ABSTRACT LEG MUSCLES AND THEIR FUNCTION: A COMPARATIVE STUDY IN COTURNIX AND BOBWHITE BY Wayne V. Shocks Although considerable work has been done on the leg muscles in birds, there are many groups and individual birds yet to be described. Furthermore, little is known about the functional aspects of leg muscles in vivo. . This study was undertaken to describe the gross morphology and function of the leg muscles in Coturnix (Coturnix coturnix japonica) and to compare the results with Bobwhite (Colinus virginianus). Muscle origin, insertion, weight, and location are described in detail for Coturnix, followed by a comparison with Bobwhite. The action of each muscle is discussed. Deductions of muscle action are based indirectly upon pulling of the tendon of freshly killed specimens. Muscle action was analyzed directly through experiments involving photographic analysis of motion pictures made of the walking pattern of birds in which the tendon of the Wayne V. Shooks muscle being studied was out. These results were compared to those of birds which had had a sham Operation. Track patterns of the experimentals and shams were made and analyzed. Based on the number of sesamoids, Coturnix is apparently not closely related to Bobwhite or to other gallinaceous birds. However, based on other characters such as the presence of M. adductor digiti II, Coturnix resembles other Phasianidae sufficiently to be placed in that family. Differences between the Blue Grouse (Dendragapus obscurus) descriptions of Hudson et al. (1959) and my descriptions of Coturnix which could not be resolved as species variations included: (1) the insertion of M. adductor digiti II on the lateral side of digit II rather than on the medial side; and (2) the origin of M. popliteus on the tibiotarsus rather than on the fibula. The drawings of Hudson et al. (1959) from the lateral View failed to show M. ambiens after the removal of M. femoritibialis medius and appear to have the muscle lengths of MM. flexor perforans et perforatus digiti II and III reversed. Muscle weight, which was used to determine the importance between size and action, was found to be var- iable. This problem was overcome by using several birds of the same age and genetic stock and obtaining a mean weight for each muscle. However, this is not possible in Wayne V. Shooks all studies, so I believe that for all future works a standardized formula should be used to determine muscle size: individual muscle belly weight Zbelly weight of all leg muscles muscle size = Coturnix and Bobwhite each has its own species- specific locomotor pattern, which is similar from the time of hatching throughout life, with the exception of footstep length and footprint size. These characteristics increase rapidly after hatching and resemble the adults by seven weeks of age. Coturnix and Bobwhite exhibit similar abnormalities in walking patterns following severance of a particular muscle. Muscles were divided into four groups on the basis of their importance in walking: (1) those vital to survival in the wild; (2) those in which loss would result in greatly reduced chances of survival in the wild; (3) those that reduce efficiency, but are not vital tosurvival; and (4) those that have no effect on survival. Importance of a muscle in walking was not neces- sarily correlated with muscle size or strength. The muscle formula devised by Garrod (1873) and expanded by Berger (1957) does include those muscles which were found to be of least importance in walking. Wayne V. Shooks While the muscle formula appears to have validity, the workers will be more apt to use computer analysis to make conclusions about avian phylogeny in the future. Workers who use numerical evaluations plugged into a com- puter are urged to refine their techniques to avoid over— emphasizing leg muscles which are subject to a large amount of adaptation. I suggest that this can best be accomplished by weighting the muscles of the muscle formula as proposed by Garrod (1873) and expanded by Berger (1957). LEG MUSCLES AND THEIR FUNCTION: A COMPARATIVE STUDY IN COTURNIX AND BOBWHITE By . v" Wayne V. Shooks A THESIS Submitted to, Michigan State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Department of Zoology 1970 ACKNOWLEDGMENTS I wish to express my sincere appreciation to Dr. George Wallace for his advice and aid throughout this study. A special thanks is also extended to Dr. Peter_Stettenheim who gave me the inspiration and much of the early help with this study. I would also like to thank Dr. M. Max Hensley and Dr. Rollin H. Baker for their helpful suggestions partic- ularly when this study was being formulated. Also a sincere thanks to Dr. Robert K. Ringer who helped see this study through when Dr. Stettenheim left the Avian Anatomy Project at Michigan State University. Gratitude is also extended to Dr. Martin Balaban who assisted in devising a method of photographic analysis and Jason Potter who provided technical knowledge on photo- graphic lighting. A special thanks to Prafula Paff, Joel Freedman, Thomas Leach, and David Lockwood of the Instruc- tional Media Center who loaned me photographic equipment and gave timely advice on the photographic facet of this study. Without the coOperation of Dr. Theo. H. Coleman, Hanna Georgis, Prafulla Pani, and Alwin Kulenkamp in the procurement of birds this study would not have been possible. ii A very special thanks is extended to my wife Linda and daughter Marcy for their cooperation, patience, and support during this study--especially in coming to the laboratory nearly every night of the week over a six month period to help me take motion pictures. iii TABLE OF CONTENTS LIST OF FIGURES . . . . . . . . . . . . . . . INTRODUCTION . . . . . . . . . . . . . . . . METHODS . . . . . . . . . . . . . . . . . . . Subjects . . . . . . . . . . . . . . . Operative and postoperative care . . . Determining locomotor pattern . . . . . Preparation of specimens for analysis . RESULTS AND DISCUSSION 0 o o o o o _. o o o 0 Natural history of Coturnix and Bobwhite . Distribution . . . . . . . Habitat . . . . . . . . . . Locomotion . . . . . . . . Foraging . . . . . . . . . Reproduction . . . . . . . . Development and comparison of walking Coturnix and Bobwhite . . . . . . . . . . . Osteology of the hind limb . . . . . . . . Muscles and their function . . . . . 