraction occurs that probably tends to reduce some of the pronation imparted by the M. pectoralis and conforms the wing into more of a lift-generating structure (Fig. 37K to between L and M). As the humerus probably is locked with the dorsal scapular border at this point, this contraction does not detract from the adductive forces applied to the brachium. The contraction contin- ues into the first phase of the upstroke to help supinate the wing and again in the flick phase to position the brachium for the down- stroke. Another contraction early in the downstroke (Fig. 37P-Q) probably reinforces the scapulo-humeral locking and stabilizes the arm against some of the pronating force applied by the M. pecto- ralis. M. teres minor.—The origin is on the posterodorsal aspect of the rim of the glenoid fossa and onto the tendon of origin of the long head of the M. triceps brachii. Insertion is on the dorsal surface of the greater tuberosity of the humerus for 1.5 mm distal to the insertion of the M. infraspinatus. The small teres minor is a weak supinator and flexor of the humerus. Suprascapular Group M. supraspinatus (Fig. 42).—The origin is from the medial 3 mm of the supraspinous fossa and adjacent ligamentous raphe over the scapular spine, and from the dorsolateral aspect of the scapular flange. Insertion is by a heavy tendon onto a groove on the medial surface of the greater tuberosity of the humerus. As in other bats (Vaughan, 1959; Norberg, 1970b), the supra- spinatus abducts, slightly supinates, and extends the humerus. Along with some of the deltoid group (Figs. 36-37), it probably stabilizes the dorsal locking of the scapula and humerus and helps abduct the humerus relative to the scapula during the upstroke in forward flight. In terrestrial locomotion, it is best suited to swing the humerus forward and, by supinating and slightly abducting the humerus, to lift the carpus off the substrate for the forward swing. In terrestrial feeding postures, when the short axis of the scapula is oriented nearly vertically, this muscle, along with the M. 90 Spec. Publ. Amer. Soc. Mamm. 6 infraspinatus and M. subscapularis, is important in moving the pec- toral limb. M. infraspinatus (Fig. 42).—Origin is from the lateral aspect of the scapular spine; lateral aspect of the medial border posterior to the spine; dorsal base of the posterior caritilaginous extension; medial aspect of the lateral border to within 3 mm of the origin of the M. triceps brachii, long head; and surfaces of the three facets (Fig. 26). Insertion is by a thick tendon, a millimeter wide, onto the dorsal aspect of the tip of the greater tuberosity of the hu- merus. The posteriorly elongate scapula in Desmodus positions the origin of the infraspinatus relatively far posterior to the insertion. The insertion on the dorsal aspect of the greater tuberosity also is dis- placed well above the fulcrum at the center of the head. Thus this muscle is the most powerful supinator of the brachium and no doubt functions in the last part of the downstroke and first part of the upstroke to raise the forearm and hand anteriorly to the body. As this muscle is not situated to provide much abductive force to the humerus, it is probably relatively important in the last half of the downstroke in counteracting the pronating forces ap- plied by the M. pectoralis, and helps position the wing into a lift- generating configuration (Fig. 19). Triceps Group M. triceps brachu, caput lateralis (Fig. 43).—The origin is from a strip a millimeter wide along the posterior surface of the humerus beginning at the base of the lesser tuberosity and extending dor- sally to the level of the top of the head. Insertion is by a large sesamoid onto the olecranon process of the ulna. M. triceps brachu, caput medialis (Fig. 43)—The origin extends over 13 mm of the posterodorsal surface of the humerus beginning 2 mm lateral to the head. A second group of short fibers, assumed to be part of this head, originates along the posterior aspect of the distal half of the humerus and inserts into the common tendon to the olecranon process of the ulna. Insertion is by a large sesamoid onto the olecranon process of the ulna. M. triceps brachu, caput longus (Fig. 43).—Origin is by two slips from the two tubercles, 1.5 mm apart, posterior to the posterior border of the glenoid fossa of the scapula. Insertion is by a large sesamoid onto the olecranon process of the ulna. Altenbach—V ampire Locomotor Morphology 9] Fic. 38. Electromyogram of right M. triceps brachii, long head, of Desmodus and corresponding locomotor behavior. The contraction of the muscle occurs slightly after the electrical event and is shown as a solid line above the electromyographic recording. Corresponding locomotor stages and portions of the myogram are in- dicated by the same letters. 92 Spec. Publ. Amer. Soc. Mamm. 6 An electromyographic record of the long head of the triceps muscle during a jump into forward flight reveals a contraction that begins during the inclination of the brachium and continues until contact with the substrate is broken (Fig. 38B-—G). After only a short period of quiesence during the first of the coasting phase (Fig. 38G—H) when contraction of the M. biceps brachu flexes and begins supination of the forearm (Fig. 40G—H), contraction begins to extend the forearm (Fig. 38H-I). The electromyogram shows an increase in amplitude that probably represents greater strength of contraction during the flick phase (Fig. 38I—K), where the fore- arm is fully extended along with the digits to provide forward thrust and to help position the wing for the first downstroke. The contraction continues during the first half of the downstroke and maintains the full extension of the arm (Fig. 383K—M). Past the level of midbody, contraction ceases and the M. biceps brachu (Fig. 40L— N) begins flexion of the forearm that continues through the first third of the upstroke. Contraction of the triceps begins at about the second third of the upstroke, stops for a few milliseconds, and then continues during the flick phase and the first half of the next downstroke (Fig. 38O-R). Although the electrodes were in the long head of the triceps, one of the leads was near (and possibly may have contacted) the posterodorsal aspect of the lateral head, and may have monitored some of its electrical activity. Although the function of the three heads may be slightly different, the nearly inseparable contact of the bellies, the close approximation of the origin of the long, lat- eral, and most of the medial head, and their common insertion on the olecranon process, suggest that their action is functionally and temporally quite similar. The long head may function to slightly flex the brachium but, because the mechanical advantage is poor for this movement, it could be easily counteracted by the scapular musculature. The large sesamoid in the insertional tendon is contoured to fit closely the concavity on the posterior side of the distal articular surface of the humerus and suggests that considerable tension is applied by this muscle group. The jump is certainly the most de- manding of the triceps, as it is the third largest muscle powering the jump and since it must move the forearm through an arc of about 140 degrees. Altenbach—Vampire Locomotor Morphology 93 Extensor Group of the Forearm M. extensor carpi radialis brevis (Figs. 46, 48).—The origin is by a tough tendon on the medial edge of the dorsal epicondyle of the humerus. Insertion is on a large tubercle on the anterodorsal base of metacarpal III by a heavy tendon and onto the dorsolateral tip of the trapezium by a rather elastic band of connective tissue. By extending the third digit, this muscle extends the fifth digit and aids the M. extensor carpi radialis longus in extending the re- mainder of the hand-wing. A detailed discussion of both muscles is included with the discussion of the M. extensor carpi radialis longus below. M. extensor carpi radialis longus (Figs. 46—48).—Origin is by a heavy tendon on the medial aspect of the dorsal epicondyle of the humerus. Insertion is onto the anterodorsal base of metacarpal II and into a depression in the lateral base of metacarpal I by a heavy tendon. In Desmodus, as in other species of bats (Vaughan, 1959; Nor- berg, 19705), this muscle and the adjacent M. extensor carpi radialis brevis are the largest muscles in the forearm. Although their origins are displaced mediad to the center of rotation of the elbow joint, the extremely large size of the bellies and the lack of a tough connective tissue covering found in many other bats suggests that these muscles are well suited to act independently of movements at the elbow. Vaughan (1959) pointed out that in other species of bats, such as Eumops perotis, Myotis velifer, and Macrotus waterhousu, these muscles can act as relatively inelastic bands and automatically extend the chiropatagium as the elbow is extended. This helps concentrate the weight toward the body and eliminate weight in the wing. The terrestrial propensity of Desmodus, and particularly its jumping behavior, necessitate complete independence of move- ments of the hand from movements of the rest of the arm, al- though there appears to be a sacrifice of added weight in the wing. The muscles are certainly stretched by extension of the elbow, but the elastic components appear to absorb this movement and allow the hand to remain folded against the forearm. This feature may help explain the strong and mechanically advantageous insertion of some of the flexors of the hand that have to hold the hand flexed while the arm is fully extended, as in terrestrial feeding 94 Spec. Publ. Amer. Soc. Mamm. 6 B D F H 2mv|_ ' 1 1 ! 1 1 l I 20 msec Fic. 39. Electromyogram of right M. extensor carpi radialis longus of Desmodus and corresponding locomotor behavior. The contraction of the muscle occurs slightly after the electrical event and is shown as a solid line above the electromy- ographic recording. Corresponding locomotor stages and portions of the myogram are indicated by the same letters. Altenbach—V ampire Locomotor Morphology 95 posture or in the powered phase of the jump. This muscle begins contraction during the powered phase of the jump and continues until late in the first downstroke (Fig. 39, B to between I and J). Shortly after the start of the coasting phase (Fig. 39E), partial ex- tension of the digits is evident; however, I cannot fully explain the early initiation of contraction. Perhaps co-contraction of antago- nists tends to brace the carpus as the thrust of the pectoral limb is directed against it and the thumb. The greater number of spikes in the electromyogram indicate that the contraction during the flick phase is stronger than that before it, suggesting that perhaps the movement meets considerable resistance. The muscle is quiescent in the last of the downstroke and first half of the upstroke (Fig. 39I-K), but contracts during the last of the flick phase and through the first half of the next downstroke (Fig. 39, between K and L—-N). The sequence of contraction is essentially similar during the last of this cycle as in the one pre- ceding it. Although no electromyographic data are available for the M. extensor carpi radialis brevis, 1 assume its function is similar to that of the M. extensor carpi radialis longus. M. supinator (Fig. 46).—Origin is by a heavy tendon onto the center of the dorsal (lateral) epicondyle of the humerus. Insertion is over 10 mm of the anterior surface of the radius beginning 3 mm distal to its proximal articular surface. As in other bats, this muscle originates by a tendon that contains a sesamoid bone and is a flexor of the forearm. The muscle lacks good mechanical advantage for this action. Thus it probably func- tions mainly to brace and stabilize the elbow joints as strong su- pinating forces, applied proximally to the humerus, raise the flexed forearm as in the first half of the upstroke (Fig. 20). The relatively large size of this muscle suggests the importance of this function. M. extensor pollicis brevis (Fig. 48).