Abstract Functional Limb Morphology of Extinct

Home , Ailuridae, American lion, Pantherinae, Promegantereon, Protopithecus, Smilodon

ABSTRACT

FUNCTIONAL LIMB MORPHOLOGY OF EXTINCT CARNIVORES SMILODON FATALIS, PANTHERA ATROX, AND CANIS DIRUS BASED ON COMPARISONS WITH FOUR EXTANT FELIDS AND ONE EXTANT CANID

Burcu Carlon, Ph.D. Department of Biological Sciences Northern Illinois University, 2014 Christopher Hubbard, Director

Adaptations for hunting and locomotor functions of animals are related to the limb functional characteristics of limb muscles, muscle attachment sites on bones, and joint articular surface shapes. This dissertation includes study of extant Felis catus, Neofelis nebulosa, Panthera leo, and Acinonyx jubatus and extinct Smilodon fatalis, Panthera atrox, and Canis dirus. The extant species exhibit different locomotor modes. The functional characteristics of extinct species are predicted based on limb bone morphology.

N. nebulosa, F. catus, and V. vulpes forelimb musculature was described, muscle maps were generated, and muscle fiber analysis was completed. Muscle attachment sizes were also compared in these species to explore the relationship between the size of a muscle and its attachment area. In addition to the bones of these three species, limb bones of extant Acinonyx jubatus, Panthera leo, Vulpes vulpes and extinct Smilodon fatalis,

Panthera atrox, and Canis dirus were analyzed using geometric morphometric techniques to examine muscle attachment sites and joint articular surfaces. This was performed to infer the degree of muscle mechanical advantage and joint mobility in the extinct species

and to suggest functional capabilities and behavior, such as different hunting and locomotion modes.

When compared to felids, V. vulpes has larger muscles crossing the shoulder joint.

Consequently, felids displayed larger ratios for muscles used for scapular and antebrachium rotation. In the geometric morphometric analysis of the forelimb, the cursorial carnivores differed from non-cursorial felids in glenoid fossa shape, humeral greater and lesser tubercles and radial tuberosity positioning, and distal radioulnar joint articular facet shape. P. atrox often clustered with P. leo. S. fatalis showed large attachment sites for scapular retraction muscles. Glenoid and distal radioulnar articular facet shapes in S. fatalis suggest increased shoulder joint and anteroposterior humerus rotation ability. In addition, shapes of elbow joint articulation and distal radioulnar articular facets in S. fatalis point to increased antebrachium rotation ability. These characters together may have aided S. fatalis during grappling with large prey. However, S. fatalis clustered with canids in the analyses of the scapula and ilium, suggesting the need for high endurance muscles needed during prey wrestling. NORTHERN ILLINOIS UNIVERSITY DEKALB, ILLINOIS

DECEMBER 2014

FUNCTIONAL LIMB MORPHOLOGY OF EXTINCT CARNIVORES

SMILODON FATALIS, PANTHERA ATROX, AND CANIS DIRUS

BASED ON COMPARISONS WITH FOUR EXTANT FELIDS

AND ONE EXTANT CANID

BURCU CARLON

A DISSERTATION SUBMITTED TO THE GRADUATE SCHOOL

IN PARTIAL FULFILLMENT OF THE REQUIREMENTS

FOR THE DEGREE

DOCTOR OF PHILOSOPHY

DEPARTMENT OF BIOLOGICAL SCIENCES

Doctoral Director: Christopher Hubbard

ACKNOWLEDGEMENTS

The author wishes to express sincere appreciation to Drs. Christopher Hubbard,

Virginia Naples, Karen Samonds, Daniel Gebo, and Richard King for their invaluable input and advice. The author would like to thank the following researchers and curators for access to the museum collections: William Stanley and William Simpson at the Field

Museum, Chicago, Illinois, John Ososky at the Museum Support Center, Suitland,

Maryland, Aisling Farrell at the George C. Page Museum, Los Angeles, CA. The funding for the research was facilitated by the Northern Illinois University Graduate Dean’s Fund.

Special thanks are due to Matt Severson for his professional bone and muscle atlas drawings of specimens. The author also acknowledges Erica Fuentes for aiding in data collection for the muscle fiber analysis. And I thank my dear parents and brother for their never-ending support.

TABLE OF CONTENTS

Page

LIST OF TABLES …………………………………………………………………… vii

LIST OF FIGURES ………………………………………………………………….. x

Chapter

1. INTRODUCTION ……………………………………………………………. 1

2. SPECIES BACKGROUND INFORMATION………………………………... 15

Felids…………………………………………………………………... 18

Canid………………………………………………………………….. 28

Extinct Species………………………………………………………… 29

3. MATERIALS AND METHODS …………………………………………….. 36

Muscle Dissection …………………………………………………….. 36

Muscle Fiber Analysis…………………………………………………. 37

Muscle Attachment Surface Area Measurements …………………….. 39

Statistical Analysis………….. ………………………………………... 39

Geometric Morphometric Analyses……….…………………………… 40

3. RESULTS …………………………………………………………………….. 58

Muscle Morphology for F. catus, N. nebulosa, and V. vulpes………… 58

A. Dorsal Extrinsic Muscle Group..…………………………… 59

Chapter Page

B. Ventral Extrinsic Muscle Group……..………………….... 82

C. Intermediate Extrinsic Muscle Group..…………………… 95

D. Lateral Scapular Muscle Group…………………………… 97

E. Medial Scapular Muscle Group………………………….... 101

F. Cranial Brachial (Gravitational) Muscle Group…………... 103

G. Caudal Brachial (Anti-Gravitational) Muscle Group…….. 107

H. Craniolateral Antebrachial Muscle Group……………….. 118

I. Caudolateral Antebrachial Muscle Group………………… 126

J. Intrinsic Manus Muscles………………………………….. 132

Species Comparisons Between Muscle Groups……………………… 136

Muscle Attachment Site Surface Area Comparisons in Extinct Species……………………………………………………………….. 137

Geometric Morphometric Analysis Results………………………….. 144

Scapula and Scapular Spine………………………………….. 144

Analysis of Scapular Borders…………………………………. 147

Glenoid Fossa…………………………………………………. 150

Humerus………………………………………………………. 154

Proximal Humeral Epiphysis…………………………………. 157

Distal Humeral Epiphysis…………………………………….. 161

Ulna…………………………………………………………… 165

Distal Ulna……………………………………………………. 167

Chapter Page

Radius…………………………………………………………. 170

Distal Radius………………………………………………….. 174

Ilium…………………………………………………………… 177

Ischium-Pubis………………………………………………… 180

Proximal Femur………………………………………………. 182

Tibia…………………………………………………………… 183

4. DISCUSSION ………………………………………………………… 189

Muscle Dissection and Data Analysis………………………… 190

Muscle Fiber Analysis and Attachment Site Surface Area…… 192

Geometric Morphometric Analysis of Forelimb and

Hindlimb Bones………………………………………………. 197

Scapular Rotation and Retraction……………………. 199

Humeral Protraction, Retraction, and Abduction…….. 200

Shoulder Joint Mobility………………………………. 202

Antebrachium Flexion and Extension………………... 202

Elbow Joint Mobility…………………………………. 204

Antebrachium Rotation………………………………. 205

Femoral Flexion and Extension………………………. 206

Chapter Page

Suggestions for Future Research……………………………… 208

Concluding Remarks…………………………………………. 211

REFERENCES ……………………………………………………………….. 215

LIST OF TABLES

Table Page

1. Summary of Species Locomotion and Hunting Style…………………… 35

2. Sample Sizes of Species for Each Bone Analyzed with Geometric Morphometric Techniques…………………………….……... 41

3. Scapula (with spine) Landmark Description……………..………...... 42

4. Scapula Periphery Landmark Descriptions……………....……………… 43

5. Glenoid Fossa Landmark Descriptions………………………………….. 44

6. Humerus Landmark Descriptions……………………………………….. 45

7. Proximal Humerus Landmark Descriptions……………………………… 46

8. Distal Humerus Landmark Descriptions…………………………………. 47

9. Ulna Landmark Descriptions…………………………………………….. 48

10. Distal Radial Articular Facet of Ulna Landmark Descriptions…………... 49

11. Radius Landmark Descriptions……………………………………...... 50

12. Distal Ulnar Articular Facet of Radius Landmark Descriptions………… 51

13. Ilium Landmark Descriptions…..……………………………………….. 52

14. Ischium Pubis Landmark Descriptions……………………………...... 53

15. Proximal Femur Landmark Descriptions……………………………….. 54

16. Tibia Landmark Descriptions……………..……………………………... 55

viii

Table Page

17. Tukey Multiple Comparisons of Means for Muscle PCSA Percentages Based on Total Forelimb Muscle Weight of Felis catus, Neofelis Nebulosa and V. vulpes………………………………………………… 60

18. Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of F. catus, N. nebulosa, and V. vulpes Scapular muscle Attachment Sites……………………………………………………….. 62

19. Tukey Multiple Comparisons of Means for Muscle Group Weight Percentages Based on Total Forelimb Muscle Weight of Felis catus, Neofelis nebulosa and V. vulpes……………………………………….. 68

20. Tukey Multiple Comparisons of Means for Muscle PCSA Percentages Based on Muscle Group Weight of Felis catus, Neofelis nebulosa and V. vulpes………………………………………………… 70

21. Tukey Multiple Comparisons of Means for Muscle Weight Percentages Based on Total Muscle Group Weight of Felis catus, Neofelis nebulosa and V. vulpes………………………………………. 79

22. Tukey Multiple Comparisons of Means for Muscle Mass to Tetanic Tension Ratios (W/Po) of Felis catus, Neofelis nebulosa and V. vulpes………………………………………………………………. 83

23. Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of F. catus, N. nebulosa, and V. vulpes Humeral Muscle Attachment Sites……………………………………………………… 92

24. Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of F. catus, N. nebulosa, and V. vulpes Radial Muscle Attachment Sites……………………………………………………….. 104

25. Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of F. catus, N. nebulosa, and V. vulpes Ulnar Muscle Attachment Sites……………………………………………………….. 111

Table Page

26. Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of S. fatalis, P. atrox, and C. dirus Scapular Muscle Attachment Sites……………………………………………………… 139

27. Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of S. fatalis, P. atrox, and C. dirus Humeral Muscle Attachment Sites……………………………………………………… 140

28. Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of S. fatalis, P. atrox, and C. dirus Ulnar Muscle Attachment Sites……………………………………………………… 141

29. Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of S. fatalis, P. atrox, and C. dirus Radial Muscle Attachment Sites……………………………………………………… 142 LIST OF FIGURES

Figure Page

1. Scapula outline with spine landmark configuration on A. jubatus scapula photograph………..………………………………………… 42

2. Scapula outline landmark configuration on A. jubatus scapula photograph …………………………………………………. 43

3. Glenoid fossa landmark configuration on A. jubatus scapula photograph …………………………………………………. 44

4. Humerus outline landmark configuration on A. jubatus humerus photograph …………..……………………………………. 45

5. Proximal humerus landmark configuration on A. jubatus humerus photograph ………………………………………………... 46

6. Distal humerus landmark configuration on A. jubatus humerus photograph ………………………………………………... 47

7. Ulna outline landmark configuration on A. jubatus ulna photograph …………………………………..………………… 48

8. Distal ulna landmark configuration on A. jubatus ulna photograph ……………………………………………………. 49

9. Radius outline configuration on A. jubatus radius photograph ……. 50

10. Distal radius landmark configuration on A. jubatus radius photograph ……………………………………………….………… 51

11. Ilium of pelvis landmark configuration on A. jubatus pelvis photograph …………………….…………………………………… 52

12. Ischium/pubis of pelvis landmark configuration on A. jubatus pelvis photograph…………………………………………………… 53 xi

Figure Page

13. Proximal femur landmark configuration on A. jubatus femur photograph …………………………..……………………………... 54

14. Proximal tibia landmark configuration on A. jubatus tibia photograph …………………………………………………………. 55

15. Lateral forelimb superficial muscles.……………………………… 64

16. Lateral scapula muscle map. A: F. catus. B: N. nebulosa ………….. 65

17. V. vulpes lateral scapula muscle map………………………………... 66

18. Medial humerus muscle map. A: F. catus. B: N. nebulosa ………… 72

19. V. vulpes medial humerus muscle map ……………………………. 73

20. V. vulpes caudal humerus muscle map …………………………….. 74

21. Intrinsic dorsal forelimb muscles……………………………….…... 76

22. Caudal scapula muscle map. A: F. catus. B: N. nebulosa………...... 77

23. V. vulpes caudal scapula muscle map……………………………..... 78

24. V. vulpes medial scapula muscle map ……………………………… 78

25. Ventral forelimb muscles ………………………………………….. 85

26. V. vulpes cranial humerus muscle map……………………………… 87

27. Medial ulna muscle map. A: F. catus. B: N. nebulosa ………………. 88

28. Lateral humerus muscle map. A: F. catus. B: N. nebulosa………….. 89

29. Cranial humerus muscle map. A: F. catus. B: N. nebulosa…………. 90

30. Caudal humerus muscle map. A: F. catus. B: N. nebulosa………….. 93 xii

Figure Page

31. Proximal humerus muscle map. A: F. catus. B: N. nebulosa………… 94

32. Medial scapula muscle map. A: F. catus. B: N. nebulosa…………… 96

33. V. vulpes lateral humerus muscle map……………………………….. 99

34. Lateral scapular muscles……………………………………………… 100

35. Medial brachial and antebrachial muscles…………………………….. 102

36. Caudal radius muscle map. A: F. catus. B: N. nebulosa……………… 105

37. V. vulpes caudal radius muscle map…………………………………… 106

38. V. vulpes cranial ulna muscle map…………………………………….. 108

39. Cranial ulna muscle map. A: F. catus. B: N. nebulosa………………... 109

40. V. vulpes medial ulna muscle map………………………………...... 110

41. Lateral ulna muscle map. A: F. catus. B: N. nebulosa………………… 112

42. V. vulpes lateral ulna muscle map…………………………………….... 113

43. Proximal ulna muscle map. A: F. catus. B: N. nebulosa…………...... 114

44. Caudal ulna muscle map. A: F. catus. B: N. nebulosa………………... 115

45. V. vulpes caudal ulna muscle map……………………………………. 116

46. Deep cranial antebrachial muscles……………………………………. 119

47. Distal humerus muscle map. A: F. catus. B: N. nebulosa…………….. 121

48. Cranial radius muscle map. A: F. catus. B: N. nebulosa…………….. 122

49. V. vulpes cranial radius muscle map…………………………………. 125

50. Pronator quadratus……………………………………………………. 133 xiii

Figure Page

51. Muscles for which PCSA ratios were significant between species. 1: significant difference between F. catus and N. nebulosa (p<0.05); 2: significant difference between F. catus and V. vulpes (p<0.05); 3: significant difference between N. nebulosa and V. vulpes (p<0.05)…………………………………………………………… 138

52. Muscle attachment site surface area measurements that were significant between felids and canids……………………………… 143

53. Scapula with spine Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes…………… 145

54. Scapula with spine Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another……….. 146

55. Scapular outline Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes……………... 148

56. Scapular outline Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another.……… 149

57. Glenoid fossa Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes……………... 151

58. Glenoid fossa Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another……………… 152

59. Glenoid fossa Discriminant Function Analysis (DFA) plot of Discriminant Function 1 (DF1) versus Discriminant Function 2 (DF2). Aj: A. jubatus; Cd: C. dirus; Fc: F. catus; Nn: N. nebulosa; Pa: P. atrox; Pl: P. leo; Sf: S. fatalis; Vv: V. vulpes………………..... 153

60. Humerus Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes……………... 155 xiv

Figure Page

61. Humerus Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another……………… 156

62. Proximal humerus Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes…………………………. 158

63. Proximal humerus Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another.……………… 159

64. Proximal humerus Discriminant Function Analysis (DFA) plot of Discriminant Function 1 (DF1) versus Discriminant Function 2 (DF2). Aj: A. jubatus; Cd: C. dirus; Fc: F. catus; Nn: N. nebulosa; Pa: P. atrox; Pl: P. leo; Sf: S. fatalis; Vv: V. vulpes……………………………….. 160

65. Distal humerus Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes………………………….. 162

66. Distal humerus Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another……………….. 163

67. Distal humerus Discriminant Function Analysis (DFA) plot of Discriminant Function 1 (DF1) versus Discriminant Function 2 (DF2). Aj: A. jubatus; Cd: C. dirus; Fc: F. catus; Nn: N. nebulosa; Pa: P. atrox; Pl: P. leo; Sf: S. fatalis; Vv: V. vulpes………………………. 164

68. Ulna Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes………………………………………….. 166

69. Ulna Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another…………………………… 168

70. Distal ulna Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes…..………….. 169 xv

Figure Page

71. Distal ulna Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another……………….. 171

72. Radius Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes……………… 172

73. Radius Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another……………….. 173

74. Distal radius Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes…………….... 175

75. Distal radius Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another………………. 176

76. Ilium Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes……………………………………… 178

77. Ilium Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another…………………………… 179

78. Ischium/Pubis Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes…………………………… 181

79. Ischium/Pubis Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another………………… 182

80. Proximal femur Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes……………………………. 184

81. Proximal femur Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another………………… 185 xvi

Figures Page

82. Proximal tibia Principal Component Analysis plot of Principal Component 1 (PC1) versus Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes…………………………… 186

83. Proximal tibia Minimum Spanning Tree (MST) based on the mean Procrustes distances of each species from one another………………………………………………………………. 188

CHAPTER 1

INTRODUCTION

Species diversity can be attributed to the evolution of new morphologies and physiologies that arise as a result of the environment and sexual selection (Mayhew,

2006). There are two types of evolutionary mechanisms: non-adaptive and adaptive radiation. A non-adaptive radiation is explained by sexual selection during mating or the emergence of morphologies that are not associated with the environment or other available resources (Dohlf, 2000). A non-adaptive radiation occurs when a species’ preference for an environment is not essential for its survival, or in cases where the environment exerts no pressure for change in habitat preference. An adaptive radiation, on the other hand, depends solely on the interaction of a species with its environment and available resources (Dohlf, 2000; Mayhew, 2006). Darwin’s theory of descent with modification relies on this process. Animals and plants have evolved a variety of external and internal morphologies to increase survival rates in their respective habitats. Of the two mechanisms that contribute to species diversity, adaptive radiation is considered to be the more significant (Dohlf, 2000; Mayhew,

2006).

Morphological characteristics are species-specific and can be used as one method to categorize a species. External morphological features such as feathers or the pattern of a fur coat as well as internal anatomical structures, such as bone or 2

muscle anatomy, can be used to differentiate species. Before the field of molecular systematics was developed in the 1960s, biological species were primarily identified on the basis of morphology (Hillis and Wiens, 2000). Although still true today, especially for fossils (i.e., morphospecies) from which DNA extraction may not be possible because of DNA fragmentation with increased sample age (Dabney et al.,

2013; Allentoft et al., 2012). Carl Linnaeus, often called the Father of Taxonomy, published his classic work describing species classifications in 1759 in the book called Systema Naturae. He believed in the separation of organisms into species based on physical appearance (Linnaeus, 1759). Linnaeus developed an organizational hierarchy for categorizing organisms based on species, genus, family, order, class, phylum, kingdom, and domain. He, in turn, subsequently developed binomial nomenclature which combines two names, a genus and a species. Prior to this unique system of nomenclature, species names were quite long, difficult to remember and generally descriptive. For example, the name of the buttercup flower was Ranunculus calycibus retroflexis, pedunculis falcatis, caule erecto, folius compositis, and this series of names mean a buttercup with reflexed sepals, curved flower stalks, erect stem, compound leaves; in short a long list of morphological terms in Latin (Mayr, 1944). To simplify naming, Linnaeus reduced the names to two, a genus and a species, and based the naming of species on the basis of morphological characters. To name flowering plants for example, he classified them on the number of the flower stamens observed in each separate plant (Freer, 2005).

Since then, morphological traits have been used to classify a variety of different clades based on their phylogenetic relationships. Species traits are generally quantifiable as morphological attributes which can be incorporated into statistical analyses to compare species (Hillis and Weins, 2000). The use of morphology to determine phylogeny has been widely used to classify bacteria (Stackebrandt, 1988;

Siefert't and Fox, 1998), plants (Doyle and Donaghue, 1986; Mishler, 1994; Albert et al., 1998), reptiles (Underwood, 1957; Arnold, 1989; Wiens and Slingluff, 2001), birds (Cracraft, 1981; Mayr and Clark, 2003) and mammals (Freeman, 2000; Gibbs et al., 2000; Geisler, 2001; Michaux et al., 2007). Some examples of key traits in plants are vascular anatomy, leaf shape, and sexual organ anatomy (Doyle and

Endress, 2000). In carnivoran mammals, skull and tooth morphology have been helpful characteristics used in classification (Mattern and McLennan, 2000, Gaubert et al., 2005; Spearing, 2013).

Species have morphological characters that are similar to those of other species and this complicates the naming process. Using morphology alone as a method for classifying species is limited and is best utilized with other methods, such as the biological species concept and molecular analyses. The biological species concept defines a species as a group of interbreeding organisms that produce viable and fertile offspring (Mayr, 1942). Molecular analysis compares similarities in DNA sequences among species to establish phylogenetic relationships. Sequences of 16S rRNA, 12S rRNA and mitochondrial cytochrome b and NADH-5 are analyzed and compared in these types of studies (Mattern and McLennan, 2000).

One advantage of using molecular data over morphological characteristics is that a higher number of characters can be analyzed. This reduces statistical variability and improves statistical estimates involving phylogeny (Hillis and Weins,

2000). Another advantage is that the genetic basis for molecular data is known, whereas morphological characters often are based on non-heritable variation such as environmental factors (Gift and Stevens, 1997; Hillis and Weins, 2000). However, molecular data obtained from a single gene or by using only a few genes in a phylogenetic study will not produce accurate results (Doyle, 1992; Hillis and Weins,

2000). In contrast, morphological characters are more likely to be derived from many different genes.

Morphological differences can be species-specific. However, unlike molecular attributes, they are often related to the functional characteristics of the species. Form and function are two concepts that are directly and sequentially related to each other. Structural studies of unicellular or multicellular organisms suggest a range of functional characteristics (Lauder, 1981; Enquist, 2002; Dillon, 2005).

Variations in morphology may point to environmental adaptations; for example, an organism’s structure may serve to enhance its ability to escape predation by enhancing some aspect of performance. The association between form and function can also be seen in other fields of study. For example, poems are constructed in ways that convey emotion to the reader (Fonagy, 1965; Berry and Erskine, 2010) while architectural design imparts structural function and esthetic significance to a building

(Greenough, 1957; Hillenbrand, 1994). The relationship between form and function is an integral part of our lives.

It is important to note that although species may belong to different clades, they may have similar morphologies with similar functions (functional analogy).

This is known as convergent evolution. Here, certain morphological characters are considered to be analogous structures that may not have been present, or may have the same shape as those possessed by the last common ancestor of the species in question (Dolph, 2000). These morphological similarities may be caused by variations in adaptation to similar environments or the utilization of similar resources. Therefore, species from different evolutionary families may evolve comparable morphologies with similar functional abilities. Flight is an interesting example. In this case, the forelimbs of bats and birds are analogous structures that accomplish flight. Both serve similar functions in terms of flying but both have evolved separately from very different structures. Thus, the ecology of the organism drives the evolution of morphological structures and ultimately speciation (Mayhew,

2006).

Correlation between form and function is apparent in many organisms.

Certain feeding and locomotor characteristics are made possible by the specific morphology of that animal. For example, the long beaks and special tongues of hummingbirds allow them to obtain nectar from long tubular flowers (Snow and

Snow, 1986; Roberts, 1995; Taylor and White, 2007). In addition, the sustained hovering locomotion of hummingbirds, convergent with insect flight, enables them

to remain in place in flight during feeding (Weis-Fogh, 1972; Warrick et al., 2005).

Aardvarks are specialized insect eaters because of their elongated snouts and sticky tongues that scoop up termites and ants, while their strong forearms are used in digging in search of prey (Andrew and Rhind, 2001; Endo et al., 2002; Knöthig,

2005).

However, caution must be taken when inferring the function of a particular type of morphology. While the shape of an anatomical structure may allow an animal to perform a certain task better than other animals, there may be additional factors that lead to the formation of the structure. The nervous system can influence the function of an anatomical structure (Lauder, 1990; Lauder 1991). The behavioral patterns of the animal may also produce certain functional characteristics (Lauder,

1995). These can take the form of learned behaviors. For example, the social organization of species is behavioral in nature and can influence hunting characteristics. Social, or pack hunters can bring down large prey by cooperating, while solitary carnivores require more strength to capture the same sized prey

(MacDonald, 1983).

An animal’s postcranial musculature and bone morphology are associated with the functional characteristics that govern environmental and feeding behavior.

This includes the size of prey captured, habitat preference, and locomotion. The study of vertebrate paleontology utilizes these living associations to predict functional characteristics in phylogenetically related extinct species. This type of study is predicated upon detailed morphologic and functional analysis in closely

related extant species to predict, with any degree of accuracy, similar characteristics in extinct species. Most often, all that is left of an extinct species are teeth and bones; therefore, the vertebrate paleontologist must rely on his/her knowledge of bone morphology to predict locomotor and behavioral characteristics using extant species morphological comparisons.

In particular, muscle scars, which are raised regions of bone produced by muscle action and remodeling response, can be used to infer muscle attachment sites and muscle functions. A muscle that generates greater forces to achieve a desired behavior (prey capture for example) will produce more rugose bone at the attachment sites than muscles producing less force (Bryant and Seymour, 1992;

Zumwalt, 2005; Zumwalt, 2006). In addition, the relative location of muscle attachment sites is important to estimate biomechanical forces. The distance of the attachment from the joint axis influences the level of mechanical advantage leading either to more forceful or more rapid or slower limb movements (McGowan, 1999;

Payne et al, 2006; Kardong, 2009) Therefore, combining the study of bone and muscle morphology can reveal important information about an extinct animal’s behavioral characteristics.

Studies of muscle morphology and physiology provide useful information to interpret movement patterns in animals. Electromyography, although not performed in this study, has been used to infer the actions of muscles at different phases of motion. This analysis involves the attachment of surface or fine wire electrodes to muscles to measure the generated motor unit action potentials during certain

movements (Basmajian and Deluca, 1985). Fine wire electrodes are surgically implanted into the muscle and the data generated are more accurate than those from surface electrodes, which are attached to the skin just superficial to the muscle in question (Loeb and Gans, 1986). Electromyography studies have been performed on various species for different muscles and muscle groups (English, 1978; Stern and

Susman, 1981; Jayne, 1988; Reilly, 1995). In these studies, synergistic muscles have been shown to be active at different gait phases. O’Donovan et al. (1982) showed that, in the domestic cat, M. flexor digitorum longus is active during the swing phase and M. flexor hallucis longus is active during the stance phase of locomotion. It was also suggested that M. flexor hallucis longus may be contributing to forward propulsion.

Muscle fiber or architecture analysis has been widely used to study muscle morphology and function. Fiber length, pennation angle, and muscle weight values are used to analyze the physiological cross-section of a muscle (Williams, 2008;

Anapol, 2003; Sacks, 1982). These data can be used to estimate a muscle’s force production and speed of contraction. This analysis has been performed in animals including reptiles (Zaaf et al, 1999; Gans et al 1985), birds (Shear and Goldspink,

1999; Vertstappen et al, 1998), primates (Oishi et al, 2008; Carlson, 2006; Payne et al, 2006), and carnivores (Williams et al, 2008; Sacks and Roy, 1982).

The information gathered from muscle fiber analyses has been compared among species that employ different locomotor patterns. In separate studies, Anapol and colleagues (2004, 2003, and 1996) compared the forelimb and hindlimb

muscles of semiterrestrial and arboreal guenons. In the forelimb, Mm. deltoideus, teres minor, and coracobrachialis had higher estimated force production values in the arboreal red-tailed monkey and Mm. teres major and triceps brachii had higher potential velocity-excursion values in the semiterrestrial vervet. In the hindlimb,

Mm. vastus lateralis and gastrocnemius lateral head showed higher force production values for the arboreal guenon. They suggested that the force may be directed medially from the lateral aspect of the thigh and leg during arboreal locomotion to support and balance on a substrate that is narrower than the body width. The results of these studies emphasize the importance of muscle morphology analysis to demonstrate locomotor differences.

While muscle fiber analysis provides useful information, it is also helpful for establishing the location of muscle attachment sites to evaluate attachment site surface areas and biomechanical information. Muscles with larger attachment sites have an increased number of muscle fibers, which leads to an increased force production by the muscle (Werdelin, 1986; Taylor, 1974; Anemone, 1993; Wang,

1993; Heinrich and Houde, 2006). This was explored previously in my Master’s thesis and the results were subsequently published (Carlon, 2012; Carlon, 2010).

Here, the hindlimb muscle attachment site surface areas were measured and compared between F. catus and N. nebulosa. Mm. rectus femoris and quadratus femoris sites were larger in N. nebulosa in comparison to those in F. catus. These results are in agreement with those of previous publications that studied and commented on these muscle attachment sites of arboreal species (Warburton, 2013;

Heinrich and Houde, 2006; Laborde, 1987). In addition, to determine if the muscle attachment surface area differences could distinguish between closely and distantly related species, pelvic muscle maps for C. latrans and V. vulpes were included in the analysis. The differences between felids and canids were much greater than the intraspecies variations, suggesting that surface area analysis may be a useful method for assessing phylogenetic relationships.