0000. H! M. iliotrochantericus posterior . . . . ., Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . ... . . . . . . . M. iliotrochantericus anterior . . . . . Description for Coturnix and comparison with Bobwhite . ... . . . . . . . . . . Action . . . . -,- . . . . . . . . . . M. iliotrochantericus medius . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . .1. . . . . . . . . M. gluteus medius et minimus . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . .1. . . . . . . . . . . . . iv Page viii 10 13 16 16 l6 16 17 l7 17 18 19 19 24 24 24 24 24 37 37 37 38 38 38 38 M. iliacus . . . . . . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . . . . . . . . . . M. ambiens . . . . . ... . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . . . . . . . . . . M. sartorius . . . . . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . . . . . . . .o. . M. iliotibialis . . . . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . .>. . . . . . . . . Action . . . . .». . . . . . . . . . . M. femoritibialis . . . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . .*. . . . . . . . . M. piriformis . . . . . . . . . . . . . . Description for Coturnix and comparison With BObWhite o o o o o o o I o o o o 0 ' Action . . . .~. ... . . . . . . . . . M. semitendinosus . .-. . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . ACtiOn o o o o o o o o o o o o o o o o ‘ M. semimembranosus . . . . . . . . .'. . Description for Coturnix and comparison with Bobwhite . . ... . . . . . . . . . Action . . . .-. . . . . . . . . . . . M. biceps femoris . . . . . . . . ... . . Description for Coturnix and comparison with Bobwhite . . . . . _,. . . . . . . Action .'. . . .~. . . . . . . . . . . M. ischiofemoralis . . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . .‘. . . . . . . . Action . . . .'. . . . . . . . . . . . M. obturator internus . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . .w. . . . . . . . Action . . . . . . . . . . . . . . . . M. obturator externus . . ... . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . . . . . . . . . . M. adductor longus et brevis . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . . . . . . . . . . V Page 39 39 39 39 39 40 40 40 41 41 41 42 42 42 43 43 43 44 44 44 45 46 46 46 47 47 47 48 48 48 49 49 49 49 49 50 50 50 51 M. tibialis anterior . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . .-. . Action . . . . . . . . . .7. . . . . . M. extensor digitorum longus . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . .9. Action . . . . . . . . . . . . . . . . M. peroneus longus . . . . .'. . . . . . Description for Coturnix and comparison With BObWhit-e o ‘0 o o o o o o o o o o o ' Action . . . . . . . . . . . . . . . . M. peroneus brevis . . . . . . . . . . . Description for Coturnix and Comparison with Bobwhite . . . .~. . . . . . . . . M. gastrocnemius . . . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . ... . . . . . . . . . . M. plantaris . .-. . . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . . . .~. . . . . . M. flexor perforans et perforatus digiti II Description for Coturnix and comparison With BObWhite o o o o o o o o o o o ‘0 o ACtiOn o o o o o o o o o o o o o o ' o o M. flexor perforans et perforatus digiti III Description for Coturnix and comparison with Bobwhite . . . . . . .>. . . . . . Action . . . . . . . . . . . . . .-. . M. flexor perforatus digiti II . . . . . Description for Coturnix and comparison with Bobwhite . ... . . . . . . . . . . Action . . .'. ... . . . . . . . . . . M. flexor perforatus digiti III . . . ._. Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . . . .-. . . . . . M. flexor perforatus digiti IV . . . . . Description for Coturnix and comparison with Bobwhite . ... . . . . . . . . . . Action . . . . . . . . . . .'. . . .-. M. flexor hallucis longus . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . . . . . . . . . . M. flexor digitorum longus . . . .'. . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . . . . . . . . . . vi Page 51 51 52 52 52 53 54 54 54 55 55 55 55 56 57 57 57 57 57 58 59 59 59 6O 60 60 61 61 62 62 62 63 64 64 64 65 65 65 M. popliteus . . . . . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . . . . . . . . . . M. extensor hallucis longus . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . .1. . . Action . . . . .-. . . . . . . . . . . M. extensor brevis digiti III . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . .'. . Action 0 O O O I O O I O O O I O O O O ' M. extensor brevis digiti IV . . . . . . Description for Coturnix and comparison with Bobwhite . . . .'. . . .,. . . . . Action . . .'. . . . . . . . . . . . . M. abductor digiti II . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . .*. . . . . . . . . . Action . . . . . . . . . . . . . . . . M. flexor hallucis brevis . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . . . . . . . . . . M. adductor digiti II . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . .'. . . . . . . . . . . . M. lumbricalis . . . . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . M. abductor digiti IV . . . . . . . . . . Description for Coturnix and comparison with Bobwhite . . . . . . . . . . . . . Action . . . . . . . . . . . . . . . . Significant morphological findings . . . . Significant findings of functional analysis SUMMARY AND CONCLUSIONS . . . . . . . . . . . LITERATURE CITED . . . . . . . . . . . . . . APPENDIX 0 O O O O O O I O O O O O C O O O 0 vii Page 66 66 66 66 66 69 69 70 70 70 70 70 70 71 71 71 71 72 72 72 72 72 72 72 73 73 79 85 90 95 Figure l. 2. 10. ll. 12. 13. LIST OF FIGURES Lateral view of the left half of the pelvic girdle and the left pelvic limb of Coturnix Medial view of the left half of the pelvic girdle and the left pelvic limb of Coturnix Lateral view of the superficial muscles of the left thigh and shank of Coturnix . . . Lateral view of a second layer of muscles of the left thigh and shank of Coturnix . . . Lateral view of a third layer of muscles of the left thigh and shank of Coturnix . . . Lateral View of a fourth layer of muscles of the left thigh and shank of Coturnix . . . Medial view of the superficial muscles of the left thigh and shank of Coturnix . . . . . Medial view of a second layer of muscles of the left thigh and shank of Coturnix . . . Anterior view of left tarsometatarsus, pos- terior view of left tarsometatarsus,and posterior view of proximal tibiotarsus showing intrinsic muscles in Coturnix . . . The locomotor pattern of Coturnix following severance of M. sartorius . . .-. . . . . . The locomotor pattern of Coturnix following severance of M. iliotibialis . . . . . . . The locomotor pattern of Coturnix following severance of M. femoritibialis . . . . . .- The locomotor pattern of Coturnix following severance of M. semitendinosus .‘. . . . . viii Page 20 22 25 27 29 31 33 35 67 95 96 97 98 Figure 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. The locomotor pattern of Coturnix following severance of M. biceps.femoris . . . . . The locomotor pattern of Coturnix following severance of M. ischiofemoralis . . . . . The locomotor pattern of Coturnix following severance of M. obturator internus . . . The locomotor pattern of Coturnix following severance of M. adductor longus et brevis The locomotor pattern of Coturnix following severance of M. tibialis anterior . . . . The locomotor pattern of Coturnix following severance of M. extensor digitorum longus The locomotor pattern of Coturnix following severance of M. gastrocnemius . .‘. . . . The locomotor pattern of Coturnix following severance of M. flexor perforans et perforatus digiti II . . . . . . . . . . The locomotor pattern of Coturnix following severance of M. flexor perforans et perforatus digiti III . . . .'. . . .-. . The locomotor pattern of Coturnix following 'severance of M. flexor perforatus digiti II The locomotor pattern of Coturnix following severance of M. flexor perforatus digiti III The locomotor pattern of Coturnix following severance of M. flexor perforatus digiti IV The locomotor pattern of Coturnix following severance of M. flexor digitorum longus . The locomotor pattern of Coturnix following severance of M. extensor hallucis longus The locomotor pattern of Coturnix following severance of M. extensor brevis digiti IV . ix Page 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 INTRODUCTION The purpose of this study was to compare leg muscles and their functions in Coturnix coturnix japonica and Colinus virginianus through the use of cinematography, track patterns, and analysis of fresh specimens. There is a need for a fresh approach to the study of leg muscles and their function. In the past, the em- phasis has been on anatomical studies based on preserved specimens. Anatomical studies have passed through several phases of development. The earliest studies were done primarily to provide information in a descriptive sense about various muscles in birds. Hudson (1937) provides an excellent historical account of the development of this descriptive period. Around the middle of the nineteenth century muscles were used to facilitate classification of birds. Sundevall (1851) isolated the Passeriformes from other birds on the basis of the absence of a vinculum between the flexors of the foot.' Somewhat later Garrod (1873, 1874a) observed considerable variability in the presence or absence of particular leg muscles and on this basis prOposed his muscle formula. This muscle formula had a major impact on subsequent studies and probably reached a peak when Hudson (1937) proposed additional muscles to supplement the orig- inal formula. Berger (1959) expanded the formula by adding other muscles, but pointed out that probably the chief value of his expansion was to call attention of researchers to those muscles that exhibit the greatest variability. Following Garrod's pioneer work there was a major surge in muscle studies which continued through the latter portion of the nineteenth and early part of the twentieth century. Many noteworthy descriptive studies which aided in classification were published.' Garrod (1874b, 1874c, 1875, 1877, 1879) led the way with many additional studies of leg myology in several groups of birds. Beddard (1889, 1890, 1891, 1896a, 1896b) did a series of papers in which he classified birds by using the myological formula as his major criterion. In Beddard's (1898) ambitious attempt to classify all the known birds he-used the muscle formula as one of his basic guidelines.