—Origin is along 10 mm of the interosseus surface of the ulna beginning 3 mm distal to the tip of the olecranon process. Insertion is by a tendon heavily bound to the anterodorsal aspect of the carpus and metacarpal I, which at- taches on the dorsal aspect of the proximal base of the first phalanx of digit I. This muscle extends the thumb and, if resisted by the flexors of the first metacarpal, extends the phalanges of the thumb. Desmodus commonly rests much of its weight on the distal pad at the meta- 96 Spec. Publ. Amer. Soc. Mamm. 6 carpophalangeal junction of digit I during terrestrial locomotion or when standing (Fig. 2), and this muscle is necessary in elevating the claw during movements of the limb from this position. When Desmodus is walking on a nervous or easily aroused host animal prior to feeding, the claws may be elevated to minimize stimulation of the skin of the host. M. abductor pollicis longus (Fig. 49).—Origin is on 7 mm of the interosseus surface of the ulna and along 16 mm of the interosseus surface of the radius beginning at the medial contact of the radius and ulna. Insertion is by a thick tendon on the anterior tip of the scaphoid. The tendon divides proximal to the scaphoid and another branch runs forward, inserts onto the ventromedial sesa- moid on the distal tip of metacarpal I, and sends fibers into the pad at the metacarpophalangeal joint of digit I. The tendon, which inserts on digit I, probably is the remnant of the M. abductor pollicis brevis, which has become tendinous and shifted its origin from the scaphoid directly to the tendon of the M. abductor pollicis longus. No doubt the elongation of the first digit in Desmodus and its use in jumping have necessitated the reduction of the M. abductor pollicis brevis to a tendon. The large and relatively long belly of the M. abductor pollicis longus on the forearm is better suited to provide power through a wide arc of movement than is a shorter and much smaller muscle originating on the hand. By becoming tendinous and shifting its origin directly to the tendon of the M. abductor pollicis longus, the M. abductor pollicis brevis allows more powerful movement of the thumb. Although no electromy- ographic data are available, it is evident that the M. abductor pollicis longus serves two important functions. Its contraction pulls the scaphoid mediad over the lunar and thus puts tension on the M. abductor digiti quinti (Fig. 49), which originates from the scaphoid, and puts tension on the pisiform itself. As Vaughan (1959) noted, this is important in bracing the fifth metacarpal and basal phalanx of digit V against upward deflection during adduction of the wing. In addition, the M. abductor pollicis longus pulls the first metacarpal ventrad and is important in terrestrial locomotion. In terrestrial feeding postures, or in terrestrial locomotion with the body held high above the substrate, this muscle shifts the weight from the basal to the distal thumb pad thus elevating the bat higher. Con- traction also aids in keeping the wing folded by flexing the fifth digit through tension on the M. abductor digiti quinti. During the Altenbach—V ampire Locomotor M orphology 97 last of the power phase of the jump, the M. abductor pollicis longus, along with the M. flexor digitorus profundus and M. palmaris longus, pull the thumb ventrad to provide the last upward thrust. In addition, all of these muscles produce flexion of at least one digit besides the first, thus helping to keep the remainder of the hand folded. M. extensor digiti quinti proprius (Fig. 48).—Origin is by a thin tendon onto the distal edge of the dorsal (lateral) epicondyle of the humerus. Insertion is onto the dorsal aspect of the proximal tip of the second phalanx of digit V by a broad tendon. At the point where this tendon meets the dorsal surface of the fifth metacarpal, it is joined by a small tendon of the M. extensor digitorum communis. This muscle deflects the phalanges of digit V upward and tends to elevate the metacarpal slightly. The relative size of the belly and the insertional tendon suggest this movement is important. High-speed photographs of Desmodus in flight (Fig. 19) show that during the first half of the downstroke the phalanges of digit V are deflected upward, thus shaping the distal plagio- patagium and medial chiropatagium into a thrust-generating structure similar to that of the distal chiropatagium. Contraction of this muscle, combined with the passive forces from the air pres- sure, would cause the upward deflection to be greater than that from the air pressure alone and would shape that part of the wing into a more efficient thrusting configuration. Simultaneous con- traction of the M. abductor digiti quinti, M. opponens digiti quinti, and M. abductor pollicis longus would overpower the M. extensor digiti quinti proprius, flex the phalanges, depress the metacarpal, and sta- bilize the phalanx against the metacarpal. M. extensor digitorum communis (Figs. 46, 48).—Origin is by two separate bellies with tendinous origin on the dorsal (lateral) epi- condyle of the humerus and fleshy origin beginning 6 mm distal to the proximal tip of the radius, and extending distad along the dorsal surface of the radius for 14 mm. Insertion is through a tendon to digit III, which runs along the dorsal aspect of the meta- carpal and sends fibers to the proximal tips of the first and second phalanges. The primary insertion of the tendon is on the postero- dorsal aspect of the proximal tip of phalanx three. The tendon to digit IV inserts on a tubercle on the dorsolateral aspect of phalanx one, 2 mm distal to the proximal base. The tendon to digit IV divides distal to the carpus and sends a 98 Spec. Publ. Amer. Soc. Mamm. 6 branch to the tendon of the M. extensor digiti quinti proprius at its proximal contact with the metacarpal, thus it aids in dorsal deflec- tion of the phalanges of digit V. The connections to digits III and IV dorsally deflect the phalanges and slightly deflect the metacar- pals. In the downstroke in forward flight (Fig. 19), the M. extensor digitorum communis probably aids the force of the air stream in the upward deflection of the phalanges to provide the propeller effect and upturned configuration of the distal chiropatagium between digits III and IV, which perhaps function to reduce tip vortices. It also provides downward acceleration of air and lift production in the last of the downstroke. More important, however, is the function of this muscle in the flick phase of the upstroke. During the first of the flick (Fig. 20N—P), when the forearm is extended, the phalanges of digits III to V are deflected ventrally by the force of the air and perhaps by contraction of the flexors of the digits. As the flick nears completion, the phalanges are fully extended to provide the last component of forward thrust and help to position the wing for the downstroke. This movement appears to be par- tially active and not simply the result of upward air pressure as adduction begins. M. extensor carpi ulnaris (Figs. 46—49).—Origin is from the deep groove and adjacent ridge on the proximal 6 mm of the postero- ventral surface of the ulna. Insertion is by a heavy tendon on the tubercle on the dorsomedial aspect of metacarpal V, 2 mm distal to its proximal tip. This muscle is a powerful flexor of digit V and, because of lig- aments that join the proximodorsal surfaces of metacarpals III and V, the entire hand-wing. In the distantly related phyllostomatid bat, Macrotus, this muscle inserts on metacarpal V but is an exten- sor. In Eumops perotis and Myotis velifer (Vaughan, 1959), this mus- cle inserts on metacarpal III and is a flexor. In Plecotus auritus (Norberg, 19706), the muscle inserts on metacarpal III and is an extensor. The tendon is the thickest one to the hand, and the belly is quite large. When the forearm is extended with the wing folded as in terrestrial feeding postures or in parts of the climbing and walking cycles (Figs. 2, 4, 6), the large M. extensor carpi radialis longus and M. extensor carpi radialis brevis are stretched and apply some passive, extensive forces to the hand. This muscle is no doubt necessary to resist these forces and keep the wing folded. Inasmuch as the radial extensors of Desmodus are not heavily invested in Altenbach—V ampire Locomotor Morphology 99 connective tissue, they are probably rather elastic and thus do not explain the need for the massive tendon of the M. extensor carpi ulnaris. However, in landing on the ground, it is critical for the wing to be quickly folded against the forearm to prevent injury to the digits. It is also important for the wing to remain tightly folded during terrestrial locomotion. The insertion seems well suited for effecting such a rapid and powerful movement. M. extensor indicis (Fig. 48).—Origin is on 14 mm of the postero- dorsal surface of the radius to within about 4 mm of the distal articular surface and on 9 mm of the interosseus surface of the ulna, beginning about 8 mm distal to the proximal articulation of the radius and ulna. Insertion is at several points. At the level of the proximal carpus, the tendon gives rise to a sheet of tendon that inserts on the anterodorsal carpus and dorsomedial aspect of the proximal half of metacarpal I. Another colateral tendon arises from the main tendon and runs to the dorsolateral aspect of the distal third of metacarpal I. The main tendon inserts by way of a sesamoid on a tubercle on the anterodorsal surface of metacarpal II, 3 mm distal to its proximal base. At the level of the sesamoid, small tendinous attachments run from the main tendon postero- laterad to insert on the dorsal aspect of the bases of metacarpals III and IV. This muscle functions with the M. extensor carpi radialis longus and M. extensor carpi radialis brevis to extend the hand-wing during the coasting phase of the jump, and during the flick phase and first half of the downstroke in forward flight. The attachments to the dorsal aspect of the third and fourth metacarpals suggest it also is important in bracing the hand against posterior and dorsal air pressure during the flick phase of the upstroke, when the digits are extended and the wing is strongly pronated and abducted. The attachments to the first digit probably help raise it when the hand is flexed by the M. extensor carpi ulnaris, as occurs in terrestrial locomotion. Pectoralis Group M. subclavius (Figs. 44—45).—Origin is by a fleshy attachment to the ventral aspect of the first costal cartilage adjacent to its attach- ment to the manubrium and by tendinous attachment to the an- terolateral border of the first costal cartilage. Insertion is on the 100 Spec. Publ. Amer. Soc. Mamm. 6 posteroventral surface of the clavicle from its distal tip to within 2 mm of its articulation with the manubrium. Because of the relatively free articulation of the clavicle and scapula, this muscle is important in both jumping and flight. Con- traction pulls the distal tip of the clavicle ventrad and slightly pos- teriad, and can effectively brace the clavicle when co-contracting with the M. clavotrapezius. Slight dominance of one or the other could swing the clavicle dorsad or ventrad and still stabilize it as a solid fulcrum for movements of the scapula and arm. High-speed photographs of a jump show that the shoulder joint is depressed, and although no direct evidence is available, this movement ap- pears to be partly the result of depression of the tip of the clavicle by this muscle. The electromyographic data for the M. clavotra- pezius (Fig. 32) indicate contraction during all but the last of the powered phase of the jump, but such contraction is necessary to stabilize the clavicle and could be overpowered by the M. subclavius. Seemingly the subclavius is not opposed by the clavotrapezius at the last of the powered phase of the jump and probably depresses the clavicle. M. pectoralis.