Determining the exact location of muscle attachment sites is necessary to evaluate muscle and limb biomechanics. Muscle mechanical advantage (l/h) is defined by the ratio of the force arm, or the perpendicular distance from the applied force to the fulcrum (l), to the resistance arm, or the perpendicular distance from the resistance to the fulcrum (h) (Hay and Reid, 1988; Smith and Savage, 1956). The force arm and resulting mechanical advantage increases as the muscle insertion point is located farther away from the fulcrum. Muscles with greater mechanical advantage are geared for higher force production and are called low gear muscles (Hildebrand,

1974). Cursorial animals, by contrast, have limbs adapted for high velocity excursion and have both a shorter lever arm and longer resistance arm.

Smith and Savage (1956) have examined muscle mechanical advantage differences in a comparison between Equus and Dasypus forelimbs. Dasypus is a highly fossorial species that depends on the strength of its limbs to overcome resistance while digging through soil. Equus is highly cursorial and the limbs must move as rapidly as possible relative to the body. The study showed that Dasypus M. teres major has a 1/4 mechanical advantage compared to a 1/13 advantage for the

same muscle in Equus (Smith and Savage, 1956). The increased length of the Equus limbs supplements the small ratio of mechanical advantage resulting in rapid limb movement.

Bone morphometric analysis is important in comparative morphology studies.

There are two types of bone morphometric analytical methods, linear and geometric morphometrics. Linear morphometrics compares bone segment length ratios. It has been used in numerous studies to analyze a variety of species (Anyonge, 1996; Gebo and Sargis, 1994; Garland, 1993; Rodman, 1979; Gonyea, 1976). The position of muscle attachment sites relative to the joint center can be measured to evaluate mechanical advantage. For example, Rodman (1979) measured the relative position of the radial tuberosity, olecranon process, and lesser trochanter and compared the values between arboreal and terrestrial macaques. The muscle insertion sites were farther away from the joints in the arboreal species, increasing the mechanical advantage of the muscles.

In linear morphometrics, homologous and evenly spaced landmarks are chosen and the lengths between the landmarks are measured. This was dubbed as the box truss analysis by Bookstein (1982). The major problem with linear morphometrics is that, due to their high number, not all possible combinations of segment lengths can be determined. For example, twelve chosen landmarks may yield more than a hundred different combinations of length segments. Subsequently, the experimenter may analyze only thirty of them. In addition, many if not most segment lengths may be redundant but it is hard to know which are more important

until the complete analysis is performed. It is also difficult to choose the most biologically relevant segments to analyze. Moreover, increasing the number of the length segments will require a higher sample size (Kocovsky et al, 2009).

Because the length segment is not examined in the traditional morphometrics, the number of shape differences that may be resolved is limited. We cannot examine how one landmark is positioned relative to the landmarks that are more dorsal, caudal or anterior. Thus, the shape as a whole is not analyzed. The landmark coordinates are also lacking from the distance measurements. Coordinates contain information about the relative positioning of the landmarks. The results of box truss analysis takes the form of numbers listing distance measurements making it more difficult to visualize small shape changes in the specimens. Furthermore, length segments ratios require data transformation, such as logarithmic or arcsine transformations, before they can be subjected to statistical analyses. This is due to proportions that form a binomial rather than a normal distribution (Zar, 1999).

Geometric morphometrics, a new approach to morphometric analysis, more accurately measures the shape differences among specimens. It is based on the

Kendall (1977) definition of shape space, which theorizes that an object’s shape is not altered by changing its location, scale (size), or by rotating it. This principle employs superimposition as a technique that aids in the comparison of specimens. In

Generalized Least-Squares Procrustes superimposition, the corresponding landmarks’ sum of squared distances for each of the specimens is minimized by centering all landmarks on a central origin (Rohlf, 1990). The landmark

configuration is then superimposed on a model landmark configuration. This is accomplished by translocating the configurations (entire set of landmarks) of each specimen on top of each other. Then, the configurations are scaled to the same size by minimizing the sums of squared distances between landmark configurations of each specimen by centering all landmark configurations on the common origin, or centroid. So, if the landmarks are further apart in one specimen compared to another, they are brought closer without altering the shape. The configurations may also be rotated if their orientations are at different angles. For example, one configuration may be at a 45 degree angle compared to the other. In summary, this process brings the separate configurations closer together. Finally, the new landmark configurations can be analyzed using the Principal Components Analysis (PCA) to show shape changes.

To date, geometric morphometrics has been mainly conducted on skulls to indicate differences in bite force in extant and extinct animals (Goswami et al, 2011;

Sicuro, 2011; Christiansen, 2008; Stayton, 2005; Singleton, 2002). More recently, however, the postcranium has been gaining attention. Among the forelimb bones analyzed are the scapula of marsupials, rodents, and primates (Astua, 2009; Morgan,

2009; Young, 2008), humerus of primates, musteloids, and felids, (Fabre et al, 2013;

Holliday and Friedl, 2013; Arias-Martorell et al, 2012; Walmsley et al, 2012;

Halenar, 2011; Schultz and Guralnik, 2007), radius of primates (Tallman, 2012), and ulna of musteloids and primates (Fabre et al, 2013; Halenar, 2011; Drapeau, 2008;

Schultz and Guralnik, 2007). Fewer studies exist for hindlimb bones: femur

(Sylvester and Pfisterer, 2008; Harmon, 2007; Schultz and Guralnik, 2007), and tibia

(Turley and Frost, 2014; Frelat et al, 2012; Turley et al, 2011; Schultz and Guralnik,

2007). Comparative geometric morphometric analysis of the pelvis is lacking in this literature.

The purpose of this dissertation is to examine felids and canids with different locomotor patterns of behavior. I employ muscle and bone morphometric methodologies to identify morphological characters associated with locomotion to compare closely phylogenetically related extant and extinct species. The extant felids analyzed include Felis catus (domestic cat), Neofelis nebulosa (clouded leopard), Acinonyx jubatus (cheetah), and Panthera leo (lion). The extant canid used is Vulpes vulpes (red fox). The extinct felids are Panthera atrox (American lion) and

Smilodon fatalis (saber-tooth cat), and the extinct canid is Canis dirus (dire wolf).

The bones of these species were analyzed using geometric morphometrics. In addition, F. catus, N. nebulosa, and V. vulpes cadaver specimens were dissected.

Their forelimb muscle attachment sites were located and muscle fiber analysis was conducted.

CHAPTER 2

SPECIES BACKGROUND INFORMATION

Phylogenetic studies of molecular and morphological characters have separated Carnivora into two superfamilies, Feliformia and Caniformia (Wozencraft,

1989; Wilson and Reeder, 1993; McKenna and Bell, 1997; Flynn and Nedbal, 1998;

Bininda-Emonds et al., 1999), as had Simpson (1945) before the development of molecular studies. These studies place Felidae within Feliformia, a group that also includes Hyaenidae, Herpestidae, and Viverridae. Caniformia is composed of seven families: Canidae, Procyonidae, Mustelidae, Ursidae, Otariidae, Phocidae, and

Ailuridae. This study primarily considers two of the carnivore families, the Felidae within the Feliformia subgrouping and the Canidae within Caniformia.

These two carnivore families, the Felidae and the Canidae, differ in habitat preference and hunting style as evidenced by morphological differences (Taylor,

1989). In addition, felids show intra-familial diversity in habitat and hunting adaptations, which are reflected in diverse morphologies. Canids are adapted primarily to open terrains, while felid habitats include a wide variety of terrains, ranging from open plains to dense forest (Ewer, 1973). Predictably, carnivore modes of locomotion are adapted to these habitats. Felids can be arboreal, scansorial, or terrestrial; while canids are strictly terrestrial, with the exception of Urocyon

16 cineroargenteus (gray fox) which is able to climb trees (Yaeger, 1938; Terres, 1939;

Taylor, 1989).

Felid hunting styles also vary within the family. Stalking and ambush predation is common among the larger felids, which involves grappling with prey

(Van-Valkenburgh, 1985; Taylor, 1999) while the pounce-pursuit hunting style involves a short chase or ambush if prey is close by (Van Valkenburgh, 1985).

Pounce-pursuit predators wrestle with prey less often than do ambush predators

(Ewer, 1973). Acinonyx jubatus (cheetah), however, is generally associated with canids in that it uses the pursuit method for prey acquisition often involving a long distance chase with little prey grappling (Van Valkenburgh, 1985; Taylor, 1989;

Nowak, 2005). Predators that employ the pursuit hunting style are generally considered cursors (Taylor, 1989).

Hunting style differences have been correlated with skull and tooth morphology. Felids have muzzles that increase biting force at the anterior part of the mouth, and they use strong canine teeth with round cross-sections, specialized to deliver a killing bite while wrestling with prey (Van Valkenburgh, 1996; Sunquist and Sunquist, 2002; Nowak, 2005). Canids, in contrast, have long muzzles and knife- like canine teeth which are used to bite and pull down prey during the chase and eventually to deliver many slashing wounds to weaken prey (Sunquist and Sunquist,

2002; Nowak, 2005). Group hunting is, therefore, advantageous among canids (Estes and Goddard, 1967).

Limb morphology is also correlated with the functional characteristics of felids and canids. Some carnivores are adapted to open-terrain, and they rely on speed to catch prey. They are called cursors and are represented in this paper by A. jubatus and canids. Their limbs exhibit smaller proximal to distal bone length ratios than other felids (Ewer, 1973; Taylor, 1989). Limb muscle mass in cursors is concentrated more proximally, and muscle insertions in these forms are closer to the joints to increase the speed of contraction compared with non-cursorial species

(Taylor, 1989). In addition, the concavities of limb joint articular surfaces are deeper to stabilize joints and restrict movement in the sagittal plane (Ewer, 1973; Jenkins,

1973).

In the present study, felid and canid species were chosen to represent a variety of locomotor groups, habitats, and major hunting styles. Some of the species included in the study of muscular anatomy were selected based on specimen availability, which were felids Neofelis nebulosa (clouded leopard) and Felis catus

(domestic cat) and canid Vulpes vulpes. In addition to these species, extant felids

Panthera leo (lion) and Acinonyx jubatus (cheetah) and extinct species from the

George C. Page museum Smilodon fatalis (saber-tooth cat), Panthera atrox

(American lion), and Canis dirus (dire wolf) limb bones were analyzed by geometric morphometric analysis. The fossil bones excavated from the tar pits are exquisitely preserved, permitting accurate muscle scar identification. The information gathered from these extant species was then used to postulate possible functional behaviors of

18 these extinct species. This chapter will provide the background information on selected carnivore species utilized in this study.

Felids

A. Neofelis nebulosa, the clouded leopard, is a medium-sized (16-23 kg) felid distributed throughout Southeast Asia belonging to the Panthera lineage

(Sunquist and Sunquist, 2002; Wozencraft, 2005). Its coat displays cloud-shaped markings, making the pelt valuable to illegal traders (Barnes, 1989). It is listed as endangered on appendix I of CITES and classified as vulnerable by the IUCN

(Baillie and Groombridge, 1996; Nowell and Jackson, 1996; Nowak, 2005).

The preferred habitat of N. nebulosa is dense primary forests (Raffles, 1821;

Selous and Banks 1935). It is considered to be the largest arboreal felid, and is capable of climbing headfirst down a tree trunk or moving upside down across horizontal branches (Hemmer, 1968; Sunquist and Sunquist, 2002). It hunts prey both in trees and on the ground, using the stalk and ambush type hunting behavior and prefers to feed off the ground while sitting on tree branches (Austin and Tewes,

1999; Ghose, 2002).

N. nebulosa skull and canine tooth morphology have been studied extensively using linear and geometric morphometric techniques (Van Valkenburgh and Ruff,

1987; Christiansen, 2006 and 2008; Meachen-Samuels and Van Valkenburgh, 2009;

Sicuro, 2011; Meloro and Slater, 2012). N. nebulosa has the longest upper and lower

19 canine teeth relative to skull length of any extant felid (Christiansen, 2006). The temporal fossa of the skull is expanded, indicating a robust M. temporalis

(Christiansen 2006). A perpendicular angle between the coronoid process of the skull and the line of action of M. temporalis increases the muscle’s leverage, thus increasing the bite force and resisting forward bending forces exerted by struggling prey (Sicuro and Oliviera, 2011).

Linear morphometric studies of limb bones have shown that N. nebulosa has shorter and more robust distal limb bones compared to proximal segments, wider humeral and femoral epicondyles, and elongated manual digits, compared to cursorial species (Gonyea, 1976; Van Valkenburgh, 1987; Meachen-Samuels and

Van Valkenburgh, 2009; Samuels et al., 2013). Gonyea (1978) has shown that N. nebulosa has a larger olecranon fossa angle relative to the long axis of the humerus, and a more robust lateral olecranon process tuberosity than that seen in cursorial species. The author proposed that these characteristics increase the forearm rotational capability. Walmsley and colleagues (2012) performed geometric morphometric analysis on the proximal and distal epiphyses of the humerus and found that N. nebulosa, along with other arboreal felids, possess a narrower lesser tubercle of the humerus, and a smaller medio-lateral width of the humeral trochlea than terrestrial felids. No geometric morphometric analysis of other limb bones has been published for this species.

Aside from my own publications, muscular morphologic studies of N. nebulosa are absent from the literature. In my Master’s thesis, I compared the hind

20 limb muscle weights and attachment sites of N. nebulosa to F. catus (domestic cat) and partially to C. latrans (coyote; Carlon, 2009, 2012). However, there appears to be nothing published on the forelimb muscle study of N. nebulosa.

B. Felis catus, or domestic cat, is a small felid with weighs ranging from four to six kg. It is believed to have been domesticated in Egypt from the African wildcat

Felis silvestris (Sunquist and Sunquist, 2002). The exact time of domestication, however, remains controversial. Unlike N. nebulosa, F. catus and F. silvestris mainly hunt on the ground, although some prey is caught in the trees (Sunquist and

Sunquist, 2002).

In contrast to the hunting style of N. nebulosa, F. catus more frequently uses a pounce-pursuit hunting style rather than ambushing its prey. It lunges at the prey at close quarters, or performs a short fast rush to capture running prey (Leyhausen,

1979; Sunquist and Sunquist, 2002). Hindlimbs provide the force for leaping on the prey, and the forelimbs grasp and position the prey. This action is followed by a killing bite delivered at the neck (Turner and Bateson, 2000; Leyhausen, 1979). The preferred prey size is similar to or smaller in body size to F. catus and includes rodents, small mammals, fish, reptiles, birds (Sunquist and Sunquist, 2002).

While F. catus has become domesticated, F. silvestris has not. Thus, F. silvestris offers a possibly more accurate view of this felid’s behavioral characteristics. F. silvestris frequents woodlands and grasslands, but it prefers scrubby landscapes to provide for cover for hunting (Sunquist and Sunquist, 2002).

Similar to F. catus, F. silvestris is scansorial and spends most of its time on the

21 ground but can climb if pursued (Nowak, 2005). It prefers to be close to prey before pouncing (Turner and Bateson, 2000; Sunquist and Sunquist, 2002). F. catus and F. silvestris hunt similarly small sized prey that requires less grappling to subdue

(Leyhausen, 1979). One major difference between the two species is that F. silvestris has a longer forelimb to hindlimb ratio compared to F. catus, causing F. silvestris’s movements to be more similar to those of A. jubatus (Sunquist and Sunquist, 2002).

Linear morphometric studies involving limb bone ratios have been performed with F. catus and F. silvestris in comparison to other felids (Steudel and Beattie,

1993; Harris and Steudel, 1997; Schmidt and Fischer, 2009; Meachen-Samuels and

Van Valkenburgh, 2009). These studies found that F. catus and F. silvestris had limb proportions similar to other scansorial and small felids that use the same pounce- pursuit hunting style. Geometric morphometric analyses of the skull (Reig et al.,

2002) and humeral epiphysis (Andersson, 2004; Walmsley et al., 2012) have been performed for F. silvestris.

Previous studies have described F. catus limb muscle morphology (Sacks and

Roy, 1982; McConathy et al., 1983; Harris and Steudel, 2002; Carlon, 2010, 2012;

Goto et al., 2013) and limb muscle electromyography (English, 1978; O’Donovan et al., 1982; Hoy and Zernicke, 1985; Pierotti et al., 1989). Sacks and Roy (1982) reported F. catus hindlimb muscle fiber analysis which showed that the hamstring muscles are associated with high velocity limb movement while the quadriceps femoris muscle group provides greater force. F. catus or F. silvestris forelimb muscle fiber analysis has not been published to date.

C. Panthera leo (lion), distributed across sub-Saharan Africa and parts of

Northwestern India, prefers wooded grasslands and short grass plains but can also inhabit deserts (Sunquist and Sunquist, 2002). Female lions weigh 83-168 kg and males weigh 145-225 kg (Silva and Downing, 1995). P. leo is mainly terrestrial, however, it has been seen climbing trees to escape large animals such as buffalos and elephants (Guggisburg, 1961; Makacha and Schaller, 1969).

P. leo predominantly uses the pounce-pursuit mode of hunting and shows both solitary and cooperative hunting behaviors (Sunquist and Sunquist, 2002;

Nowak, 2005; Schaller 2009). The animal prefers to be within thirty meters of prey before beginning the chase, after which it knocks the prey off balance using a forelimb blow to the rump or by slamming its body into the animal (Sunquist and

Sunquist, 2002). During grappling, both forepaws are used, while the hindlimbs remain on the ground (Sunquist and Sunquist, 2002; Schaller, 2009). A bite to the throat of the prey is administered to strangle the animal (Leyhausen, 1965; Ewer,

1973; Biknevicius and Van Valkenburgh, 1996; Sunquist and Sunquist, 2002,

Nowak, 2005; Wroe et al., 2005; Wheeler, 2011).

Stander (1992) observed the cooperative hunting by P. leo. He saw that a few lions wait close to the prey by hiding in the tall grass or bushes, while others wait in a circle around the prey. If any prey animals escape from the lionesses in the center, they are caught by the lionesses waiting at the periphery.

P. leo specializes in hunting prey that weigh as much or more than themselves (Sunquist and Sunquist, 2002, Nowak, 2005). The large prey include

23 wildebeests, zebras, giraffes, and buffalo (Prins and Iason, 1989; Sunquist and

Sunquist, 2002). The killing of large prey is accomplished through cooperative hunting (Sunquist and Sunquist, 2002). Small prey, such as hares, chital deer, impalas, porcupines, are caught if larger prey is not available, but provide less meat, especially if the kills are shared with the other members of the pride (Eloff, 1973;

Ruggiero, 1991). Therefore, P. leo pride prefers to hunt large prey over small

(Sunquist and Sunquist, 2002).

Studies of limb bone length ratios of P. leo have grouped it with other terrestrial felids living in open environments and using the pounce-pursuit hunting style (Harrington, 1969; Gonyea, 1976, 1978; Anyonge, 1996b; Harris and Steudel,

1997; Meachen-Samuels and Van Valkenburgh, 2009; Meloro et al., 2013).

Harrington (1969) and Anyonge (1996b) have commented on the similarity of P. leo to the extinct P. atrox, based on limb proportions. Hartstone-Rose et al. (2012) showed the similarity of P. leo and P. atrox clavicles. However, Anyonge (1996b) noted that the cross-sectional geometric properties of the P. atrox limb bones approach those of Ursus arctos (brown bear). According to Kurten (1952),

Scandinavian bears, in preparation for the killing bite, place one paw over the prey’s shoulder and one paw over the face. This bends the prey’s head, which exposes its arch of the throat and brings blood vessels in ventral neck upward (Wheeler, 2011).

The similarity of P. atrox limb bones to U. arctos may indicate similar hunting behavior and increased need for musculo-skeletal strength in P. atrox.

Geometric morphometric studies on P. leo have been predominately published for the skull (Wroe and Milne, 2007; Christiansen, 2008; Christiansen and

Harris, 2009; Meloro, 2011; Meloro and Slater, 2012; Piras et al., 2013). Proximal and distal epiphyses of the humerus were also analyzed through geometric morphometrics that grouped P. leo with other felids that grapple with prey and use terrestrial locomotion (Andersson, 2004; Walmsley et al., 2012).

In addition to bone morphometric studies, the muscular anatomy of P. leo has been published by Cuvier and Geoffroy (1824), Haughton (1867) and Barone (1967).

However, the muscle maps of the limb muscles are not extensive. Also, limb muscle fiber analysis is lacking in the literature.

D. Acinonyx jubatus, the cheetah, is a medium-sized felid weighing in the range of 40 to 65 kg (Caro, 1991). It is distributed in central, eastern, and southern

Africa, but is also seen in some Asian countries, such as Afghanistan and Pakistan

(Sunquist and Sunquist, 2002). Habitat of A. jubatus is sandy plains, grassy plains, and open woodlands, but it prefers habitats with grassy cover to hide from its predators, such as lions, leopards, and hyenas (Caro, 1994; Sunquist and Sunquist,

2002; Nowak, 2005).

Most of the prey that A. jubatus hunts weigh less than 40 kg, or less than the body weight of A. jubatus (Sunquist and Sunquist, 2002). The preferred prey includes impala, Thomson’s and Grant’s gazelles, reedbuck, springbok, and warthogs (Mills, 1984; Sunquist and Sunquist, 2002). Large prey like wildebeests of

80 kg are hunted cooperatively. In this case, the prey is chased among the cheetahs until the animal is brought to exhaustion (Sunquist and Sunquist, 2002).

A. jubatus employs a fast pursuit chase to catch prey by accelerating rapidly

(Ewer, 1973; Taylor, 1989; Turner and Anton, 1997). Unlike canids, it does not pursue prey for long distances, giving up after a few hundred meters (Kruuk and

Turner, 1967; Sunquist and Sunquist, 2002) A. jubatus likes to approach prey using tall grass cover. But if there is not enough cover, A. jubatus openly stalks animals by using slow and fast approach techniques (Sunquist and Sunquist, 2002). The slow approach involves repetitive running forward and stopping to get within thirty meters of prey; the fast approach is done by trotting openly up to prey and starting the run when within 200 meters (Frame, 1975; Caro, 1994). During the chase, A. jubatus hooks the prey’s hindlimb with its curved dewclaw or strikes the prey’s rump with the forepaw, to bring down the animal (Sunquist and Sunquist, 2002). Once the animal is on the ground, the killing bite to the throat is administered, which closes off the trachea and suffocates the animal (Caro, 1994).

Hildebrand (1959, 1961, and 1975) commented on the running characteristics of A. jubatus, especially on the curvature of the back and how it differs from other felids. The hyperextension of the back during the stride provides the ability of the forelimbs to reach farther forward and prolongs propulsion of the body off the ground. During landing, the back is flexed, causing the hindlimbs to touch the ground farther forward than forelimbs to increase stride length. Hudson et al. (2012) showed that A. jubatus uses a lower stride frequency but a longer stride length than a

26 racing greyhound (Canis familiaris). A. jubatus also supports more of its body weight on its hindlimbs than the greyhound, which may help to reduce the risk of slipping, especially when chasing a zig-zagging animal.

A. jubatus morphology shows adaptations to cursoriality and the use of a pursuit hunting style. It is short-faced and lacks a prominent sagittal crest, which reflects a shorter temporalis muscle than is seen in other felids. This morphology reduces the gape and bite force (Ewer, 1973; Sunquist and Sunquist, 2002), and is correlated to the cheetah’s unspecialized killing bite (Ewer, 1973). The clavicle is small relative to body size when compared to other felids, which allows the scapula to swing farther antero-posteriorly, therefore, increasing the stride length (Ewer,

1973). Hartstone-Rose et al. (2013) also reported a thicker acromial end of the clavicle in A. jubatus than in other felids, which may serve as an increased area of muscle attachment.

The limb bone morphology of A. jubatus shows major cursorial adaptations.

When compared to other felids, it has a large humeroradial index, in which the radius is longer than the humerus, and a large femorotibial index, or a longer tibia than the femur (Gonyea, 1976; Anyonge, 1995). These traits are seen in other cursorial species. Other cursorial features in A. jubatus are long metatarsals relative to femur length, long metacarpals relative to phalanges, caudally bent olecranon process of the ulna, and less-curved claws (Van Valkenburgh, 1985, 1987). Long metacarpals and metatarsals increase the stride length (Ewer, 1973). A caudally bent olecranon

27 process increases the leverage of M. triceps brachii when the elbow is extended

(Taylor, 1974).

Geometric morphometric analysis of A. jubatus bones have been published mainly for the skull and mandible (Wroe and Milne, 2007; Slater and Van

Valkenburgh, 2009; Prevosti et al, 2010; Sicuro, 2011; Christiansen and Harris,

2012; Meloro and Slater, 2012; Segura et al., 2013; Geraads, 2014). When compared to other felids, these results showed it to have a shorter but laterally wider skull, and antero-posteriorly shorter dentary with flared coronoid processes. These traits were also seen in extinct cheetah-like cats such as, Miracinonyx inexpectatus and

Miracinonyx trumani (Van Valkenburgh et al., 1990; Sicuro, 2011). Proximal and distal humeral epiphyses have been analyzed using geometric morphometrics

(Andersson, 2004; Walmsley, 2012). These studies found A. jubatus to have wider lesser tubercle, mediolaterally narrower distal humeral epiphysis, increased depth of the mid-trochlear furrow, and increased size of humero-ulnar articulation site on trochlea. The characteristics were opposite of those in arboreal felids and more similar to canids and hyaenids.

Valuable studies on limb muscles of A. jubatus exist in the literature

(Williams et al., 1997; Hudson et al. 2011). Fiber type composition of Mm. vastus lateralis, gastrocnemius, and soleus were recorded by Williams and his colleagues

(1997). In the forelimb muscle fiber analysis study by Hudson and his colleagues

(2011), A. jubatus had higher physiological cross-sectional areas for Mm. supraspinatus, infraspinatus, subscapularis, and teres major, extensor digitorum

28 communis, and digital flexor muscles than those of the racing greyhound (C. familiaris). The authors suggested that this may be an adaptation for making rapid, high angle turns during prey chases by A. jubatus (Hudson et al., 2011a). In the hindlimb, A. jubatus had lower physiological cross-sectional areas for Mm. biceps femoris and pectineus and a higher value for M. psoas major than the greyhound

(Hudson, 2011b). The back muscles of A. jubatus, instead of hip extensor muscles, may be generating the force necessary for rapid acceleration, and M. psoas major is used for forceful protraction of the hindlimb in canids and felids (Hudson, 2011b).

Canids

Vulpes vulpes, or the red fox, is a small canid weighing between 4.1 and 5.4 kg (Ables, 1975, Nowak, 2005). It is distributed in Eurasia, northern Africa, northern

India, Canada, and the United States (Ables, 1975; Lloyd, 1975; Stains, 1975;

Nowak, 2005). The habitat is highly variable, ranging from farmland and open prairie to dense forests (Ables, 1975; Nowak, 2005). V. vulpes is highly terrestrial, able to run at speeds of 48 km/hr (Haltenorth and Roth, 1968). Its prey mostly consists of rodents and small mammals such as mice and rabbits, but its diet also includes insects and fruits (Ables, 1975; Nowak, 2005). It has also been observed to scavenge on dead livestock and the afterbirths of cattle (Lloyd, 1975).

V. vulpes uses the pursuit hunting style, either by outrunning prey or approaching stealthily before the final rush (Murie, 1936; Scott, 1947; Ables, 1975).

These methods are similar to those described previously for A. jubatus. Once close to the prey, V. vulpes leaps on it with stiffened forelimbs to pin it down (Scott,

1947). Bites to the pectoral region of prey may be administered to pull it to the ground (Ables, 1975).

V. vulpes has been included in studies comparing the skull and mandible shape among canids and extant and extinct hyaenids (Werdelin, 1989; Van

Valkenburgh et al., 2003; Ferreti, 2007). In these studies, V. vulpes grouped with C. lupus in premolar shape, longer snout but narrower mandible (shorter inter-coronoid process length), and flatter forehead when compared to hyaenids. The hyena features aid to dissipate the forces encountered during bone crushing. Postcranial bone studies of V. vulpes are few in the literature. Van Valkenburgh (1985, 1987) included

V. vulpes in comparative studies of terrestrial versus arboreal carnivores. It grouped with the terrestrial species in having longer metacarpals relative to phalangeal lengths, longer metatarsals relative to femur length, and a shorter olecranon process angled more caudally relative to those of arboreal carnivores. These characteristics were similar to those observed for A. jubatus. After an extensive review of the literature, no geometric morphometric skeletal analysis or detailed muscular anatomical study has been published to date for V. vulpes.

Extinct Species

A. Smilodon fatalis was a saber-tooth cat known from the late Pleistocene belonging to the subfamily Machairodontinae (Turner and Anton, 1997; Hoek et al.

2006; Christiansen, 2013). Its bones are found primarily in North America but are also known from Pacific coastal areas of South America (Kurten and Werdelin,

1990; Turner and Anton, 1997). It is larger than Smilodon gracilis, a counterpart from the early Pleistocene known from the southeastern part of North America

(Turner and Anton, 1997; Christiansen and Harris, 2005). However, it is smaller than

Smilodon populator, which is known from the eastern part of South America (Turner and Anton, 1997; Christiansen and Harris, 2005). Body size estimate studies using limb bone ratios of the three species assigned a weight of 55-100 kg for S. gracilis,

160-280 kg for S. fatalis, and 220-360 kg for S. populator (Christiansen and Harris,

2005). S. fatalis upper canine teeth are of the dirk-tooth type, long and narrow with fine serrations (Kurten, 1968; Martin, 1980; Wheeler, 2011). It has been shown that long canine teeth are more prone to breakage (Binder and Van Valkenburgh, 2010).

Anyonge (1996a) reported less microwear on S. fatalis canine teeth than seen in extant predators, and suggested that S. fatalis avoided contact with prey bones during hunting and feeding. However, its carnassial microwear is similar to bone crushing canids, which may indicate that S. fatalis consumed the bones of carcasses, as well as the flesh (Binder and Van Valkenburgh, 2010; DeSantis et al., 2012).

It has been proposed that S. fatalis used the canine shear bite technique to kill its prey (Akersten, 1985; Martin, 1980; Christiansen, 2006; McHenry et al., 2007).

