SMITHSONIAN INSTITUTION MUSEUM O F NATURAL HISTORY UNITED STATES NATIONAL MUSEUM BULLETIN 273 The Muscular System of the Red Howling Monkey MIGUEL A. SCHON The Johns Hopkins University School of Medicine SMITHSONIAN INSTITUTION PRESS WASHINGTON, D.C. 1968 Publications of the United States National Museum The scientific publications of the United States National Museum include two series, Proceedings of the United States National Museum and United States National Museum Bulletin. In these series are published original articles and monographs dealing with the collections and work of the Museum and setting forth newly acquired facts in the fields of anthropology, biology, geology, history, and technology. Copies of each publication are distributed to libraries and scientific organizations and to specialists and others interested in the various subjects. The Proceedings, begun in 1878, are intended for the publication, in separate form, of shorter papers. These are gathered in volumes, octavo in size, with the publication date of each paper recorded in the table of contents of the volume. In the Bulletin series, the first of which was issued in 1875, appear longer, separate publications consisting of monographs (occasionally in several parts) and volumes in which are collected works on related subjects. Bulletins are either octavo or quarto in size, depending on the needs of the presentation. Since 1902, papers relating to the botanical collections of the Museum have been published in the Bulletin series under the heading Contributions from the United States National Herbarium. This work forms number 273 of the Bulletin series. Frank A. Taylor Director, United States National Museum U.S. GOVERNMENT PRINTING OFFICE WASHINGTON : 1968 For sale by the Superintendent of Documents, U.S. Goverrunent Printing Office Washington, D.C. 20402 - Price $1.25 Contents Page Introduction 1 Muscles of the head 3 Trigeminal Group 3 Facial Group 13 Facial musculature 13 Deep musculature 20 Glossopharyngeal group 21 Vago-accessory group 22 Extraocular group 28 Lingual group 30 Muscles of the trunk 32 Expaxial musculature 32 Superficial oblique system 33 Long system 34 Deep oblique system 41 Short system 43 Hypoaxial musculature 46 Lateral group 46 Subvertebral group 56 Perineal group 59 Perineal musculature— Male 60 Perineal musculature—Female 62 Caudal group 64 Ventral group 65 Muscles of the upper extremity 71 Dorsal (extensor) musculature 71 Shoulder girdle group 71 Extrinsic series 71 Intrinsic series 81 Upper arm group 86 Forearm group 89 Superficial series, radial division 89 Superficial series, intermediate division 92 Superficial series, ulnar division 93 Deep series 96 Ventral (flexor) musculature 99 Shoulder girdle group 99 Extrinsic series 99 Intrinsic series 103 Upper arm group . 104 Forearm group 105 Superficial series, radial division 105 Superficial series, intermediate division 107 Superficial series, ulnar division 110 Deep series Ill VI U.S. NATIONAL MUSEUM BULLETIN 2 73 Muscles of the upper extremity— Continued Page Ventral (flexor) musculature— Continued Hand group 113 Superficial series, superficial layer 113 Superficial series, deep layer 116 Deep series, superficial layer 117 Deep series, deep layer 118 Muscles of the lower extremity 123 Dorsal musculature 123 Coxofemoral group 123 Prepelvic 123 Postpelvic 133 Cruropedal group 139 Lateral division 139 Anterior division 142 Pedal group 145 Ventral musculature 146 Coxofemoral group 146 Prepelvic 146 Postpelvic 149 Cruropedal group 152 Pedal group 159 Superficial series, superficial layer 159 Superficial series, deep layer 162 Deep series, superficial layer 162 Deep series, deep layer 163 Conclusions 166 Literature cited 177 Alphabetical listing of muscles 183 The Muscular System of the Red Howling Monkey Introduction The howling monkeys, which are members of the superfamily Ceboidea (Simpson, 1945), inhabit a very extensive area in the tropical and subtropical forests of Central and South America. They are well known among travelers and naturaUsts for their prodigious roars, which can be heard for very long distances. The voice-producing organs have been extensively studied in the past. The pertinent bibUography can be found in the sunmiary account of Starck and Schneider (1960) and the recent study by Kelemen and Sade (1960). Schon (1964a) added further information about the pharyngolingual musculature of this animal and emphasized certain functional aspects of these structures. The muscular system of the whole animal was investigated by Santi Sirena (1871), who compared it with man, the great apes, and some catarrhine monkeys; unfortunately, this work has remained little known among modern students of primate anatomy. Sirena used three specimens preserved in alcohol. They were tentatively classified as Mycetes fuscus, a synonym for the accepted name Alouatta fnsca (Hershkovitz, 1964). Two were males, but Sirena could not ascertain the sex of the other animal because its genito-urinary organs had been removed. Each one