—This muscle appears to be divided into three ma- jor bellies in Desmodus. However, I distinguish only between cla- vicular and sternal portions, as the clavicular portion is widely sep- arate from the remainder of muscle. As Vaughan (1959) described for other species of bats, I have noted considerable individual vari- ation in the degree of separation and arrangement of the non- clavicular portion and consider it the posterior (sternal) division. M. pectoralis, anterior (clavicular) division (Fig. 44).—Origin is on the anteroventral aspect of the proximal base of the clavicle and along the anterior and ventral aspect of the proximal half of its shaft. Insertion is from the dorsal aspect of the medial tip of the pectoral ridge, laterally for about 9 mm, superficial to the insertion of the posterior (sternal) division of the M. pectoral. The clavicular M. pectoralis pulls the humerus craniad and ad- ducts and pronates it slightly. This movement is not part of the normal wingbeat cycle or of a jump, but occurs as the limb is positioned prior to alighting on a horizontal surface (Fig. 23) and in backward climbing (Fig. 6). In terrestrial locomotion, this muscle probably functions along with the M. clavodeltoideus to swing the humerus forward in the recovery stroke (Fig. 4). When cocontract- ing with the sternal division of M. pectoralis, the clavicular division Altenbach—V ampire Locomotor Morphology 101 can assist in adduction and pronation of the humerus and is prob- ably responsible for much of the cranial inclination of the path of the wing in the last half of the downstroke (Fig. 19). M. pectoralis, posterior (sternal) division (Fig. 44).—Origin of one belly is on the lateral aspect of the ventral arm of the manubrium, the ventral aspect of the lateral arms to within 2 mm of their distal tips, and the ventrolateral aspect of the posterior arm; that of the other belly is on the ventral aspect of the body of the sternum to within 2 mm of the posterior tip of xiphisternum and on a ten- dinous raphe over the midline, beginning anteriorly on the tip of the ventral arm of the manubrium and extending posterior to the posterior tip of the body of the sternum. Insertion is onto the ventral half of the anterior face of the proximal end of the pectoral ridge and laterally for 10 mm along the anterior and ventral edge of the pectoral ridge. The bellies of this massive muscle are the major adductors and pronators of the humerus, and consequently of the arm and hand. The origin over the manubrium, body, and xiphoid process of the sternum makes this muscle effective in moving the humerus through a variety of planes, as Vaughan (1959) pointed out for other species. However, photographic evidence for Desmodus in flight indicates that there is relatively little variability in the plane through which the wing is adducted. The heavy wing loading in this species (Hartman, 1963), combined with the proportionally large meals that are consumed (Wimsatt, 1969), seem to have re- sulted in relatively unvarying wingbeat patterns as opposed to hov- ering, nectar-feeding species such as Leptonycteris sanborni (Alten- bach, 1968). Along with the M. serratus anterior, posterior division, the sternal M. pectoralis adducts the humerus during the powered phase of the jump. It is doubtful that the angle of the jump is controlled by the M. pectoralis, as a jump, particularly when the bat has a full stomach of blood, probably requires contraction of the entire mus- cle. Variation in the rotation of the humerus during the jump is likely under the control of the M. subscapularis, suprascapular group, deltoid group, clavicular M. pectoralis, and M. latissimus dorsi. During the wingbeat cycle, the strong pronation of the arm and hand, which orients the wing into a thrusting configuration during the first half of the downstroke, is a result of contraction of the 102 Spec. Publ. Amer. Soc. Mamm. 6 sternal division of M. pectoralis. There is perhaps more variability in the function of this muscle during a wingbeat cycle than in a jump. Greater contraction of specific parts of the muscle mass can vary the degree of pronation and the plane of adduction of the wing. As in a jump, the rotational stability is also controlled by the supraspinatus, infraspinatus, subscapularis, deltoid group, clavic- ular M. pectoralis, and M. latissumus dorsz. In terrestrial locomotion, the sternal M. pectoralis probably sup- ports most of the weight directed against the pectoral limbs. When the bat is in elevated walking postures or standing in terrestrial feeding posture with much of the weight probably supported by the clavicle and posterior division of the M. serratus anterior, moving the brachium is the task of the clavicular M. pectoralis, deltoid group, and M. latissimus dorst. Sudden movements from these pos- tures would seemingly require the power of the sternal M. pecto- ralas. M. pectoralis abdominalis (Fig. 44).—Origin is on the abdominal fascia beginning 2.5 mm lateral to the midline at the level of the posterior tip of the xiphoid process and extending posterolaterad for roughly 9 mm. Insertion is by a flat tendon, which attaches to the medial 2 mm of the ventral aspect of the pectoral ridge pos- terior to the insertion of the M. pectoralis. As in other species, the M. pectoralis abdominalis is a rotator (pro- nator) and flexor of the humerus. During the downstroke it can increase pronation to form more of the medial wing into a thrust- ing attitude or can oppose the supinating force exerted by the M. biceps brachu. The pronation during the flick phase is probably aided by this muscle along with the M. latissimus dorsi and M. teres major. In terrestrial locomotion, the power stroke of the pectoral limb is probably aided by this muscle as it pronates and flexes the hu- merus. The forearm is forced downward and posteriad by this movement, thus driving the body forward. Flexor Group of the Arm M. coracobrachialis (Fig. 45).—Origin is on the dorsal third of the anterior face of the coracoid process. Insertion is over about 4 mm of the anteroventral surface of the humerus beginning approxi- mately 11 mm lateral to the medial end of the pectoral ridge. Altenbach—V ampire Locomotor Morphology 103 2mv| 20 msec SN a lc eet awe lin Wh mibcieretas aehme caret eT A BCODEFGHitJsés KLMNOPQRS TU-YV Fic. 40. Electromyogram of right M. biceps brachii, coracoid head, of Desmodus and corresponding locomotor behavior. The contraction of the muscle occurs slightly after the electrical event and is shown as a solid line above the electromy- ographic recording. Corresponding locomotor stages and portions of the electro- myogram are indicated by the same letters. The M. coracobrachialis is a rather weak adductor and extensor of the humerus. It probably aids in adduction of the wing and exerts a stabilizing force to the brachium. M. biceps brachu (Figs. 42, 44—47).—The origin of the coracoid 104 Spec. Publ. Amer. Soc. Mamm. 6 head is on the posterior and lateral aspect of the ventral three- fourths of the tip of the coracoid process. The origin of the glenoid head is by a tough tendon from the tubercle a millimeter anterior to the glenoid fossa on the lateral aspect of the base of the coracoid process. Insertion is by a heavy tendon that runs over the ridge on the proximal end of the radius and attaches into the flexor fossa on the posterior side of the radius. As in other bats (Vaughan, 1959; Norberg, 1970b), the bellies of the biceps are flexors of the forearm and, because of the articu- lation of the radius and humerus that allows only flexion and ex- tension, supinators of the arm. Electromyographic data from a jump into flight were recorded from electrodes in the coracoid head, but probably are representative of the function of both heads. There is little or no activity during the powered phase of the jump (Fig. 40D-G) and the first contraction is a short burst during the initial part of the coasting phase, which flexes the fore- arm (Fig. 40G—H). Contraction again begins at the first of the downstroke and continues until the beginning of the flick phase of the upstroke (Fig. 40K—N). When opposed by contraction of the M. triceps brachu, the biceps causes adduction of the arm and, as Vaughan (1959) pointed out, provides rotational stability as it op- poses the pronating forces applied by the M. pectoralis. When the M. triceps brachu ceases contraction in the last half of the down- stroke (Fig. 38), the biceps flexes and supinates the arm (Fig. 40L-— N). The function is similar in the next two cycles (Fig. 40O-V). M. brachialis (Figs. 46—47).—Origin is over about 9 mm of the anterior face of the humerus beginning 12 mm lateral to the distal end of the pectoral ridge. Insertion is into the flexor fossa of the radius in common with the tendon of the M. biceps brachu. This muscle probably assists in the flexion and stabilization of the fore- arm, as suggested in other species of bats (Vaughan, 1959, 1970c; Norberg, 1970b). No electromyographic data are available. Flexor Group of the Forearm M. flexor carpi ulnaris (Figs. 47, 49).—Origin is on the ventral aspect of the ulna from its medial tip laterally for 5 mm and on the adjacent M. palmaris longus about 4 mm distal to its origin. Insertion is onto the posteromedial surface of the pisiform a third of the distance to its ventral tip. Altenbach—V ampire Locomotor M orphology 105 As in several other species of bats (Vaughan, 1959), this is a flexor of the fifth metacarpal and thus the hand, because forces applied to the pisiform are transmitted to the fifth metacarpal. However, the belly is relatively small and the tendon is extremely thin, indicating that the duty of flexion of the fifth metacarpal has been taken over by other muscles such as the M. extensor carpi ulnaris. As in Macrotus (Vaughan, 1959), the origin allows complete independence of movement at the elbow and facilitates the ab- duction of the extended hand-wing anterior to the body to provide low drag on the upstroke. M. palmaris longus (Figs. 47, 49)—Origin is by a heavy tendon on the distal tip of the spinous process of the ventral (medial) epicondyle of the humerus and from the ventral side of the prox- imal 6 mm of the M. flexor digitorum profundus. Insertion is by an aponeurosis onto the basal and distal thumb pads, on the ventral sesamoids at the first metacarpophalangeal junction, on the ante- rior face of metacarpal II, about 13 mm distal to its base, and on the ventral aspect of the proximal few millimeters of metacarpals III and V. The relatively heavy attachments on the first digit and the rather large belly of the palmaris longus in Desmodus suggest that this muscle is important in ventral flexion of the thumb during the jump and perhaps in terrestrial locomotion. The attachments on the second and third metacarpals are suited to flex them toward the radius and probably aid the M. flexor carpi radialis, M. flexor carpi ulnaris, and M. extensor carpi ulnaris in keeping the wing tightly folded during the jump and in terrestrial locomotion. When the hand is fully extended in flight, the radial extensors of the hand easily overpower this muscle, but it can function to ventrally brace the second and third metacarpals against the force of the air stream and help strengthen the leading edge of the wing. The attachment to the fifth metacarpal probably serves a relatively passive bracing function, as it is not suited to flex the metacarpal toward the radius. The electromyographic data for the palmaris longus are not ideal, because the bat did not fully extend the left wing during most of the flight. However, the recorded activity of the muscle is probably similar to that in normal locomotor activity. Sporadic con- traction occurs during the step and partial hop before the bat jumps into flight (Fig. 41A—G) and during the powered phase of the jump (Fig. 41 H-I). The flick phase does not seem typical (par- 106 Spec. Publ. Amer. Soc. Mamm. 6 20 msec Fic. 41. Electromyogram of right M. palmaris longus of Desmodus and