Skull and mandible biomechanical studies found that S. fatalis had less mechanical advantage for M. temporalis and decreased jaw adductor muscle force generation capaibility than in felids of comparative size (Christiansen, 2007; McHenry et al.,

2007). Researchers have suggested that neck muscles were used to flex neck and stab prey with the canine teeth. Because of the weak jaw adductor muscles and easily breakable canine teeth, it was harder to resist the extrinsic lateral forces incurred by struggling prey (Therrien, 2005a; McHenry et al. 2007; Binder and Van

Valkenburgh, 2010). Therefore, it was important for S. fatalis to subdue the prey completely before initializing the canine shear bite.

Postcranial bone studies place S. fatalis in the ambush predator category

(Gonyea, 1976; Anyonge, 1996; Meachen-Samuels and Van Valkenburgh, 2010;

Meachen-Samuels, 2012; Samuels et al., 2013). Similar to arboreal felids and ambulatory carnivores, S. fatalis exhibits a low ratio of radius to humerus bone lengths, low ratio of tibia to femur bone lengths, and nearly equal lengths of anterior and posterior limbs (Gonyea, 1976; Anyonge, 1996). But antero-posterior thickening of humerus and femur is more similar to cursors than ambulators (Anyonge, 1996).

Traits such as high humeral and femoral cross-sectional areas and wide epicondyles are indicative of the use of forelimbs to subdue prey (Meachen-Samuels and Van

Valkenburgh, 2010; Meachen-Samuels, 2012; Samuels et al., 2013).

Geometric morphometric studies have been performed mainly on the skulls and mandibles of S. fatalis to infer bite force, as explained above (Christiansen,

2008; Meloro, 2011; Christiansen and Harris, 2012). Martin-Serra and colleagues

(2014) included Smilodon in the geometric morphometric study of forelimb bones; however, they listed the name as “Smilodon sp.” and did not specify which species of

Smilodon was actually studied. The results showed that the S. fatalis scapula, humerus, ulna, and radius bones were more robust than the other terrestrial carnivores such as canids and hyaenids. The radial tuberosity was more laterally positioned and the radial styloid process was more expanded than in ursids and procyonids.

B. Panthera atrox was a conical-toothed cat from the Pleistocene era and was distributed in North America and possibly parts of northwestern South America

(Merriam and Stock, 1932; Martin, 1980; Kurten and Anderson, 1980; Turner and

Anton, 1997). It belongs to the subfamily Felinae, along with modern felids (Turner and Anton, 1997; Christiansen, 2009). Its body size is estimated to be larger than S. fatalis based on skull and limb bone lengths (Anyonge, 1993; Christiansen and

Harris, 2009; Meachen-Samuels and Van Valkenburgh, 2010).

There is dispute among researchers on the phylogeny of P. atrox. It has been considered to be a close relative of the extinct Eurasian cave lion Panthera leo spelaea/Panthera spelaea and extant African lion, Panthera leo, based on similar skull and limb bone dimensions (Kurten, 1965, 1985; Harrington, 1969; Herrington,

1986; Turner and Anton, 1997). Others have suggested that the P. atrox skull

33 morphology more closely resembles that of P. onca (jaguar) (Kabitzsch, 1960;

Dietrich, 1968). Christiansen and Harris (2009) analyzed and compared the craniomandibular linear morphometrics of P. atrox with extant P. leo, P. onca, and

P. tigris. They found that P. atrox was similar to P. leo in the position of the frontal- nasal suture and incisive foramina and elongated muzzle. But a rectangular mandibular ramus and a long and ventrally deflected angular process were P. onca and P. tigris affinities. Based on these findings, Christiansen and Harris (2009) suggested that P. atrox did not derive from the extinct Eurasian or Asiatic lion but its ancestor entered North America at an earlier time than the Old World lion evolution.

Study of P. atrox skull and mandibular suggests that its canine bite was strong; however the mandibular symphysis was not adapted to withstand lateral torsion incurred by struggling prey (Therrien, 2005b). P. atrox data were more similar to those of N. nebulosa than of P. leo. The author suggested that P. atrox had to subdue prey before administering the killing bite, to prevent mandibular injury

(Therrien, 2005b). This specific study did not include S. fatalis or any other sabertooth predator.

The humerus and femur of P. atrox were found to be robust when compared to felids of similar size. This conclusion placed P. atrox in the ambush group, rather than the cursorial felid group (Anyonge, 1996; Sorkin, 2008; Meachen-Samuels and

Van Valkenburgh, 2010). The distal to proximal limb bone ratios of P. atrox were also comparable to those of ambush predators (Anyonge, 1996). However, the values obtained fell short of S. fatalis. This suggests that P. atrox did not grapple with prey

34 as much as did S. fatalis. In addition, the bone robustness of radius and ulna relative to body size was more comparable to those of open-terrain felids that need less cover to ambush prey (Schellhorn and Sanmugaraja, 2014). This suggests that P. atrox used the pounce-pursuit hunting style as does P. leo.

C. Canis dirus, or the dire-wolf, is a canid that was distributed in North and

South America during the Pleistocene (Berta, 1988; Dundas, 1999; Wang and

Tedford, 2010). Based on cross-sectional and linear measures of the femur, the body mass of C. dirus was estimated to be 60-68 kg, about one-and-a-half times the size of

Canis lupus, the modern wolf (Anyonge and Roman, 2006). C. dirus is believed to have evolved from Canis ambrusteri, a fossil canid slightly smaller than C. dirus that migrated to North America from Asia in the early Pleistocene (Wang and Tedford,

2010).

Studies of skull and mandibular morphology found that C. dirus had a stronger canine bite and a greater mechanical advantage for the M. temporalis than

C. lupus (Therrien, 2005b; Wroe et al., 2005; Anyonge and Baker, 2006). The stronger bite force of C. dirus suggests that it hunted larger prey than does C. lupus

(Therrien, 2005b). Nevertheless, the overall C. dirus mandibular morphology is similar to extant canids. This led Therrien (2005b) to imply that C. dirus delivered shallow bites and used a pack hunting style to bring down prey. Bone consumption was suggested based on molar microwear, but the degree of microwear did not approach that of hyaenids or the specialized bone crushing habits of extinct borophagine dogs (Hill, 1991; Anyonge et al., 2003; Anyonge and Baker, 2006).

Morphometric studies of postcranial bones reported the similarity of C. dirus to other cursorial species (Stock et al. 1946; Nigra & Lance 1947; Stock & Lance

1948). Samuels and colleagues (2013) included C. dirus in a comparative study of limb bone ratios, and reported longer distal than proximal limb bones and relatively narrow humeral and femoral epicondyles. These traits are similar to those of cursorial species (Samuels et al., 2013). Published C. dirus geometric morphometric studies are on skull and mandible, and interpret bite force and to compare tooth wear and fracture (Wroe and Milne, 2007; Meloro, 2011; Christiansen and Harris, 2012;

O’Keefe et al., 2014). Geometric morphometric studies of limb bones appear to be absent in the literature. Table 1 provides a summary of locomotor and hunting styles for the extant species. It also includes the predicted habits of the extinct species based on the literature. The references are listed in the text above.

Table 1. Summary of Species Locomotion and Hunting Style

Species Locomotion Hunting Style Extant Species Felids Neofelis nebulosa Arboreal Ambush Felis catus Scansorial Pounce-Pursuit Panthera leo Terrestrial Pounce-Pursuit Acinoynx jubatus Terrestrial Pursuit-Cursorial Canid Vulpes vulpes Terrestrial Pursuit-Cursorial Extinct Species (Predicted) Smilodon fatalis Terrestrial Ambush Panthera atrox Terrestrial Pounce-Pursuit Canis dirus Terrestrial Pursuit-Cursorial

CHAPTER 3

MATERIALS AND METHODS

Muscle Dissection

Two deceased N. nebulosa specimens were obtained on loan from the Smithsonian

Institution (USNM, Suitland, MD). Both animals were captive bred at the Smithsonian

National Zoological Park as part of the endangered species captive breeding program and died of natural causes. Three specimens of F. catus preserved in the proprietary solution of the NASCO Biological Supply Company, from which they were purchased, were dissected. Two V. vulpes specimens were donated by the Willowbrook Wildlife Center

(Naperville, Illinois). The clouded leopards and foxes were skinned and placed in 50% ethanol in normal saline solution. The domestic cats arrived preserved, and their muscles were sprayed with a 4% formaldehyde solution in distilled water regularly to keep them moist. The forelimb muscles of each specimen were dissected and weighed. To normalize the weight data so that a comparison could be made among species, the ratio of each muscle weight to forelimb muscle total weight, referred to as “muscle weight to total ratio,” was determined. In addition, the ratio of each muscle weight to its muscle group total weight, referred to as “muscle weight to group ratio,” was calculated. Photographs were taken during the dissection using an Olympus E520 digital camera. A forelimb

muscle atlas of N. nebulosa was completed. Muscle attachment site maps were produced by outlining their perimeters on bone drawings.

Muscle Fiber Analysis

To permit easy separation of muscle fibers for the analysis, each muscle was treated using the methods described by Sacks and Roy (1982). Following removal of each muscle from a limb, it was placed in a 0.4 M phosphate buffer solution (pH 7.2) for 24-48 hours to remove residual ethanol or formaldehyde. It was then immersed in a 15% sulfuric acid solution in distilled water until the muscle fibers could easily be teased apart. This process generally lasted approximately 48 hours for each muscle. Following the acid treatment, muscles were placed back in 0.4 M phosphate buffer solution for 24 hours to remove the acid solution. Muscles were stored in a 50% glycerol solution at room temperature if measurements were not taken soon after removal from the buffer solution.

To obtain muscle physiological cross-sectional area (PCSA), muscle weight, muscle fiber length and muscle fiber pennation angle (Ө) were measured. PCSA was calculated using these variables in an equation published by Schumacher (1961) and

Haxton (1944):

PCSA= [(muscle weight) (cos Ө)] / [(fiber length) (muscle density=1.0564gcm-3)]

Muscle fiber lengths from the proximal, middle, and distal parts of the muscle were measured using SE 784EC digital caliper. These lengths were then averaged for each muscle. Muscle fiber pennation angle was taken by placing a transparent protractor’s base parallel to muscle’s line of contraction. A ruler was placed running from the protractor origin parallel to the muscle fibers allowing for determination of the corresponding fiber angle. This was done in the proximal, middle, and distal parts of the muscle in one dimension. The angles were then averaged for each muscle. Muscle density is listed as a constant of 1.0564gcm-3 (Mendez and Keys, 1960; Sacks and Roy, 1982). PCSA was then calculated and normalized by dividing each muscle PCSA by total forelimb muscle total weight. This ratio will be referred to as “PCSA to total”. Each muscle PCSA was also divided by its total muscle group weight, which will be referred to as the “PCSA to group” ratio. A high PCSA ratio indicates increased muscle force production (Sacks and Roy,

1982).

Maximum tetanic tension (P0) is an estimate of muscle force production (Sacks,

1982). It is the product of PCSA and specific tension, which is a constant (2.3 kg/cm2).

The same tension value has been used for cats (Sacks and Roy, 1982) and primates

(Anapol, 2003). Muscle mass to tetanic tension ratio (W/Po) is a measure of contraction velocity to force production. It will be referred to as “speed to force ratio”. When compared among species, a muscle with a higher speed to force ratio has increased contraction velocity, and a low ratio corresponds to stronger muscle contraction.

Muscle Attachment Surface Area Measurements

After removal of the muscles of forelimb bones of F. catus, N. nebulosa, V. vulpes forelimb bones were subjected to completion of the removal of soft tissues following the method described previously by Carlon (2012). Depending on the bone, several different views were photographed to give an optimal view of the muscle attachment sites using an

Olympus E520 digital camera. Lateral, inferior, and medial surfaces were photographed for the scapula. Medial and lateral surfaces of the humerus and ulna were photographed while cranial and caudal surfaces of the radius were photographed. Muscle attachment sites were measured as described previously by Carlon (2012). Briefly, for each specimen based either on dissection results (extant animals) or bone rugosity (extinct species) the exact muscle attachment site location was outlined on a digital photograph the of bone specimen using a graphics pad with accompanying software (Wacom). The area of the selected muscle attachment site was then determined using ImageJ 1.30v software. The ratio of each individual attachment site surface area to the sum of the muscle surface areas on the respective bone surface was determined. This number will be referred to as a particular muscle attachment site “surface area” in the following text.

Statistical Analysis

The Tukey test was performed to compare the muscle weight means, PCSA, speed to force (W/Po), and muscle attachment surface area ratios among F. catus, N. nebulosa,

40 and V. vulpes. Because ratios are not normally distributed, they were arcsine transformed prior to use in statistical analysis (Zar, 1999). Statistical analysis was carried out with

SPSS v.21.0 software.

Geometric Morphometric Analyses

An Olympus E520 digital camera was used to take photographs of the forelimb and hindlimb bones of A. jubatus, C. dirus, F. catus, N. nebulosa, P. atrox, P. leo, S. fatalis, and V. vulpes. Photographs of the specimens of the extant species A. jubatus, F. catus, N. nebulosa, P. leo, V. vulpes were taken at the National Museum of Natural

History, Smithsonian Institution (USNM) (Museum Support Center, Suitland, Maryland) and Field Museum of Natural History (FMNH) (Chicago, IL). The extinct species P. atrox, P. leo, and S. fatalis were photographed at the George C. Page Museum of La Brea

Discoveries (Los Angeles, CA) and the Field Museum of Natural History (Chicago, IL).

Table 2 lists the bones analyzed and the sample sizes for each species. Each bone from all specimens was photographed in the same orientation. Two-dimensional homologous landmarks were located and digitized on each of the photographs using the computer program tpsdig2 (Rohlf, 2004). A description of the landmarks is shown on

Tables 3-11. In addition, Figures 1-8 show the location of each of the landmarks on a photograph of an A. jubatus bone.

The landmark data sets were then analyzed using Morphologika 2 software for

Generalized Procrustes Analysis (GPA) and Principal Components Analysis (PCA)

(O’Higgins and Jones, 1998). In this analytical method, GPA reduces the sum of the squared distances between the landmark configurations of all of the specimens being analyzed by centering the landmarks on a common origin, translating the landmarks relative to each other, and scaling them all to the same relative size (Rohlf, 1990).

Following these transformations, GPA places all possible object shapes into a Kendall

Shape Space as described by Kendall (1985).

Table 2 Sample Sizes of Species for Each Bone Studied using Geometric Morphometric Analysis

A. C. F. N. P. P. S. V. Bone Views jubatus dirus catus nebulosa atrox leo fatalis vulpes Scapula with 8 10 6 8 5 9 10 8 spine Scapula- 8 10 6 8 5 9 10 8 periphery Humerus 8 6 10 8 9 8 10 8 Ulna 7 10 4 7 10 8 10 8 Radius 6 5 10 7 10 7 10 7 Glenoid Fossa 8 10 5 8 4 9 10 8 Greater 8 4 10 8 9 8 10 7 Tubercle Distal Humerus 8 10 4 8 9 8 10 7 Distal Ulna 6 4 3 4 5 5 8 5 Distal Radius 6 7 5 4 2 5 8 5 Ilium 7 10 6 7 4 5 7 8 Ischium Pubis 7 10 6 8 4 4 9 8 Femoral head 6 6 4 6 7 7 7 8 Proximal Tibia 4 6 4 4 6 4 6 4

Table 3 Scapula Outline with Spine Landmark Description

Landmark Description Number 1 Supraglenoid tubercle 2 Superior point on glenoid 3 Superior neck of glenoid 4 Between 3 & 5 5 Most superior point of supraspinous fossa 6 Between 5 & 7 7 Most caudal point (start of spine) 8 Between 7 & 9 9 Teres major tubercle 10 Midpoint on inferior border of infraspinous fossa 11 Inferior neck of glenoid 12 Infraglenoid tubercle 13 Center of glenoid 14 Mid-spine 15 Caudal point at start of metacromion 16 Tip of metacromion 17 Cranial point at end of metacromion 18 Tip of acromion

Figure 1. Scapula outline with spine landmark configuration on photograph of A. jubatus (USNM 161922) scapula.

Table 4 Scapula Periphery Landmark Descriptions

Figure 2. Scapula periphery landmark configuration on photograph of A. jubatus (USNM 161922) scapula.

Table 5 Glenoid Fossa Landmark Descriptions

Landmark Description Number 1 Inferior supraglenoid tubercle 2 Most medial point on supraglenoid tubercle 3 Medial neck of glenoid 4 Between 3 & 5 5 Most medial point on glenoid 6 Between 5 & 7 7 Most inferior point on glenoid 8 Between 7 & 9 9 Most lateral point on glenoid 10 Lateral glenoid tubercle 11 Lateral supraglenoid tubercle 12 Most superior point on supraglenoid tubercle 13 Center of glenoid fossa

Figure 3. Glenoid fossa landmark configuration on photograph of A. jubatus (USNM 161922) scapula.

Table 6 Humerus Landmark Descriptions

Landmark Description Number 1 Most distal point on head 2 Most medial point on head 3 Most proximal point on head 4 Proximal anatomical neck 5 Most proximal point on greater tubercle 6 Most lateral point on greater tubercle 7 Distal end of deltoid tuberosity 8 Between 7 & 9 9 Across from lateral supracondylar crest 10 Distal epiphyseal border (curve) 11 Medial point on capitulum 12 Distal point on capitulum 13 Lateral point on capitulum 14 Lateral supracondylar crest 15 Between 14 & 16 16 Across from 7 (distal deltoid tuberosity)

Figure 4. Humerus as a whole landmark configuration on photograph of A. jubatus (USNM 161922) humerus.

Table 7 Proximal Humerus Landmark Descriptions

Landmark Description Number 1 Most medial point on head 2 Most proximal point on head 3 Proximal anatomical neck 4 Proximal medial greater tubercle 5 Proximal lateral greater tubercle 6 Between 5 & 7 7 Most lateral point on greater tubercle 8 Lesser tubercle 9 Curve leading to head 10 Most distal point on head 11 Most distal point on greater tubercle

Figure 5. Proximal humerus landmark configuration on A. jubatus (USNM 161922) humerus photograph.

Table 8 Distal Humerus Landmark Descriptions

Landmark Description Number 1 Medial epicondyle 2 Between 1 & 3 3 Tip of trochlea 4 Between trochlea and capitulum (distal) 5 Between 5 & 6 6 Lateral capitulum 7 Between 6 & 8 8 Lateral proximal capitulum 9 Lateral epicondyle 10 Between trochlea and capitulum (proximal) 11 Proximal medial trochlea

Figure 6. Distal humerus landmark configuration on A. jubatus (USNM 161922) humerus photograph.

Table 9 Ulna Landmark Descriptions

Landmark Description Number 1 Caudal proximal olecranon 2 Cranial proximal olecranon 3 Proximal tip of trochlear notch (anconeal process) 4 Center of trochlear notch 5 Coronoid process 6 Mid ulna (cranial) 7 Distal radioulnar articular surface 8 Tip of styloid process 9 Across from 7 (curve) 10 Mid ulna (caudal) 11 Distal end of olecranon process

Figure 7. Ulna as a whole landmark configuration on A. jubatus (USNM 161922) ulna photograph.

Table 10 Distal Radial Articular Facet of Ulna Landmark Descriptions

Landmark Description Number 1 Most lateral distal point 2 Lateral midpoint (distal) 3 Lateral midpoint (proximal) 4 Most proximal lateral point 5 Most proximal medial point 6 Medial midpoint (proximal) 7 Medial midpoint (distal) 8 Most distal medial point 9 Most distal point 10 Center of articular surface

Figure 8. Distal ulna landmark configuration on A. jubatus (USNM 161922) ulna photograph.

Table 11 Radius Landmark Descriptions

Landmark Description Number 1 Lateral proximal head 2 Medial proximal head 3 Medial distal head 4 Neck of radius (lateral) 5 Mid radius (lateral) 6 Medial epiphyseal border (curve) 7 Radioulnar articular surface 8 Tip of styloid process 9 Across from 7 (curve) 10 Lateral epiphyseal border (curve) 11 Mid radius (medial) 12 Distal radial tuberosity 13 Center radial tuberosity 14 Proximal radial tuberosity

Figure 9. Radius as a whole landmark configuration on A. jubatus (USNM 161922) radius photograph.

Table 12 Distal Ulnar Articular Facet of Radius Landmark Descriptions

Landmarks Description Number 1 Most distal cranial point 2 Cranial midpoint (distal) 3 Cranial midpoint (proximal 4 Most proximal cranial point 5 Most proximal caudal point 6 Caudal midpoint (proximal) 7 Caudal midpoint (distal) 8 Most distal caudal point 9 Distal midpoint 10 Center of articular surface

Figure 10. Distal radius landmark configuration on A. jubatus (USNM 161922) radius photograph.

Table 13 Ilium Landmark Descriptions

Landmark Description Number 1 Dorsal caudal iliac spine 2 Dorsal cranial iliac spine 3 Between 2 & 4 4 Most cranial point on ilium 5 Between 4 & 6 6 Ventral cranial iliac spine 7 Ventral caudal iliac spine 8 Narrowest point – ventral side 9 Narrowest point – caudal side

Figure 11. Ilium of pelvis landmark configuration on A. jubatus (USNM 161922) pelvis photograph.

Table 14 Ischium Pubis Landmark Descriptions

Landmark Description Number 1 Ilium to ischium connection (dorsal) 2 Ischial spine 3 Ischial tuberosity 4 Between 3 & 5 5 M. biceps femoris origin 6 Most caudal point on pubis 7 Most cranial point on pubis 8 Pecten pubis (curve) 9 Iliopubic eminence (M. psoas minor insertion)

Figure 12. Ischium/Pubis of pelvis landmark configuration on photograph of A. jubatus (USNM 161922) pelvis.

Table 15 Proximal Femur Landmark Descriptions

Landmark Description Number 1 Lesser trochanter 2 Distal medial neck of humerus 3 Most distal point on head 4 Center of head (medial) 5 Between 4 & 6 6 Proximal tip of head 7 Lateral distal head 8 Medial base of greater trochanter 9 Proximal tip of greater trochanter 10 Lateral tip of greater trochanter 11 Across from landmark 3 12 Medial proximal tibial shaft

Figure 13. Proximal femur landmark configuration on A. jubatus (USNM 161922) femur photograph.

Table 16 Tibia Landmark Descriptions

Landmark Description Number 1 Distal tip of tibial tuberosity 2 Cranial tip of tibial tuberosity 3 Cranial proximal tibia 4 Caudal proximal tibia 5 Caudal tip of proximal tibia 6 Proximal caudal tibial shaft

Figure 14. Proximal tibia landmark configuration on A. jubatus (USNM 161922) tibia photograph.

Kendall’s Shape Space is a non-Euclidean, or non-linear, manifold. The dimension number of this space depends on the number of landmarks and the dimensionality of the landmarks, whether it is two- or three-dimensional. The number of landmarks is denoted by "k." The shapes are embedded in the Euclidean space of “m” dimensions. The translation, scaling, and rotation of the landmark configurations in GPA reduce the dimensionality of the Kendall Shape Space. For translation “m” dimensions, for scaling one dimension, and for rotation m (m-1)/2 dimensions are removed. Therefore, the

Kendall Shape Space dimension number is km-m-1-m (m-1)/2. For two- dimensional landmarks, it yields 2k-4. Therefore, if we pick 10 landmarks on a specimen, the number of dimensions will be 16. For three-dimensional landmark configurations, the dimension of the Kendall Shape Space is 3k-7 (Kendall, 1977).

The multidimensional space is then converted into Euclidean, or linear measurements, for statistical analyses. The shapes are projected onto a tangent space to the Kendall Shape Space manifold at the Procrustes mean. The Principal Components

Analysis selects the most important linear combinations of variables to generate Principal

Component Scores for the specimens. The number of PC scores depends on the dimensionality of the Kendall Shape Space manifold. The first set of PC scores (PC1) explains the highest level of variance, PC2 explains the second highest, and so on.

Morphologika was used to visualize shape changes in the specimen wireframe renditions according to the PC scores. GPA and PCA were also conducted on the means of each species group to find the Procrustes distance between the means, or the square root of the sum of the squared distances between each group mean landmark

57 configuration. Using the Procrustes distances between the means, a minimum spanning tree (MST) was generated, using the statistical program R with the package igraph (Czardi and Nepusz, 2006; R Core Team, 2013). MST was placed over the PC1 and PC2 graphs to show the most similar mean landmark configurations in the multidimensional space.

If a clear separation between cursorial and non-cursorial species was apparent,

MANOVA was performed, using the statistical program R to compare the first three PC scores between the cursorial and non-cursorial species. In addition, the PC scores were analyzed through the Discriminant Analysis of Principal Components (DAPC) in R using the package “adegenet” (Jombart, 2008). The reason for conducting DAPC is that PCA examines the variability among individuals, while the Discriminant Analysis maximizes the differences between groups (Jombart, 2008).

CHAPTER 4

RESULTS

Muscle Morphology for F. catus, N. nebulosa, and V. vulpes

The following is a general description of the muscles for F. catus, N. nebulosa, and V. vulpes that is applicable to all three species, together with comments regarding any species-specific differences. N. nebulosa is a highly arboreal animal whose anatomy has not yet been documented in the literature. F. catus, a common and easily-obtainable felid, was chosen for comparison to N. nebulosa. A non-felid V. vulpes, also easily obtainable, was included to supplement the comparison to show phylogenetically-related differences.

Except for the muscles of the manus, the ratios of muscle weight mean to total forelimb muscle weight, to muscle group weight, and to tetanic tension (Po) and the ratios of physiological cross-sectional area (PCSA) to total forelimb muscle

PCSA and to muscle group PCSA were calculated for the muscles described below.

Also, the surface area ratios of origin and insertion were calculated for the muscles, except those of the manus. Results of significant difference for these parameters

59 among the species are reported in the descriptions. Anatomical terminology is according to Nomina Anatomica Veterinaria (2012).

A. Dorsal Extrinsic Muscle Group

1. M. trapezius consists of a cervical component, M. trapezius cervicis, and a thoracic component, M. trapezius thoracis. This muscle is located caudal to M. cleidocervicalis and cranial to M. latissimus dorsi.