‘ Forbes (1882) studied the myology of some of the petrels, while Mitchell (1894, 1913) examined the flexor muscles and emphasized the importance of the peroneal muscle in classification. Ffirbringer (1886, 1888) described many muscles including those of the leg. The only comprehensive myological work done in the United States during this period was that of Shufeldt (1890) on the Raven. In the twentieth century, evolution became the motivating force for the study of muscles. The initial impetus was probably furnished by Howell (1936, 1938) who emphasized evolutionary relationships of vertebrate groups and whose influence carried over to others. Miller (1937), for example, studied the myology and adaptations of the Hawaiian Goose (Nesochen sandvicensis) and then through comparison with other geese proposed its evolutionary relationships. Burt (1930) analyzed adaptations in wood- peckers, including the leg muscles, and concluded that there were two major lines of descent. Fisher (1946) examined phylogenetic relationships of vultures. There were several other investigations which followed this gen- eral pattern and included leg myology, at least in part, as evidence for the conclusions reached (Avery, 1951; Berger, 1952, 1953, 1956a, 1956b, 1956c, 1957; Fisher and Goodman, 1955; Gaunt, 1969; Holmgren, 1955; Stallcup, 1954). Hudson et a1. (1959, 1964), increasingly aware of evolutionary relationships, applied numerical evaluations to taxonomic studies. In an even more extensive attempt to unravel the evolutionary relationships between groups of birds, Hudson et al. (1966, 1969) applied computer analysis to studies of bird appendages. Unfortunately, this last approach, when done on preserved specimens, tends to restrict one to the evolu- tion which has happened, subsequently ignoring what is taking place at the present time in an evolutionary sense. To understand what is occurring in evolution, one must look at the muscle in terms of function. For some reason this latter approach has been ignored. The point may readily be illustrated by the fact that George and Berger (1966) fail, in their book, to deal with muscle function at the gross anatomical level. This is not to say that muscle function has been totally ignored. Watson (1869) decided to cut the M. ambiens in some chickens to challenge Borelli (1680) who had suggested that the M. ambiens was the perching muscle. Stolpe (1932) did research on joint mechanics which indi— rectly related to muscle function. Steinbacher (1935) studied muscle functions in the feet of various types of birds. Hudson (1937) mentioned what he considered to be the muscle function of each of the leg muscles. Berger (1952) analyzed muscle function in Coccyzus and Geococcyx, applying general mathematical concepts to their types of locomotor movement. Miller (1937) analyzed the function of leg muscles in the Hawaiian Goose while Richardson (1942) did a similar study in woodpeckers. Both apparently based their results solely on the use of alcoholic specimens. Fisher (1957) pointed out that the results of gross dissec- tion and study of muscle attachment, are frequently incon- clusive and inaccurate because of differential action of the muscle and synergistic action of other muscles. Therefore, Fisher cut the M. piriformis in vivo and studied the action of the muscle before and after this severance. In contrast to the gross anatomical studies of muscle function, a more recent innovation at the other extreme of the continuum is the histophysiological approach, which emphasizes photomicrography plus histochemical and biochemical techniques. On the basis of fiber diameter, myoglobin content, metabolite load, and lipase and succinic dehydrogenase levels, George et al. (1965) attempted to explain the "nature" of the muscle function at the molecular level. While most of the work in this area pertains to flight muscles, Chandra-Bose (1967) used this method to study the M. gastrocnemius of a few birds. Thus there exists a great gulf between the gross morphological studies and the molecular studies. There is a need to fill this void particularly in the nonhuman element of the animal kingdom. The physicaleducation per- sonnel, long interested in improving performance, have studied locomotion and muscle function. They have used cinematography to study locomotion and electromyography to investigate muscle function. By inserting a pair of elec- trodes in the muscle and then observing the electrical potential during a particular movement, one is able to deduce muscle function.‘ Basmajian (1967) points out the real problem with this approach is the fact that the results are often difficult to interpret. Locomotor studies in physical education have been undertaken merely to improve performance of the individual, rather than to determine muscle function. Medical personnel have also been inter- ested in muscle function and locomotor analysis because of their value in physical therapy and rehabilitation of patients. The interest in locomotor analysis in birds through the use of some form of cinematography dates back to the nineteenth century. Hellbrandt (1960) points out that Leland Stanford, Jr. of California, who was interested in training race horses, hired Eadweard Muybridge to study the horse in motion. According to Hellbrandt (1960), Muybridge did this by having the horse run past a series of cameras placed parallel to the line of motion. As the horse passed each successive camera it broke a thread which tripped the shutter. Marey (1882, 1883) seized upon this concept and applied it to locomotor analysis of birds. Bangert (1960) studied the locomotor pattern of baby chicks. However, in no instance has there been an attempt to use locomotor analysis through cinematography as a tool to gain under- standing of muscle function. By photographing and analyzing birds in which individual muscles have been cut, an under- standing of the function of each muscle and its importance to the bird can better be understood. Therefore this study not only is an attempt to increase knowledge of muscle function in vivo, it is also an attempt to discover the importance of the individual muscles to the bird and conse- quently to the dynamic process of evolution. Furthermore, a comparison of the leg myology of Coturnix was made with that of the Bobwhite. By correlating