corre- sponding locomotor behavior. The contraction of the muscle occurs slightly after the electrical event and is shown as a solid line above the electromyographic re- cording. Corresponding locomotor stages and portions of the electromyogram are indicated by the same letters. Altenbach—V ampire Locomotor Morphology 107 a clavotrapezius occipito-pollicalis rhomboideus omocervicalis levator scapulae acromiotrapezius spinodeltoideus acromion proc. supraspinatus acromiodeltoideus () p " infraspinatus clavodeltoideus Pp medial scapular border triceps lateralis FG ANY, 7q N triceps longus spinodeltoideus teres major serratus anterior, post. div. latissimus dorsi i spinotrap. (cut) biceps brachii lat. dor. (cut) spinotrapezius Fic. 42. Dorsal view of pectoral girdle musculature of Desmodus. Superficial muscles (left of midline) and view with M. acromiotrapezius, M. spinotrapezius, M. latissimus dorsi, and M. acromiodeltoideus removed (right of midline). ticularly the movements of the right wing with the implanted elec- trodes), but contraction occurs through this phase, perhaps to “fa- vor” the wing and keep it partially flexed (Fig. 41L—N). Contraction again occurs 1n the first half of the downstroke and ceases until the middle of the upstroke, when a short burst occurs, perhaps to partially flex the digits and “cock” them for extension in the flick phase (Fig. 410-S). The contraction at the beginning of the flick phase may be to resist the radial extensors and let their contraction build up maximal tension before relaxation of the palmaris, and perhaps other flexors, suddenly releases the hand. This could con- tribute to a “snap” of the chiropatagium to provide considerable thrust. The wing is more extended at this point and contraction occurs during the entire downstroke. M. flexor carpi radialis (Figs. 47, 49).—Origin is on the postero- ventral aspect of the proximal half of the belly of the M. pronator teres. Insertion is on a large tubercle on the anteroventral base of metacarpal II. In phyllostomatids such as Macrotus, the insertion of this muscle 108 Spec. Publ. Amer. Soc. Mamm. 6 Scapula humerus triceps brachii lateral head medial head long head medial head B Fic. 43. Ventral view of M. triceps brachu of Desmodus: A, intact; B, medial head removed. is on the third metacarpal (Vaughan, 1959). The insertion on metacarpal II in Desmodus permits the leading edge of the wing to be actively flexed against the radius rather than passively flexed by flexors of the third, fourth, or fifth digits. The position of the insertion also reflects the need to rapidly fold the wing in an alight- ing maneuver and to hold it firmly folded during terrestrial lo- comotion, climbing, and jumping. M. pronator teres (Fig. 47).—Origin is on the tip of the spinous process of the ventral (medial) epicondyle of the humerus. Inser- tion is on 10 mm of the ventral aspect of the radius beginning 8 mm distal to the tip of the spinous process. As the humero-radial articulation allows little but flexion and extension, this muscle acts as a weak flexor and a powerful ventral brace of the radius. In terrestrial locomotion or alighting maneu- vers, forces against the carpus are transferred to the humerus as a strong supinating torque. The elbow must be strongly braced against these forces without excessive connective tissue binding that would reduce mobility. Co-contraction of the M. supinator also stabilizes the radius against the humerus. M. flexor digitorum profundus (Figs. 47, 49).—The origin includes the ulna from 5 mm of its interosseus and ventral surface distal to Altenbach—V ampire Locomotor Morphology 109 its contact with the radius; the tip of the spinous process of the humerus; and a few fibers from the posterior surface of the radius 5 mm distal to the spinous process of the humerus. Insertion is as follows: the tendon divides at the carpus into 1) a heavy tendon that inserts on the middle of the ventral aspect of the first phalanx of digit I (a tiny tendon diverges from this tendon and is the origin for a small muscle inserting on the anterolateral aspect of the distal tip of metacarpal I); 2) a tendon that runs over the pisiform and inserts on the proximoventral tips of the first and second phalanges of digit III; and 3) a tendon of origin for one belly on the M. interossei that inserts on the posterior surface of metacarpal III, 10 mm distal to its proximal base. This rather massive muscle supplies most of the ventral flexive force to the thumb as it provides the last upward thrust in the powered phase of the jump. The attachments to the metacarpal and the two proximal phalanges of digit III flex the third digit and help keep the wing tightly folded during the jump and in terrestrial locomotion. Also, all of the forearm flexors of the thumb, the M. flexor digitorum profundus, M. palmaris longus, and the M. abductor pollicis longus have flexive attachments to at least one of the other digits and help keep the chiropatagium folded against the radius during ventral flexion of the thumb. In flight, contraction of the flexor digitorum profundus would ventrally brace the metacarpal and phalanges of the third digit and could control depression of much of the leading edge of the wing and the degree of upward deflection of the phalanges of digit III by opposing the upward force of the air. Extensors of the Manus M. interosseus dorsale (Figs. 48—49).—Origin is on the posteroven- tral surface of the base of metacarpal II. Insertion is by an apo- neurosis on the anteroventral aspect of the tip of metacarpal III and on the proximal half of the anteroventral surface of the first phalanx of digit III. It seems odd that this muscle should be absent in Macrotus and Myotis (Vaughan, 1959) and present in Ewmops (Vaughan, 1959), Plecotus auritus (Norberg, 1970b), and Desmodus. In Desmodus it pulls the first phalanx of digit III anteroventrad and tightens the chiropatagium between digits III and IV. It also braces the first 110 Spec. Publ. Amer. Soc. Mamm. 6 occipito-pollicalis clavicular pectoralis subclavius clavodeltoideus coracoid process pectoral ridge sternal pectoralis biceps brach. AN seraceiaiaaae -—— Za biceps brachii coracoid head glenoid head serratus ant. ) posterior div. N \ * \ pect. abdom. coraco-cutaneus l pectoralis abdom. | \ \ Fic. 44. Ventral view of pectoral girdle musculature of Desmodus. Superficial muscles (left of midline) and view with M. pectoralis, sternal division, and M. clav- odeltoideus removed (right of midline). phalanx of digit III against upward deflection, and limits upward deflection to phalanges two and three. Flexor Group of the Manus M. abductor pollicis brevis (Fig. 49).—See the account of M. ab- ductor pollicis longus. M. flexor pollicis brevis (Fig. 49).—Origin is by a long tendon from the anteroventral tip of the lunar and from the ligament between the anterolateral tip of the trapezium and the anterior base of metacarpal II. Insertion is on the medial aspect of the distal tip of metacarpal I and on the lateral aspect of the distal tip of metacar- pal I. The two bellies of this muscle are ventral flexors of metacarpal I if contracting simultaneously and, if contracting singly, are ven- trolateral or ventromedial flexors of the first metacarpal. As pow- erful ventral flexion of the thumb is the function of the M. flexor digitorum profundus, M. palmaris longus, and M. abductor pollicis lon- gus, the flexor pollicis brevis probably is more important in moving Altenbach—Vampire Locomotor Morphology Haul clavicle subclavius serratus ant., ant.div. coracoid process subscapularis lesser tuberosity tendon of orig. for y'SS Soe ZN 5 ie cl brach. : biceps brachii coracoid head / serratus ant. a post. div. VA SS IN coracobrachialis biceps brach. glenoid head wi U Fic. 45. Ventral view of deep pectoral girdle musculature of Desmodus. View (left side) with M. pectoralis, sternal division, M. clavodeltoideus, M. pectoralis abdom- inalis, M. pectoralis, clavicular division, removed and view (right side) with the above- mentioned muscles and the M. subclavius and M. biceps brachu, coracoid head, re- moved. the thumb in delicate maneuvers during terrestrial locomotion or climbing. In elevated walking or in a terrestrial feeding posture, this muscle helps shift the weight from the basal pad of the thumb to the distal pad at the metacarpophalangeal junction (Fig. 2C). When the bat feeds from the neck or head of an animal, the thumbs must be moved occasionally to give the claws purchase on the skin or hair, and these muscles probably function in such move- ments. M. adductor pollicis (Figs. 48—49).—Origin is on the anteroventral aspect of metacarpal II, 1.5 mm distal to the insertion of the M. flexor carpi radialis and on the ventral aspect of metacarpal III distal to its articulation with the carpus. Insertion is by an aponeurosis on the dorsolateral aspect of the distal tip of metacarpal I and by a tendon on the dorsal base of the second phalanx of digit I. The more delicate ventrolateral movements of the thumb during terrestrial locomotion, climbing, and perhaps feeding are powered by this muscle and the lateral belly of the M. flexor pollicis brevis. If the first metacarpal is braced by both bellies of the latter muscle, 112 Spec. Publ. Amer. Soc. Mamm. 6 propatagialis proprius e.d.q.p. Fic. 46. Dorsal view of superficial musculature of the right forearm of Desmodus. Abbreviations: e.c.r.b., M. extensor carpi radialis brevis; e.c.r.1., M. extensor carpi radialis longus; sup., M. supinator; e.d.c., M. extensor digitorum communis; e.c.u., M. extensor carpi ulnaris; e.p.b., M. extensor pollicis brevis; e.d.q.p., M. extensor digiti quinti proprius. the M. adductor pollicis could elevate the terminal digit and claw, and draw the entire digit ventrolaterad. M. interosser (Fig. 49).—Individual muscles of this group are as follows: 1) Origin is by a tendon on the ventral tip of the trapezium. Insertion is on the posterior half of the ventral base of phalanx one, digit III. Along with the M. interosseus dorsale, this muscle stabilizes the first phalanx of digit III against deflection upward by the force of the air stream during adduction of the wing. 2) Origin is from the magnum and a tendon from the ventro- lateral aspect of the base of metacarpal IV. Insertion is on the ventrolateral aspect of the tip of metacarpal IV and on the ven- trolateral aspect of the proximal tip of phalanx one. This is a weak flexor of the first phalanx of digit IV and serves, along with the third belly of this group of muscles, to brace the Altenbach—V ampire Locomotor Morphology 113 f. d. p. Fic. 47. Ventral view of superficial musculature of the right forearm of Des- modus. Abbreviations: f.c.r., M. flexor carpi radialis; e.c.r.1., M. extensor carpi radialis longus; p.t., M. pronator teres; f.d.p., M. flexor digitorum profundus; p.l., M. palmaris longus; e.c.u., M. extensor carpi ulnaris; f.c.u., M. flexor carpi ulnaris. fourth metacarpal against upward deflection during adduction of the wing. It also assists in flexing the phalanges as the wing is folded during an alighting maneuver or for terrestrial locomotion. 3) Origin is from the magnum and a small tendon from the ventromedial aspect of the proximal base of metacarpal IV. Inser- tion is on the ventral base of the first phalanx of digit IV by a tendon. This muscle works along with the second belly of this group, and its function is essentially identical. 