had fourteen pairs of ribs, and at least one was an adult. The purpose of my research was to compare the entire muscular system of Alouatta with that of the spider, woolly, and woolly spider monkeys, on the one hand, and the capuchin on the other. All of these animals have prehensile tails. The howler is usually grouped with Ateles, Lagothrix, and Brachyteles as a brachiator (Erikson, 1963) or as a semibrachiator (Ashton and Oxnard, 1963). Cehus is classified as a chmber (Erikson, 1963) or as a quadruped (Ashton and Oxnard, 1963). It is hoped that by contrasting the differences and similarities between the howUng monkey and the other four, the muscular adap- 1 2 U.S. NATIONAL MUSEUM BULLETIN 2 73 tations of Alouatta which have permitted this genus to follow its own evolutionary path will become evident. Four enbaimed specimens of the red howling monkey (Alouatta seniculus) were dissected under an Aloe Dazor fluorescent lamp with a magnifier head. Three were adult males, two from central (Guarico State) Venezuela, and one from eastern (Delta Amacuro Territory) Venezuela. The adult female was obtained through animal dealers centered in Leticia, Colombia. In addition, the masticatory and palatine muscles on the severed heads of two young adult females and one adult male from central Venezuela were studied. The ventral neck muscles were also observed in this male. It was not possible to observe the facial and dorsal trunk muscles in the female because they had been damaged while removing the brain and spinal cord. In the following account all this information has been pulled together. Variations are indicated wherever present. The data are organized according to a sUghtly modified version of a scheme developed by W. L. Straus, Jr. (unpublished), which is based on his own experience and on the previous work of A. B. Howell (1936, 1939). The recently approved Nomina Anatomica (1966) has been employed, but other commonly known anatomical terms have occasionally been used. To facilitate the comparison of the facial musculature of the howler with that of the Atelinae and Cehus, I have adhered to the terminology used by Schreiber (1928) and Huber (1930, 1931, 1933). It was found that some former students called their specimens by names accepted today only as synonyms. These are followed in this text by a parenthesis containing the name which is now accepted. In this work every muscle is first described and comments are added about observations made by other authors on the same structure of Alouatta. This is followed by the innervation and inferences about the function. The latter were based on the top- ographical arrangement and on what is presumed to be the action of the particular muscle in man or other primates (Howell and Straus, 1933). Finally, the comparative anatomy is reviewed. Sometimes groups of muscles are treated together in relation to functional and comparative aspects. This work is based on the dissertation presented by the author to the Graduate Board of the Johns Hopkins University in partial fulfillment of the requirements for the degree of Doctor of Philosophy, June 1966. It was aided in part by a training grant from the National Institutes of Health. I wish to express my appreciation to Dr. W. L. Straus, Jr., De- partment of Anatomy, Johns Hopkins University School of Medicine, for his guidance and indispensable advice, and to Dr. D. Bodian, Chairman of that Department, who arranged for financial support. MUSCULAR SYSTEM OF THE RED HOWLING MONKEY 3 The collaboration of Drs. G. Bergold and L. Carbonell of the Institute Venezolano de Investigaciones Cient'ficas, Dr. E. Mondolfi, Prof. A. Bodini, Prof. M. de Montbrun, Prof. R. Bodini, and Mr. C. Sanchez of the Universidad Central de Venezuela, and Mr. W. Pantin is here acknowledged. Mrs. Ranice Birch Crosby, Director of the Department of Arts as Applied to Medicine, Johns Hopkins University School of Medicine, gave most valuable help with figures 23 and 35. Mrs. R. Kimmerer, Mrs. P. Spencer, and Mrs. O. Schon helped in typing the manuscript. Muscles of the Head Trigeminal Group M. temporalis: It is an extensive but not very thick triangular muscle whose base corresponds to the linea temporalis and lambdoid crest, the apex to the insertion on the mandible (fig. 1). The linea is more marked in older individuals of both sexes where it is seen as a long, sharp ridge extending from about the middle of the lambdoid crest to the superciliary arch. Origin of the muscle is by fleshy fibers from (1) the back of the orbit on the facies temporalis of the alisphenoid and frontaUs. A crest which follows the sphenomalar articulation is occasionally seen at the point of attachment of these fibers; (2) the entire medial waU of the temporal fossa where its fibers ascend to the temporal line; (3) the lambdoid crest; and (4) the cranial side of the transverse root of the zygoma. Finally, (5) many bundles come from the caudal half of the inner surface of the temporal aponeurosis and also invade the jugal arch on its deep aspect.