1A. M. trapezius cervicis in F. catus and N. nebulosa begins at the level of the fourth cervical vertebra and ends at the first thoracic vertebra. It extends from the sixth cervical to the third thoracic vertebrae in V. vulpes. This muscle is not directly attached to these vertebrae; however, it has an aponeurotic attachment to the median fibrous raphe median fibrous raphe, which is a longitudinal fibrous septum located on either side of M. transversospinalis. M. trapezius cervicis inserts onto the dorsal border of the scapular spine. In F. catus and N. nebulosa, this attachment is the same length as the origin of the scapular spinous attachment of M. spinodeltoideus, but is located more dorsally. The insertion is longer than the M. spinodeltoideus origin and extends to the dorsal border of the spine in V. vulpes. PCSA to total was larger in F. catus than N. nebulosa (Table 17). Surface area insertion on the scapula was larger in

V. vulpes than both F. catus and N. nebulosa (Figs 15-17; Tables 17 and 18).

Table 17 Tukey Multiple Comparisons of Means for Muscle PCSA Percentages Based on

Total Forelimb Muscle Weight of Felis catus, Neofelis nebulosa and V. vulpes

% Mean of Total PCSA N. nebulosa Muscle Groups Muscles F. catus (3) (2) V. vulpes (2) Trapezius cervicis1 4.53±0.49 2.42±0.13 2.78±0.26 Trapezius thoracis1 3.89±0.38 1.98±0.01 3.40±0.40 Latissimus dorsi1,2 5.86±0.18 3.95±0.02 4.73±0.21 Dorsal Omotransversarius 2.23±0.13 1.73±0.01 2.04±0.20 Extrinsic R. capitus 1.49±0.20 1.40±0.14 0.78±0.01 R. cervicis 3.08±0.42 2.55±0.30 4.13±0.45 R. thoracis I1 3.87±0.38 2.08±0.39 3.14±0.13 R. thoracis II 2,3 2.39±0.16 1.36±0.20 0.00 Cleidocervicalis 4.64±0.40 2.86±0.14 2.58±0.59 Cleidomastoideus 2.40±0.26 1.68±0.03 2.55±0.03 Cleidobrachialis1,2 4.27±0.26 2.76±0.26 2.64±0.14 Pec sup desc sup 2.52±0.20 1.66±0.03 2.30±0.21 Ventral Pec sup desc prof2,3 2.82±0.11 2.75±0.13 0.00 Extrisic Pec prof cranial 3.78±0.34 2.77±0.10 2.46±0.18 Pec prof inter 2,3 2.06±0.21 1.66±0.14 3.47±0.26 Pec prof caudal 3.29±0.14 3.53±2.80 4.03±0.56 Xiphihumeralis1 2.35±0.16 1.59±0.09 2.04±0.07 Pec sup transversus 5.19±0.50 3.67±1.51 4.50±0.25 5.12±0.33 4.26±0.30 4.98±0.19 Intermediate Serratus vent cervicis Extrinsic Serratus vent 6.30±0.44 4.19±0.23 5.67±0.16 thoracis1 Spinodeltoideus 3.42±0.30 2.46±0.01 3.18±0.04 Acromiodeltoideus 3.49±0.19 2.63±0.25 3.19±0.50 Scapular 1,3 7.72±0.26 4.50±1.12 7.36±0.27 Lateral Infraspinatus Supraspinatus 8.33±1.55 5.59±1.30 7.65±0.12 Teres minor1,3 2.49±0.17 1.31±0.02 2.37±0.05 Scapular Teres major 4.79±0.22 3.72±0.52 4.08±0.16 Medial Subscapularis 8.85±0.52 6.94±0.09 7.24±0.47 1,2,3 1.76±0.08 1.01±0.10 2.68±0.25 Cranial Coracobrachialis Brachial Biceps brachii 5.24±0.62 4.13±2.95 5.63±0.61 (gravitational) Brachialis 3.06±0.45 2.74±0.18 2.61±0.20

(Continued on following page)

Table 17 (continued)

Tensor fascia antebrachii2 2.71±0.19 2.28±0.17 1.71±0.03 Triceps brachii long 9.36±0.34 7.75±1.34 9.92±0.75 Caudal Triceps brachii lateral1,3 5.04±0.14 3.89±0.04 5.43±0.29 Brachial 2,3 1.82±0.32 1.77±0.16 0.00 (anti- Triceps brachii short gravitational) Triceps brachii int2,3 2.83±0.08 2.40±0.24 4.21±0.30 Triceps brachii accessory 2.95±0.27 2.40±0.04 3.65±0.34 Anconeus 2.81±0.59 2.22±0.09 2.42±0.04 Brachioradialis2,3 1.61±0.25 1.99±0.04 0.00 Extensor carpi radialis 2.27±0.22 2.29±0.24 3.83±0.51 longus 2,3 Extensor carpi radialis 3.06±0.16 1.96±0.17 0.00 brevis1,2,3 Extensor digitorum 2.85±0.14 2.03±0.04 2.51±0.25 Craniolateral communis Antebrachial Extensor digitorum 3.46±0.27 2.39±0.02 1.76±0.35 lateralis 2 Ulnaris lateralis 4.66±0.19 3.84±0.05 3.51±1.04 Supinator 3.33±0.08 2.63±0.13 2.37±0.69 Abductor pollicis longus 3.82±0.15 2.93±0.81 2.72±0.82 Extensor indicis pollicis2,3 1.46±0.16 1.22±0.11 0.00 Pronator teres 3.76±0.19 3.75±0.17 2.81±0.72 Flexor carpi radialis 2.91±0.29 2.61±0.24 2.74±0.44 Flexor dig sup 4.06±0.63 4.41±0.81 4.45±1.80 Flexor dig brevis2,3 1.95±0.26 1.75±0.24 0.00 Interflexorius2,3 1.67±0.08 1.48±0.09 0.00 Flexor carpi ulnaris ulnar 3.34±0.33 3.55±0.61 2.47±0.74 Caudolateral Flexor carpi ulnaris 4.42±0.29 3.48±0.20 3.69±1.39 Antebrachial humeral Flexor dig prof I 2.75±0.32 2.74±0.15 3.36±0.27 Flexor dig prof II 2.20±0.07 1.68±0.02 2.99±0.87 Flexor dig profundusIII 2.29±0.28 2.41±0.03 2.99±0.14 medial most head Flexor dig prof ulnar1,2,3 3.19±0.10 3.91±0.32 1.41±0.14 Flexor dig prof radial2,3 2.83±0.11 2.47±0.04 1.13±0.004 Pronator quadratus 3.42±0.43 1.92±0.03 3.15±0.19

(Continued on following page)

Table 17 (continued)

N numbers for each species are listed in parentheses beside the name. 1 = significant difference between F. catus and N. nebulosa (p<0.05) 2 = significant difference between F. catus and V. vulpes (p<0.05) 3 = significant difference between N. nebulosa and V. vulpes (p<0.05)

Table 18 Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of F. catus, N. nebulosa, and V. vulpes Scapular muscle Attachment Sites

Mean ± SEM Surface Areas Lateral Scapular Muscles N. nebulosa F. catus (3) V. vulpes (2) (2) Supraspinatus1,2,3 46.11±0.09 43.60±0.05 40.47±0.31 Infraspinatus1,2 37.19±0.09 40.70±0.20 40.96±0.24 Trapezius cervicis2,3 9.58±0.09 10.16±0.16 11.63±0.36 Trapezius thoracis 4.17±0.14 4.26±0.11 4.34±0.38 Rhomboideus cervicis 8.09±0.16 6.82±0.39 8.54±0.57 Rhomboideus thoracis1,3 9.66±0.21 8.04±0.05 9.70±0.14 Teres major2,3 5.68±0.21 5.29±0.32 9.72±0.17 Teres minor 5.34±0.09 5.71±0.16 6.19±0.53 Acromiodeltoideus2 5.21±0.09 4.48±0.16 3.82±0.24 Omotransversarius1,3 4.99±0.12 3.76±0.02 4.94±0.12 Medial Scapular Muscles Subscapularis1,2,3 72.13±0.03 73.27±0.10 70.29±0.05 Serratus ventralis cervicis1,2,3 11.06±0.19 9.25±0.03 15.43±0.18 Serratus ventralis thoracis2,3 13.35±0.16 13.35±0.17 11.19±0.05 Coracobrachialis2,3 1.76±0.06 1.52±0.17 2.68±0.25 Biceps brachii 3.12±0.11 3.14±0.01 3.18±0.17

(Continued on following page)

Table 18 (continued)

Caudal Scapular Muscles 1 Infraspinatus 62.89±0.07 55.52±0.003 51.81±0.70 1,3 Teres major 14.98±0.28 21.36±0.02 16.58±0.72 Teres minor 10.90±0.32 13.21±0.47 10.11±0.56 2,3 Triceps brachii long 13.30±0.13 13.82±0.05 21.34±0.10 2 Acromiodeltoideus 7.11±0.15 6.57±0.06 5.76±0.23 2,3 Omotransversarius 4.61±0.10 5.37±0.29 8.07±0.16 Spinodeltoideus 8.51±0.14 10.69±0.45 13.13±0.76 1,2,3 Serratus ventralis thoracis 5.24±0.08 8. 58±0.007 13.67±0.37

Lateral muscles. forelimbsuperficial Lateral

Figure 15. Figure

Figure 16. Lateral scapula muscle map. A: F. catus. B: N. nebulosa.

Figure 17. V. vulpes lateral scapula muscle map.

1B. M. trapezius thoracis is located just caudal to M. trapezius cervicis and superficially covers the cranial one-third of M. latissimus dorsi. In F. catus and N. nebulosa, it originates directly from the spinous processes of the second through the eleventh thoracic vertebrae. Its origin is from the third to the eighth thoracic vertebrae in V. vulpes. The insertion in the three species is by tendinous attachment to the spine of the scapula. This muscle is strongly attached to M. latissimus dorsi in

V. vulpes. The mean weight to total weight ratio was larger for F. catus than N. nebulosa and V. vulpes (Table 19). PCSA to total was larger for F. catus than N. nebulosa (Table 17). The PCSA to group ratio was larger for both F. catus and V. vulpes than N. nebulosa (Figs 15-17; Tables 17, 19, and 20).

2. M. latissimus dorsi originates from the spinous processes of the fifth thoracic through sixth lumbar vertebrae by the thoracolumbar fascia in all three species. It inserts with the Mm. teres major as part of a conjoined tendon onto the medial proximal humerus next to the M. pectoralis insertion. M. tensor fasciae antebrachii is attached to the conjoined tendon at the point of origin. The mean weight to total weight ratio and PCSA to total was larger for both F. catus and V. vulpes than N. nebulosa (Figs 15, 18-20, Tables 17 and 19).

3. M. omotransversarius attaches cranially to the lateral caudal border of the transverse process of the atlas, also known as the wing of the atlas. It inserts on the tip of the metacromion process of the scapula. PCSA to group ratio was larger for both N. nebulosa and V. vulpes than F. catus. Insertion point surface area on the scapula was larger in both F. catus and V. vulpes than N. nebulosa (Table 18). When

Table 19

Tukey Multiple Comparisons of Means for Muscle Weight Percentages Based on

Total Forelimb Muscle Weight of Felis catus, Neofelis nebulosa and V. vulpes

Muscle % Mean of Total Forelimb Muscle Weight Groups Muscles F. catus (3) N. nebulosa (2) V. vulpes (2) Trapezius cervicis 7.92±0.52 7.46±0.55 6.54±0.29 Trapezius thoracis1 8.23±0.13 7.08±0.38 7.19±0.19 Latissimus dorsi2 21.01±0.46 19.82±0.48 17.57±0.23 Dorsal Omotransversarius 5.39±0.32 5.72±0.24 6.24±0.89 Extrinsic R. capitus2,3 4.15±0.34 5.26±0.40 2.02±0.17 R. cervicis2 6.25±0.44 6.77±0.47 9.08±0.50 R. thoracis I 6.47±0.33 5.46±0.65 5.83±0.03 R. thoracis II2,3 4.57±0.23 3.80±0.71 0.00 Cleidocervicalis 11.07±0.66 11.23±0.41 7.61±1.33 Cleidomastoideus 5.00±0.21 4.84±0.30 6.77±0.93 Cleidobrachialis2,3 10.16±0.19 9.99±0.37 7.21±0.07 Pec sup desc sup 6.42±0.20 6.18±0.52 5.69±0.02 Ventral Pec sup desc prof 1,2,3 6.19±0.39 9.08±0.16 0.00 Extrinsic Pec prof cranial2,3 10.12±0.42 9.39±0.51 6.30±0.02 Pec prof inter 2 6.14±0.34 6.57±0.27 10.85±1.64 Pec prof caudal 9.68±0.90 11.06±1.26 14.17±0.95 Xiphihumeralis 7.79±1.12 6.34±0.01 7.16±0.17 Pec sup transversus 11.28±0.52 10.90±0.03 10.27±0.23 Intermediate Serratus vent cervicis2,3 10.23±0.16 10.41±0.22 12.21±0.33 Extrinsic Serratus vent thoracis1,2 14.53±0.27 13.03±0.10 12.91±0.19 Spinodeltoideus 6.04±0.48 6.14±0.10 7.13±0.19 Acromiodeltoideus1,3 5.16±0.03 5.59±0.13 4.96±0.05 Scapular 1,3 Lateral Infraspinatus 11.69±0.11 10.22±0.01 12.11±0.25 Supraspinatus3 13.55±0.22 12.97±0.45 14.67±0.15 Teres minor 2.84±0.23 2.13±0.09 2.91±0.07 Scapular Teres major1 9.46±0.08 11.00±0.49 9.88±0.40 Medial Subscapularis 13.01±0.15 11.73±0.63 11.78±0.01 1,2,3 Cranial Coracobrachialis 1.79±0.04 1.40±0.03 3.03±0.02 Brachial Biceps brachii 8.28±0.20 9.92±0.48 9.24±0.19 (gravitational) Brachialis 6.49±0.30 6.88±0.11 6.12±0.28

(Continued on following page)

Table 19 (continued)

Tensor fascia antebrachii1,3 4.85±0.11 5.98±0.04 3.95±0.35 Triceps brachii long2,3 15.21±0.18 15.05±0.99 19.52±0.53 Caudal Triceps brachii lateral 9.86±0.59 9.60±0.30 11.77±0.31 Brachial 2,3 (anti- Triceps brachii short 1.83±0.15 2.16±0.01 0.00 gravitational) Triceps brachii int2,3 5.04±0.23 5.39±0.35 8.50±0.01 Triceps brachii accessory 5.25±0.28 5.84±0.01 7.57±0.94 Anconeus 3.74±0.70 3.97±0.16 2.99±0.09 Brachioradialis1,2,3 3.23±0.13 6.24±0.10 0.00 Extensor carpi radialis longus2 4.58±0.27 5.55±0.48 7.20±0.83 Extensor carpi radialis brevis2,3 5.14±0.18 4.71±0.19 0.00 Extensor digitorum Craniolateral communis 4.97±0.34 4.06±0.12 4.23±0.13 Antebrachial Extensor digitorum lateralis1,2,3 4.08±0.07 3.27±0.15 2.71±0.05 Ulnaris lateralis 4.77±0.28 4.70±0.26 4.08±0.01 Supinator3 2.79±0.17 3.23±0.12 2.07±0.07 Abductor pollicis longus2,3 4.32±0.35 5.08±0.03 2.86±0.03 Extensor indicis pollicis2,3 2.42±0.19 1.91±0.07 0.00 Pronator teres2,3 4.47±0.25 5.51±0.20 3.23±0.18 Flexor carpi radialis 3.72±0.19 3.90±0.04 3.57±0.19 Flexor dig sup 4.78±0.23 5.86±0.28 5.07±0.51 Flexor dig brevis2,3 1.37±0.07 1.79±0.17 0.00 Interflexorius2,3 2.00±0.23 2.14±0.02 0.00 Flexor carpi ulnaris ulnar2,3 3.42±0.01 4.13±0.46 2.12±0.23 Caudolateral Flexor carpi ulnaris Antebrachial humeral2 4.91±0.14 4.74±0.04 4.13±0.05 Flexor dig prof I 4.13±0.28 4.31±0.03 5.70±0.81 Flexor dig prof II 3.24±0.24 2.87±0.01 3.98±0.96 Flexor dig profundus III2,3 3.39±0.23 3.99±0.08 5.01±0.01 Flexor dig prof ulnar2,3 4.98±0.57 6.08±0.24 2.36±0.02 Flexor dig prof radial2,3 4.44±0.30 4.87±0.21 1.87±0.15 Pronator quadratus 2.94±0.31 2.91±0.07 2.42±0.09

Table 20 Tukey Multiple Comparisons of Means for Muscle PCSA Percentages Based on

Muscle Group Weight of Felis catus, Neofelis nebulosa and V. vulpes

% Mean of Muscle PCSA Group Total Muscle N. nebulosa Groups Muscles F. catus (3) (2) V. vulpes (2) Trapezius cervicis 24.89±1.90 21.49±1.76 18.55±0.61 Trapezius thoracis1,3 22.83±0.53 17.47±0.36 23.19±1.09 Latissimus dorsi 33.86±1.51 36.71±0.65 33.51±1.27 Dorsal Omotransversarius1,2 11.99±0.11 15.17±0.48 13.86±0.26 Extrinsic R. capitus1,2,3 8.77±0.31 12.26±0.90 5.24±0.41 R. cervicis2,3 18.07±0.95 22.66±2.10 29.27±0.45 R. thoracis I 22.20±0.59 19.11±2.24 21.42±0.62 R. thoracis II2,3 13.37±0.73 12.18±2.36 0.00 Cleidocervicalis 24.62±1.95 20.45±2.15 16.06±2.70 Cleidomastoideus 12.89±1.08 11.81±0.83 16.30±1.10 Cleidobrachialis 22.77±0.15 20.56±3.73 16.65±0.18 Pec sup desc sup1,3 13.39±0.04 11.37±0.53 14.38±0.47 Ventral Pec sup desc prof 1,2,3 14.60±0.18 19.64±1.97 0.00 Extrinsic Pec prof cranial2,3 20.12±0.93 19.61±0.26 15.69±0.12 Pec prof inter2,3 11.19±0.05 12.49±2.38 22.20±3.20 Pec prof caudal 15.76±0.12 24.45±5.56 25.92±1.95 Xiphihumeralis 12.01±0.81 10.91±0.96 12.82±0.39 Pec sup transversus 28.90±0.66 24.94±3.94 29.30±0.19 Intermediate Serratus vent cervicis 39.00±1.24 41.57±3.44 40.53±1.14 Extrinsic Serratus vent thoracis 51.00±1.24 48.43±3.44 49.47±1.14 Spinodeltoideus 17.09±1.78 17.33±0.84 16.47±0.74 Acromiodeltoideus 17.44±1.43 18.68±2.59 16.29±2.17 Scapular 36.49±0.02 33.70±8.49 38.24±2.15 Lateral Infraspinatus Supraspinatus 40.06±2.09 42.90±10.09 39.98±0.25 Teres minor 1 13.27±0.78 9.11±0.26 11.99±0.66 Scapular Teres major 31.11±0.82 33.90±8.76 33.39±0.89 Medial Subscapularis 58.89±0.82 56.10±8.76 56.61±0.89 2,3 17.16±1.38 13.09±0.61 23.93±0.45 Cranial Coracobrachialis Brachial Biceps brachii 51.17±2.37 48.05±1.30 54.80±1.34 (gravitational) Brachialis2,3 33.53±1.68 38.97±1.04 24.17±1.24

(Continued on following page)

Table 20 (continued)

Tensor fascia antebrachii2,3 14.13±0.65 14.25±0.09 8.09±0.36 Triceps brachii long 47.90±0.40 48.07±3.64 49.35±2.23 Caudal Triceps brachii lateral 24.13±0.30 24.37±2.96 25.35±2.51 Brachial 2,3 9.19±0.99 26.10±1.0 0.00 (anti- Triceps brachii short gravitational) Triceps brachii int2,3 13.89±0.36 14.75±0.46 19.15±0.02 Triceps brachii accessory 14.96±0.32 14.56±1.14 16.22±0.22 Anconeus2 15.56±0.50 13.38±1.49 10.70±0.80 Brachioradialis2,3 10.64±1.08 15.11±0.91 0.00 Extensor carpi radialis 16.79±1.81 18.80±0.94 32.18±4.48 longus2,3 Extensor carpi radialis 20.06±0.41 16.34±0.20 0.00 brevis1,2,3 Extensor digitorum 19.04±0.35 14.87±3.02 21.78±3.06 Craniolateral communis Antebrachial Extensor digitorum 20.03±0.84 17.91±1.06 15.57±0.24 lateralis2 Ulnaris lateralis 28.39±0.48 31.95±1.85 30.06±4.04 Supinator 20.37±0.19 20.93±1.45 18.89±1.36 Abductor pollicis longus 23.61±0.88 22.70±5.49 22.14±2.39 Extensor indicis pollicis1,2,3 9.99±0.26 8.45±0.48 0.00 Pronator teres 20.40±1.44 21.45±2.43 16.42±0.86 Flexor carpi radialis 13.37±0.46 14.23±1.45 15.88±1.30 Flexor dig sup 22.40±1.30 23.90±4.46 25.29±5.22 Flexor dig brevis2,3 9.17±0.78 8.42±1.96 0.00 Interflexorius1,2,3 8.75±0.26 7.07±0.19 0.00 Flexor carpi ulnaris ulnar 16.32±1.02 22.79±0.56 14.68±1.81 Caudolateral Flexor carpi ulnaris 22.83±0.53 18.82±0.75 21.40±4.18 Antebrachial humeral Flexor dig prof I 13.80±1.03 14.25±0.63 20.32±3.01 Flexor dig prof II2,3 11.39±0.57 9.37±0.67 15.45±0.32 Flexor dig profundus III 11.10±0.97 11.75±0.80 16.81±0.67 medial most head2,3 Flexor dig prof ulnar1,2,3 16.48±0.31 20.70±1.68 8.58±0.72 Flexor dig prof radial2,3 14.69±0.19 13.17±0.01 7.07±1.73 Pronator quadratus 20.04±2.35 11.09±0.84 21.05±6.59

A B

Figure 18. Medial humerus muscle map. A: F. catus. B: N. nebulosa.

Figure 19. V. vulpes medial humerus muscle map.

Figure 20. V. vulpes caudal humerus muscle map.

75 measured on the inferior view of the scapula, the surface area was larger in V. vulpes than both F. catus and N. nebulosa (Figs 15-17, 21-23; Tables 18 and 20).

4. M. rhomboideus capitus originates from the nuchal crest from the external occipital protuberance of the occipital bone. It is a long thin band of muscle with a small insertion point on the caudal border of the scapula next to the insertion of M. serratus ventralis cervicis. The mean weight to total weight ratio was larger for both

F. catus and N. nebulosa than V. vulpes (Table 19). The mean weight to group ratio and PCSA to total ratio was larger for N. nebulosa than V. vulpes (Tables 17 and 21).

PCSA to group ratio was larger for both F. catus and N. nebulosa than V. vulpes, and it was larger for N. nebulosa than F. catus (Figs 16, 21, and 24; Tables 17, 19, 20,

21).

5. M. rhomboideus cervicis has no bony origin, as it is attached to the median fibrous raphe, the longitudinal fibrous septum located on either side of the epaxial muscles of Transversospinalis. This muscle originates at the level of C2-C3 and extends to C7 in F. catus and N. nebulosa while the origin is from C3 to T3 in V. vulpes. Insertion is on the lateral caudal border of the scapula extending to the level of the spine, being dorsal to the M. rhomboideus thoracis I insertion site. In V. vulpes, the insertion is by a strong tendon. The mean weight to total weight ratio was larger for V. vulpes than F. catus (Table 19). The mean weight to group weight ratio was larger for V. vulpes than both F. catus and N. nebulosa (Figs 16-17, 21, 24;

Tables 19 and 21).

Figure 21. Intrinsic dorsal forelimb muscles.

Figure 22. Caudal scapula muscle map. A: F. catus. B: N. nebulosa.

Figure 23. V. vulpes caudal scapula muscle map.

Figure 24. V. vulpes medial scapula muscle map.

Table 21 Tukey Multiple Comparisons of Means for Muscle Weight Percentages Based on

Total Muscle Group Weight of Felis catus, Neofelis nebulosa and V. vulpes

% Mean of Muscle Group Total Muscle F. catus N. nebulosa Groups Muscles (3) (2) V. vulpes (2) Trapezius cervicis 17.42±1.08 17.17±0.99 16.10±0.23 Trapezius thoracis 18.12±0.43 16.26±0.59 17.78±0.10 Latissimus dorsi 50.75±1.22 50.44±0.41 47.43±1.16 Dorsal Omotransversarius 11.81±0.61 13.14±0.37 15.33±1.72 Extrinsic R. capitus3 9.05±0.80 12.07±1.13 4.92±0.25 R. cervicis2,3 13.71±1.06 15.57±1.38 22.63±0.50 R. thoracis I 14.05±0.75 12.62±1.62 14.35±0.40 R. thoracis II2,3 10.01±0.54 8.58±1.42 0.00 Cleidocervicalis 2 23.65±0.77 23.67±0.16 16.74±2.53 Cleidomastoideus 10.54±0.72 10.04±0.93 14.92±1.67 Cleidobrachialis2,3 21.66±0.28 20.93±1.38 15.92±0.57 Pec sup desc sup 13.53±0.11 12.81±0.71 12.51±0.36 Ventral Pec sup desc prof 1,2,3 13.02±0.50 18.97±0.21 0.00 Extrinsic Pec prof cranial2 21.64±1.35 19.47±0.66 13.88±0.40 Pec prof inter 2 12.96±0.84 13.59±0.88 24.47±4.59 Pec prof caudal2 20.61±1.78 23.17±2.14 32.20±1.47 Xiphihumeralis 16.38±1.94 13.12±0.32 15.77±0.75 Pec sup transversus 24.22±1.35 22.88±0.67 19.60±3.23 2,3 Intermediate Serratus vent cervicis 35.25±0.83 38.66±0.34 43.45±1.09 Extrinsic Serratus vent thoracis2,3 54.75±0.83 51.34±0.34 46.55±1.09 Spinodeltoideus 17.89±1.35 19.36±0.56 19.85±0.44 Acromiodeltoideus1,3 15.21±0.12 17.57±0.64 13.68±0.06 Scapular 1 Lateral Infraspinatus 36.21±0.15 33.36±0.48 35.01±0.64 Supraspinatus 43.04±0.55 44.03±1.25 43.87±0.84 Teres minor 8.31±0.76 6.62±0.36 7.97±0.25 Scapular Teres major1,2,3 36.15±0.14 43.22±0.27 40.00±1.09 Medial Subscapularis1,2,3 53.85±0.14 46.78±0.27 50.00±1.09 1,2,3 Cranial Coracobrachialis 9.67±0.20 6.69±0.40 15.37±0.50 Brachial Biceps brachii 50.89±0.96 54.64±0.86 53.50±0.37 (gravitational) Brachialis 2 37.44±0.95 34.53±0.77 32.16±0.68

(Continued on following page)

80 Table 21 (continued)

Tensor fascia antebrachii1,2,3 13.71±0.53 16.71±0.39 8.83±0.58 Triceps brachii long 47.37±0.50 45.65±2.02 48.29±0.29 Caudal Triceps brachii lateral 28.71±1.78 27.43±1.80 27.14±1.41 Brachial 2,3 (anti- Triceps brachii short 5.15±0.39 23.02±0.17 0.00 gravitational) Triceps brachii int 2,3 14.24±0.41 14.97±0.54 19.31±0.45 Triceps brachii accessory 14.88±0.86 16.28±0.51 17.14±1.85 Anconeus 10.52±1.91 11.03±0.77 6.69±0.34 Brachioradialis 1,2,3 15.15±1.18 27.54±0.24 0.00 Extensor carpi radialis longus 2,3 21.66±0.39 24.39±2.45 43.87±2.68 Extensor carpi radialis brevis 1,2,3 24.44±0.67 20.49±0.68 0.00 Extensor digitorum Craniolateral communis 1,3 23.47±0.64 17.54±0.41 24.33±0.72 Antebrachial Extensor digitorum lateralis1 19.25±1.00 14.09±0.57 15.34±0.45 Ulnaris lateralis 22.55±0.68 20.41±1.00 23.52±1.57 Supinator 12.98±0.58 13.87±0.41 11.68±0.31 Abductor pollicis longus3 20.21±0.76 22.15±0.31 16.28±1.16 Extensor indicis pollicis1,2,3 11.20±0.52 8.15±0.24 0.00 Pronator teres 3 18.61±0.49 20.91±1.33 14.82±0.51 Flexor carpi radialis 15.52±0.22 14.61±0.50 16.42±0.57 Flexor dig sup 19.96±0.28 22.22±0.56 23.64±2.03 Flexor dig brevis2,3 5.56±0.07 6.63±0.47 0.00 Interflexorius2,3 12.00±3.22 7.95±0.25 0.00 Flexor carpi ulnaris ulnar 3 14.23±0.87 15.46±1.39 9.66±0.82 Caudolateral Flexor carpi ulnaris humeral 20.52±0.76 17.86±0.30 18.99±0.57 Antebrachial Flexor dig prof I 17.17±0.42 16.19±0.27 26.80±4.53 Flexor dig prof II 13.40±0.35 10.70±0.30 18.41±4.36 Flexor dig profundusIII medial most head2,3 13.99±0.35 14.92±0.07 23.13±0.51 Flexor dig prof ulnar2,3 4.98±1.33 6.08±0.37 2.36±0.25 Flexor dig prof radial2,3 4.44±1.01 4.87±0.34 1.87±0.81 Pronator quadratus 2.94±0.58 2.91±0.04 2.42±0.66

6. M. rhomboideus thoracis consists of two parts in F. catus and N. nebulosa: M. rhomboideus thoracis I and M. rhomboideus thoracis II, while V. vulpes lacks M. rhomboideus thoracis II.

6A. M. rhomboideus thoracis I is a triangular muscle that is attached to the supraspinous ligament, which runs along the dorsal aspects of the spinous processes of the thoracic and lumbar vertebrae. This attachment begins at C7 and the bony origin is directly on the spinous processes of T1 and T2. It is separated from R. cervicis by a thin aponeurosis. The origin of M. rhomboideus thoracis I extends from

T3-T5 in V. vulpes. The muscle in all three species inserts onto the lateral caudal border of the scapula starting at the level of the spine. Surface area of insertion on the scapula was larger for both F. catus and V. vulpes than N. nebulosa (Figs 16-17,

21; Table 18).

6B. M. rhomboideus thoracis II, absent in V. vulpes, originates directly from the third and fourth thoracic vertebrae spinous processes and inserts obliquely onto the lateral caudal border at the ventral angle of the scapula. This insertion site is different than R. thoracis I in that it is more ventral being at the level of M. teres major origin.

(Figs 16-17, 21; Tables 17, 19-22).

B. Ventral Extrinsic Muscle Group

1. M. brachiocephalicus is composed of two muscles, M. cleidocephalicus and M. cleidobrachialis. The origin is on the rudimentary clavicle, which is thin in the two felids but much thinner and shorter in the fox. The clavicle in the three species is attached to the manubrium and scapula by a band of connective tissue. The proximal and distal components of M. brachiocephalicus originate on the superficial surface of the clavicle and the associated connective tissue. The term "clavicular intersection" is given to this junction (Evans and de Lahunta, 2004). M. cleidocephalicus is subdivided into the superficial M. cleidocervicalis and deep M. cleidomastoideus.

1A. M. cleidocervicalis is ventral to M. trapezius cervicis and it originates from the clavicular intersection. It is a broad but thin muscle covering M. cleidomastoideus.

This muscle inserts on the nuchal crest and on the occipital protuberance. In F. catus and N. nebulosa, this muscle extends by a median fibrous raphe to the level of the third cervical vertebra and attaches to the epaxial muscles. In V. vulpes, the muscle extends to the sixth cervical vertebra. The mean weight to group weight ratio was larger for F. catus than V. vulpes (Figs 15, 21, 25; Table 21).

1B. M. cleidomastoideus is a narrow strap muscle coursing deep to M. cleidocervicalis. It originates from the clavicular intersection and inserts onto the mastoid process of the temporal bone on the skull (Fig 21).