4) Origin is from a slip of the tendon of the M. flexor digitorum profundus. Insertion is on the posteromedial surface of metacarpal III 10 mm distad to its proximal tip. When the M. flexor digitorum profundus contracts to ventrally flex the thumb during a jump or in terrestrial locomotion, the origin of this muscle is stretched, and the force, transmitted through the belly, flexes the third digit against the radius. Contraction of this belly of the M. interosseus under these conditions applies more force 114 Spec. Publ. Amer. Soc. Mamm. 6 .c.r. |. fan - " , m LE Z ooo ut FAS Tt : 0 add. poll. Fic. 48. Dorsal view of the musculature and tendons of the right carpus of Desmodus. All of the M. extensor indicts, except its major insertional tendon, is re- moved. Abbreviations: e.c.r.l., M. extensor carpi radialis longus; e.c.r.b., M. extensor carpi radialis brevis; e.i., M. extensor indicts (major tendon); e.p.b., M. extensor pollicis brevis; e.c.u., M. extensor carpi ulnaris; e.d.q.p., M. extensor digiti quinti proprius; e.d.c., M. extensor digitorum communis; i.d., M. interosseus dorsale; add. poll., M. adductor pollicis; I-V, metacarpals I-V; 1, 2, phalanges of digit I. and holds the third digit against the radius more firmly. When the wing is extended during the wingbeat cycle, the elastic properties of this muscle allow contraction of the M. flexor digitorum profundus to ventrally brace the third metacarpal and first phalanx of digit III but only apply minimal flexive force. M. abductor digiti quinti (Fig. 49).—Origin is by a tendon from the posterior tip of the scaphoid. Insertion is by a broad aponeu- rosis on the ventromedial aspect of the distal tip of metacarpal V and on the ventromedial base of phalanx one. This muscle is large in Desmodus and is situated to brace the fifth metacarpal against the force of the airstream during adduction of the wing and ventrally flex the first phalanx of digit V. In Macrotus (Vaughan, 1959), this muscle is quite tendinous and acts as an inelastic brace; however, the relatively large, fleshy belly suggests its function is more variable in Desmodus. Relaxation during the first half of the downstroke allows the upward deflection of the phalanges (Fig. 19), which provides thrust from the middle of the wing. Contraction ventrally flexes the phalanges and shapes this Altenbach—V ampire Locomotor Morphology 115 palm. long. int. (2,3) Fic. 49. Ventral view of the musculature and tendons of the right carpus of Desmodus: A, view of the insertion of the M. palmar longus; B, view of the anatomy with the palmaris removed. Abbreviations: f.c.u., M. flexor carpi ulnaris; abd. p.1., M. abductor pollicis longus (and perhaps brevis); int. (1-4), bellies of Mm. interossez; f.c.r., M. flexor carpi radials; f.p.b., M. flexor pollicis brevis; f.d.p, M. flexor digitorum profundus; add. poll., M. adductor pollicis; abd. d.q., M. abductor digiti quinti; 0.d.q., M. opponens digiti quinti; e.c.u., M. extensor carpi ulnaris; II-V, metacarpals of digits II-V (metacarpal I not visible); 1, 2, phalanges of digit I. part of the wing into a cambered surface suited for production of lift. This function is probably aided by contraction of the M. ab- ductor pollicis longus, which displaces the origin proximally. M. opponens digitt quinti (Fig. 49).—Origin is by a tendon on a tubercle of the posteroventral aspect of the pisiform adjacent to its articulation with metacarpal V. Insertion is by an aponeurosis on the ventrolateral aspect of the tip of metacarpal V. The tendons of this muscle and the M. abductor digiti quinti fuse distally, thus their function is essentially the same. However, be- cause the opponens digiti quinti originates on the pisiform, it is not affected by contraction of the M. abductor pollicis longus and can flex the phalanges of the fifth digit, even if the abductor is relaxed. Co-contraction of all three can powerfully flex the pha- langes and overpower the M. extensor digiti quinti proprius to hold the fifth digit at a high and rigid camber. DISCUSSION Terrestrial Locomotor Behavior pose rotundus is the most terrestrially oriented of bats; its agility in quadrupedal locomotion far surpasses that of other species and even that of many small rodents and carnivores. As several authors have described (Beebe, 1927; Price, 1950; Ditmars and Greenhall, 1935, 1936; Dalquest, 1955; Wimsatt, 1959), it runs along horizontal or vertical surfaces with ease and executes sudden evasive maneuvers that make it difficult to capture. This terrestrial facility is closely involved with feeding behavior, as no other bat except Desmodus (and perhaps the other sanguivorous bats, Diaemus and Diphylla) shows such agility in terrestrial locomotion. Obser- vations of Desmodus scrambling over the backs and necks of host animals prior to feeding (or to avoid movements of the host animal to brush them off), and running or hopping about on the ground while feeding, illustrate the adaptive value of this effective terres- trial locomotion. Although several other species of bats easily move about on the ground and occasionally catch food to alight prior to catching the food, Desmodus, and perhaps to a lesser extent the other two sanguivorous bats, are the only chiropterans that have become so specialized in feeding as quadrupeds. According to Vaughan (1959, 1970d, 1970e), bats probably evolved as crevice dwellers and thus, initially, were adapted for terrestrial locomotion in confined spaces. Even in bats such as Eu- mops perotis, Myotis velifer (Vaughan, 1959), Antrozous pallidus (Burt, 1934), Nyctalus noctula (Anonymous, 1969), Rhinolophus ferrume- quinum (Southern, 1964), and Eptesicus fuscus (Altenbach, 1968), which readily move about in quadrupedal fashion on the ground or other surfaces, the limbs are directed more or less lateral to the body, which is typically held quite close to the surface. The power strokes are directed posterolaterally by flexion and slight pronation of the brachii, extension of the elbows, and by posterior swings of the laterally extended pelvic limbs. These types of movements are necessary in a crevice or in confined roosts, but are inefficient, inasmuch as the weight is supported on laterally directed limbs. The large M. pectoralis is well suited to support much of the weight, 116 Altenbach—V ampire Locomotor Morphology 117 but the muscles that move the limbs have to work against the forces that maintain posture. As described in the section on locomotion, Desmodus inclines the body and holds it well above a horizontal surface when walking or running. The shanks are directed almost vertically, the brachii are directed relatively posterolaterally, and the forearms are partially flexed and directed anteroventrally and slightly laterally. The net result of this posture is that the contact of the limbs with the surface is shifted nearer the body and more below it, requiring less effort to maintain the posture. Thus greater muscular effort can be de- voted to moving the limbs, resulting in more rapid and complex movements. Posteroventral thrusts with both pectoral and pelvic limbs produce a hopping gait that rapidly carries the bat over the ground and allows chasing of host animals. The orientation of the hind limbs makes them well suited to pulling, thus the bats typically climb backwards. The pectoral limbs incline the body away from the surface and aid climbing by for- ward thrusts. With the body in a climbing position, the pectoral limbs are able to thrust the bat outward into flight or laterally in an avoidance reaction. There are few records of predators feeding upon bats in roosts, thus the agility on vertical surfaces in roosts appears to be a secondary advantage of locomotor mechanisms evolved for terrestrial feeding. Desmodus regularly consumes a large volume of blood, often as much as 100 per cent of its body weight, in a single feeding period (Wimsatt, 1969). This, and the habit of feeding from the ground or moving about on the ground between feeding periods, require the ability to launch into flight from the ground when heavily loaded. Host species, such as large ungulates, often are found in the open and some distance from trees or rock outcrops on which the bats could climb and from which they could drop into flight. Many other species of bats require a drop from a roost to build the air speed necessary for flight. Bats other than Desmodus that can fly from the ground, such as some nectar feeding species (Lep- tonycterts, Glossophaga) and lightly-loaded insectivorous taxa (Antro- zous, Myotis, Plecotus), push off from the surface with partially or fully extended wings and begin flight with a lift-generating wing- beat cycle. The ability to shift the pectoral limbs almost directly under the 118 Spec. Publ. Amer. Soc. Mamm. 6 body and several other anatomical modifications allow Desmodus to achieve flight from the ground by a powerful jump, which carries it, even when fully gorged on blood, high enough above the surface to initiate a high-amplitude wingbeat cycle. The jump is effected by a powerful adduction of the brachii, extension of the elbows, and ventral flexion of the thumbs. The extreme elongation of the thumbs, which are proportionally longer than in any other bat, provides a long lever arm for this flexive movement that adds the final upward momentum during the jump. The pelvic limbs supply little of the upward thrust, as they function primarily to shift the center of gravity over the powerful pectoral limbs. The jumping behavior also plays an important role in avoiding being stepped on by a large host animal and perhaps avoiding terrestrial predators. Although jumps into flight are directed primarily forward and upward, a direction that allows maximal thrust from the pectoral limbs, avoidance jumps can occur in any direction. Both avoidance jumps and jumps into flight are powered by the pectoral limbs, while the hind limbs shift the weight into the line of the jump. Alighting maneuvers on a horizontal surface are essentially the reverse of the movements used in a jump into flight. Contact with the substrate is made first with the thumbs. The downward mo- mentum is slowed by muscular resistance to hyperextension of the thumbs, flexion of the elbows, and abduction of the brachu. The movement effectively breaks the force of the landing and is prob- ably advantageous for alighting softly on or near a host animal. Rodney Honeycutt, Ira Greenbaum, and Robert Baker (personal communication) speculate that because obligate blood feeding ap- pears in mammals only in the genera Desmodus, Diphylla, and Diae- mus, these bats probably evolved from a common ancestor that was already a sanguivore. I cannot speculate about the evolutionary development of sanguivory in bats, but I feel that Desmodus is cer- tainly the most derived, from a locomotor morphological stand- point, of the Desmodontinae. The morphological modifications of the limbs and girdles reflect selective pressures somewhat different than those expected to have acted on a bat that typically parasitizes large domestic animals of man. The habit of feeding on large ungulates from the ground, and the ability to feed from relatively active terrestrial rodents, suggest that perhaps the bats initially fed on small terrestrial mammals or other vertebrates and that the facility for terrestrial locomotion Altenbach—V ampire Locomotor Morphology 119 developed in response to this mode of feeding. Seemingly, if the bats had fed initially on large ungulates, they could have readily fed from the back or neck and the ability to run on the ground would not have been necessary. With only a small thrust of the limbs, the bats could have dropped off the back or neck into flight. Thus, the complex energy-demanding jump would not have been necessary. Probably the mechanisms of the jump evolved as a means to rapidly negotiate rough terrain in pursuit of a small mammal or other vertebrate, rather than to avoid movements of larger animals. Elongation of the thumbs, no doubt, facilitated rapid locomotion and permitted increasingly longer hops. Tran- sition from a long hop to flight by initiation of the wingbeat cycle does not seem a great step. Once developed, the jumping behavior probably allowed larger meals to be taken in a single feeding pe- riod and perhaps permitted feeding on the limbs of larger animals, as it facilitated avoidance maneuvers. Flight and Aerodynamic Considerations Investigators of bat locomotor morphology have characterized bats as relatively derived or underived on the basis of the degree of anatomical and behavioral