the new knowledge obtained about Coturnix with that which is known about Bobwhite from this~and previous studies, it is hoped that the information obtained may help clarify the taxonomic position of Coturnix.) Finally, this study attempts to substantiate and broaden the work which Hudson et al. (1959, 1966) have done on the pelvic limb myology of galliform birds. METHODS Subjects Birds used in this study were captive Coturnix (Coturnix coturnix japonica) and Bobwhite (Colinus virginianus) quail. For the sake of brevity, throughout the text the birds are referred to as Coturnix and Bobwhite. A11 birds were obtained from the Department of Poultry Science at Michigan State University, East Lansing, Michigan., The birds, ranging in age from O to 33 months, were kept in a Petersime Brood Unit. Coturnix and Bobwhite used in muscle dissection and muscle severance portions of this study ranged in age from 11 to 16 months unless other-t wise noted. All birds were fed a commercial preparation of quail breeder mash and had water available at all times. Operative and postgperative care Ether was used as the general anesthetic. The wing~ feathers were clipped and the bird was strapped by a ster- ilized gauze bandage to the surgical tray. The leg to be cut was held in place under the dissecting microscope by a sterilized gauze bandage tied from the leg to an adjacent stand. The leg was plucked of feathers and washed with an antiseptic followed by swabbing with alcohol. 8 All instruments were sterilized and the dissecting microscope was scrubbed with antiseptic solution to reduce the possibility of infection.~ A small incision was made through the skin in the appropriate area and the tendon or fleshy insertion of the muscle in question was isolated. In four Coturnix this tendon or fleshy insertion was then cut and in the fifth bird it was not. This fifth bird provided a sham operation. The same procedure was repeated on the other leg of all birds and care was taken to keep the entire procedure a constant length for a given muscle. In Bobwhite the experimental procedure was the same for the M. gastrocnemius, M. tibialis anterior, and M. peroneus longus. In the remaining muscles the number of birds was reduced to one experimental and one sham. The birds were then placed in a recovery box for one hour after which they were put back into a Petersime Brood Unit. They remained there until motion pictures and track patterns were made between 30 and 42 hours after the initial operative procedure had begun. Just prior to the taking of the motion pictures, the tarsometatarsus joint and the posterior surface of the thigh were marked with a felt marker to assist in analyzing the film. After filming and tracking were completed, the birds were sacrificed to ascertain that only the appropriate cut had been made. This procedure was carried out on all leg muscles unless otherwise specified. 10 Determininglocomotor pattern To determine the walking pattern of the birds, slow motion photography and track patterns were employed.. The birds were released on a track which they traversed while motion pictures were taken of their movements. The track consisted of a box 101 cm. long, 21 cm. deep, and 40 cm. high. The front and sides of the box were removed and a piece of gray illustration board was attached to the back. A grid pattern was constructed on the surface of the illus- tration board using 3.2 mm. wide Chart-Pak tape spaced 12 mm. apart. The substrate on which the birds walked con- sisted of a firm wood surface covered by a shag rug.‘ The 16 mm.-Pa11aird Bolex camera with a 70 mm. single reflex zoom lens was mounted two meters in front of the track on a tripod which could be moved parallel to the track. A 650 watt flood light was mounted directly above the camera. All motion was recorded at 64 frames per second using Kodak Plus-X Reversal film. The film was analyzed by using a Centapix SR single frame motion picture analyzer. The step was divided into 13 different parts and only those 13 frames which correlated to those parts of the step were analyzed. These were: (1) last frame where digits of the right foot are completely on the substrate; (2) digits of the right leg clearly beginning to be lifted off substrate; (3) last frame before the digits of the right leg are totally free of the substrate; (4) 11 digits of the right leg pass the left leg; (5) right leg reaches its highest point anteriorly; (6) last frame before digits of right leg make contact with the substrate; (7) first frame where digits of right leg complete contact with the substrate; (8) digits of the left leg clearly beginning to be lifted off substrate; (9) last frame before the digits of the left leg are totally free of the substrate; (10) digits of the left leg pass the right leg; (11) left leg reaches its highest point anteriorly; (12) last frame before digits of left leg make contact with the substrate; (13) first frame where digits of left leg completes contact with the substrate. For each frame analyzed, the angle at the distal end of the shank and proximal end of the tarsometatarsus was recorded. Hereafter that angle is referred to as the tarsometatarsus angle and merely the tarsus on the graphs. The angle of the posterior portion of the shank, using the line horizontal to the substrate as a reference line, was also recorded. In addition, the total angle of the leg from the tip of the third digit to the base of the tail was recorded by using a line perpendicular to the substrate as the reference line. The angle of the hallux to the tarso- metatarsus was also recorded. Also the angle of the digits was measured from the tip through the highest point using a line parallel to the plane of the substrate as the reference line. The angle of the digits was considered