83 Table 22 Tukey Multiple Comparisons of Means for Muscle Mass to Tetanic Tension Ratios

(W/Po) of Felis catus, Neofelis nebulosa and V. vulpes

% Mean of Muscle Group Total Muscle F. catus N. nebulosa Groups Muscles (3) (2) V. vulpes (2) Trapezius cervicis 1.20±0.14 1.66±0.02 1.61±0.14 Trapezius thoracis 1.44±0.18 1.92±0.05 1.41±0.18 Latissimus dorsi 2.35±0.22 2.66±0.11 2.39±0.15 Dorsal Omotransversarius 1.63±0.17 1.80±0.02 1.98±0.04 Extrinsic R. capitis 1.93±0.21 2.03±0.02 1.70±0.09 R. cervicis 1.40±0.17 1.44±0.02 1.43±0.08 R. thoracis I 1.13±0.13 1.39±0.01 1.24±0.11 R. thoracis II2,3 1.29±0.13 1.47±0.02 0.00 Cleidocervicalis 1.61±0.18 2.11±0.11 1.93±0.18 Cleidomastoideus 1.42±0.19 1.56±0.12 1.70±0.19 Cleidobrachialis 1.61±0.18 1.96±0.05 1.81±0.16 Pec sup desc sup 1.74±0.22 2.01±0.15 1.66±0.23 Ventral Pec sup desc prof 2,3 1.49±0.21 1.77±0.05 0.00 Extrinsic Pec prof cranial 1.83±0.19 1.81±0.01 1.66±0.18 Pec prof inter 2.02±0.17 2.13±0.03 2.04±0.22 Pec prof caudal 1.97±0.21 1.74±0.27 2.30±0.25 Xiphihumeralis 2.24±0.35 2.16±0.06 2.32±0.24 Pec sup transversus 1.47±0.17 1.65±0.30 1.50±0.13 Intermediate Serratus vent cervicis 1.35±0.15 1.33±0.01 1.65±0.13 Extrinsic Serratus vent thoracis 1.54±0.13 1.69±0.01 1.48±0.11 Spinodeltoideus 1.19±0.13 1.35±0.03 1.46±0.07 Acromiodeltoid 0.99±0.08 1.16±0.12 0.94±0.12 Scapular 1.09±0.06 1.27±0.27 1.07±0.02 Lateral Infraspinatus Supraspinatus 1.12±0.07 1.30±0.22 1.25±0.02 Teres minor 0.76±0.05 0.88±0.02 0.79±0.04 Scapular Teres major 1.31±0.08 1.60±0.11 1.49±0.01 Medial Subscapularis 1.00±0.02 1.01±0.16 1.24±0.11 0.68±0.05 0.76±0.06 0.73±0.04 Cranial Coracobrachialis Brachial Biceps brachii 1.75±0.50 1.47±0.11 1.11±0.09 (gravitational) Brachialis 1.49±0.21 1.37±0.04 1.48±0.01

(Continued on following page)

84 Table 22 (continued)

Tensor fascia antebrachii 1.21±0.12 1.44±0.04 1.48±0.13 Triceps brachii long 1.08±0.03 1.19±0.21 1.27±0.03 Caudal Triceps brachii lateral 1.29±0.05 1.34±0.02 1.35±0.08 Brachial 2,3 0.73±0.11 0.67±0.05 0.00 (anti- Triceps brachii short gravitational) Triceps brachii int 1.18±0.03 1.24±0.02 1.29±0.03 Triceps brachii accessory 1.20±0.06 1.33±0.04 1.34±0.13 Anconeus 0.89±0.05 0.98±0.05 0.82±0.04 Brachioradialis2,3 1.44±0.18 1.77±0.09 0.00 Extensor carpi radialis 1.36±0.12 1.46±0.03 1.29±0.11 longus Extensor carpi radialis 1.11±0.01 1.32±0.05 0.00 brevis1,2,3 Extensor digitorum 1.16±0.05 1.09±0.10 1.08±0.01 Craniolateral communis Antebrachial Extensor digitorum 0.80±0.03 0.75±0.03 0.93±0.17 lateralis Ulnaris lateralis 0.74±0.08 0.66±0.01 0.80±0.26 Supinator 0.57±0.04 0.67±0.06 0.61±0.11 Abductor pollicis longus 0.80±0.07 1.00±0.24 0.81±0.27 Extensor indicis pollicis2,3 1.19±0.13 0.87±0.06 0.00 Pronator teres 0.93±0.09 0.80±0.02 0.76±0.13 Flexor carpi radialis 0.87±0.08 0.85±0.08 0.88±0.1 Flexor dig sup 0.86±0.11 0.74±0.13 0.87±0.26 Flexor dig brevis2,3 0.48±0.06 0.58±0.06 0.00 Interflexorius2,3 0.80±0.05 0.80±0.01 0.00 Flexor carpi ulnaris ulnar 0.71±0.03 0.70±0.13 0.57±0.12 Caudolateral Flexor carpi ulnaris 0.78±0.05 0.74±0.06 0.84±0.32 Antebrachial humeral Flexor dig prof I 1.03±0.11 0.85±0.02 1.11±0.19 Flexor dig prof II 0.97±0.04 0.93±0.03 0.99±0.11 Flexor dig profundusIII 1.01±0.10 0.92±0.01 1.14±0.17 medial most head Flexor dig prof ulnar 1.02±0.06 0.85±0.07 1.04±0.10 Flexor dig prof radial 1.06±0.06 1.07±0.10 1.05±0.20 Pronator quadratus1,3 0.58±0.05 0.81±0.02 0.53±0.01

1C. M. cleidobrachialis is superficial to M. brachialis and cranial to Mm. acromiodeltoideus and the long head of triceps brachii. This muscle originates from the clavicular intersection. This muscle inserts into the thick conjoined tendon with

M. brachialis onto the medial ulna distal to the trochlear notch in F. catus and N. nebulosa. However, in V. vulpes, it inserts onto the middle one-third of lateral humerus just distal to the M. deltoideus insertion along with M. pectoralis

Figure 25. Ventral forelimb muscles.

superficialis transversus. A tendon was seen to originate from M. cleidobrachialis near its insertion to course and attach to M. extensor carpi radialis in V. vulpes. The mean weight to total weight ratio and group weight ratio was significantly larger for both F. catus and N. nebulosa than V. vulpes (Tables 19 and 21). PCSA to total was larger for F. catus than N. nebulosa and V. vulpes (Figs 15, 21, 25-27; Tables 17, 19,

21).

2. M. pectoralis superficialis pars descendens superficialis originates from the manubrium and to the first rib. It extends distally in the direction of the elbow where it joins the antebrachial fascia along with a small attachment to M. cleidobrachialis in F. catus and N. nebulosa. In V. vulpes, the muscle inserts onto the anterior lateral humerus just distal to M. deltoideus insertion and proximal to the M. cleidobrachialis insertion site. PCSA to group ratio was larger for both F. catus and V. vulpes than N. nebulosa (Figs 25, 26; Table 20).

3. M. pectoralis superficialis pars descendens profundus is absent in V. vulpes, but is situated deep to M. pectoralis superficialis descendens superficialis and is attached to it by a fascia in F. catus and N. nebulosa. It originates on the manubrium and is more cranial than the narrow M. pectoralis superficialis descendens. This muscle courses cranially to insert on the cranial middle third of the humerus where its fibers are closely associated with M. pectoralis superficialis transversus. The mean weight to total weight ratio and group weight ratio plus PCSA to total and group ratio was statistically larger for N. nebulosa than F. catus (Figs 25, 28-29;

Tables 17, 19-22).

Figure 26. V. vulpes cranial humerus muscle map.

A B

Figure 27. Medial ulna muscle map. A: F. catus. B: N. nebulosa.

A B

Figure 28. Lateral humerus muscle map. A: F. catus. B: N. nebulosa.

A B

Figure 29. Cranial humerus muscle map. A: F. catus. B: N. nebulosa.

4. M. pectoralis profundus has four parts: cranial, intermediate, caudal, and xiphihumeralis.

4A. M. pectoralis profundus cranial head, originates between the second and cranial border of eighth sternebra, unfused elements of the sternum, in F. catus and

N. nebulosa. In V. vulpes, the origin is from the manubrium to the second sternebra.

This muscle inserts onto the greater tubercle by a strong tendon at the level of the M. supraspinatus insertion site, being more medial and closer to the head of the humerus. The mean weight to total weight ratio and PCSA to group ratio was statistically larger for both F. catus and N. nebulosa than V. vulpes (Tables 19 and

20). The mean weight to group weight ratio was larger for F. catus than V. vulpes

(Tables 21). The surface area of insertion was larger in F. catus and N. nebulosa than

V. vulpes (Figs 18, 19, 25, 26, 30-31; Tables 19-21 and 23).

4B. M. pectoralis profundus intermediate originates from the caudal half of the seventh sternebra and whole length of the eighth sternebra in F. catus and N. nebulosa. In V. vulpes, the origin is from the third to the fifth sternebra. Its insertion in all species is on the cranial surface of the humerus at the distal end of the greater tubercle. The mean weight to total weight ratio and weight to group weight ratio was larger for V. vulpes than F. catus (Tables 19 and 21). PCSA to total ratio and group ratio was larger in V. vulpes than both F. catus and N. nebulosa (Tables 17 and 20).

The surface area of insertion was larger in F. catus and N. nebulosa than V. vulpes

(Figs 18, 19, 25, 26, 30-31; Tables 17, 19, 20, 21, and 23).

Table 23 Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of F. catus, N. nebulosa, and V. vulpes Humeral Muscle Attachment Sites

Mean ± SEM Surface Areas Lateral Humeral Muscles F. catus (3) N. nebulosa (2) V. vulpes (2) Supraspinatus 10.21±1.11 11.89±0.04 11.89±0.33 Infraspinatus2,3 13.41±0.40 12.79±0.18 7.67±0.24 Teres minor1,3 4.63±0.21 7.16±0.43 3.70±0.09 Deltoideus1,2,,3 18.34±0.45 28.27±0.54 13.98±0.27 Brachialis1,2,3 51.00±1.03 42.87±0.62 61.10±0.10 Triceps brachii accessory head 10.88±0.62 12.75±0.39 11.52±0.10 Anconeus2,3 20.19±0.51 18.12±0.62 13.13±0.18 Extensor carpi radialis longus 7.12±0.27 5.86±0.97 8.13±0.99 Extensor digitorum1,2,3 5.78±0.14 7.48±0.30 4.03±0.07 Extensor digitorum lateralis 4.46±0.32 5.11±0.78 4.09±0.28 Ulnaris lateralis 4.37±0.22 4.28±0.15 4.68±0.22 Supinator1,2,3 6.29±0.17 7.86±0.19 3.90±0.01 Medial Humeral Muscles Subscapularis2,3 25.33±0.56 26.85±0.48 20.48±1.35 Pectoralis profundus cranial2,3 14.55±0.80 14.96±0.11 10.06±0.06 Pectoralis profundus intermediate2,3 24.19±1.55 23.66±0.68 12.46±0.30 Pectoralis profundus caudal1,2,3 26.63±0.58 21.70±0.17 9.75±0.37 Xiphihumeralis1,2,3 11.00±0.27 7.00±0.02 8.19±0.17 Teres major2,3 20.70±0.28 22.69±1.08 15.23±1.67 Coracobrachialis2,3 15.48±0.82 18.83±0.33 48.67±0.82 Pronator teres1,2 8.57±0.44 10.71±0.12 11.00±0.15 Flexor carpi radialis2 9.85±0.24 8.82±0.06 8.21±0.52 Flexor digitorum profundus III 9.05±0.70 9.64±0.31 7.08±0.24 Flexor digitorum superficialis2,3 9.91±0.39 10.72±1.12 6.02±0.10 Flexor carpi ulnaris humeral 6.93±0.60 6.68±0.36 5.75±1.57 Flexor digitorum profundus I,II 9.84±0.28 9.76±0.24 8.80±0.77

A B

Figure 30. Caudal humerus muscle map. A: F. catus. B: N. nebulosa.

A B

Figure 31. Proximal humerus muscle map. A: F. catus. B: N. nebulosa.

4C. M. pectoralis profundus caudalis originates on the caudal end of eighth sternebra and cranial xiphoid process in F. catus and N. nebulosa. The origin is from the fifth sternebra to cranial xiphoid in V. vulpes. The insertion of this muscle is onto the cranial surface of the humerus just past the greater tubercle. The mean weight to total ratio and to group ratio was larger for V. vulpes than F. catus (Tables 19 and

21). The surface area of insertion was larger in F. catus and N. nebulosa than V.

vulpes, and it was larger in F. catus than N. nebulosa (Figs 18, 19, 25, 26, 30-31;

Tables 19, 21, 23).

5. M. xiphihumeralis originates from the entire surface of the xiphoid process with an insertion site on the cranial surface of the humerus past the greater tubercle.

PCSA to total was larger for F. catus than N. nebulosa (Table 17). The surface area of insertion was larger in F. catus and V. vulpes than N. nebulosa, and it was larger in V. vulpes than N. nebulosa (Figs 18, 19, 25, 26, 30-31; Tables 17 and 23).

6. M. pectoralis superficialis pars transversus is partly covered by M. pectoralis superficialis pars descendens. The origin of this muscle is from the manubrium and extends to the cranial border of the fourth sternebra. Its insertion is on the cranial humerus, starting at the distal half of the greater tubercle and extending to half the length of humerus (Figs 25, 26, 28-29).

C. Intermediate Extrinsic Muscle Group

1. M. serratus ventralis has cervical and thoracic divisions.

1A. M. serratus ventralis cervicis originates in F. catus and N. nebulosa from the transverse processes of the third through seventh cervical vertebrae. In V. vulpes, the origin is from the fourth to seventh cervical vertebrae. The insertion is onto the mediocaudal border of the scapula with the insertion of M. rhomboideus capitus. The mean weight to total weight ratio and group weight ratio was larger for V. vulpes than both F. catus and N. nebulosa (Tables 19 and 21). The surface area of insertion

96 A

Figure 32. Medial scapula muscle map. A: F. catus. B: N. nebulosa.

was larger in both F. catus and V. vulpes than in N. nebulosa, and it was larger in F. catus than N. nebulosa (Figs 21-24, 32; Tables 18, 19, and 21).

1B. The M. serratus ventralis thoracis origin is from ribs one through nine and the associated cartilages in F. catus and N. nebulosa. In V. vulpes, the origin is from ribs one through eight. The insertion is onto the medio-caudal border of the scapula, inferior to the M. serratus ventralis cervicis insertion and is more tendinous in F. catus and N. nebulosa than in V. vulpes. It is especially tendinous in N. nebulosa.

The mean weight to total weight ratio was larger for F. catus than both N. nebulosa and V. vulpes (Table 19). The mean weight to group weight ratio, however, was larger for both F. catus and N. nebulosa than V. vulpes (Table 21). PCSA to total was larger for F. catus than N. nebulosa (Table 20). The surface area of insertion in the inferior view of the scapula was larger in V. vulpes than both F. catus and N. nebulosa, and it was larger in N. nebulosa than F. catus (Table 18). When measured in the medial view of the scapula, the surface area was larger in both F. catus and N. nebulosa than V. vulpes (Figs 21-24, 32; Tables 18-21).

D. Lateral Scapular Muscle Group

1. M. deltoideus has two heads: M. acromiodeltoideus and M. spinodeltoideus. The surface area of the M. deltoideus insertion was larger in both F. catus and N. nebulosa than V. vulpes, and it was larger in N. nebulosa than F. catus (Table 23).

1A. M. acromiodeltoideus originates from the acromion process of the scapula and extends to the metacromion process. Once the muscle is reflected from its insertion site, the axillary nerve can be seen piercing it. This muscle inserts along with M. spinodeltoideus onto the deltoid tuberosity on the lateral proximal half of the humerus. The mean weight to total weight ratio and group ratio was larger for N. nebulosa than both F. catus and V. vulpes (Tables 19 and 21). The surface area of origin on the scapula was larger in F. catus than V. vulpes (Figs 15-17, 22, 23, 26,

28-29, 33; Tables 19, 21, and 23).

1B. M. spinodeltoideus originates from the ventral surface of the spine of scapula next to M. trapezius insertion. The muscle attaches by a thin fascia to M. triceps lateralis. This muscle’s insertion is combined with M. acromiodeltoideus onto the deltoid tuberosity on the lateral proximal half of the humerus. The surface area of origin was larger in V. vulpes than both F. catus and N. nebulosa, and it was larger in

N. nebulosa than F. catus (Figs 16-17, 22, 23, 26, 28-29, 33; Table 18, 23).

2. M. infraspinatus originates from the infraspinous fossa. This muscle inserts on the caudal surface of the greater tubercle distal to the M. supraspinatus insertion.

This insertion is by a tendon in V. vulpes. In F. catus and N. nebulosa, a direct fibrous attachment was seen. The mean weight to total weight and PCSA to total ratio was larger for both F. catus and V. vulpes than N. nebulosa (Tables 17 and 19).

The mean weight to group ratio was larger for F. catus than N. nebulosa (Table 21).

Surface area of origin was larger in both N. nebulosa and V. vulpes than F. catus

(Table 18). When measured from the inferior view of the scapula, the origin surface

area was larger in F. catus than both N. nebulosa and V. vulpes, it was larger for N. nebulosa than V. vulpes (Table 18). Surface area of insertion was larger in both F. catus and N. nebulosa than V. vulpes (Figs 15-17, 22, 23, 26, 28, 31, 33, and 34;

Tables 17-19, 21, and 23).

Figure 33. V. vulpes lateral humerus muscle map.

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3. M. supraspinatus originates from the supraspinous fossa on the lateral scapula and dorsal surface of the spine and cranial border of the acromion process. The insertion is by a tendon on the proximal, lateral border of the greater tubercle, surrounded by M. pectoralis profundus cranially. The mean weight to total weight ratio was larger for V. vulpes than N. nebulosa (Table 19). Surface area of origin was larger in both F. catus and N. nebulosa than V. vulpes, and it was larger in F. catus than N. nebulosa (Figs 16-19, 26, 28-31, 33, 34-35; Tables 18 and 19).

Figure 34. Lateral scapular muscles.

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4. M. teres minor is deep and ventral to M. infraspinatus. It originates from the ventral border of the scapula cranial half, starting near the glenoid fossa and extending to the origin of M. teres major. In N. nebulosa, the origin of this muscle was less aponeurotic and more fibrous than in F. catus. In V. vulpes, the attachment was mainly aponeurotic. The muscle insertion is on the caudal humerus on the ridge proximal to the neck. PCSA to group ratio was larger for F. catus than N. nebulosa

(Table 20). PCSA to total ratio was larger for both F. catus and V. vulpes than N. nebulosa (Table 17). Surface area of origin and insertion was larger in N. nebulosa than both F. catus and V. vulpes (Figs 16-17, 20, 22, 23, 28, 33-34; Tables 17, 18,

20, and 23).

E. Medial Scapular Muscle Group

1. M. teres major originates from the ventral caudal border of the scapula extending to about a third of the length. The insertion is combined with the conjoined tendon of

Mm. latissimus dorsi and teres major on the cranial humerus between the greater and lesser tubercle crests. The mean weight to total weight ratio was larger for F. catus than N. nebulosa (Table 19). However, the mean weight to group weight ratio was larger for N. nebulosa than both F. catus and V. vulpes, and it was larger for V. vulpes than F. catus (Table 21). The surface area of origin on the scapula was larger in V. vulpes than both F. catus and N. nebulosa (Table 18). When measured in the inferior view, the origin surface area was larger in N. nebulosa than both F. catus

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Medial brachial and antebrachial muscles. Medialantebrachial and brachial

Figure 35 Figure

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and V. vulpes (Table 18). The insertion surface area was larger in F. catus and N. nebulosa than V. vulpes (Figs 16-20, 22-24, 34-35; Tables 18, 19, 21, 23).

2. M. subscapularis originates from the subscapular fossa on the medial surface of the scapula. It inserts by a tendon on the lesser tubercle of the humerus. The insertion tendon runs deep to M. coracobrachialis. The mean weight to group weight ratio was larger for F. catus than both N. nebulosa and V. vulpes, and it was larger for V. vulpes than N. nebulosa (Table 21). The surface area of origin was larger in N. nebulosa than both F. catus and V. vulpes, and it was larger in F. catus than V. vulpes (Table 18). The surface area of insertion was larger in F. catus and N. nebulosa than V. vulpes (Figs 18-20, 21, 24, 30-32, 35; Tables 18, 21, and 23).

F. Cranial Brachial (Gravitational) Muscle Group

1. M. coracobrachialis originates from the coracoid process of the scapula by a long tendon that runs superficial to M. subscapularis. The muscle inserts onto the cranial humerus just distal to the lesser tubercle. The mean weight to total weight ratio and group weight ratio and PCSA to total ratio and group ratio was larger for V. vulpes than both F. catus and N. nebulosa (Tables 17, 19-21). Also, all ratios were larger for

F. catus than N. nebulosa. The surface area of origin was larger in V. vulpes than both F. catus and N. nebulosa (Table 18). The surface area of insertion was larger in

V. vulpes than both F. catus and N. nebulosa (Figs 17-20, 24, 30, 32, 35; Tables 17-

21, and 23).

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2. M. biceps brachii has only one head. It originates from the supraglenoid tubercle of the scapula by a long tendon. The tendon courses through the intertubercular groove and is held down by the transverse humeral retinaculum attached between the greater and lesser tubercles. Near the elbow joint, the muscle gives off a tendon that inserts onto the radial tuberosity. In V. vulpes, this tendon joins with that of M. brachialis. The surface area of insertion was larger in F. catus than N. nebulosa (Figs

17, 24, 32, 35-37; Table 24).

Table 24 Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of F. catus, N. nebulosa, and V. vulpes Radial Muscle Attachment Sites

Mean ± SEM Surface Areas Cranial Radial Muscles F. catus (3) N. nebulosa (2) V. vulpes (2) Supinator2,3 31.51±0.20 32.34±0.06 45.94±0.33 Pronator teres1,3 13.19±0.38 9.03±0.31 13.52±0.24 Abductor pollicis1,2,3 55.23±0.12 56.12±0.05 40.91±0.22 Caudal Radial Muscles Biceps brachii1 14.31±0.12 11.33±0.11 12.95±1.22 Flexor digitorum profundus 35.23±1.30 37.02±0.46 32.60±1.11 radial Pronator quadratus 51.12±1.32 50.71±0.49 54.27±0.50

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A B

Figure 36. Caudal radius muscle map. A: F. catus. B: N. nebulosa.

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Figure 37. V. vulpes caudal radius muscle map.

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3. M. brachialis has a large area of origin on the caudal surface of the humerus. The origin extends more proximally than the M. extensor carpi radialis longus origin. The insertion tendon unites with that of M. cleidobrachialis to insert on the medial ulnar tuberosity. The mean weight to group weight ratio was larger for F. catus than V. vulpes (Table 21). PCSA to group ratio was larger for both F. catus and N. nebulosa than V. vulpes (Table 20). The surface area of origin was larger in F. catus and V. vulpes than N. nebulosa, and it was larger in V. vulpes than F. catus (Figs 15, 20, 26-

28, 30, 33, 35, 38-39; Tables 20, 21, and 23).

G. Caudal Brachial (Anti-Gravitational) Muscle Group

1. M. tensor fasciae antebrachii covers the medial surface of M. triceps brachii long head and attaches to antebrachial fascia. M. tensor fasciae antebrachii is a thin broad muscle that is attached proximally to the conjoined tendon of Mm. latissimus dorsi and teres major near the brachium. In F. catus and N. nebulosa, the muscle inserts onto the medial proximal border of the olecranon process by a thin fascial attachment near the insertion of the M. triceps short head. In V. vulpes, the insertion is combined with that of the M. triceps brachii long head. The mean weight to total weight ratio and group weight ratio was larger for N. nebulosa than both F. catus and

V. vulpes (Table 19 and 21). F. catus mean weight to group weight ratio and PCSA to total ratio was also significantly larger than V. vulpes (Tables 17 and 21). PCSA to

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group ratio was larger for both F. catus and N. nebulosa than V. vulpes (Figs 27 and

40; Tables 17, 19, 20, and 21).

Figure 38. V. vulpes cranial ulna muscle map.

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A B

Figure 39. Cranial ulna muscle map. A: F. catus. B: N. nebulosa.

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Figure 40. V. vulpes medial ulna muscle map.

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2. M. triceps brachii, in F. catus and N. nebulosa, has lateral, long, accessory, intermediate, and short heads that all insert on the olecranon process of the ulna. V. vulpes has lateral, long, accessory, and medial heads. The medial head is analogous to the intermediate head.

2A. M. triceps brachii long head originates by a strong tendon from the ventral border of the scapula near the glenoid fossa. The muscle thickens as it nears the insertion on the proximal apex of the olecranon process of ulna. The mean weight to total weight ratio was larger for V. vulpes than both F. catus and N. nebulosa (Table

19). Surface area of origin on the scapula and insertion on the ulna was larger for V. vulpes than both F. catus and N. nebulosa (Figs 15, 17, 22-24, 27, 35, 40-45; Tables

18-19, 25).

Table 25 Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of F. catus, N. nebulosa, and V. vulpes Ulnar Muscle Attachment Sites

Mean ± SEM Surface Areas Lateral Ulnar Muscles F. catus (3) N. nebulosa (2) V. vulpes (2) Anconeus1,3 25.93±0.38 28.47±0.66 25.89±0.17 Triceps brachii lateral2,3 6.49±0.67 10.25±1.49 15.83±0.37 Abductor pollicis1,2 63.14±0.57 59.37±0.04 59.01±0.07 Medial Ulnar Muscles Triceps brachii long2,3 4.87±0.40 4.47±0.10 7.49±0.62 Tensor fasciae antebrachii 9.35±0.93 7.65±0.71 9.51±1.20 Flexor carpi ulnaris ulnar2,3 8.63±0.44 8.50±0.91 23.14±0.03 Brachialis 9.04±0.19 9.28±0.68 9.77±0.55 Flexor digitorum profundus 65.44±0.41 67.12±0.97 40.53±4.34 ulnar2,3 Pronator quadratus2,3 17.58±0.48 16.34±0.02 36.11±4.09

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A B

Figure 41. Lateral ulna muscle map. A: F. catus. B: N. nebulosa.

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Figure 42. V. vulpes lateral ulna muscle map.

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Figure 45. V. vulpes cranial ulna muscle map.

A B

Figure 43. Proximal ulna muscle map. A: F. catus. B: N. nebulosa.

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A B

Figure 44. Caudal ulna muscle map. A: F. catus. B: N. nebulosa.

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Figure 45. V. vulpes caudal ulna muscle map.

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2B. M. triceps brachii lateral head originates by an aponeurosis from the caudal humerus just distal to the insertion of M. teres minor. Distally, the muscle broadens as it inserts on the lateral surface of the olecranon process. PCSA to total ratio was larger for both F. catus and V. vulpes than N. nebulosa (Figs 15, 20, 28, 30, and 33;

Table 17).

2C. M. triceps brachii short head is a short muscle that originates from the medial caudal surface of the humerus near the supracondylar foramen. It inserts onto the proximal medial olecranon process. It covers the ulnar nerve which passes through the supracondylar foramen. This muscle is absent in V. vulpes. (Figs 18, 27, 30, 35;

Tables 17, 19-22).

2D. M. triceps brachii intermediate head originates from the craniomedial humerus just distal to origin of the accessory head. The insertion is on the medial- proximal olecranon process next to the origin of M. flexor carpi ulnaris. In V. vulpes, the muscle is called M. triceps brachii medial head, and has a much smaller origin than in F. catus and N. nebulosa. In V. vulpes, the origin is by a thin aponeurosis on the medial proximal humerus between the insertions of Mm. coracobrachialis and teres major. The insertion for this muscle in V. vulpes is the same as described above for the two felids. Although the muscle origin is smaller in V. vulpes, its mean weight to total weight ratio and group weight ratio and PCSA to total ratio and group ratio was larger than both F. catus and N. nebulosa (Figs 18-20, 27, 30, 35, 38-40,

43-44; Tables 17, 18, and 21).

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2E. M. triceps brachii accessory head originates from the proximal fourth of the mediocaudal surface of the humerus just distal to the head of the humerus. Its origin borders that of M. brachialis proximally. The muscle is covered by the long and lateral heads of M. triceps brachii, and is superficial to the intermediate head. At the distal third of the humerus, it gives off a tendon that inserts on the proximal olecranon process just cranial to long head insertion. PCSA to total ratio was higher for V. vulpes than F. catus (Figs 18, 20, 28, 30, 33, 35, 38, 41, 43-44; Table 17).

3. M. anconeus originates from the distal lateral supracondylar ridge of the humerus and the lateral epicondyle. The insertion is onto the lateral olecranon process. The

PCSA to group ratio was larger in F. catus than V. vulpes (Table 21). The surface area at the origin was larger in F. catus and N. nebulosa than V. vulpes (Table 23).

The insertion surface area was larger in N. nebulosa than F. catus and V. vulpes (Figs

19, 20, 28, 30, 33, 38-39, 41-42, 46-47; Tables 21, 23, and 25).

H. Craniolateral Antebrachial Muscle Group

1. M. brachioradialis, absent in V. vulpes, originates on a tubercle proximal to the styloid process of the radius from the lateral-caudal humerus. It wraps around M. brachialis as it courses to the distal medial radius. This is a very long muscle capable of exerting a great amount of leveraged force. In N. nebulosa, the origin is twice as long on the humerus and the muscle is thicker than in F. catus. The mean weight to

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Deep cranial muscles. Deep antebrachial cranial

Figure

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total weight ratio and to group weight ratio and PCSA to total ratio was larger for N. nebulosa than F. catus. (Figs 15, 28, 30, 35, 36; Tables 17, 19, 21-22).

2. M. extensor carpi radialis longus originates from the cranial aspect of the lateral supracondylar ridge. In V. vulpes, a tendinous connection was observed between this muscle and M. cleidobrachialis. In F. catus and N. nebulosa, the muscle runs parallel with Mm. brachioradialis and extensor carpi radialis brevis. In V. vulpes, these two muscles are absent. At the distal third of the antebrachium, it gives off a tendon, which passes under the tendon of M. abductor pollicis longus. In F. catus and N. nebulosa, the insertion is onto the dorsal surface of the second metacarpal, just distal to the base. In N. nebulosa, it was observed that this insertion was more distal on the bone than in F. catus. However, in V. vulpes the tendon of M. extensor carpi radialis longus separates into two tendons at the distal third of the antebrachium. One tendon inserts onto the dorsal base of the second metacarpal, and the other onto the third metacarpal. The mean weight to total weight ratio and PCSA to total ratio was larger for V. vulpes than F. catus (Tables 17 and 19). PCSA to group ratio was larger in V. vulpes than both F. catus and N. nebulosa (Figs 15, 20, 26, 28-29, 33, 35, 46; Tables

17, 19, and 20).