modification contributing to efficient flight. In most species characterized by efficient flight, sometimes described as relatively derived, there are anatomical features of the pectoral limbs and girdles that automatically move distal parts of the wings when more medial parts are moved. These features also limit the planes of movement possible for the wings, but per- mit great mechanical advantage for muscles to power the move- ments and allow concentration of muscle mass nearer the center of gravity. Such species can fly rapidly over relatively long distances with minimal energy expenditure and are well suited for long feed- ing periods in flight or for migration. Species with inefficient flight, often characterized as underived, are better suited to feeding on nectar or fruits, or feeding and maneuvering in a cluttered environment, and necessarily lack the anatomical features that restrict planes of movement and provide automatic movements of more distal parts of the wings. The great- er variability of movements permits slow, intricate, or hovering flight or terrestrial locomotion necessary for feeding. It is important to note that the morphological features of the 120 Spec. Publ. Amer. Soc. Mamm. 6 limb and girdle that permit either highly efficient flight (or flexible, relatively inefficient flight) may be equally derived and probably reflect considerable evolutionary modification. Desmodus 1s certain- ly an example of a morphologically derived bat that has specialized in the tremendous variability and amplitude of movements that are necessary for flight, rapid terrestrial locomotion, and also for jumping, which effects the transition between flight and terrestrial locomotion. The momentum imparted by the jump is sufficient to carry the body approximately 20 to 30 cm above the ground, giving the bat time to unfold and position the wings for the first down- stroke. However, both forward and upward velocity rapidly de- crease during this coasting phase. Desmodus derives forward thrust from unfolding the wings, which is similar to a movement in the last half of the upstroke in Desmodus and in certain other phyllo- stomatid (Altenbach, 1968), vespertilionid, and rhinolophid bats (Eisentraut, 1936), and which Norberg (1970a) termed the flick phase. In this movement the digits and forearm are extended and the entire arm is powerfully abducted and pronated. The dorsal surface of the wing is directed posteriorly and dorsally against the air stream, thus providing a component of forward thrust to rein- force the forward momentum of the bat prior to initiation of the wingbeat cycle. Several muscles power this flick; thus it can gen- erate more thrust than can abduction of the wing alone. The wingbeat cycle of Desmodus is peculiar because it shows both the high amplitude downstroke typical of many vespertilionid bats and the extended wing, low drag upstroke, and flick typical of the phyllostomatid nectar-feeders to which Desmodus is closely related (Forman et al., 1968). The same morphological features of the shoulder girdle that permit the limbs to be directed ventral to the body in terrestrial locomotion and in the jump allow a downstroke of high amplitude. Although the flick, prior to the first downstroke after a jump, supplies some increase in forward speed, the air speed and upward velocity are low at the start of the downstroke; thus maximal thrust and lift are necessary to initiate forward flight. As in other bats (Eisentraut, 1936; Vaughan, 1959, 1970d; Alten- bach, 1968; Norberg, 1970a), the force of the air as the wing is adducted deflects the phalanges of digit IV upward, thus making the portion of the wing adjacent to digit IV a thrusting surface. However, the arm is strongly pronated to orient the leading edge Altenbach—V ampire Locomotor Morphology 12] of the wing well below the trailing edge, forming all but the prox- imal third of the plagiopatagium and the chiropatagium, nearly 80 per cent of the wing area, into a thrusting structure. This contrasts sharply with published estimates that only 20 per cent of the wing area is configured to provide thrust in other bats. Photographs taken several wingbeats after initiation of flight indicate that the phalanges of the fifth digit also are deflected upward to increase this thrusting effect. The distal portion of the chiropatagium often is not fully unfolded during the first, and occasionally the second or third, downstroke; yet motion pictures indicate rapid accelera- tion during this period. Obviously, thrust is being produced by the more medial parts of the wing and not by just the propeller effect of the distal chiropatagium as is typically described for bat flight. During the downstroke, both the upward and forward velocity of the body increases, apparently the result of downward and back- ward acceleration of air produced by the adduction of the wings. Eisentraut (1936) stated that upward drive is produced by the ad- duction of the wings in the downstroke but more recent discussions of bat flight (Vaughan, 1959, 1966, 1970d, 1970e) suggest lift is only produced by air flow over a cambered surface. In Desmodus, as in any bat, the latter is perhaps the case in more rapid forward flight. However, at least in Desmodus, much of the lift in the initial flight following a jump and in the slow accelerating flight that follows, is the result of acceleration of air ventrally during adduc- tion of the wings. An upward deflection of the distal two phalanges of digit II during the downstroke perhaps reduces the formation of tip vor- tices and, during the last half of the stroke, provides additional lift. Adduction of the wings continues slightly anteriorly in the last half of the downstroke and the tips occasionally meet below the body. The high amplitude of the stroke permits production of continuous air acceleration and thus thrust and lift production for a relatively long period. As in some nectar-feeding species of phyllostomatids, the down- stroke gives way to the upstroke by a gradual change of direction and position of the wing. Drag is minimized by raising the wings anterior to the body, while they are fully extended, and with the plane oriented vertically. A pronounced flick, similar to that de- scribed by Eisentraut (1936) and Norberg (1970a) in other species, completes the upstroke and provides additional thrust. The flick 122 Spec. Publ. Amer. Soc. Mamm. 6 can occur only in bats with great freedom of movement of the arm and hand. In species that have evolved more efficient, high-speed flight, anatomical modifications of the pectoral limb allow more automatic extension and flexion of the hand and centralization of weight and do not permit this type of upstroke and flick. There is little doubt that this movement produces forward thrust in Des- modus, as Eisentraut (1936) believed it does in several other species. The most conclusive evidence is the rapid acceleration during this movement prior to the first upstroke following a jump. Although of greater amplitude, the initial flick is similar to that observed in subsequent wingbeats of slow forward flight. There is only slight flexion of the digits toward the forearm during the first half of the upstroke in slow forward flight, thus extension of the digits plays a lesser role in flight than it does in the initial flick. Although no high-speed photographic data are available on rap- id flight, the flick is certainly more important in slow flight than in rapid flight. During the flick, thrust is derived by a posterior swing of the more distal portions of the wing against the air. Ob- viously, as the forward speed of the bat increases, the thrust from the flick decreases. The high thrust required during the initial flight following a jump is probably not so vital at high cruising speeds and the upstroke is basically a recovery stroke. There is almost certainly a modification of the wingbeat cycle during rapid forward flight, but it remains for high-speed photographs to illus- trate it. Perhaps the amplitude of the downstroke is less and the stroke begins at a lower angle above horizontal (and continues quite deep), as in some molossid bats, which are best suited for this type of flight (Vaughan, 1959, 1966, 1970d). Inasmuch as Desmodus is anatomically suited for the upstroke with the wing positioned anterior to the body and its plane oriented vertically, this portion of the stroke may remain relatively unchanged, and a pronounced flick may occur. However, it may be more passive than in initial flight after a jump or in slow forward flight. Desmodus has a heavy wing loading (4.8 cm?/g), as do molossids such as Molossus bondae (4.0 cm?/g), and phyllostomatids such as Phyllostomus hastatus (3.4 cm?/g), and Artibeus jamaicensis (4.5 cm?/ g)—Hartman, (1963). However, its aspect ratio is low (2.66) as compared to Molossus bondae (3.6) and Phyllostomus hastatus (3.48). Struhsaker’s data (1966), calculated by slightly different methods, place Desmodus (4.9) and Leptonycteris sanborni (4.6) below Molossus Altenbach—V ampire Locomotor Morphology 123 nigricans (5.9) and Tadarida brasiliensis (6.7), and above several species varying from 4.13 (Myotis velifer) to 2.44 (Antrozous pallidus). These data illustrate that Desmodus is somewhat unique in having both a heavy wing loading and a low aspect ratio. Other investi- gators have associated high aspect ratio and high wing loading with relatively high-speed, unmaneuverable direct flight, such as that of many molossid bats. Many of the species with low aspect ratio wings, such as Antrozous pallidus, Myotis lucifugus, and Pipistrellus hesperus are lightly loaded and have delicate, even hovering, flight. Although Leptonycteris is less heavily loaded than is Desmodus, Struhsaker (1961) found its loading more comparable to Desmodus than to the other bats he investigated. The flight of these two bats, however, is quite different. In slow and hovering flight, Leptonyc- teris gains high lift from a medial and anterior swing of the forearm and hand produced by a flexion of the elbow in the last half of the downstroke (Altenbach, 1968). This movement supplies lift with- out movement of the body through the air stream. The length of the hand compared to that of the arm is relatively greater in Lep- tonycteris than in Desmodus (Findley et al., 1972) and reflects the role of the hand in lift production. Desmodus exhibits no such mod- ification of the wingbeat cycle, and the relatively shorter and small- er hand-wing probably reflects evolutionary compromises for both flight and terrestrial locomotion. Desmodus appears to utilize a high amplitude downstroke to provide maximal thrust and lift during the wingbeat cycles following a jump. As thrust is certainly pro- duced during the downstroke by much of the plagiopatagium in addition to the chiropatagium, a large chiropatagium is not nec- essary for thrust production. Elongation of the wings would be disadvantageous, because the jump carries the bat less than 0.3 m above the ground and contact of the wings with the ground at the bottom of a deep stroke would certainly reduce acceleration. The short hand can be folded quickly in an alighting maneuver to pre- vent damage to the rather delicate digits and, when folded, is not bulky enough to hamper quick movements necessary in the rapid terrestrial locomotion typical of this bat. The need for a relatively long limb in quadrupedal locomotion and particularly for jumping probably prevents reduction in the length of the antebrachium and brachium. Thus, to maintain a wing of the proportions necessary for production of high thrust and lift, and, at the same time to keep its length minimal and 124 Spec. Publ. Amer. Soc. Mamm. 6 provide a long limb for quadrupedal locomotion and jumping, the relative length of the hand is reduced. Since flight serves primarily to move the vampire bat relatively short distances between roosting and feeding areas, there is no need of anatomical modification for highly efficient