to be 180 12 degrees if perfectly flat; as flexion increased this angle decreased. In the event the digit was inverted, the line was drawn through the lowest point and this angle was-con- sidered greater than 180 degrees. One step of each of the four Coturnix experimentals and two steps of the Coturnix sham were analyzed. From- these numbers a mean value for each measurement at each frame was obtained. The Bobwhite were used as comparisons, so only one experimental and one sham footstep were analyzed unless there appeared to be a difference from that found in Coturnix. The information on the angle of the tarsometatarsus joint, digits, and hallux could be directly plotted on graphs; however, the angle formed at the distal end of the thigh and the proximal end of the shank, which hereafter is referred to as the tibiotarsus angle and merely as the tibia on the graphs, had to be extrapolated from otherinformation that had been obtained.. Likewise the angle formed at the proximal end of the thigh had to be extrapolated indirectly from the data obtained, since the loose skin on this part. of the bird made direct measurements impossible. This angle is referred to as the angle of the femur in the remainder of this paper and merely the femur on the graphs. To find the angles of the tibiotarsus and the femur, a model was constructed to duplicate the movement of the leg. Since the approximate length of the bones, the size 13 of the leg, and the heretofore mentioned angles that were measured are known, the model can be set in the appropriate position and the angles sought can be directly read from the model. The two angles sought were extrapolated in the following manner. The angle of the femur was measured using a reference line perpendicular to the axis of the pelvic girdle at the level of the acetabulum. A point just distal to the base of the pelvic girdle was selected as the vertex and the angle formed between the perpendicular referencey line and a line drawn to the point of division between the shank and thigh calculated. The angle of tibiotarsus was measured using the posterior surface of the shank as the‘ one line, the point of division between the thigh and shank as the vertex, and a line drawn from this vertex to the. vertex used to construct the angle of the femur., These angles were also plotted on graphs. The track pattern was obtained by allowing the birds to walk on,a transparent plastic surface covered by a thin layer of moist kitchen cleanser._ When the cleanser dried the tracks made were transferred to transparent plastic sheets by tracing over the footprints with a felt marker. Preparation of specimens for analysis For-description of muscle function through analysis of fresh specimens, one Bobwhite and one Coturnix were killed at the same time so that muscle action could be 14 compared simultaneously. The tendon of the muscle being checked was then pulled and a description made.. No bird was used for more than 30 minutes after death for this purpose. Each muscle description was based on a dissection of at least four preserved specimens which varied in age from 11 to 24 months. These specimens were placed in a 10 percent formalin solution for eight hours, rinsed in fresh water for two hours and then placed in a 70 percent ethyl alcohol solution until used. In some instances fresh specimens were used in dissection since differences in color of muscles help isolate them. Drawings were traced from actual projections made of the muscles by using a modified overhead projector. To prepare the specimens for this procedure the bird was sac- rificed, the skin was removed and the exposed muscles were moistened immediately with a buffered formalin_solution. They were kept moistened throughout the dissection and subsequent projection for tracing. Skeletons for study and drawings were made from fresh specimens. The bird was killed, much of the muscle and viscera were removed,-and then the bird was placed in a mixture of three parts of a bioenzyme soap to one part meat tenderizer. The solution was changed every two days until the remaining flesh was readily removed. (The length of this time is a function of the temperature; the higher the temperature, the shorter the time.) 15 Muscle weights were taken on eight specimens of each species.. Birds were sacrificed, the muscles removed one at a time and weighed. Only the belly of the muscle was weighed.. Weights were made to the nearest .0001 grams and rounded back to the nearest .001 grams. Caution was taken to keep the skin cover over the areas of the leg not being dissected to prevent drying out. Hudson et al. (1959) was used as the main reference for all descriptions, drawings, and muscle abbreviations. In this way-it is hoped that the information gathered in this paper can readily be compared to that already obtained by Hudson and his students. And at the same time the dif- ferences between Hudson's interpretations and mine can be quickly-isolated for evaluation. RESULTS AND DISCUSSION Natural history of Coturnix and Bobwhite In order to interpret better the meaning of varia- tions of muscles and their function in terms of their im- portance in an evolutionary sense, it is necessary to summarize briefly the natural history of Coturnix and Bobwhite. Distribution Since Moreau and Wayre (1968) pointed out there is confusion on just what birds of the Far East constitute the species Coturnix coturnix, it is difficult to be certain of their range. The birds used in this study definitely occur in Japan and may be the same species as those of the far eastern mainland from Lake Baikal to Korea. Aldrich (1946) stated that the Bobwhite, including all the subspecies, occur over a vast area of the eastern, midwestern, and southern United States and southward through Central