3. M. extensor carpi radialis brevis, absent in V. vulpes, originates from the lateral epicondylar crest at about the same level as M. extensor digitorum communis but at a more cranial region along the crest. The muscle runs deep to M. extensor carpi radialis longus and M. extensor digitorum communis. In F. catus, it has a

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considerably thicker belly and tendon than M. extensor carpi radialis longus compared to N. nebulosa. At the distal fourth of the antebrachium, the muscle gives off a tendon that passes under the tendon of M. abductor pollicis longus. The M. extensor carpi radialis longus tendon is thinner than that of M. extensor carpi radialis brevis. The M. extensor carpi radialis brevis tendon inserts onto the third metacarpal somewhat distal to its base, and more medially. The mean weight to total weight ratio and PCSA to total ratio and group ratio was larger for F. catus than N. nebulosa

(Tables 17, 20, and 21). The speed to force ratio was larger in N. nebulosa than F. F. catus (Figs 15, 28, 29, 46; Tables 17, 19-22).

A B

Figure 47. Distal humerus muscle map. A: F. catus. B: N. nebulosa.

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Figure 48. Cranial radius muscle map. A: F. catus. B: N. nebulosa.

4. M. extensor digitorum communis originates from the lateral epicondylar crest just distal to the M. extensor carpi radialis longus origin and caudal to the M. extensor carpi radialis brevis origin. It gives off a tendon at the distal third of the antebrachium that passes deep to the extensor retinaculum and divides into four tendons. Its tendons insert onto the medial bases of the distal phalanges of digits two through five. The mean weight to group weight ratio was larger for both F. catus and

V. vulpes than N. nebulosa (Table 20). Surface area of origin was larger in F. catus

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and N. nebulosa than V. vulpes, and it was larger in N. nebulosa than F. catus (Figs

15, 26, 28-29, 33; Tables 20 and 23).

5. The M. extensor digitorum lateralis origin is on the lateral epicondylar crest.

The muscle gives off a tendon at the distal third of the antebrachium. In F. catus and

N. nebulosa, the tendon divides into three tendons which pass under the extensor retinaculum. All tendons join the tendons of M. extensor digitorum communis that runs to digits three, four, and five to insert onto the distal phalanx of the respective digits. The tendons also have a small attachment to the lateral sesamoid bones at the metacarpophalangeal joints. In V. vulpes, however, only two tendons were seen diverging from the common tendon to course to digits four and five. The mean weight to total weight ratio was larger for F. catus than both N. nebulosa and V. vulpes, and it was larger for N. nebulosa than V. vulpes (Table 19). The mean weight to group weight ratio was larger for F. catus than N. nebulosa (Table 21). PCSA to total ratio and group ratio was larger for F. catus than V. vulpes (Figs 15, 20, 26, 28,

33, and 37; Tables 17, 19-21).

6. M. ulnaris lateralis (or M. extensor carpi ulnaris) originates by a wide tendon from the lateral epicondyle and extends to the distal end of the humerus. In V. vulpes, the muscle also originates from the lateral proximal ulna. The wide insertion tendon attaches to the lateral side of the fifth metacarpal. There is also an attachment on the ligament between the accessory carpal and fifth metacarpal (Figs 15, 28, 33, 42, and

47).

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7. The M. supinator origin is on the lateral epicondyle depression and is more anterior and proximal than the M. ulnaris lateralis origin. In F. catus and N. nebulosa, the origin is by a strong tendon that contains a sesamoid bone. In V. vulpes, the origin is by a small weak tendon, which appeared to attach to the head of the radius lacking a sesamoid. The insertion surrounds the proximal radius bordering

M. flexor digitorum profundus laterally and M. abductor pollicis longus medially. M. pronator teres also inserts at the tip of this insertion site. The mean weight to total weight ratio was larger for N. nebulosa than V. vulpes (Table 17). The surface area of origin was larger in F. catus and N. nebulosa than V. vulpes, and it was larger in N. nebulosa than F. catus (Table 23). The surface area of insertion was larger in V. vulpes than F. catus and N. nebulosa (Figs 26, 28, 33, 36, 46-49; Tables 17, 23-24).

8. M. abductor pollicis longus originates from the lateral surfaces of the radius and ulna and the interosseus membrane. On the radius, the origin begins just distal to the radial tuberosity and extends to the distal fourth of the radius. The origin on the ulna is thinner, starting at the level of the coronoid process, and extending to the distal radio-ulnar articulation. The insertion of the muscle is on the base of the first metacarpal and the adjacent sesamoid bone. In N. nebulosa, the tendon was thicker and stronger than in F. catus and V. vulpes. The mean weight to total weight ratio was statistically larger for both F. catus and N. nebulosa than V. vulpes (Table 19).

The mean weight to group weight ratio was larger for N. nebulosa than V. vulpes

(Table 21). The surface area of origin was larger in F. catus than N. nebulosa and V. vulpes (Table 25). The surface area of insertion was larger in F. catus and N.

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nebulosa than V. vulpes, and it was larger in N. nebulosa than F. catus (Figs 15, 37,

38, 39, 41-42, 46, 48; Tables 19, 21, 24-25).

Figure 49. V. vulpes cranial radius muscle map.

9. M. extensor indicis proprius et pollicis origin is from the lateral ulna that borders the origin of M. flexor digitorum profundus ulnar head cranially, and it is caudal to the origin of M. abductor pollicis longus. In F. catus and N. nebulosa, the origin covers almost the entire length of the ulna laterally extending up to the lateral aspect of the olecranon process. In V. vulpes, the origin is shorter in length and extends from the distal fourth of the ulna laterally. In F. catus and N. nebulosa, the muscle gives off two tendons at the carpus. The lateral tendon runs to the second digit and inserts onto the dorsal sesamoid bone at the metacarpophalangeal joint and on the lateral proximal interphalangeal joint. The medial tendon separates into two

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tendons at the carpo-metacarpal joint. One tendon goes to the first digit and inserts onto the sesamoid bone at the metacarpophalangeal joint and the base of the distal phalanx of the first digit. The other tendon joins the tendon of M. interrosseus II and inserts on to the base of the proximal phalanx on the medial surface. The fibers of the tendons also join the extensor hood of M. extensor digitorum communis. In V. vulpes, the muscle is extremely thin. It is not mentioned in the Guide to the

Dissection of the Dog (Evans and de Lahunta, 2004). Therefore it went unnoticed in my dissections until I discovered it in my last specimen. For this reason, I failed to obtain weights for this muscle. Unlike in F. catus and N. nebulosa, the muscle in V. vulpes only has one tendon emerging from it at the distal antebrachium which merges with the M. extensor digitorum communis tendon that then runs to and attaches to digit two where it inserts onto the base of the second distal phalanx. The mean weight to total weight ratio and group weight ratio and PCSA to group ratio was larger for F. catus than N. nebulosa (Figs 36, 39, 46; Tables 17-20, and 22).

I. Caudolateral Antebrachial Muscle Group

1. M. pronator teres origin has an extensive attachment to the medial epicondyle.

The insertion is by a tendon on the mediocranial surface of the radius at halfway along the bone length. The insertion borders the insertion of M. supinator medially.

The mean weight to total weight ratio was larger for both F. catus and N. nebulosa than V. vulpes (Table 20). The mean weight to group weight ratio was larger for N.

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nebulosa than V. vulpes (Table 21). The surface area of origin was larger in N. nebulosa and V. vulpes than F. catus (Table 23). The surface area of insertion was larger in F. catus and V. vulpes than N. nebulosa (Figs 18-19, 26, 29, 35, 46, 48-49;

Tables 19, 21, 23-25).

2. M. flexor carpi radialis is located on the medial antebrachium. It originates from the medial epicondyle of the humerus by a thick tendon. The insertion tendon arises at the distal third of the antebrachium and inserts onto the proximal plantar at the base of the second and third metacarpals. The origin surface was larger in F. catus than V. vulpes (Figs 18-19, 28, 35, and 47; Table 23).

3. M. flexor digitorum superficialis originates by a tendon attached to the medial epicondyle of the humerus. At the distal antebrachium, the muscle gives off a tendon, and in F. catus and N. nebulosa, M. flexor digitorum brevis arises from this tendon. In V. vulpes, M. flexor digitorum brevis is absent. The tendon of M. flexor digitorum superficialis passes under the flexor retinaculum, after which it gives off separate tendons. In F. catus and N. nebulosa, it divides into five tendons, while in V. vulpes, it divides into four tendons. In F. catus and N. nebulosa, the medialmost tendon inserts onto the base of the distal phalanx of the first digit. V. vulpes lacks a tendon going to the first digit. The second and third tendons join the M. interflexorius tendons at the metacarpophalangeal joints II and III. The fourth tendon joins Mm. interflexorius and flexor digitorum brevis. The fifth (lateralmost) tendon joins the tendon of M. flexor digitorum brevis. Then, all of these joined tendons at digits two through five separate into two tendons after passing deep to the proximal

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annular ligament (at the metacarpophalangeal joint). The separated tendons course along the medial and lateral sides of the M. flexor digitorum profundus tendons and then pass deep to the distal annular ligament (at the interphalangeal joint). After passing the ligament, the tendons run deep to the M. flexor digitorum profundus tendons of digits two through five to insert onto the bases of the middle phalanx of the respective digits. The surface area of origin for the M. flexor digitorum superficialis was larger in F. catus and N. nebulosa than V. vulpes (Figs 18, 19, 30,

35; Table 23).

4. M. flexor digitorum brevis, absent in V. vulpes, arises from the M. flexor digitorum superficialis tendon at distal antebrachium. The muscle gives off two tendons. The medial tendon joins the M. flexor digitorum superficialis tendon IV to insert on the base of the middle phalanx of the fourth digit. The lateral tendon separates further into two tendons. The medial of these tendons joins M. flexor digitorum superficialis tendon V to insert on the base of the middle phalanx of the fifth digit. The lateral tendon inserts on the proximal phalanx of digit five at a point about three-fourths of the length away from the proximal end of the bone. (Figure

35; Tables 17, 19-21, and 23).

5. M. interflexorius, absent in V. vulpes, is a very small muscle that originates from the ulnar and humeral heads of M. flexor digitorum profundus. The muscle then divides into three tendons at the carpus. The tendons join the tendons of Mm. flexor digitorum superficialis and flexor digitorum brevis and course to the bases of middle

129 phalanges of digits two through four. PCSA to group ratio was larger in F. catus than

N. nebulosa (Figure 35; Tables 17, 19-21, and 23).

6. M. flexor carpi ulnaris (ulnar head) originates from the medial olecranon process of the ulna. The origin attachment site narrows near the level of the coronoid process but does not reach it. In V. vulpes, the origin does extend to the coronoid process. In F. catus and N. nebulosa, the muscle gives off a tendon at the distal third of the antebrachium. In V. vulpes, the tendon begins at the proximal third of antebrachium. In all species, the insertion tendon joins that of the M. flexor carpi ulnaris humeral head. This conjoined tendon then inserts onto the base of the accessory carpal bone. The mean weight to total weight ratio was larger for both F. catus and N. nebulosa than V. vulpes (Table 19). The mean weight to group weight ratio was larger for N. nebulosa than V. vulpes (Table 21). Surface area of origin was larger in F. catus and N. nebulosa than V. vulpes (Figs 27, 35, 38-40, 46; Tables 19,

21, and 25).

7. M. flexor carpi ulnaris (humeral head) is tendinous at the proximal and distal ends. The muscle originates from the medial epicondyle of the humerus. The tendon of origin is on the deep surface of the muscle while the insertion tendon is seen on the superficial surface. In F. catus and N. nebulosa, the fibers of M. flexor digitorum profundus humeral head (most lateral head) appear to be attached to M. flexor carpi ulnaris (humeral head) near the origin. At the distal antebrachium, the humeral and ulnar head tendons of the M. flexor carpi ulnaris join to form a conjoined tendon, which then inserts onto the base of the accessory carpal (sesamoid) bone. The mean

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weight to total ratio was larger for F. catus than V. vulpes (Figs 18, 19, 35, 46-47;

Table 19).

8. M. flexor digitorum profundus humeral has three heads. They are designated as

I, II, III. All originate on the medial epicondyle of the humerus and join the common tendon of M. flexor digitorum profundus near the distal antebrachium. This common tendon then divides into five tendons that insert onto the bases of distal phalanges of all digits (Figs 18-19, 29, 35, and 47).

8A. M. flexor digitorum profundus humeral I is the most lateral and superficial of the M. flexor digitorum profundus humeral heads (total of three). It is covered by the

M. flexor carpi ulnaris humeral head. The muscle originates from the medial epicondyle of the humerus. The tendinous fibers at the origin are interlinked with the fibers of the deeper M. flexor digitorum profundus humeral head II. M. flexor digitorum profundus humeral I gives off a tendon at about the distal third of the antebrachium which joins the common tendon of M. flexor digitorum profundus.

8B. M. flexor digitorum profundus humeral head II originates from the medial epicondyle of the humerus deep to M. flexor digitorum profundus humeral I. In V. vulpes, the origin is tendinous. The insertion tendon in F. catus and N. nebulosa arises at the distal antebrachium. In V. vulpes, the insertion tendon starts at mid- antebrachium. The tendon then joins the M. flexor digitorum profundus common tendon. PCSA to group ratio was larger in V. vulpes than both F. catus and N. nebulosa (Table 20).

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8C. M. flexor digitorum profundus III is the most medial of the M. flexor digitorum profundus humeral heads. Its origin is closely associated with the humeral medial epicondyle origin of M. flexor carpi radialis. The tendons of both muscles are slightly joined, but can be separated from each other. Near the carpus, the M. flexor digitorum profundus III tendon of insertion joins the common tendon of M. flexor digitorum profundus. The mean weight to total weight ratio and group weight ratio and PCSA to group ratio was larger for V. vulpes than both F. catus and N. nebulosa

(Tables 19-21).

8D. M. flexor digitorum profundus (ulnar head) originates from the lateral surface of the ulna. This origin starts about at the level of the radioulnar articulation and extends to distal fifth of the ulna. The origin is bordered anteriorly and cranially by the M. extensor indicis proprius et pollicis longus. M. flexor digitorum profundus is partially covered posteriorly by the M. flexor carpi ulnaris. Near the distal antebrachium, a tendon arises which joins the common tendon of M. flexor digitorum profundus and inserts onto the bases of distal phalanges of all digits. The mean weight to weight total ratio and group weight ratio was larger for both F. catus and N. nebulosa than for V. vulpes (Tables 19 and 21). PCSA to total ratio and group ratio was higher for both F. catus and N. nebulosa than V. vulpes, and both ratios were larger in N. nebulosa than F. catus (Tables 17 and 20). The surface area of origin was larger in F. catus and N. nebulosa than V. vulpes (Figs 27, 39, 40, 42, 44-

45; Tables 17, 19, 20, 21, and 25).

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8E. M. flexor digitorum profundus radial head is deep to M. flexor carpi radialis.

In F. catus and N. nebulosa, it originates from the posterior/caudal surfaces of the ulna and radius and is attached to the interosseus membrane. In V. vulpes, the origin is from the middle third of the radius. The insertion tendon joins the common tendon of M. flexor digitorum profundus and inserts onto the bases of the distal phalanges of all digits. The mean weight to total weight ratio and group weight ratio and PCSA to total ratio and group ratio was larger for both F. catus and N. nebulosa than V. vulpes

(Figs 27, 35-37, 39; Tables 17, 19-21).

9. M. pronator quadratus is the deepest muscle in the caudal antebrachium. It originates from the distal third of the ulna and inserts slightly distally on the radius.

The fibers run diagonally from the ulna to the radius. The speed to force ratio was larger in N. nebulosa than both F. catus and V. vulpes (Table 22). The surface area of origin was larger in V. vulpes than F. catus and N. nebulosa (Figs 27, 36-38-40, 50;

Tables 22 and 25).

J. Intrinsic Manus Muscles

1. Mm. lumbricals originate in the manus from the tendons of M. flexor digitorum profundus. There are four lumbrical muscles that insert distal to the bases of the bones on the palmar medial surfaces of the proximal phalanges of digits two through five. In V. vulpes, the insertion is onto the sesamoid bones of the metacarpophalangeal joints. After inserting, each tendon continues distally to join the extensor digitorum tendon.

133

Pronatorquadratus.

. 50

Figure

134

2. M. flexor pollicis brevis in all species originates from the lateral distal end of the radial (scaphoid) carpal bone. It inserts onto the medial sesamoid bone of the metacarpophalangeal joint and the base of the proximal phalanx of the first digit. In

V. vulpes, it was seen as a very thin muscle.

3. M. adductor pollicis, in F. catus and N. nebulosa, originates from the proximal base of the third distal carpal bone (the capitate). In V. vulpes, the origin is from the first and third distal carpal bones. The insertion, in all three species, is onto the distal and lateral end of the proximal phalanx of the first digit and on the lateral sesamoid bone at the metacarpophalangeal joint.

4. M. adductor digiti quinti, in all three species, has two heads that originate jointly from the third distal carpal bone (capitate). In F. catus and N. nebulosa, the lateral and smaller head inserts onto the fifth metacarpal, and the medial head inserts onto the base of the proximal phalanx of the fifth digit. In V. vulpes, the smaller head inserts onto the lateral side of the fifth metacarpophalangeal joint. The larger head inserts onto the medial side of the fifth metacarpophalangeal joint and the distal half of the fifth metacarpal.

5. M. abductor digiti quinti, in all three species, originates from the distal end of the accessory carpal bone. A tendon arises distal to the carpus and inserts on the distal lateral end of the fifth metacarpal and on the sesamoid bone of the metacarpophalangeal joint. In F. catus and N. nebulosa, after inserting, a thin tendon separates and inserts on the lateral base of the middle phalanx of the fifth digit.

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6. M. adductor digiti secundi, in F. catus and N. nebulosa, originates from the first distal carpal bone (trapezium) and the base of the third metacarpal bone. In V. vulpes, the origin is from the third distal carpal bone. The insertion in all three species is onto the base of the proximal phalanx of the second digit on the lateral surface.

7. M. abductor digiti secundi originates from the first distal carpal bone

(trapezium) and the base of the first metacarpal. In F. catus and N. nebulosa, it inserts on the medial side of the proximal phalanx of the second digit. A tendon separates and inserts onto the base of the middle phalanx of the second digit. This insertion is located closer to the dorsal medial surface of the middle phalanx. In V. vulpes, the insertion is only onto the medial side of the base of the proximal phalanx of the second digit.

8. Mm. interossei, are made up of four heads that cover the proximal half of the metacarpals of digits two through five. In all three species, M. interosseus I, serving digit II, originates by a tendon from the third distal carpal bone (capitate). M. interosseus II courses to digit III. In F. catus and N. nebulosa, it has three origins: 1) the proximal plantar medial surface of the fourth metacarpal, 2) the lateral and medial surfaces of the proximal third metacarpal, and 3) the proximal lateral surface of the second metacarpal. In V. vulpes, the origin is from the third distal carpal and bases of the third and fourth metacarpals. In F. catus and N. nebulosa, M. interosseus

III going to the fourth digit has three origins: 1) the proximal medial plantar surface of the fifth metacarpal, 2) by a tendon from the fourth distal carpal, and 3) the

136 proximal plantar end of the fourth metacarpal. In V. vulpes, the origin is from the third and fourth distal carpals and the fourth metacarpal. In F. catus and N. nebulosa,

M. interosseus IV, serving digit V, originates from the proximal plantar surface of the fifth metacarpal and the fourth distal carpal. The origin in V. vulpes is from the base of the fifth metacarpal and the fourth distal carpal. In all three species, M. interossei insert onto the sesamoid bones located on either side of the metacarpophalangeal joints at the respective digits. The tendons separate after the insertion to join the extensor hood of M. extensor digitorum communis on the dorsal manus.

Species Comparisons Between Muscle Groups

The dorsal extrinsic muscle group weight was higher in F. catus than V. vulpes. The intermediate extrinsic and lateral scapular muscle groups weighed more in both F. catus and V. vulpes than N. nebulosa. The caudal brachial muscle group weight was higher in both F. catus and N. nebulosa when compared to V. vulpes. The craniolateral antebrachial muscle group had a greater weight in N. nebulosa than V. vulpes. Over all, the PCSA ratios did not differ among the muscle groups. The speed to force ratio for the lateral scapular muscle group was larger for N. nebulosa than both F. catus and V. vulpes (Tables 19, 22, and 24). Graph shown in Figure 51 summarizes the significant muscle PCSA differences between felids and V. vulpes.

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Muscle Attachment Site Surface Area Comparisons in Extinct Species

Tables 26-29 show muscle attachment site surface area comparisons among extinct S. fatalis, P. atrox, and C. dirus. Figure 52 summarizes significant differences among extant and extinct felids and canids. The Mm. deltoideus insertion site and flexor digitorum profundus ulnar head origin site were significantly larger for felids.

The Mm. brachialis origin site, triceps brachii insertion site, pronator quadratus origin site, and flexor carpi ulnaris ulnar head origin site were significantly larger for canids.

138

V. vulpes V.

and and

0.05).

(

F. catus F.

1: significant difference difference significant 1:

V. vulpes V.

and and

N.nebulosa

0.05); 2: significant difference between between difference 2: significant 0.05);

(

N. nebulosa N.nebulosa

and and

0.05); 3: significant difference between between difference 3: significant 0.05);

(

. Muscles for which PCSA ratios were significant between species. between significant were which PCSA ratios for Muscles .

F. F. catus

between between Figure 51 Figure

139

Table 26 Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of S. fatalis, P. atrox, and C. dirus Scapular muscle Attachment Sites

Mean ± SEM Surface Areas Lateral Scapular Muscles S. fatalis (9) P. atrox (4) C. dirus (8) Supraspinatus 44.21±0.56 44.65±0.21 44.28±0.63 Infraspinatus 38.12±0.63 39.90±0.38 38.84±0.53 Trapezius cervicis 9.88±0.47 10.11±0.34 10.64±0.32 Trapezius thoracis 6.46±0.32 5.70±0.55 7.19±0.33 Rhomboideus cervicis1,3 9.57±0.31 7.05±0.44 6.66±0.48 Rhomboideus thoracis 8.50±0.50 6.68±0.35 7.80±0.43 Teres major1,2 8.49±0.59 5.33±0.28 7.85±0.27 Teres minor1,3 5.73±0.20 4.56±0.44 4.83±0.15 Acromiodeltoideus 3.72±0.21 4.47±0.24 4.38±0.18 Omotransversarius3 2.83±0.15 3.29±0.27 3.81±0.16 Medial Scapular Muscles Subscapularis3 70.67±0.70 70.88±1.12 73.12±0.24 Serratus ventralis cervicis 15.19±0.73 14.39±1.13 13.16±0.37 Serratus ventralis thoracis 10.62±0.36 11.22±0.43 9.34±0.51 Coracobrachialis 3.42±0.15 3.39±0.12 3.06±0.15 Biceps brachii1,2 3.05±0.12 3.60±0.11 2.86±0.10

N numbers for each species are listed in parentheses beside the name. 1 = significant difference between S. fatalis and P. atrox (p<0.05) 2 = significant difference between P. atrox and C. dirus (p<0.05) 3 = significant difference between S. fatalis and C. dirus (p<0.05)

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Table 27 Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of S. fatalis, P. atrox, and C. dirus Humeral muscle Attachment Sites

Mean ± SEM Surface Areas Lateral Humeral Muscles S. fatalis (9) P. atrox (4) C. dirus (8) Supraspinatus3 12.04±0.41 11.10±0.50 10.49±0.40 Infraspinatus2 13.84±0.30 14.99±0.59 12.67±0.51 Teres minor 5.05±0.23 5.00±0.48 5.35±0.13 Deltoideus2,3 28.52±0.61 28.17±0.56 23.71±0.70 Brachialis2,3 39.54±0.76 40.52±1.49 48.31±1.05 Triceps brachii accessory head 19.46±1.05 19.53±0.98 16.75±0.69 Anconeus3 16.89±0.69 14.70±0.25 13.23±0.79 Extensor carpi radialis longus 8.80±0.40 9.37±0.55 7.94±0.33 Extensor digitorum 4.43±0.28 4.18±0.22 4.72±0.11 Extensor digitorum lateralis1,2 4.21±0.23 6.59±0.62 4.42±0.41 Ulnaris lateralis 5.37±0.21 5.91±0.42 5.03±0.19 Supinator 6.78±0.20 5.71±0.48 5.89±0.23

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Table 28 Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of S. fatalis, P. atrox, and C. dirus Ulnar muscle Attachment Sites

Mean ± SEM Surface Areas Lateral Ulnar Muscles S. fatalis (9) P. atrox (4) C. dirus (8) Anconeus2 37.79±1.10 33.75±2.11 40.90±1.87 Triceps brachii lateral 7.50±0.56 7.87±0.50 7.63±0.44 Abductor pollicis2 51.15±1.10 55.08±2.16 48.04±1.96 Medial Ulnar Muscles Triceps brachii long2,3 4.97±0.26 4.86±0.49 13.42±0.69 Tensor fasciae antebrachii2,3 6.44±0.49 5.21±0.74 12.37±0.53 Flexor carpi ulnaris ulnar2,3 5.84±0.41 5.02±0.40 32.19±0.90 Brachialis1,2,3 12.57±0.43 10.11±0.76 15.87±0.51 Flexor digitorum profundus 63.16±0.82 69.56±0.64 36.73±0.90 ulnar1,2,3 Pronator quadratus1,2,3 20.58±1.01 14.98±0.59 25.12±0.70

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Table 29 Tukey Multiple Comparisons of Arcsine Transformed Surface Area Means of S. fatalis, P. atrox, and C. dirus Radial muscle Attachment Sites

Mean ± SEM Surface Areas Cranial Radial Muscles S. fatalis (9) P. atrox (4) C. dirus (8) Supinator1,2 38.57±0.53 27.80±0.29 38.07±1.12 Pronator teres 8.24±0.29 7.72±0.98 8.33±0.40 Abductor pollicis1,2 50.22±0.58 60.91±0.59 50.66±1.07 Caudal Radial Muscles Biceps brachii 17.67±0.55 18.99±1.16 19.84±1.28 Flexor digitorum profundus 33.67±1.10 38.89±1.05 32.64±2.50 radial Pronator quadratus 50.73±0.93 44.93±0.99 50.07±2.47

143

between felids canids. and between

Muscle attachment site surface area measurements that were significant were that measurements area Musclesite attachment surface

. . Figure 52 Figure

144

Geometric Morphometric Analysis Results

Scapula and Scapular Spine

The analysis of the scapula performed here, including the scapular spine landmarks, was not able to separate the cursorial from the non-cursorial species

(Figure 53). Metacromion position and acromion length were the driving characters that formed PC 1 and which represented 50.7% of the variation. S. fatalis, C. dirus, and V. vulpes were at the positive end of the PC 1 scale with the metacromion position at the level of the glenoid fossa with a short acromion process that extends past the glenoid fossa. In addition, the origin site of M. teres major was positioned closer to the glenoid border compared to specimens aligned along the negative end of the PC 1 scale. N. nebulosa, F. catus, and A. jubatus were located at the negative end of the PC 1 axis. In these taxa the metacromion is larger and closer to the vertebral border of the scapula, and the acromion is also longer but does not extend past the glenoid fossa. P. leo and P. atrox clustered together in the mid-PC 1 axis region. Body size was approximated using ln centroid data for each specimen in this

PC analysis, and the regression analysis of PC 1 versus ln centroid size was significant (Adjusted R-squared: 0.08318, F-value: 6.716, P≤0.05).

PC 2 accounted for 12.2% of shape variation. Positive PC 2 represented supraspinous fossa enlargement, while negative PC 2 values are associated with the enlargement of the infraspinous fossa. A. jubatus, P. leo, P. atrox, and S. fatalis

145

Principal Component 2 (PC2). Wireframe renditions are shown for shown PC2 PC1 renditions and axes. are (PC2). 2 Component Principal Wireframe

Figure 53. Scapula with spine Principal Component Analysis plot Principal of Component (PC1) 1 Analysis Component Scapula 53. versus Principal spine with Figure

146

aligned along the positive end of the PC 2 axis while F. catus, N. nebulosa, and C. dirus were positioned at the negative end with V. vulpes located at the negative extreme. Regression analysis of PC 2 versus ln centroid size was significant

(Adjusted R-squared: 0.5843, F-value: 89.55, P≤0.001). The Minimum Spanning

Tree (MST) in Figure 55 shows that the most similar species mean landmark configurations are within the multidimensional space with Procrustes distances. For extinct species, MST linked P. atrox with P. leo (0.047), S. fatalis with C. dirus

(0.0842), and C. dirus with V. vulpes (0.0720) (Figure 54). DFA provided same results as PCA.

Figure 54. Scapula with spine Minimum Spanning Tree (MST) based on the

mean Procrustes distances of each species from one another.

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Analysis of the Scapular Borders

The PCA analysis of the scapular borders is shown in Figure 55. PC 1 accounted for 52.5% of the shape variation. The positive end is occupied by S. fatalis with a dorsal extension of the scapular spine that is closer to the scapular vertebral border. At the negative extreme is a ventral elongation of M. teres major origin and was associated with N. nebulosa, F. catus, and V. vulpes. A. jubatus, C. dirus, P. leo and P. atrox were positioned in the mid-PC 1 axis region. Regression analysis of PC

1 versus ln centroid size was significant (Adjusted R-squared: 0.4124, F-value:

45.22, P≤0.001). Body size may be the driving force for the shape variances in this analysis.

PC 2 represents 14.7% of shape variation. The positive end, occupied by P. leo and P. atrox, showed increased supraspinous fossa roundness. The negative end represented a narrower scapula, elongation of the glenoid neck, and ventral rotation of the glenoid fossa. Cursorial species such as C. dirus and A. jubatus were at the extreme negative end, while V. vulpes was positioned with N. nebulosa, F. catus, and

S. fatalis at the mid-PC 2 axis area. MST linked P. atrox with P. leo (0.0376), S. fatalis with P. leo (0.0913), and C. dirus with A. jubatus (0.0535) and P. leo (0.0557)

(Figure 56). DFA provided same results as PCA. Regression analysis of PC 2 versus ln centroid size was not significant, showing that PC 2 is not related to body size.

(Adjusted R-squared: 0.01551, F-value: 0.03767, p-value: 0.8467; P≤0.05).

148

plot Principal of Component (PC1) 1 Analysis Component outline Scapular Principal

Figure 55. 55. Figure for shown PC2 PC1 renditions and are axes. (PC2). 2 Component Principal Wireframe versus

149

Figure 56. Scapular outline Minimum Spanning Tree (MST) based on the mean

Procrustes distances of each species from one another.

150

Glenoid Fossa

The analysis of the glenoid fossa placed A. jubatus closer to C. dirus and V. vulpes along the PC 2 axis (Figure 57) than to other non-cursorial felids. PC 1 only accounts for 20% of the shape variation, and this test failed to separate cursorial species from non-cursorials. Positive PC 1 holds F. catus, V. vulpes, P. atrox, and N. nebulosa. S. fatalis, P. leo, A. jubatus, and C. dirus are aligned with negative PC 1 values.

Positive PC 1 shows a rounder glenoid fossa with a wide supraglenoid tubercle and an origin for M. biceps brachii, relative to negative PC 1 scores where the wire rendition shows the supraglenoid tubercle positioned farther from the glenoid fossa, and with a narrow neck between the connection of the glenoid fossa and the supraglenoid tubercle. Shape differences along PC 1 appear to be size-dependent because the regression analysis of PC 1 versus ln centroid size showed significant differences. (Adjusted R-squared: 0.2706, F-value: 23.67, P≤0.001).

PC 2 accounted for 19% of shape variation. S. fatalis, N. nebulosa, and P. atrox were located in the positive PC2 region, showing increased lateral concavity of the glenoid fossa when compared to the negative region PC 2 occupied by V. vulpes and C. dirus. The mid-PC 2 axis was occupied by F. catus, A. jubatus, and P. leo.

The negative extreme end of PC2 showed increased roundness of the glenoid fossa and positioning of the supraglenoid tubercle toward the medial border of the scapula.

Regression analysis of PC 2 versus ln centroid size was significantly different

(Adjusted R-squared: 0.1227, F-value: 9.535, P≤0.05). MST shown in Figure 58

151

Principal Component 2 (PC2). Wireframe renditions are shown for PC1 and PC2 axes. PC2 PC1 for and shown renditions are Wireframe (PC2). 2 Component Principal

Figure 57. Glenoid fossa Principal Component Analysis plot of Principal Component 1 (PC1) versus (PC1) 1 Component plot Glenoid 57. Principal of versus fossa Analysis Component Principal Figure

152

Figure 58. Glenoid fossa Minimum Spanning Tree (MST) based on the mean

Procrustes distances of each species from one another.

153

;

leo P.

Pl: ;

P. atrox P.

Pa: ;

N.nebulosa

; Nn: Nn: ;

F. catus F.

vulpes V. ; Fc: Fc: ;

Vv: ;

C.dirus S. fatalis S.

Cd: ; Sf:

A. jubatus A.

Figure 59. Glenoid fossa Discriminant Function Analysis (DFA) plot of Discriminant Function 1 (DF1) versus (DF1) 1 plot of Function (DFA) Discriminant Glenoid 59. Analysis fossa Function Discriminant Figure

2 Aj: Function (DF2). Discriminant

154

linked P. atrox with P. leo (0.0607) and N. nebulosa (0.0631). S. fatalis linked with

P. leo (0.0612). C. dirus was most similar to A. jubatus (0.0638), second to P. leo

(0.0665), and last to V. vulpes (0.0927). DFA showed better separation of cursorial and non-cursorial species by clustering A. jubatus, C. dirus, V. vulpes, and F. catus at the negative DF 1 axis end (Figure 59). The remaining species were positioned at the positive DF 1 end. Body size may be responsible for F. catus positioning within the negative DF 1 area.

Humerus

The humerus outline analysis appeared to depend on size differences (Figure

60). With 54.2% of shape variation associated with PC 1. S. fatalis, P. atrox, P. leo, and N. nebulosa were located at the positive end while F. catus and V. vulpes were at the negative PC 1 end. A. jubatus and C. dirus were positioned in the mid PC 1 region. Positive PC 1 represents increased humeral robustness, a wider greater tubercle, and an enlarged capitulum, compared to species in the negative PC 1 region. The regression analysis of PC 1 versus ln centroid size was significantly different (Adjusted R-squared: 0.1204, F-value: 10.03, P≤0.05). PC 2 accounted for

22.6% of shape variation. S. fatalis and C. dirus are located in the negative PC 2 region indicating increased humeral robustness. The remaining species are in the positive PC 2 area showing the opposite with decreased humeral robustness.

Regression analysis of PC 2 versus ln centroid size was not significantly different,

155

renditions are shown for shown renditionsPC2 PC1 and are axes.

Figure 60. Humerus Principal Component Analysis plot of Principal Component 1 (PC1) 1 Component Humerus 60. plot Analysis Component Principal of Principal Figure

(PC2). 2 Component Principal Wireframe versus

156

making this PC 2 analysis independent of body size (Adjusted R-squared: 0.01487,

F-value: 1.996, p-value: 0.1625; P≤0.05). MST first linked P. atrox with P. leo

(0.0267) and then with S. fatalis (0.0406). S. fatalis was also similar to C. dirus

(0.0496) (Figure 61). DFA did not provide any additional results.

Figure 61. Humerus Minimum Spanning Tree (MST) based on the mean Procrustes

distances of each species from one another.

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Proximal Humeral Epiphysis

Proximal humeral analysis clustered A. jubatus with C. dirus, V. vulpes, and

F. catus along the PC 1 axis, accounting for 38.8% of the shape variation (Figure

62). The species noted above were located on the negative end of PC 1 with the remaining taxa located in the positive PC 1 area. When compared to positive PC 1, the negative axis represents a narrower greater tuberosity that extends beyond the humeral head and the insertion site of M. teres minor that is closer to the shoulder joint. However, the regression analysis of PC 1 versus ln centroid size showed significant effects indicating body-size is a factor in this analysis (Adjusted R- squared: 0.1084, F-value: 8.663, P≤0.05). PC 2 shape changes accounted for 16.5%.

The distance between the humeral head and the greater tubercle increased toward the negative PC 2 end which includes N. nebulosa and V. vulpes. The remaining species are located at the positive PC 2 end. C. dirus specimens are scattered across the PC 2 axis. Regression analysis of PC 2 versus ln centroid size is also significant (Adjusted

R-squared: 0.1903, F-value: 15.81, P≤0.05). MST connected C. dirus with F. catus

(0.0648), V. vulpes (0.0665), and P. atrox (0.0833) (Figure 63). P. atrox was also linked with S. fatalis (0.0581), N. nebulosa (0.0786), and P. leo (0.0837). DFA positioned A. jubatus away from C. dirus, V. vulpes, and F. catus (Figure 64). In addition, N. nebulosa was separated farther from P. leo, P. atrox, and S. fatalis.

158

versus Principal Component 2 (PC2). Wireframe renditions are shown for shown PC2 PC1 renditions and are axes. (PC2). 2 Component Principal Wireframe versus Proximal 62. (PC1) 1 Component plot Analysis Component Principal of Principal humerus Figure

159

Figure 63. Proximal humerus Minimum Spanning Tree (MST) based on the mean

Procrustes distances of each species from one another.

160

Fc: ;

C.dirus

s ; Cd: Cd: ;

vulpe V. A. jubatus A.

Vv: ;

S. fatalis S.

; Sf: Sf: ;

P. leo P.

; Pl: ;

atrox P. ; Pa: ;

N.nebulosa ; Nn: Nn: ;

Figure 64. Proximal humerus Discriminant Function Analysis (DFA) plot of Discriminant (DFA) Discriminant of plot Proximal 64. Function Analysis Discriminant humerus Figure 2 versus (DF1) 1 Aj: Function (DF2). Function Discriminant catus

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Distal Humeral Epiphysis

The distal humeral epiphysis PCA graph is shown in Figure 65. PC 1 represents 54.1% of the shape variation. Positive PC 1, occupied by P. atrox, P. leo,

S. fatalis, and N. nebulosa, display a longer capitulum than trochlea, medial epicondyle enlargement, and proximodistal shortening of the distal epiphysis when compared to the negative PC 1end of the axis. C. dirus, V. vulpes, A. jubatus, and F. catus are associated with negative PC 1 values. The regression analysis of PC 1 versus ln centroid size was significant (Adjusted R-squared: 0.3887, F-value: 41.06,

P≤0.001).

PC 2 accounted for 19.9% of the shape variation. A. jubatus was located at the positive end of PC 2 showing an enlarged lateral epicondyle, a reduced medial epicondyle, and a proximodistal longer distal epiphysis when compared to the negative PC 2 end where N. nebulosa, S. fatalis, and F. catus were located. C. dirus,

V. vulpes, and P. atrox are located in the mid-PC 2 region. P. leo is located in the more positive part of the PC 2 axis. The regression analysis of PC 2 versus ln centroid size was not significant, therefore PC 2 was not body size dependent

(Adjusted R-squared: 0.03505, F-value: 3.288, p-value: 0.0746; P≤0.05). MST linked C. dirus with V. vulpes (0.0371) (Figure 66). P. atrox was closest to P. leo

(0.0520), second to S. fatalis (0.0768), and third to A. jubatus (0.1361). S. fatalis was also linked with N. nebulosa (0.0916). DFA resulted in a somewhat different clustering of species (Figure 67). S. fatalis clustered with P. atrox and P. leo. C.

162

plot Principal of Component(PC1) 1 Component Analysis

versus Principal Component 2 (PC2). Wireframe renditions are shown for shown PC2 PC1 renditions and are axes. (PC2). 2 Component Principal Wireframe versus Figure 65. Distal humerus Distal 65. Principal Figure

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dirus joined with V. vulpes. Between the two clusters along DF 1 was A. jubatus. N. nebulosa and F. catus clustered together in negative DF 2.

Figure 66. Distal humerus Minimum Spanning Tree (MST) based on the mean

Procrustes distances of each species from one another.

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Fc: ;

. C.dirus

; Cd: Cd: ;

vulpes V.

Vv: ;

A. jubatus A. Aj: Aj:

S. fatalis S.

; Sf: ;

P. leo P.

; Pl: ;

P. atrox P.

; Pa: ;

N.nebulosa

; Nn: Nn: ;

Figure 67. Distal humerus Discriminant Function Analysis (DFA) of plot humerus Distal 67. Function Discriminant Analysis Discriminant Figure 2 versus (DF1) 1 Function (DF2). Function Discriminant catus F.

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Ulna

The ulna outline PCA graph is shown in Figure 68. PC 1, with 58.3% of shape variation, shows increasing ulnar robustness toward the positive end. S. fatalis,

P. leo, and P. atrox, are located at the positive end of PC1 while negative PC 1 values include F. catus, V. vulpes, A. jubatus, and C. dirus. N. nebulosa was located in an intermediate region along PC 1. The regression analysis of PC 1 versus ln centroid size was significant (Adjusted R-squared: 0.07623, F-value: 6.199, P≤0.05).

PC 2 (18.4%) demonstrated caudal concavity of the ulnar shaft. N. nebulosa, located at the PC 2 positive extreme, showed a straighter ulna compared with the caudally concave ulna of C. dirus at the negative extreme of PC 2. P. leo, P. atrox, A. jubatus,

S. fatalis, F. catus, and V. vulpes were in an intermediate region. Complete separation of cursorial from non-cursorial species was not apparent. Regression analysis of PC 2 versus ln centroid size was significant (Adjusted R-squared: 0.231,

F-value: 19.92, P≤0.001). MST (Figure 69) linked C. dirus with A. jubatus (0.0497) and P. leo (0.0549). S. fatalis linked with P. atrox (0.0529) which was joined by P. leo (0.0295). DFA did not provide additional data of interest.

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(PC1) 1 omponent versus

for shown PC2 PC1 renditions and axes. are (PC2). 2 Component Principal Wireframe Figure 68. Ulna 68. plot Principal C Component Figure Principal of Analysis

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Distal Ulna

The PCA graph of the distal ulna is shown in Figure 70. PC 1 accounted for

82.0% of the variance. C. dirus, V. vulpes, and A. jubatus all showed negative PC 1 values which represented proximo-distal elongation of the articular facet. P. leo, P. atrox, S. fatalis, and N. nebulosa occupied the positive PC 1 space and showed medio-lateral expansion of the facet. F. catus was located in the intermediate region.

Regression analysis of PC 1 versus ln centroid size was not significant (Adjusted R- squared: 0.000464, F-value: 1.029, p-value: 0.3143; P≤0.05). PC 2 accounted for only 3.8% of the shape variation and appeared to represent different angulation directions of the facet relative to the horizontal axis of the ulnar shaft. There was no clear separation of the species along PC 2. Regression analysis of PC 2 versus ln centroid size was significant (Adjusted R-squared: 0.2145, F-value: 18.2, P≤0.001).

MANOVA was conducted using the first three PC scores to compare cursorial species including A. jubatus, V. vulpes, and C. dirus with the non-cursorial felid group. The results showed significant differences between the two groups (P≤0.001).

MST results showed close links in the articular facet shape of C. dirus to that of V. vulpes (0.0555) (Figure 71). V. vulpes was linked secondly with A. jubatus

(0.2480). P. atrox was most similar to P. leo (0.0879). S. fatalis was close to P. leo and N. nebulosa (0.0794 and 0.1230, respectively). DFA did not provide any significant additional results.

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Figure 69. Ulna Minimum Spanning Tree (MST) based on the mean Procrustes

distances of each species from one another.

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Component 2 (PC2). Wireframe renditions are shown for shown PC2 PC1 renditions and are axes. Component(PC2). 2 Wireframe

Distal ulna Principal Component Analysis plot of Principal Component 1 (PC1) 1 Principal ulna Distal Component plot Analysis Component Principal of

70. Figure versus Principal Principal versus

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Radius

The PCA graph for the radius is shown in Figure 72. PC 1, with 67% of shape variation, showed increasing radial shaft robustness toward its positive end. S. fatalis, and P. atrox was located in the positive PC 1 region. P. leo, N. nebulosa, and

C. dirus were intermediate and F. catus, A. jubatus, V. vulpes were found in the negative region of PC 1. PC 1 demonstrated the positioning of radial tuberosity relative to radial length. At the positive end of PC 1, the radial tuberosity was farther away from the radial head relative to the negative PC 1 values. Regression analysis of PC 1 versus ln centroid size was significant (Adjusted R-squared: 0.109, F-value:

8.477, P≤0.05).

PC 2 (10.9% shape variation) represented radial head angulation and enlargement of the distal epiphysis. C. dirus and V. vulpes located at the positive PC

1 end of the axis showing a perpendicular radial head relative to the vertical axis of the radius. At the negative PC 2 end of the axis was N. nebulosa, P. leo, P. atrox, and

F. catus. These taxa are represented with a higher lateral than medial proximal radial head and an expanded distal epiphysis. S. fatalis and A. jubatus are located at an intermediate position on the PC 2 axis. PC 2 Regression versus ln centroid size was not significant (Adjusted R-squared: 0.00349, F-value: 1.213, p-value: 0.275;

P≤0.05). MST linked C. dirus with N. nebulosa (0.0528) (Figure 73). S. fatalis was most closely joined with P. atrox (0.0554), which was also linked with P. leo

(0.0291). DFA did not provide additional results.

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Figure 71. Distal ulna Minimum Spanning Tree (MST) based on the mean

Procrustes distances of each species from one another.

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Principal Component 2 (PC2). Wireframe renditions are shown for shown PC2 PC1 renditions and axes. are (PC2). 2 Component Principal Wireframe

(PC1) 1 Principal Radius 72. versus Component Component plotPrincipal of Analysis Figure

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Figure 73. Radius Minimum Spanning Tree (MST) based on the mean Procrustes

distances of each species from one another.

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Distal Radius

The distal ulnar articular facet of the radius shown in Figure 74 demonstrates that PC 1, which accounted for 84.9% of the shape variation, separated the non- cursorial felids on the extreme positive end of the PC 1 axis from A. jubatus and the canids at the negative end. Here, a negative PC 1 value represents a proximo-distally elongated articular facet while a positive PC 1 score suggests a medio-lateral expansion. Regression analysis of PC 1 versus ln centroid size was not significant

(Adjusted R-squared: 0.0195, F-value: 1.892, p-value: 0.176; P≤0.05).

PC 2 represented only 4.5% of the variation and appears to be based on slight angulation of the facet direction with respect to the horizontal axis of the radius shaft. No clear separation of species groups is apparent along PC 2. Regression analysis of PC 2 versus ln centroid size was significant (Adjusted R-squared: 0.114,

F-value: 6.815, P≤0.05). MANOVA was conducted using the first three PC scores to compare cursorial species including A. jubatus, V. vulpes, and C. dirus with the non- cursorial felid group. The results showed significant differences between the two groups (P≤0.001). MST shown in Figure 75 linked C. dirus with V. vulpes (0.0471) and A. jubatus (0.1112). P. atrox was most closely associated with P. leo (0.1173) and second with A. jubatus (0.3109). S. fatalis linked with P. leo (0.0786) and N. nebulosa (0.0846). DFA did not provide additional results.

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cipal Component 2 (PC2). Wireframe renditions (PC2). 2 Component cipal Wireframe

are shown shown PC1 PC2 and axes. for are

Figure 74. Distal radius Principal Component Analysis plot of Principal plot Principal of radius Distal 74. Principal Analysis Component Figure Component 1 (PC1) versus Prin Component(PC1) 1 versus

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Figure 75. Distal radius Minimum Spanning Tree (MST) based on the mean

Procrustes distances of each species from one another.

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Ilium

The PC 1 analysis of the ilium (Figure 76) represented 55.8% of the shape variation. A. jubatus did not cluster with the canids. C. dirus and V. vulpes were in the positive end of PC 1. The negative PC 1 extreme region included F. catus, N. nebulosa, P. atrox, and P. leo. The mid-PC 1 region included A. jubatus and S. fatalis. Positive PC 1 scores indicate dorsal ilium shortening and ventral ilium lengthening. In addition, the dorsal and ventral cranial iliac spines expand outward widening the cranial half of the ilium. Negative PC 1 scores, occupied by the other felids, shows a dorsal cranial iliac spine extending cranially. Regression analysis of

PC 1 versus ln centroid size was not significant (Adjusted R-squared: 0.0490, F- value: 3.73, p-value: 0.0589; P≤0.05).

There was no clear separation of species along the PC 2 axis except that A. jubatus was found in a positive PC 2 axis region. Positive PC 2 showed ventral ilium lengthening and cranial ilium narrowing when compared to the negative PC 2 scores.

Regression analysis of PC 2 versus ln centroid size was not significant (Adjusted R- squared: 0.00991, F-value: 1.530, p-value: 0.222; P≤0.05). MST shown in Figure 77 linked C. dirus with V. vulpes (0.0979). S. fatalis was associated with P. leo

(0.0749), A. jubatus (0.1253), and V. vulpes (0.1470). P. atrox was closest to F. catus

(0.0594). DFA did not provide additional results of interest.

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Principal Component Analysis plot of Principal Component 1 (PC1) versus (PC1) 1 Component plot Principal of Principalversus Component Analysis

Principal Component 2 (PC2). Wireframe renditions are shown for shown PC2 PC1 renditions and axes. are (PC2). 2 Component Principal Wireframe

Figure 76. Ilium 76. Ilium Figure

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Figure 77. Ilium Minimum Spanning Tree (MST) based on the mean Procrustes

distances of each species from one another.

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Ischium-Pubis

The PCA graph for the PC 1 analysis of the ischium-pubis is shown in Figure

78, and PC 1 was responsible for 40% of the shape variation. V. vulpes and C. dirus were located on the negative end of PC 1 and demonstrate a dorsally positioned ischial tuberosity, a longer M. biceps femoris origin site, a shorter pubis, increased length between ischium and pubis, and a closer M. psoas minor insertion site

(iliopubic eminence) relative to the pubis and acetabulum when compared to positive

PC 1 values occupied by felids. Regression analysis of PC 1 versus ln centroid size was not significant (Adjusted R-squared: 0.0389, F-value: 3.228, p-value: 0.0780;

P≤0.05).

PC 2 contributed 22.8% of the variation. A. jubatus, P. atrox, and P. leo were in the negative PC 2 region and separated from the other species at the positive end.

When compared to positive PC 2 end, negative PC 2 showed ischium lengthening, a more caudally positioned ischial tuberosity, a decreased length between the ischium and pubis, and a shorter pubic ramus, making the pubis closer to the acetabulum.

Regression analysis of PC 2 versus ln centroid size was not significant (Adjusted R- squared: 0.000493, F-value: 0.973, p-value: 0.328; P≤0.05). MST in Figure 79 shows C. dirus pairing with V. vulpes (0.0720) and S. fatalis with N. nebulosa

(0.1144). P. atrox linked with A. jubatus (0.0910), P. leo (0.0989), and N. nebulosa

(0.1006). DFA did not provide additional results.

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Principal Component 2 (PC2). Wireframe renditions are shown for shown PC2 PC1 renditions and are axes. (PC2). 2 Component Principal Wireframe

versus versus plot Principal of Component 78. (PC1) 1 Analysis Component Principal Ischium/Pubis Figure

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Figure 79. Ischium/Pubis Minimum Spanning Tree (MST) based on the mean

Procrustes distances of each species from one another.

Proximal Femur

The PCA graph for the proximal femur is shown in Figure 80. The PC 1 analysis shows clustering of A. jubatus with C. dirus and V. vulpes and provided

31% of the shape variation. N. nebulosa, A. jubatus, C. dirus, and V. vulpes are on the positive end and separated by the rest of the species at the negative PC 1 end.

When compared to negative PC 1, the shapes showed a decreased distance between

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the femoral head and the greater trochanter, which is the insertion site for Mm. gluteus medius and gluteus profundus. In addition, the lesser trochanter and M. iliopsoas insertion site was positioned medially and located closer to the femoral head, while the femoral neck is angled medio-distally. Regression analysis of PC 1 versus ln centroid size was significant (Adjusted R-squared: 0.275, F-value: 21.46,

P≤0.001).

PC 2 represented 21.9% of the shape variation separating N. nebulosa, F. catus, and S. fatalis on positive end from A. jubatus, V. vulpes, C. dirus, P. atrox, and P. leo on negative end. A negative PC 2 score represented an increase in trochanter position being at a level higher than the femoral head. In addition, the lesser trochanter was positioned closer to the femoral head. Regression analysis of

PC 2 versus ln centroid size was not significant (Adjusted R-squared: 0.00689, F- value: 0.631, p-value: 0.431; P≤0.05). MST in Figure 81 shows C. dirus linking with

V. vulpes (0.0504) and A. jubatus (0.0629). P. leo was closely associated with both S. fatalis (0.0736) and P. atrox (0.0709).

Tibia

A. jubatus did not cluster with the canids in the tibia PCA analysis (Figure

82). Here, PC 1 accounted for 57.1% of the shape variation. At the positive PC 1 end was S. fatalis, C. dirus, and V. vulpes. The patellar ligament attachment site was longer and more parallel to the tibial shaft when compared to the negative PC 1

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for shown PC2 PC1 renditions and axes. are (PC2). 2 Component Principal Wireframe

Figure 80. Proximal femur Principal Component Analysis plot Principal of Component (PC1) 1 Analysis Component Proximal 80. versus Principal femur Figure

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Proximal femur Minimum Spanning Tree (MST) based on on based (MST) Tree ProximalMinimum femur Spanning

the mean Procrustes distances of each species from distances each of Procrustes another. one mean the Figure 81. 81. Figure

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(PC1)

versus Principal Component 2 (PC2). Wireframe renditions are shown for shown PC2 PC1 renditions and are axes. (PC2). 2 Component Principal Wireframe versus Figure 82. Proximal tibia Principal Component Analysis plot of Principal plot Proximal 82. Principal of Component 1 Analysis Component tibia Principal Figure

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location occupied by the other felids. Regression analysis of PC 1 versus ln centroid size was significant (Adjusted R-squared: 0.210, F-value: 10.84, P≤0.05).

PC 2 accounted for 23.9% of variation. At its positive end it represented increased cranio-caudal width and the proximal end of the tibia. Located in this region was S. fatalis, P. atrox, and P. leo. At the negative PC 2 end was C. dirus, V. vulpes, N. nebulosa, F. catus, and A. jubatus. Regression analysis of PC 2 versus ln centroid size was significant (Adjusted R-squared: 0.319, F-value: 18.36, P≤0.001).

MST (Figure 83) shows the association of C. dirus with V. vulpes (0.1374) and S. fatalis (0.1478). S. fatalis also linked with P. atrox (0.1321), which was also joined with P. leo (0.0991).

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on the on mean Procrustes

distances of each species another. one each of from distances Figure 83. Proximal tibia Minimum Spanning Tree (MST) based Proximal 83. based (MST) Tree tibia Minimum Figure Spanning

DISCUSSION

The study of muscle morphology is a valuable tool for the comparison of carnivores as demonstrated in this dissertation, and muscle function is often correlated with musculoskeletal characteristics of a given species. For example, cursorial species often evolve muscles for increased speed of contraction while ambush predators require muscles capable of generating sufficient force to bring down prey quickly. In these ways, muscle fiber and muscle attachment sites have been shown to provide biomechanical information that characterizes basic muscle types as well as musculoskeletal function (Anemone, 1993; Carlson, 2006; Payne, 2006). Joint articular construction also reflects adaptations by the relative degree of joint mobility

(Ashton and Oxnard, 1964; Andersson, 2004). In the end, a musculoskeletal functional analysis can, in turn, be used to extrapolate behavioral characteristics of extinct species using phylogenetically related extant species as models.

This dissertation has for the first time described the forelimb musculature of N. nebulosa (the clouded leopard) and V. vulpes (the red fox) and generated muscle maps for each species. A number of muscle attachment sites were observed to differ between

V. vulpes and the two felids. Interestingly, some muscles were absent in V. vulpes relative to the felids. An analysis of muscle fibers combined with muscle attachment surface area showed that specific muscles may be able to separate arboreal versus

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cursorial modes of locomotion. For some muscles, attachment site surface areas and location were correlated with modes of locomotion noted in the literature for extinct species. The addition of forelimb and hindlimb bone geometric morphometric analysis highlighted several key cursorial and non-cursorial characteristics. These involved muscle attachment sites as well as joint articular surfaces.

Muscle Dissection and Data Analysis

Dissections comparing the two felids and V. vulpes showed differences in muscle arrangement and in muscle architecture. Distal forelimb muscles had longer tendons in V. vulpes when compared to felids. The insertion site for M. infraspinatus on the caudal aspect of the humeral greater tubercle was tendinous in V. vulpes while it is a direct fibrous attachment in the felids. Tendons store and release elastic energy during locomotion compared to muscle fiber shortening, thereby saving energy

(Williams et al., 2008). This implies that V. vulpes displays increased locomotor efficiency and high energy recovery by the elastic recoil of longer tendons (Biewener and Baudinette, 1995).

M. cleidobrachialis showed a major attachment location difference in V. vulpes when compared to the felids. Its origin, the cartilaginous clavicle, was the same in all three carnivores. However, in felids the insertion site was by a strong tendon on the ulna along with M. brachialis, while in V. vulpes this site is only on the humerus. M.

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cleidobrachialis is a forearm flexor in felids and an arm flexor in V. vulpes (Howell,

1944). This suggests that cursorial species such as V. vulpes rely less on flexion of the elbow and more on humeral protraction during locomotion. In addition, the clavicle is extremely thin in V. vulpes when compared to that of felids. It is important to note that in all three species, the clavicle is attached to the manubrium and scapula by a band of connective tissue (Rozenweig, 1990; Evans and de LaHunta, 2004).

V. vulpes lacks a number of muscles that the felids possess. One reason may be related to restricted range of movement to emphasize parasagittal movement with reduced circumduction, abduction, and medial rotation (Howell, 1944). In felids, M. rhomboideus thoracis clearly separates into cranial and caudal heads, described in the results as I and II, respectively. M. rhomboideus thoracis II inserts with a thick tendon onto caudal dorsal scapular angle. However, in V. vulpes M. rhomboideus thoracis II is missing. This results in a lower weight of M. rhomboideus thoracis in V. vulpes relative to the felids. As a consequence, scapular retraction may be hindered in V. vulpes (Rozenweig, 1990; Evans and de LaHunta, 2004).

Antebrachium muscles that are absent in V. vulpes include Mm. brachioradialis, extensor carpi radialis brevis, flexor digitorum brevis, and interflexorius. Decreased antebrachium muscle weight, observed in cursorial species is believed to increase locomotion speed by reducing limb swing inertia (Howell, 1944;

Ewer, 1973; Lee at al., 2004). The combined craniolateral antebrachium muscle weight percentage to total forelimb in V. vulpes was significantly lower than in N.

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nebulosa. The absence of M. brachioradialis, antebrachium supinator and flexor in V. vulpes, may reflect reduced antebrachium rotation ability. In contrast, M. brachioradialis in N. nebulosa appeared to be much thicker than in F. catus.

There were also differences in tendons in certain antebrachium muscles. M. flexor digitorum superficialis sends a tendon to digits two through five in V. vulpes but lacks the tendon to the first digit seen in felids. This reduces first digit flexion ability in V. vulpes. M. extensor digitorum lateralis splits into two tendons going to digits four and five while felids possess three tendons controlling digits three, four, and five.

Additionally, perhaps due to the absence of M. extensor carpi radialis brevis in V. vulpes, M. extensor carpi radialis longus separates into two tendons in V. vulpes to insert on the second and third metacarpals. In felids, M. extensor carpi radialis longus inserts on the second metacarpal while M. extensor carpi radialis brevis inserts on the third metacarpal.

Muscle Fiber Analysis and Attachment Site Surface Area

Higher PCSA ratio muscles in one species when compared to another indicates increased muscle contraction strength in that species (see Materials and Methods). On the other hand, a higher speed to force ratio (W/Po) muscle in one species compared to another shows a faster contraction rate. Muscle fiber analysis studies generally show that muscle weight ratios correlate with PCSA ratios (Sacks and Roy, 1982; Anapol

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and Gray, 2003). In this study, greater differences in muscle weight ratios were observed than in PCSA ratios between felids and canids. This may be due to a low sample size as the two V. vulpes specimens showed high intraspecies variation. A possible explanation for the high variation may be measurement error. This leads to

Type II error, failure to reject the null hypothesis when it is false (Zar, 1999).

Differences between the speed to force ratio (W/Po) were even fewer.

Normalization of data may be the leading cause for these results. Anapol and Gray

(2003) did not normalize the speed to force ratio in their comparative study of guenons. However, in the present study, N. nebulosa has a body size that is much larger than that of V. vulpes and F. catus, making a comparison without normalization impossible. It was necessary to normalize for body size to interpret the speed to force ratios by using the muscle weight to total ratio and PCSA to total ratio.

Nevertheless, for many muscles there was a correlation between muscle weight ratio and PCSA ratio. M. rhomboideus is an example of a significant correlation. This muscle causes scapular retraction and caudal scapular rotation where the glenoid fossa is rotated ventrally (McEvoy, 1982). This action is believed to be especially important for arboreal species when lifting the body up the tree trunk against gravity (Taylor,

1978; McEvoy, 1982). Because M. rhomboideus thoracis II is absent in V. vulpes, the combined M. rhomboideus thoracis weight and PCSA ratios are considerably lower than in felids.

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Muscles crossing the shoulder joint, specifically the rotator cuff muscles, stabilize this joint. Interestingly, Mm. infraspinatus, teres minor, and coracobrachialis weight and PCSA ratios were higher in V. vulpes than the felids. Additionally, F. catus had higher ratios for these muscles than N. nebulosa. This has also been observed in quadrupedal versus suspensory primates (Anapol and Gray, 2003; Kikuchi et al., 2012;

Larson and Stern, 2013). It has been suggested that M. infraspinatus stabilizes the shoulder joint (Larsen and Stern, 2013). Suspensory primates, such as the gibbon, possess a lower PCSA ratio for M. infraspinatus than in the more terrestrial primates.

Decreased use of M. infraspinatus frees the shoulder joint, allowing protraction of the limb during climbing (Larson and Stern, 2013). Furthermore, M. coracobrachialis may be important for shoulder joint stability and forelimb protraction during sustained running in V. vulpes (Herrel et al., 2008).

There was a reduction in the weight of muscles occupying the medial and lateral sides of the antebrachium in V. vulpes compared to the felids. Mm. brachioradialis and extensor carpi radialis brevis are absent in V. vulpes. These muscles are important for antebrachium rotation and are more important for arboreal species, as seen in the panda (Davis, 1964) and in primates (Heinrich and Rose, 1997).

The results obtained here are comparable to results obtained for arboreal versus terrestrial primates (Kikuchi, 2010). Additionally, the radial and ulnar heads for M. flexor digitorum profundus showed the most significance between canid and felid species. These muscles had much higher weight and PCSA ratios in felids compared to

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V. vulpes. The ulnar head of M. flexor digitorum profundus had a PCSA ratio that is significantly larger in N. nebulosa than F. catus. M. flexor digitorum profundus was also larger in weight and PCSA ratios in the arboreal versus terrestrial primates, suggesting an importance for grasping tree branches during arboreal locomotion

(Kikuchi, 2010; Youlatos, 2010).

There were a few muscle correlations with the surface area of muscle origin and relative muscle weight and/or PCSA ratio across these taxa. However, it was less than expected. Large surface areas for muscle origins increase muscle fiber population, and studies have shown a correlation between muscle origin surface area and muscle weight and/or PCSA ratios (Endo, 2007; Bello-Hellegouarch et al., 2013; Larson and

Stern, 2013).

Here, the origin of M. infraspinatus on the scapula was larger in V. vulpes compared to felids. This origin surface corresponds to a large M. infraspinatus muscle weight and PCSA ratios in V. vulpes. The origin of M. coracobrachialis on the scapula and insertion on humerus was also larger in V. vulpes. This muscle’s weight and PCSA ratios were larger in V. vulpes. As discussed above, Mm. infraspinatus and coracobrachialis are important for shoulder joint stability, a cursorial adaptation

(Herrel et al., 2008; Larson and Stern, 2013).

In caudal view, the scapular origin of the long head of M. triceps brachii and its insertion site on the ulna show larger surface areas for V. vulpes in comparison to this muscle for felids. Muscle weight and PSCA ratios were also larger for V. vulpes (not

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significant) than felids. M. triceps brachii long head muscle weight ratio has been reported in the literature to be higher in cursorial species when compared to non- cursors (Gambaryan, 1974; Salesa et al., 2007; Williams et al., 2007). Williams and colleagues (2007) have suggested that the cursorial M. triceps brachii stabilizes the elbow joint and it may prevent elbow joint flexion during the stance phase of running.

Mm. flexor digitorum profundus ulnar and radial surface areas of origin on ulna and radius respectively, were larger in the felids compared to V. vulpes (not significant), and the weight and PCSA ratios of the muscles were also larger in the felids. As discussed above, M. flexor digitorum profundus has been suggested in the literature to be important for tree branch grasping (Kikuchi, 2010; Youlatos, 2010).

Surface area measurements of extant and extinct species were compared. Some of the muscle attachment site surface area measurements were similar in comparisons between extant and extinct species. Felids were generally separate from canids. N. nebulosa was closer to S. fatalis and P. atrox. V. vulpes was matched with C. dirus. M. deltoideus insertion and M. flexor digitorum profundus ulnar head origin surface areas were larger for the felids. However, F. catus was closer to the canids for the M. deltoideus insertion. On the other hand, M. brachialis origin, M. triceps brachii long head insertion, M. flexor carpi ulnaris ulnar head origin, and M. pronator quadratus origin surface areas were larger for canids than for felids.

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Geometric Morphometric Analysis of Forelimb and Hindlimb Bones

First, it is important to note that whole bone analyses yield results that are dependent on the body size of the species. This was also observed by Martin-Serra and colleagues (2014), who performed three-dimensional analyses on mammalian forelimb bones. In larger species, limb bones tend to become more robust while in smaller species they are more gracile because of allometry. The present study has shown that analyzing the proximal or distal ends of limb bones provides more information than bone outline analysis on limb biomechanical differences based on muscle attachment site locations. The degree of joint mobility may also be inferred from joint articular surface shape.

In the geometric morphometric results, the extinct Panthera atrox often clustered with the extant lion Panthera leo. There is disagreement in the literature on whether or not P. atrox is closely associated with P. leo (Kabitzsch, 1960; Dietrich,

1968; Christiansen and Harris, 2009). Although P. atrox had a much larger body size than P. leo, MST (Minimum Spanning Tree) linked the two species. S. fatalis, however, was linked with canids in analyses of the scapula, ilium, and tibial shape.

This association may suggest high endurance requirement by S. fatalis during grappling with prey. Canis dirus was always associated with Vulpes vulpes. Table 30 summarizes the limb morphological differences observed between cursors and ambushers.

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Table 30 Observed Limb Morphological Character Differences Between Cursorial and Ambush

Felids and Canids

Morphological Cursors Ambushers Characters Scapula Width Narrow Wide Scapula – Vertebral Reduced width of M. Enlarged width of M. Border rhomboideus insertion rhomboideus insertion Scapula – Supraspinous Narrow Enlarged, rounded Fossa Glenoid Fossa Round, caudally oriented Narrow, lateral concavity Glenoid Neck Elongated Wide and short Greater Tubercle of Narrow and extends Wide and closer to level Humerus farther past humeral head of humeral head Lesser Tubercle of Closer to shoulder joint Farther laterally from Humerus shoulder joint Distal Humerus Capitulum and trochlea Capitulum wider than same width, medial trochlea, medial epicondyle reduced epicondyle enlarged Ulna Caudal concavity of ulnar Straighter ulnar shaft shaft Olecranon Process Short relative to ulnar Long relative to ulnar length length Distal Radioulnar Proximodistal elongation Mediolateral elongation Articular Facet of Ulna Radial Tuberosity Proximally closer to radial Farther distally from head radial head Distal Radioulnar Proximodistal elongation Mediolateral elongation Articular Facet of Radius Ilium Dorsal ilium shortening, Dorsal ilium longer ventral ilium lengthening Iliopubic Eminence Closer to acetabulum Farther from acetabulum Ischial Tuberosity More dorsally oriented Level with ischium Greater Trochanter of Short, level with femoral Long, extends farther past Femur head femoral head Lesser Trochanter of Closer to hip joint Farther distally and Femur laterally from hip joint

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Scapular Rotation and Retraction

Taylor (1978) commented on the importance of caudal scapular rotation and scapular retraction in climbing. Caudal scapular rotation results in ventral rotation of glenoid fossa. This movement, along with scapular retraction, allows the thorax to resist the pull of gravity (Taylor, 1978; McEvoy, 1982). For cursorial species, it has been suggested that cranial scapular rotation, in which the glenoid turns to face more dorsally, is of greater importance than caudal scapular rotation (Howell, 1944; Taylor,

1978). During the swing phase, the scapula rotates cranially and the brachium is protracted toward the head (Howell, 1944).

The scapular analysis showed the metacromion process positioned closer to the glenoid fossa in canids, when compared to felids. Interestingly, S. fatalis was positioned closer to canids in this respect. The metacromion process is the origin site for M. omotransversarius which inserts onto the transverse process of atlas. This muscle is believed to flex the neck laterally but also to rotate the scapula cranially

(Rozenweig, 1990; McEvoy, 1982). If the scapular rotation axis is considered to be at the center of scapula, then positioning the metacromion farther from the rotation axis, as in canids and S. fatalis, may increase the mechanical advantage of M. omotransversarius during cranial scapular rotation. This muscle may be important for increasing endurance in canids during running. A. jubatus did not display this characteristic, which may relate to its ability to only run short distances.

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The scapula in S. fatalis showed its vertebral border to be enlarged and pointed more dorsally when compared to other species. The vertebral border of scapula is the insertion site for M. rhomboideus, a scapular retractor. The enlarged scapular vertebral border may suggest increased size and force generation capability in M. rhomboideus to assist with prey grappling (Argot, 2002).

Humeral Protraction, Retraction and Abduction

In canids and S. fatalis, the acromion process extends past the glenoid process.

M. acromiodeltoideus originates from the acromion process. In an F. catus shoulder muscle electromyography study, M. deltoideus was active during the swing phase when the brachium is protracted (English, 1978). According to Howell (1944), M. acromiodeltoideus functions more in limb protraction in cursorial species rather than for abduction of the brachium. A. jubatus once again was not associated with the canids in this respect. In canids, this may suggest extended endurance while running.

The M. teres major origin site on the caudal angle of the scapula also differed between canids and felids. M. teres major is an important brachium retractor (McEvoy,

1982). In canids, the site is closer to the glenoid fossa. In a study that compared arboreal and terrestrial primates, the terrestrial primate Macaca nemestrina M. teres major origin was closer to the shoulder joint when compared to the arboreal Macaca fascicularis (Rodman, 1979). Rodman (1979) suggested that origins closer to shoulder

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joint may decrease the angle between the M. teres major insertion and humerus long axis. Tendon insertion angle is used in the calculation of torque. A more acute angle implies a greater arc of movement but reduced muscle contraction force. However, the insertion site position relative to joint axis must also be considered.

A. jubatus clustered with the canids with its caudally-oriented glenoid fossa.

This has also been observed in quadrupedal primates when compared to brachiators

(Oxnard and Ashton, 1964). Oxnard and Ashton (1964) suggested that a more cranially directed glenoid fossa increases range of motion in the shoulder joint. But a caudally oriented glenoid results in faster brachium retraction, an important function for cursorial species.

The lesser tubercle of the humerus, an insertion site for M. teres minor, was closer to the shoulder joint in the cursorial species, yet more lateral in the felids. N. nebulosa was at the extreme end, with a lesser tuberosity that is located farther from the shoulder joint. M. teres minor retracts the brachium and stabilizes the shoulder joint (Rozenweig, 1990). An insertion site located farther from the joint axis increases the muscle’s mechanical advantage (Ewer, 1973). Therefore, in N. nebulosa, contraction of the M. teres minor may generate increased force compared to the other species in this study. However, M. teres minor in N. nebulosa had a lower PCSA ratio than that seen in F. catus and V. vulpes.

A. jubatus and canids humeral greater tubercle extended farther proximally past the humeral head. An elevated greater tubercle increases the lever arm of M.

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supraspinatus which can produce a more powerful recovery phase of the forelimb during a chase (Walker, 1974). Quadrupedal primates also have an elevated greater tuberosity compared to arboreal primates and the vertical clingers and leapers (Walker,

1974).

Shoulder Joint Mobility

The glenoid fossa analysis positioned A. jubatus closer to canids than felids suggesting its shape is correlated with degree of shoulder joint mobility. MST also linked A. jubatus with C. dirus. The primary character associated with cursorial species was the roundness of the glenoid fossa. Felids, on the other hand, showed lateral concavity of the glenoid fossa. A narrower glenoid fossa has been reported in arboreal species, and it has been suggested to increase shoulder joint mobility and is often referred to as “pear-shaped” in the literature (Fleagle and Simons, 1982; Larson and Stern, 1989; Gebo and Rose, 1993; Heinrich and Rose, 1997).

Antebrachium Flexion and Extension

The radial tuberosity is positioned more distally relative to the radius long axis in non-cursorial species when compared to A. jubatus and the canids. The radial tuberosity is the insertion site for M. biceps brachii, an antebrachium flexor. A

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more distal insertion site increases muscle mechanical advantage and a more proximal insertion decreases the muscle lever arm and increases the arc of the antebrachium movement (Rodman, 1979; Wroe et al., 2008; Janis and Figueirido, 2014). This suggests that ambush predators benefit from stronger antebrachium flexion.

In the ulnar analysis, the olecranon process, M. triceps brachii insertion site, appeared to be shorter relative to ulnar length in cursorial species when compared to non-cursorial species. However, F. catus grouped with the canids. This may be due to the small body size of F. catus. Here, the whole outline of the ulna was analyzed, and the regression analysis of ulna shape was significantly dependent on body size.

Nevertheless, the observed difference in the olecranon process length relative to ulna length may be related to M. triceps brachii biomechanics. Rodman (1979) suggested that a shorter olecranon process allows full elbow extension, which in turn increases stride length. He added that a short olecranon process increases the antebrachium movement arc, but a longer olecranon process allows for a more forceful antebrachium extension.

It is also important to note the ulnar curvature difference seen in comparisons between cursorial and non-cursorial species. The C. dirus ulna is concave caudally and the N. nebulosa ulna is straight. Taylor (1974) suggested that a caudally directed olecranon process may increase M. triceps brachii length and contraction speed. In a qualitative study of the limb bones of Arctitis, Neofelis, Hyaena, and extinct borhyaenoids, Argot (2003) described the different degrees of ulnar curvature. Arctitis

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binturong ulna was convex caudally, and Neofelis nebulosa displayed a straighter ulna than the caudally concave ulna of Hyaena hyaena. It was suggested that a more caudally convex ulna increases the grasping ability of the manus by increasing the leverage of M. flexor digitorum profundus ulnar head (Argot, 2003).

The medial epicondyle, origin site of M. pronator teres and carpal and digital flexor muscles in the antebrachium, was relatively larger in N. nebulosa, S. fatalis, P. atrox, and P. leo compared to cursorial species. In addition, the medial epicondyle was more proximal in the non-cursorial species when compared to A. jubatus and canids.

The medial epicondyle is also larger in arboreal primates (Walker, 1974; Fleagle and

Simons, 1982, 1995; Stevens et al., 2005) and arboreal viverrids (Taylor, 1974). M. pronator teres, in particular, may play a major role in prey grappling and aiding arboreal animals during clinging to tree trunks and branches.

Elbow Joint Mobility

A. jubatus and canids were characterized by a capitulum and trochlea that were equally wide mediolaterally. The non-cursorial felids showed a wider capitulum than trochlea. This characteristic was observed in arboreal primates and is believed to increase rotational movements of the radius (Rose, 1988, 1993; Harrison, 1989;

Nakatsukasa, 1994; Egi et al., 2007). Also in non-cursorial felids, a distally expanded trochlear flange was observed. Andersson (2004) suggested that it may act to

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counteract the lateral forces incurred during prey grappling. This may be especially important for N. nebulosa when balancing on tree branches.

Antebrachium Rotation

Distal radioulnar articular surface analyses resulted in a significant separation of cursorial and non-cursorial species. A. jubatus was closely grouped with C. dirus and V. vulpes. These cursorial species showed proximodistal elongation of both distal radial and ulnar articular surfaces. Non-cursorial species, on the other hand, were characterized by mediolaterally expanded articular surfaces. Comparative studies of arboreal to terrestrial primates (Corruccini, 1978; Harrison, 1982; Read, 2001;

Tallman, 2012) and musteloids (Fabre et al., 2013) reported broader distal radioulnar articular surfaces in the arboreal species. These studies suggested that proximo-distally oriented articular surfaces may stabilize the joint during running, an important cursorial adaptation. But mediolaterally expanded facets may allow for a greater range of supination required for arboreal habits and ambush predation (Fabre et al., 2013).

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Femoral Flexion and Extension

The origin of M. iliacus is on the ventral border of the ilium and extends to the iliopubic eminence (Carlon, 2012). M. iliacus is a thigh flexor (Gebo and Sargis, 1994;

Argot, 2002). Additionally, the iliopubic eminence is the insertion site for M. psoas minor, a lumbar and pelvis flexor (Li and Luo, 2006). The position of the iliopubic eminence was cranially farther from the acetabulum in non-cursorial felids and closer to the acetabulum in cursorial species. It is possible that if the iliopubic eminence is farther from the hip joint it may enhance the moment arm of M. iliacus and psoas minor and increase muscle torque. However, muscle moment arm measurements must be performed using a method such as the one described by Williams and colleagues

(2008).

The lesser trochanter, M. iliopsoas insertion site, was positioned farther laterally and distally from the hip joint in the non-cursorial felids when compared to A. jubatus and canids. This may increase the M. iliopsoas mechanical advantage in non- cursorial felids, thus increasing force production (Taylor, 1976; Rodman, 1979).

Consequently, cursorial species may benefit from a more proximally inserted M. iliopsoas to increase hip flexion speed (Taylor, 1976; Rodman, 1979; Argot, 2003).

There was a difference in the relative length of the dorsal iliac spine and the origin for M. gluteus medius, between cursorial and non-cursorial species in the present study. M. gluteus medius is a femoral extensor (Smith and Savage, 1956).

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Although A. jubatus did not cluster with C. dirus and V. vulpes, the three species exhibited a shortened dorsal iliac spine, where the dorsal cranial iliac spine was located closer to the acetabulum of the hip joint. It was interesting that S. fatalis was positioned closer to the canids in this analysis than felids. Rodman (1979) has found that the arboreal Macaca fascicularis had a longer ilium compared to the terrestrial

Macaca nemestrina. He suggested that a closer origin site in relation to joint axis may decrease the angle of tendon insertion relative to long axis of the insertion site

(Rodman, 1979). Decreased force application angle decreases the muscle’s torque thus increasing the speed and movement arc (Knudson, 2007). However, this must be tested on complete skeletons.

The greater trochanter, the M. glutei insertion site, was higher proximally and more lateral than the femoral head in non-cursorial felids, especially for S. fatalis, than in cursorial species. This has also been observed by Rodman (1979) in his comparative study of arboreal and terrestrial Macaca. It has been suggested that a proximally projected greater trochanter may increase the M. gluteus medius lever arm and lead to more forceful thigh extension (Taylor, 1976; Rodman, 1979; Sargis, 2004). However, the greater trochanter in N. nebulosa and F. catus did not extend as proximally as it did in S. fatalis, P. atrox, or P. leo. Sargis (2004) suggested that a proximally- projected greater trochanter decreases hip joint mobility and hip abduction. A greater trochanter that is slightly lower than the femoral head may be an arboreal adaptation.

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Although A. jubatus and canids did not cluster in the ischium analysis, the ischial tuberosity was deflected more dorsally in these cursorial species when compared to non-cursorial felids. The ischial tuberosity is the origin of the hamstring muscle group (Carlon, 2012). Argot (2003) has suggested that this characteristic in cursorial species may provide faster thigh extension. Also, the M. biceps femoris origin extended more caudally in the cursorial species. This may increase M. biceps femoris length relative to hindlimb length. Gowitzke and Milner (1980) suggested that longer muscles may increase the joint movement arc and contract more rapidly than muscles with shorter fibers.

Suggestions for Future Research

In future studies, the use of a laser scanner would benefit muscle attachment site surface area measurements. Because muscles attach on curved surfaces of bones, two-dimensional measurement is not as accurate as three-dimensional measurement

(Zumwalt, 2005). For example, Mm. supraspinatus and infraspinatus attach on the relatively flat surface of scapula, but they also attach onto the cranial and caudal surface of the scapular spine. In this study, I was not able to measure the total attachment area for these muscles using two-dimensional analysis. Also, published studies have reported a better correlation between muscle PCSA ratios and three-

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dimensional surface area measurement, when compared with two-dimensional measurements (Bello-Hellegouarch et al., 2013; Larson and Stern, 2013).

Additionally, the degree of muscle attachment site rugosity can be measured with a three-dimensional laser scanner. It has been suggested that attachment site rugosity may be an indicator of relative muscle force (Bryant and Seymour, 1990). For example, the degree of rugosity of the humeral greater and lesser tuberosities may correlate with muscle PCSA ratios.

Geometric morphometric analysis may provide more accurate results if inputted with three-dimensional landmarks. This would be especially useful when analyzing joint articular surface shapes. Cursorial species are characterized by having a deeper glenoid cavity than arboreal animals, and this is believed to be an adaptation for increasing joint stability (Heinrich and Rose, 1997; Argot, 2003). Relatively shallow glenoid cavities observed in Arctitis and Ursus may reflect increased shoulder mobility and their slow locomotion rates may reduce the risk of dislocation despite reduced stability (Argot, 2002). This type of analysis may be able to separate the arboreal N. nebulosa from non-arboreal felids.

The distal radioulnar articular surface analysis provided the best separation of cursorial and non-cursorial species. N. nebulosa was expected to separate from the non-cursorial felids because of its highly arboreal specialization. However, this was not the case. Three-dimensional landmarks of the distal ulnar notch of the radius will provide concavity information. Fabre and colleagues (2013) performed a three-

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dimensional landmark analysis of musteloid distal radioulnar articular facets. They reported that in musteloids with high grasping ability, the distal ulnar facet of the radius was more rounded and concave than in musteloids with poor grasping ability.

Muscle moment arm measurements describe muscle mechanical advantage and have been performed in comparative studies of various species (Payne et al., 2006;

Hudson et al., 2011 a, b; Fujiwara and Hutchinson, 2012). The moment arm is defined to be the shortest perpendicular distance from the joint center to the muscle line of action (Payne et al., 2006). As moment arm increases, the muscle’s force production increases at the expense of angular velocity (Lieber & Friden, 2001). Therefore, muscle moment arm measurement may be a useful analysis in the future. There are different methods for measuring moment arms. One method is the tendon travel method (Spoor and van Leeuwen, 1992). This method is based on the principle that when a circle’s radius moves an angle of one radian to a new position, then the arc length travelled is equal to the distance between the new point and circle’s center.

With the tendon travel method, the distance travelled by the tendon while the limb moves one radian is equal to the perpendicular distance between the tendon and joint center axis (Spoor and van Leeuwen, 1992). This perpendicular distance is a measure of muscle moment arm. The ratio of distance traveled by tendon to the joint angle change in radians is calculated. Then, the derivative of the ratio is taken. The measurements are recorded at mid-stance and at minimum and maximum joint angles.

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Another method relies solely on bone measurements. For example, Fujiwara and Hutchinson (2012) measured the distance between the muscle insertion point on a bone and the joint center axis. For the M. triceps brachii moment arm, the distance between the most proximo-caudal point on olecranon process and the elbow joint axis was measured. For M. biceps brachii, the radial tuberosity and elbow joint axis were the two measurement points. Masticatory muscle moment arms on fossil skulls have also been measured through this technique (Christiansen and Adolfssen, 2005;

Anyonge and Baker, 2006). But this method does not take into effect the different limb postures or joint position angles which impact moment arms. Therefore, caution about the results has been suggested (Fujiwara and Hutchinson, 2012).

Concluding Remarks

Forelimb morphology is an especially important indicator of prey capture technique. Ambushing prey requires strong forelimb muscles to subdue prey (Ewer,

1973; Martin, 1980; Turner and Anton, 1997; Akersten, 2005; Martin et al., 2011;

Naples, 2011). Adaptations for increased rotational ability of scapula, brachium, and antebrachium was seen in the ambush carnivores. Grasping struggling prey is made possible by strong digital flexors. On the other hand, cursorial adaptations are stabilized joints, powerful humeral protraction, fast antebrachium flexion and extension, and reduced pronation-supination. The hindlimb differences between

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cursorial and non-cursorial carnivores were fewer than for the forelimb. Adaptations for forceful thigh flexion and extension are possessed by ambush carnivores, while cursorial characters are suited for hindlimb excursion speed.

Smilodon fatalis and Panthera atrox were most likely ambush predators based on their similarity in forelimb morphology to the extant non-cursorial felids N. nebulosa and P. leo. Strong scapular retraction, important for prey wrestling, was especially apparent in S. fatalis scapula shape. Its vertebral border of the scapula, the

M. rhomboideus insertion site, was robust and dorsally pointed. The glenoid fossa shape showed lateral concavity, as in extant non-cursorial carnivores, which is believed to increase shoulder joint mobility (Fleagle and Simons, 1982; Argot, 2002).

However, Naples (2011) suggested that the head of the humerus in S. fatalis is anteroposteriorly elongated, which reduces the degree of abduction of the humerus.

Therefore, the large M. deltoideus surface area of humeral insertion in S. fatalis may be related to the need for forceful humeral protraction to assist with prey grappling with the additional recruitment of body wall and scapular muscles (Naples, 2011). A relatively distal radial tuberosity and long olecranon process indicate strong antebrachium flexion and extension in S. fatalis and P. atrox. Increased antebrachium rotation capability is inferred by a wide humeral capitulum, large humeral medial epicondyle, and medio-laterally elongated distal radioulnar articular facets. Together, these morphological characters may enhance the ability of the forelimbs to bring down large prey. In the hindlimb, the more proximally projected femoral greater trochanter

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and relatively more distal femoral lesser trochanter in S. fatalis and P. atrox may increase the mechanical advantage for the M. gluteus medius and M. iliopsoas, respectively. These adaptations may aid balancing on the hindlimbs while prey wrestling.

Based on its similarity to V. vulpes and A. jubatus, C. dirus was most likely cursorial and engaged in group hunting. Cursorial forelimbs are adapted to increase stride length and speed and are used to a lesser degree when bringing down prey.

These species exhibited an adaptation for forceful humeral protraction, evident the in proximally longer greater tubercle of the humerus, the M. supraspinatus insertion site.

Therefore, the M. supraspinatus mechanical advantage is increased in cursorial species to allow for powerful recovery phase during the chasing of prey (Walker, 1974). It is suggested that high speed locomotion requires a more stable shoulder joint (Argot,

2002). The rounded shape of the glenoid fossa, a shared cursorial character, may serve to increase shoulder joint stability (Argot, 2002). In addition, muscles crossing the shoulder joint, such as Mm. infraspinatus and coracobrachialis, were larger in muscle weight and PCSA ratios in V. vulpes than in felids, further demonstrating the necessity for cursorial shoulder joint stability. Relatively more proximal positioning of the radial tuberosity and the short olecranon process allow for fast antebrachium flexion and extension, respectively. Narrow humeral capitulum and proximo-distally oriented radioulnar articular facets demonstrate that antebrachium rotation is sacrificed to increase limb excursion speed in cursorial carnivores. In the hindlimb, thigh flexion

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and extension speed is increased by the more proximal insertions of M. iliopsoas and

M. gluteus medius.

This dissertation has identified several key cursorial and non-cursorial morphological adaptations using quantitative analyses. Habitat type and prey availability result in the convergence of distantly related carnivores, as seen here with

A. jubatus and canids. Carnivores living in open terrain are adapted for speed because of the lack of grassy cover needed to ambush prey. The cursorial adaptations identified were more stable joints and muscles adapted for high velocity of contraction and increased limb excursion. On the contrary, ambushers rely on the element of surprise by stalking from concealment. Their more mobile joints and stronger forelimb muscles allow them to overpower large prey. The forelimb morphology of S. fatalis is especially indicative of its forelimb use to subdue prey and deliver the killing bite to the throat. In future analyses, the use of three-dimensional landmarks will most likely provide additional functional information. I plan to also analyze other extinct carnivoran species to infer about their locomotor and hunting habits.

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