flight, typical of species that feed in flight or cover long distances in feeding and migration. Great freedom of movement of the limbs, however, is necessary in the terrestrial feeding behavior of this bat and espe- cially for the transition from terrestrial locomotion to flight. Thus specialization of the appendicular anatomy has been toward ex- treme variability and amplitude as well as independence of move- ment. Features that allow maximal muscular mass to power high energy demanding movements have permitted development of jumping behavior for transition between terrestrial and aerial modes of locomotion. Some of these same features also permit extremely high thrust and lift production necessary to sustain flight after a jump and while carrying a heavy load of blood. In effect, Desmodus has specialized in variability to feed as a ter- restrial vertebrate and yet retain the advantages of a flying verte- brate. Thus, this bat has reduced competition with other bats for food resources, yet has retained the advantage of mobility and ability to use secluded roosts that are inaccessible to most preda- tors. Anatomical Considerations Perhaps the most striking osteological feature of the pectoral girdle is the nature of articulation of the clavicle and scapula, which allows the scapula to rock freely about its long axis. In other species of bats such as Plecotus auritus (Norberg, 1970b), Eumops perotis and Myotis velifer (Vaughan, 1959), and Eptesicus fuscus (Altenbach, 1968), the clavicle is bound distally to both the acromion process and the base of the coracoid process. This feature stabilizes the pectoral girdle and gives the muscles that rock the scapula and the wing, when the humerus and scapula are locked dorsally or ven- trally, great mechanical advantage. However, the amplitude and variability of movements of the wing are greatly restricted. Thus, efficiency is gained at the expense of flexibility.of movement. In phyllostomatids such as Leptonycteris sanborni (Altenbach, 1968) and Macrotus waterhousu (Vaughan, 1959), the articulation of the scap- Altenbach—V ampire Locomotor Morphology 125 ula and clavicle is similar to that of Desmodus, but the arrangement in Desmodus allows much greater freedom of movement. The relatively small angle through which the humerus can be adducted or abducted relative to the scapula is surprising, consid- ering the great amplitude of the movement of the brachium during terrestrial locomotion, jumping, and flight, but suggests that some of the muscles that insert on the scapula (M. serratus anterior, tra- pezius group, and M. rhomboideus) are important in moving the arm. The spinous process of the ventral (median) epicondyle of the humerus has no distal projection typical of many fast-flying molossid, vespertilionid, and mormoopid bats; thus, muscles orig- inating from it are not affected by movements at the elbow. The ulna is strongly fused to the radius distally and rigidly ar- ticulated with it proximally. The elevated carriage of the body in terrestrial locomotion and jumping in this bat directs forces against the long axis of the forearm, thus bracing is needed. In addition, the relative independence of the hand from movement at the el- bow requires more muscle mass in the forearm, and the rigid ulna supplies a solid structure for the origin of such muscle. Investment of the distal end of the radius with deep grooves and ridges for confinement of insertional tendons of forearm muscles reflects the large forces involved during terrestrial locomotion and jumping. The carpus is not highly specialized except, as in other bats, to limit the movements of all but digit I to a single plane, thus bracing the hand-wing against the forces of the air stream in flight. How- ever, digit I is greatly elongated, almost 30 per cent the length of the forearm, and the articulation of the first metacarpal and tra- pezium allows considerable freedom of movement. The articula- tion is bound by ligaments ventrally and the articular surfaces slope away dorsally from the ventral binding, allowing the thumb to be oriented laterally when the forearm is directed perpendicularly against a surface. The thumb thereby functions in maintaining balance when the body is elevated in terrestrial locomotion, and can be flexed powerfully from this position to supply the last up- ward thrust in a jump and to provide thrust in rapid terrestrial lomotion. The metacarpophalangeal joints of digits IV and V and the first interphalangeal joint of digit III permit considerable upward de- flection of the phalangeal elements distal to them, thus enabling the posterior part of the chiropatagium and distal part of the pla- 126 Spec. Publ. Amer. Soc. Mamm. 6 giopatagium to supply high thrust during the downstroke. This appears unique among bats as, in others, only the phalanges of digit IV deflect upward to provide the propeller effect described by Vaughan (1959) and Eisentraut (1936). The myology of the pectoral girdle and limb was described in detail earlier and only the outstanding features, unique to Desmo- dus, will be discussed here. The M. clavotrapezius is large and its complete separation from the M. acromiotrapexius and its heavy origin reflect importance in bracing and moving the clavicle. In bats that have the clavicle bound in two points to the scapula, the division between these muscles is obscure and their function nearly identical, inasmuch as rotational forces applied to the scapula are transferred directly to the clavicle. The antagonist of the M. clavotrapezius, the M. sub- clavius, also is large, and together these muscles stabilize the clavicle and probably lower and raise it during jumping and flight. The remainder of the trapezius group functions much as in other bats to stabilize the scapula and rock it about its long axis. Electromyographic data indicate the deltoid group, at least the acromio- and spinodeltoids, functions to stabilize the dorsal scap- ulohumeral articulation during the powered phase of the jump and much of the downstroke in forward flight. This indicates, in- directly, that the posterior division of the M. serratus anterior aids the M. pectoralis in adducting the humerus through nearly the entire jump and much of the downstroke. Vaughan (1959) sug- gested that in other bats, particularly those having the scapula and clavicle bound in two places, the posterior division of the serratus only stops the upstroke and initiates the downstroke, the remain- der of the downstroke being powered by the M. pectoralis and M. subscapularis as they adduct the humerus using the scapula as a fulcrum. In Desmodus, the two largest pectoral muscles, the M. pectoralis and the posterior division of M. serratus anterior, are pos- sibly responsible for nearly all of the brachial adduction in a jump and for much of the brachial adduction in flight. The M. clavodeltoideus is situated to extend the humerus, and its size and complete separation from the clavicular M. pectoralis sug- gest importance of this movement, which produces a power stroke in backward climbing and in positioning the pectoral limbs for alighting on a horizontal surface. The pronators of the arm, the M. latissemus dorsi, M. pectoralis Altenbach—V ampire Locomotor Morphology 127 abdominalis, M. teres major, M. subscapularis, and the posteriormost fibers of the sternal M. pectorals play an important role in the flick phase of the upstroke. Pronation of the arms after initial abduction of the wings in a vertical orientation anterior to the body swings the distal half of the wings posteriorly against the air and provides forward thrust. Although Eisentraut (1936) described the flick and believed it produced thrust in several species of bats, recent in- vestigators have implied the entire upstroke is entirely a recovery stroke and provides no thrust. Indeed, in the molossids and many vespertilionids, particularly those with features that limit freedom of movement of the wings and provide highly efficient flight, the flick is nearly impossible and the upstroke is a recovery stroke. However, in rhinolophids, a few vespertilionids (Eisentraut, 1936; Norberg, 1970a), and many phyllostomatids, including Desmodus, the flick is important in providing thrust, as the relatively large size of the muscles involved and the good mechanical advantage for the movements they power, suggest. In addition to the above- mentioned muscles the three heads of the M. triceps brachu extend the elbow to aid this movement, and the two largest forearm mus- cles, the M. extensor carpi radialis longus and M. extensor carpi radialis brevis, along with the M. extensor indicts, powerfully extend the chi- ropatagium. The relatively small acromio- and spinodeltoids are certainly not large enough to power a thrust-producing upstroke, but they are well suited to raise the wing anteriorly to the body by supination of the humerus and thus elevate the flexed forearm. This type of upstroke seems quite typical of most phyllostomatids, rhinolophids, some vespertilionids, and certainly Desmodus. It re- duces drag initially and positions the wing for the flick, in contrast to the case in the molossids and mormoopids where the upstroke is a recovery stroke and the entire movement is essentially wasted effort. The M. biceps brachii is adapted to provide a strong, supinating force to the arm and to flex the forearm as in other species. It probably aids somewhat in the downstroke, even though the hu- merus is dorsally locked with the scapular border. However, its main function is very likely control of rotational stability of the arm and flexion of the forearm at the first of the upstroke. The importance of the thumb in Desmodus is evidenced by the size of the tendons and bellies of the muscles that ventrally flex it. The M. flexor digitorum profundus, the M. palmaris longus, and the 128 Spec. Publ. Amer. Soc. Mamm. 6 M. abductor pollicis longus all have large tendons running to the ventral aspect of the first digit. In other bats, the M. abductor pollicis longus inserts on the scaphoid, and, in at least one species, Plecotus auritis, the M. abductor pollicis brevis originates there and inserts on the first digit. In Desmodus, the latter muscle has become tendinous and originates directly on the tendon of the former, thus permit- ting a longer and larger forearm muscle to power the flexion of the thumb. The muscles of the hand, M. abductor pollicis and M. flexor pollicis brevis, which insert ventrally on the thumb, are well suited to move the thumb to give the claw purchase in such ma- neuvers as climbing or walking. All of the above-mentioned fore- arm flexors of the thumb have at least one flexive attachment to digits II through V. Thus, as they flex the thumb in a jump or in terrestrial locomotion, they also aid in keeping the digits flexed toward the forearm and flex the phalanges. The major flexor of the hand wing, the M. extensor carpi ulnaris, inserts on the medial base of metacarpal V where it has great mechanical advantage. The insertional tendon is massive and suggests the importance of this muscle in holding digit V and, because of ligamentous attach- ments between the metacarpals of digits III and V, the rest of the hand-wing against the forearm, and in rapidly folding the hand- wing during an alighting maneuver. The other major flexor of the hand, the M. flexor carpi ulnaris, inserts on the pisiform as in other species, but is small and probably only weakly assists M. extensor carpi ulnaris. M. flexor carpi radialis is best suited to ventrally brace the second metacarpal, and thus the leading edge of the hand- wing. This is important when the leading edge of the wing is ori- ented below the trailing edge for high thrust production in the downstroke. Because of the capacity for upward deflection of the phalanges of digits IV and V and all but the basal phalanx of digit II, and the capacity to vary greatly the degree of pronation or supination of the arm, Desmodus can vary greatly the angle of attack, camber, and degree of thrusting configuration of the wing. M. extensor dig- itorum communis is well suited to actively deflect the phalanges of digits III and IV, and the M. extensor digiti quinti proprius is suited to deflect the phalanges of digit V. The upward deflection of the phalanges of digit V is evident only during about the first half of the downstroke, whereas that of digits III and IV persists to the end of the downstroke. Thus it is critical that there be independent Altenbach—V ampire Locomotor Morphology 129 control of digit V. As M. abductor digitt quinti originates on the scaphoid in Desmodus, flexion of the phalanges of digit V is partially under control of the M. abductor pollicis longus, which inserts on the scaphoid and first digit. Along with the M. opponens digiti quinti, these muscles can ventrally flex the phalanges of digit V to elimi- nate the thrusting contour of the wing in that region and transform it into a more cambered lift-generating surface. During a jump or in terrestrial locomotion, the M. abductor pollicis longus can keep the phalanges of the fifth digit flexed as it flexes the thumb by pulling the origin of the M. abductor digiti quinti. The large M. extensor carpi radialis longus and M. extensor carpi radialis brevis originate medial to the center of the elbow joint and thus are stretched slightly by extension of the elbow. However, they are not invested in a tough connective tissue sheath of deep fascia, as is the case in many molossids and vespertilionids, and do not automatically extend the digits when the elbow is extended. When the flexors of the hand-wing relax, particularly if the elbow is partially or fully extended, these muscles can powerfully and rapidly extend the fingers. SUMMARY Fes mechanisms of terrestrial locomotion, jumping behavior, and flight of the common vampire bat, Desmodus rotundus, were analyzed with high-speed photographs and electromy- ographs, and were correlated with osteological and myological fea- tures of the pectoral girdle and limbs. Great freedom of movement at the articulation of the scapula and clavicle, and independence of movement in the arm and hand, allow the pectoral limbs to be positioned below the body for efficient, rapid, and extremely agile terrestrial locomotion. These same anatomical modifications, cou- pled with specialization at the shoulder joint, enable the two largest muscles in the bat, the M. pectoralis and the posterior division of the M. serratus anterior, to power a deep adduction of the arms to effect a jump into flight. Extreme elongation and development of powerful associated flexor musculature permit the thumbs to pro- vide an additional upward thrust in the jump. The jump is vital to achieve flight after taking a blood meal from a prey animal on the ground. The anatomical features of the pectoral girdle and limb 130 Spec. Publ. Amer. Soc. Mamm. 6 that facilitate both the jump and the remarkable terrestrial loco- motion are the most spectacular anatomical modifications in this bat. They suggest Desmodus became evolutionarily specialized for feeding terrestrially from small active prey animals. Feeding from the backs or necks of large prey species seemingly would not have necessitated the development of such rapid and agile hopping lo- comotion. More important is that this manner of feeding would not necessitate the extreme modification of the limbs and girdles to execute the jump into flight so characteristic of this bat. The habit of feeding from backs and necks of the large domestic ani- mals of man is probably an opportunistic utilization of a relatively new and more abundant food source. During the downstroke of the initial flight following a jump, up to 80 per cent of the area of the wings is configured to provide thrust. The same large muscles of the pectoral girdle that provide adductive power in jumping are able to power at least the first half of a deep downstroke that initially supplies high thrust and sub- sequently supplies both lift and thrust vital to initiation of forward flight. The upstrokes in initial flight occur ahead of the body and are terminated in a pronounced flick that provides additional thrust and positions the wing for a subsequent downstroke. The first few wingbeats following a jump into flight illustrate that thrust and lift production are the result of the acceleration of air back- ward and downward by movement of the wings. The amplitude and directionality of the wingbeat, and the velocity and configu- ration of the wings during the wingbeat cycle, determine the mag- nitude and direction of the air acceleration. Thus a downstroke could produce almost pure lift or pure thrust depending upon how it was directed and the configuration of the wings. This view contrasts with interpretations of bat flight, which suggest that lift is produced by differential velocity of airflow over opposite sides of the cambered plagiopatagium and that thrust is produced ex- clusively by the distal chiropatagium. In many of the flights re- corded in this study, the distal part of the chiropatagium, the por- tion often said to be the prime producer of thrust, remained folded as the bat rapidly accelerated. Thrust was obviously being pro- duced by more medial portions of the wing. Among many evolutionary compromises seen in the vampire bat are the relative shortening of the hand and the retention of a large muscle mass distally in the wing to control the hand movements. Altenbach—V ampire Locomotor Morphology 131 A relatively long hand would be advantageous for lift and thrust production, but would be difficult to quickly fold and unfold in transition to and from terrestrial locomotion, and would be likely to strike the ground on a high amplitude downstroke in the initial flight following a jump. It also would be advantageous to have more muscle mass concentrated near the center of gravity and to have movements in the hand more automatic, as in certain other bats, but the need for independent movement in the hand has necessitated retention of considerable muscle mass distally. ‘The tight folding of the digits during extension of the arm during a jump, and the extended orientation of the digits as the arm is flexed during the first half of the upstroke, are good examples of this independence of movement. CEE RAPOEE Chip ALTENBACH, J. S. 1968. The functional morphology of two bats: Leptonycteris and Eptesicus. Master’s thesis, Colorado State University, 85 pp. . 1972. A silicone rubber plug for chronic exteriorization of EMG leads in small mammals. J. Mamm., 53:630-632. Anonymous. 1969. The walking, running, leapfrogging bat. New Sci., 42:280. BasmaJIAN, J. V. 1962. Muscles alive, their functions revealed by electromyogra- phy. 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INDEX (page numbers in italic type denote illustrations) flight aerodynamics aspect ratio, 122-123 relative hand length, 123 wing loading, 122 aerodynamic requirements, 42-43 anatomical specialization for, Aerodynamics (see Locomotion, flight) Anatomy (see Myology, Osteology) Climbing (see Locomotion, climbing) Electromyograph of M. acromiodeltoideus, 85, 86, 87 of M. biceps brachu, 103, 104 of M. clavotrapezius, 76, 78 of M. extensor carpi radialis longus, 94, 95 of M. latissimus dorsi, 82, 83-84 124-129 downstroke, 42, 43, 46, 47, 48, 49 lift and thrust generation during, 43-44 of M. palmaris longus, 105, 106, wing configuration during, LU eee 42, 43-44, 46-49 of M. spinodeltoideus, 87, 88, 89 efficiency of, 119-120 of M. spinotrapezius, 77, 78-79 rapid, 122 of M. triceps brachu, 91, 92 upstroke and flick, 44, 45, 46, Electromyography 47 48, 49 interpretation of, 72, 73 $ lift and thrust generation techniques of, 6, 7-8, 10 during, 45-46, 49 hanging, JJ, 12 transition to flight from, 12, 29, 30 hoppinger (tio ld. luli evolution of, 119 initial flight acceleration during, 120-121 aerodynamic requirements of, Flight (see Locomotion, flight, initial flight) Hanging (see Locomotion, hanging) Hopping (see Locomotion, hopping) Jump (see Locomotion, jump) Locomotion 120-121 alighting anatomical specialization for, adaptive significance of, 51, 2B) 118 coasting and initial flick on horizontal surface, 49, 50, acceleration during, 33, 121 51, 118 duration of movement, 31, on vertical surface, 51—52 38 similarity to jump, 51 wing movement during, 31, climbing 32, 33. BI, W2Y ascending, 16, 17, 18, 117 first downstroke, 33-35, 120- descending, 18 (22 135 136 Spec. Publ. Amer. Soc. Mamm. 6 acceleration 35, I20=I12 1 lift and thrust generation during, 34, 35, 120-121 flick (see upstroke and flick) flight path during, 31 into steep flight path, 39, 40 thrust production during, 120-121 turn during, 39, 40, 41 upstroke and flick, 35-39, 120-122 acceleration during, 38 wing configuration during, 120-121 during, jump adaptive significance of, 21-22, Ly anatomical specialization for, 58, 59-60, 125-129 backward, 27, 28 evolution of, 119 in other bats, 117 into flight anterolaterally, 27 coasting phase, 20, 21, 22, 25-26, 118 from vertical surface, 29, 30 from walking gait, 29 prejump posture, 22, 23 thrusting phase, 20, 21, 22, 23-25, 118 variation in, 22—23 standing, 9, 10-11 terrestrial (see also climbing, hop- ping, walking) agility during, 117 anatomical specialization for, 58, 59-60, 125-129 evolution of, 118-119 in other bats, 116 significance of limb position, 117 walking, 12-13, 14, 117 Myology M. M. M. M. abductor digits quinti, 114, 115 abductor pollicis brevis, 95-97, 115 . abductor pollicis longus, 96-97, JD) . acromiodeltoideus, 85-86, 107 . acromiotrapezius, 78, 107 . adductor pollicis, 111-112, 114, IND . biceps brachu, 103-104, 107, WAG, HA, NZ, HS . brachialis, 104, 112, 113 . cClavotrapezius, 75-78, 107 clavodeltoideus, 84-85, 107, 110 . coracobrachialis, 102—103, 111 . coraco-cutaneous, 75, 110 . extensor carpi radialis brevis, 93, BIZ PIED, . extensor carpi radialis longus, OB), Cay, EZ iis), Il il4} . extensor carpi ulnaris, 98-99, WAZ, HAG, WIE, IS . extensor digitorum communis, 97-98, 112, 114 . extensor digiti quinti proprius, 7, HAZ, Id . extensor indicis, 99, 114 . extensor pollicis brevis, 95-96, 112, 114 flexor carpi radials, 107-108, 1B TTD: flexor carpi ulnaris, 104-105, 3, HAS M. flexor digitorum profundus, 108— M. M. 109, 113, 115 flexor pollicis brevis, 110-111, HAUS infraspinatus, 90, 107 Mm. interossei, 112-114, 115 M. M. interosseus dorsale, 109-110, 114, 115 latissmus dorsi, 83-84, 107 Altenbach—V ampire Locomotor Morphology ND . levator scapulae, 79, 107 . occipito-pollicalis, 73-74, 107, 110 . omocervicalis, 83, 107 . opponens digiti quinti, 115 . palmaris longus, 105-107, 113, 115 M. pectoralis, 100-102, 110 . pectoralis abdominalis, 102, 110 . pronator teres, 108, 113 . propatagialis proprius, 74-75, Te, . rhomboideus, 81, 83, 107 . serratus anterior, anterior divi- sion, 79, 107, 111 . serratus anterior, posterior divi- Son, GO, i, HOW, 1010, 100 M. spinodeltoideus, 87, 89, 107 M. spinotrapezius, 78-79, 107 M. subclavius, 99-100, 110, 111 M. subscapularis, 84, 111 M. supinator, 95, 112 M M M Ss sss SS Ss Ss Sss M. supraspinatus, 89-90, 107 . teres major, 84, 107 . teres minor, 89 M. triceps brachu, 90-92, 108 Osteology cervical vertebrae, 53 clavicle, 59-60 articulation with scapula, 59- 60 digit I, 66, 67, 68 digit II, 66, 67, 69 digit III, 66, 67, 69-70 digits IV-V, 66, 67, 70-71 humerus, 60, 6/7, 62-64 articulation with radius and ulna, 64 articulation with scapula, 58, 62 lumbar vertebrae, 54—55 manus, 66, 67, 68 radius and ulna, 63, 64-66 ribs, 56 sacral vertebrae, 55 scapula, 56, 57, 59, 80 articulation with clavicle, 58, 59-60, 80 articulation with humerus, 58, 62, SO orientation, 58, 59-60, 80 sternum, 54, 55-56 thoraic vertebrae, 53-54 ulna (see radius and ulna) Photographic techniques electromyographic, 6, 7-8 motion picture, 6, 7 Suilll, 7 Positional terminology, 52, 53 iin 3 2044 062 338 5 if (HUN Wdetilalifelebai rH if Hi Py i ess Hien bind) ate ree ewe Dr > papen i 0?! re — a a a i AH Hina! Hh inate SHA hy Mit PDH RE THERE