America. Habitat Yamashina (1961) indicated that Coturnix live on grass1ands, riversides, and on seashores that have thick 16 17 grass. According to Stoddard (1931), Bobwhite occur in open woodland, marshes, cultivated fields, and brushy regions wherever food is available. Locomotion Coturnix are poor fliers and when flushed fly only short distances (Yamashina, 1961). They depend primarily on their legs to move from one location to another. Stoddard (1931) states that Bobwhite are fast fliers, but are not capable of long sustained flights. Because they are rapid runners, flight is not essential to their survival except when escaping certain enemies. Foraging According to Etchec0par and Hue (1967), Coturnix are primarily seedeaters, taking an occasional insect. In captivity they were fed Quail breeder which contained some grain beetles which they ate eagerly. Judd (1905) found that approximately 80 percent of the Bobwhite diet was vegetative, consisting of grain, weedseeds, and fruits, while the remainder of the diet consisted of insects. Reproduction Coturnix in captivity are prolific producers of eggs at an early age. They begin laying at between 40 and 50 days of age and lay up to 200 eggs during their first year. Yamashina (1961) notes that in the wild Coturnix lay a clutch of seven to eight eggs. Bobwhite do not begin 18 laying in captivity until six months of age even though Stoddard (1931) points out they reach a mature weight by 15 weeks. According to Bent (1932) Bobwhite clutch size ranges from 12 to 20 eggs. Development and comparison of walking of Coturnix and Bobwhite Coturnix and Bobwhite are precocial at hatching. Motion pictures taken within 24 hours after hatching indi- cate that the walking locomotor pattern of the young resem- bles that of the adult. Motion pictures taken of other age groups indicate that this general pattern of walking is continuous throughout life. The basic differences observed between the young birds and the adults were that the young had a reduced step length and a smaller sized footprint. However, young Bob- white develop rapidly, and young Coturnix even more rapidly, so that by seven weeks of age the step length and track‘ pattern size resemble that of the adults. There were differences in the walking locomotor pattern of Coturnix and Bobwhite.- Coturnix flexes its~ digits to a greater degree than Bobwhite as the foot moves anteriorly. The tarsometatarsal angle is slightly smaller in Coturnix when standing, but the tarsometatarsal angle is greater in Coturnix as the leg reaches its highest point forward. At this highest point forward the digits are 19 flexed more in Coturnix than in Bobwhite. In fact, at this point digit III is frequently inverted in Bobwhite. When the foot is on the substrate, Coturnix bends its digits about 15 degrees in order that the nails may make contact with the substrate, while Bobwhite bends its digits only 10 degrees to make contact with the substrate. Coturnix has a smaller footprint and also takes a slightly shorter step when walking than does the Bobwhite. Osteology of the hind limb The pelvic girdle and limb of Coturnix (Figures 1 and 2) have the same general anatomical features as Bobwhite. Two osteological variations which are of importance to this study are the longer bones and larger nails on the foretoes in Bobwhite. The longer bones make it possible for the Bobwhite to take a longer step, while the longer nails make possible_a reduction in the amount of flexion of the digit necessary to reach the substrate. Muscles and their function Since there is no justifiable reason to arrange the muscles in any one particular sequence, the arrangement of the muscle descriptions follows that used by Hudson et al. (1959). Muscle weights are given as the mean followed by standard error. All weights are rounded to the nearest 20 Figure l.--(Coturnix coturnix japonica) Lateral view of the left half of the pelvic girdle and the left pelvic limb. Abbreviations for pelvic girdle and limb: ant. il,g£ggt = Anterior iliac crest. gap, gig. = Caput fibulae. gaud. yegt. = Caudal vertebrae. ext. condyle = External condyle. Egy.‘il. apt. = Fovea iliaca anterior. ilio-isch. fenestra = Ilio-ischiatic fenestra. inn. 23, greet = Inner cnemial crest. med, dggs. £;§ge = Median dorsal ridge. pgst.,il. greet = Posterior iliac crest. 923. foramen = Obturator foramen. out. cn. crest = Outer cnemial crest. spine pf fib. = Spine of Fibula. 21 Fov. il. ant. Ant. 11. crest 1”»: Post. 11. crest " Ilio-isch. fenestra ZF-—Caud. vert. .1, x .. bt. foramen ‘\- Pygostyle “§i\ Ischium cn. crest Pubis cn. crest Patell Cap. fib. Tibiotarsus Ext. condyle—rf-f?b ,iéf—~Hypotarsus 1 cm. /A+——Tarsometatarsus ../ BI / I t Phlanges /fi, / \ III Figure l 22 Figure 2.--(Coturnix coturnix japonica) Medial view of the left HaIf of the pe1V1c g1rdle and the left pelvicrlimb. Abbreviations for pelvic girdle and limb: ilio-isch. fenestra = Ilio-ischiatic fenestra. int. condyle = Internal condyle. med. dors. ridge = Median dorsal ridge. obt. foramen = Obturator foramen. 23 audal vertebrae Pygostyleh—{rv432nw 11fiz11rrllium Ilio-isch. fenestr ““*“§__ C3Q3“‘~v—Med dors. ridge ..v N. Pectinal process Femur fiL~Patella Tibiotarsus ‘ Int. condyle Hypotarsus ’ [ arsometatarsus l //:) {'1 I it! hlan es ‘ Figure 2 24 .001 grams. Generally the muscles of Coturnix and Bobwhite are similar; in those cases where they are not, the varia- tions are pointed out. M. iliotrochantericus posterior Description for Coturnix and comparison with Bob- white.--(Figures 4, 5, 7, and 8.) This, the largest of the iliotrochantericus muscles, is located at the anterior proximal end of the femur below the M. sartorius and the aponeurosis of the M. iliotibialis. It occupies the anter- ior iliac fossa. It originates fleshy from the anterior iliac fossa and iliac crest, the belly remaining fairly wide up to the very short, stout tendon which inserts on the lateral surface of the trochanter of the femur. Coturnix Wt.: 30.367 1‘ 0.024, 90.384 x 0.017; Bobwhite Wt.: 80.684 1 0.025, 90.791 1 0.086. Action.--In Coturnix and Bobwhite this muscle pulls the head of the femur inward and slightly forward at the same time, thus causing the posterior portion of the thigh to move outward and forward. When the tendon was cut, differences in the track and locomotor pattern when walking were not measurable, but this muscle appeared to be more important in preventing leg rotation than in pulling the thigh forward. M. iliotrochantericus anterior Description for Coturnix and comparison with Bob- white.--(Figures 4, 5, 6, 7, and 8.) This triangular muscle 25 Figure 3.--(Coturnix coturnix jeponica) Lateral view of the superficial muscles of the left thigh and shank. Abbreviations for muscles (after Hudson et al., 1959): bic. fem. = M. biceps femoris. f. dig. 1. = M. flexor digitorum longus. f. p, et p, g. II = M. flexor perforans et pefforatus dIgiti II. E. p, EE.E: g, III = M. flexor perforans et perforatus digiti III. gas. (p. ext.) =,M. gastrocnemius (pars externa) gas. (p, int.) = M. gastrocnemius (pars interna) i1. tib. = M. iliotibialis. per. brev. = M. peroneus brevis. per. long. = M. peroneus longus. pirif. (p. caud. fem.) = M. piriformis (pars caudofemoralis). sar. = M. sartorius. semit. = M. semitendinosus. tib. ant. = M. tibialis anterior. 26 Sar. ’1‘ Semit. ;'AE.6 1. vggV‘f;:« Pirif. (P. ’ - ~..';:.':5-;;§.’ ~. ‘ ~. caUd. fem. ) ISM B10 0 fem. I Gas. (P. ext.) Gas. (P. int.) F. p. at p. do III 3; ‘x o 3 o 0 '3). Pen brev. 1 cm. Figure 3 27 Figure 4.--(Coturnix coturnix japonica) Lateral view of a second layer offmuscles of the left thigh and shank. The following muscles have been removed wholly or in part: M. gastrocnemius, M. ilio- tibialis, M. sartorius, M. peroneus longus. Abbreviations for muscles (after Hudson et al., 1959): acc. = Accessory portion of M. semitendinosus. add. long. = M. adductor longus et brevis. bic. fem. = M. biceps femoris. fem. tib. med. = M. femoritibialis medius. flex. dig. 1. = M. flexor digitorum longus. f. E, et p. d. I£.= M. flexor perforans et perfofatus dig1ti II. f. p, gt_p. d, III = M. flexor perforans et ‘— perforatus digiti III. flex. per. g, III = M. flexor perforatus digiti III. flex. per. g. IV = M. flexor perforatus digiti IV. i1. troc. ant. = M. iliotrochantericus anterior. i1. troc. med. = M. iliotrochantericus medius. i1. troc. p253, = M. iliotrochantericus posterior. r. brev. = M. peroneus brevis. (8 pirif. (p. caud. fem.) = M. piriformis (pars caudofemoralis). pirif. (p, 11. fem.) = M. piriformis (pars ilio- femoralis). semit. = M. semitendinosus. tib. ant. = M. tibialis anterior. 28 Il. troc. post. ‘5; ‘_ 1 Il. troc. ant. ‘ fiQy.’ ' ll. troc. med / 1'. .0 11. fem. Pirif. ’. caUJ. fem. Fem. tib. med. Add. long. , if) emit. Bic. fem. F. p. at p. d. II Flex. per. d. III F. p. et p. d. III Flex. per. d. IV Tib. ant. Flex. dig. 1. Flex. per. d. III \ ‘ Per. brev. gfifi 1____1 1 cm. Figure u 29 Figure 5.--(Coturnix coturnix ‘a onica) Lateral view of a third layer of musc es 0 the left thigh and shank. In addition to the muscles listed in Figure 4, the following muscles have been wholly or partly removed: M. biceps femoris, M. femo- ritibialis, M. flexor perforans et perforatus digiti II, M. flexor perforans et perforatus digiti III, M. semitendinosus, M. tibialis anterior. Abbreviations for muscles (after Hudson et al., 1959): acc. = Accessory portion of M. semitendinosus. add. long. = M. adductor longus et brevis. ambiens = M. ambiens. 21g, Egg, M. biceps femoris. ggE, 11g, 1. = M. extensor digitorum longus. Egg, E12, ext. = M. femoritibialis externus. E, g1g, 1, = M. flexor digitorum longus. E1gg, ng. E, III = M. flexor perforatus digiti III. flex. per. 1, IV = M. flexor perforatus digiti IV. glut. med. gE_min. = M. gluteus medius et minimus. troc. ant. = M. iliotrochantericus anterior. 11. 11. troc. ggg, = M. iliotrochantericus medius. _1, EEgg, pggE, = M. iliotrochantericus posterior. Eggg, Egg, = M. ischiofemoralis. ggE, 1gE. = M. obturator internus. per. brev. = M. peroneus brevis. pirif. (p, caud. fem.) = M. piriformis (pars caudofemoraIis). pirif. (p, 11. fem.) = M. piriformis (pars ilio- femoralis). semi. g, = M. semimembranosus. semit. = M. semitendinosus. 3O Il. troc. ant: Il. troc. post. -T1. troc. med- lut. med. et min. Ubtz o 1111’. 0 Isch. fem. P. 11. fem. Pub P. caud. feL. Flex. per. d. IV Ambiens Add. long. (P. ext., Fem. tib. ext. Acc. Biceps 100p Ext. dig. lofl lex. per. d. III F. dig. 1. Per. brev. 1 cm. Figure 5 31 Figure 6.--(Coturnix coturnix japonica) Lateral view of a fourth layer of muscles of the left thigh and shank. In addition to the muscles listed in Figures 4 and 5 the following muscles have been removed wholly or in part: M. ambiens, M. extensor digitorum longus, M. flexor tibialis externus, M. flexor digitorum longus, M. flexor perforatus digiti III, M. flexor perforatus digiti IV, M. iliotrochantericus posterior, M. piriformis. Abbreviations for muscles (after Hudson et al., 1959): add. long. (p, ext.) M. adductor longus et brevis pars externa). add. long. (p, int.) M. adductor longus et brevis pars interna). M. flexor hallucis longus. 'E. p31. 1, E1gg, Egg, 1, 1_!= M. flexor perforatus digiti II. g1gE,'ggg, gE_ggg, = M. gluteus medius et minimus. 11, EEgg, ggE, = M. iliotrochantericus anterior. 11. EEgg, ggg, =‘M. iliotrochantericus medius. 1ggg, Egg, = M. ischiofemoralis. ggE, ggE, = M. obturator externus. gEE, 1gE. = M. obturator internus. per. brev. = M. peroneus brevis. semim. = M. semimembranosus. 32 Il. troc. ant. 4;. 11. trOC. med. . 1ut.med.et min: