University of Alberta
The Evolution and Function of Theropod Dinosaur Tails
by
Walter Scott Persons
A thesis submitted to the Faculty of Graduate Studies and Research in partial fulfillment of the requirements for the degree of
Master of Science in Systematics and Evolution
Department of Biological Sciences
©Walter Scott Persons Fall 2011 Edmonton, Alberta
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Unlike extant birds and mammals, most non-avian theropods had large muscular tails. Digital muscle reconstructions based on measurements of fossil
specimens and dissections of modem reptiles show that theM. caudofemoralis of many non-avian theropods was exceptionally large. Because M.the caudofemoralis is the primary hindlimb retractor, largeM. caudofemoralis masses give new evidence in favor of greater athleticism. The tails of theropods had a dynamic evolution and became specialized for a wide range of additional functions in various lineages. In Ceratosaurus the tail may have been adapted for swimming. In the South American abelisaurs, the angle of the caudal ribs was gradually adjusted to facilitate an even largerM. caudofemoralis that probably increased maximum running performance. In oviraptorosaurs, the tail supported a fan of feathers, and appears to have become modified for courtship displays. In dromaeosaurs, caudal rods may have allowed the tail to serve as an aerial rudder. ACKNOWLEDGEMENTS
This research was made possible by the support of the Dinosaur Research
Institute, the Korean-Mongolian International Dinosaur Project and the University of Alberta China Institute. I wish to thank John Acorn (University of Alberta),
Victoria Arbour (University of Alberta), Robert Bakker (Houston Museum of
Natural Science), Philip Currie(University of Alberta), Robert Holmes (University of Alberta), Pierre Lemelin (University of Alberta), Heinrich Mallison (Museum fiir Naturkunde), Alison Murray, and Eric Snively (Ohio University) for their repeated council and for many fruitful discussions about dinosaur tails. I also wish to extend my gratitude to Rinchen Barsbold (Paleontological Center of the
Mongolian Academy of Sciences), Michael Brett-Surman (Smithsonian
Institution National Museum of Natural History), Paige Johnson (Natural History
Museum of Los Angeles County), Carl Mehling (American Museum of Natural
History), Mark Norell (American Museum of Natural History), Brandon Strilisky
(Royal Tyrrell Museum of Palaeontology), and Chinsorig Tsogtbaatar
(Paleontological Center of the Mongolian Academy of Sciences) for their indispensable assistance in navigating the enormous storerooms of their respective institutions. Scott Hartman and Lida Xing merit my gratitude (and envy) for their stunning artistic skills and talents, which were graciously lent to this project. Special thanks are also owed to Joe Barter (Duke University) for his hospitality and assistance in recording tail measurements and to Eva Koppelhus
(University of Alberta) and Alejandro Kramarz (Museo Argentino de Ciencias Naturales “B. Rivadavia”) for their help in photographing specimens. Lastly, I thank Michael Caldwell for his unhesitating willingness to sacrifice many tails from his sizable frozen reptile collection. TABLE OF CONTENTS
Abstract
Acknowledgements
List of Tables
List of Figures
Institutional Abbreviations
Introduction...... 1
Chapter 1 The Tail ofTyrannosaurus : Reassessing the Size and Locomotive Importance of theM. caudofemoralis in Non-avian Theropods...... 5
1.1 Introduction...... 5
1.2 Anatomy...... 8
1.3 Computer Modeling...... 11
1.4 Biomechanics...... 12
1.5 Caudal Musculature and Osteological Correlates of Extant Reptiles...... 16
1.6 Evidence for the Posterior Taper Point and Ventral Boundary of the M. caudofemoralis in Non-avian Theropods...... 24
1.7 Evidence for the Lateral Boundary ofM. the caudofemoralis in Non-avian Theropods...... 30
1.8 Muscle Reconstruction...... 32
1.9 Biomechanics...... 39
1.10 Discussion...... 39
1.11 Bibliography...... 47 Chapter 2 Dinosaur Speed Demon: Caudal MusculatureCarnotaurus of and Implications for the Evolution of South American Abelisaurids...... 54
2.1 Introduction...... 54
2.2 Reconstruction Method and Assumptions...... 59
2.3 Reconstruction Results...... 69
2.4 Functional Implications...... 74
2.5 Evolutionary Context...... 77
2.6 Conclusion...... 81
2.7 Bibliography...... 84
Chapter 3 Oviraptorosaur Tail Forms and Functions...... 88
3.1 Introduction...... 88
3.2 Caudal Osteology...... 89
3.3 Caudal Musculature...... 93
3.4 Discussion...... 98
3.5 Bibliography...... 105
Chapter 4 Dragon Tails: Convergent Caudal Morphology in Winged Archosaurs...... I l l
4.1 Introduction...... I l l
4.2 Materials and Methods...... 115
4.3 Results...... 120
4.4 Muscle Mass and Flexibility...... 125
4.5 Evolutionary Context...... 130
4.6 Bibliography...... 134 Chapter 5 An Overview and Reanalysis of Theropod Tail Morphology, Function, and Evolution...... 139
5.1 Introduction...... 139
5.2 Musculature Reconstruction Methodology and Results 141
5.3 The Caudofemoral Complex and the Origin of Archosaur
Bipedality...... 146
5.4 Tails of Non-coelurosaurian Theropods...... 150
5.5 Tails of Non-deinonychosaurian Coelurosaurs...... 162
5.6 Tails of Deinonychosaurian Coelurosaurs and the Origin of
Dinosaur Flight...... 174
5.7 Conclusions and Discussion...... 185
5.8 Bibliography...... 189
Conclusion...... 198
Appendix A...... 200
Appendix B...... 205 LIST OF TABLES
Chapter 1
TABLE 1.1. Caudal muscle mass of theropods and extant reptiles.
TABLE 1.2. Cross-sectional area in the M. caudofemoralis among theropod taxa.
TABLE 1.3. Summary of previously reported ST (specific tension) values for hind limb muscles of extant animals.
TABLE 1.4. True M. caudofemoralis mass vs. estimated mass, based on digital models, in the extant reptiles.
TABLE 1.5. Summary of estimated biomechanical data for theM. caudofemoralis of the theropods
Chapter 2
TABLE 2.1. Mass estimation results from the conservative and robust models of Camotaurus
TABLE 2.2. Estimated conservative caudal muscle masses of Camotaurus and other theropods
Chapter 3
TABLE 3.1. Estimated caudal muscle masses of oviratorosaurs and other non- avian coelurosaurs
Chapter 4
TABLE 4.1. Results of caudal muscle mass reconstructions for Velociraptor and Rhamphorhynchus
TABLE 4.2. Mid-caudal cross-section measurements of YMP 5202 (Deinonychus antirrhopus
Chapter 5
TABLE 5.1. Compilation of caudal muscle mass estimations for 5 extant reptiles and 14 non-avian theropods Appendix A
TABLE A.I. Measurements of LACM 127704
TABLE A.2. Comparison of mass estimations from the test of muscle mass variation
Appendix B
TABLE B.l. Alternative caudal muscle mass estimations for Ceratosaurus LIST OF FIGURES
Chapter 1
FIGURE 1.1. Tyrannosaurus and Alligator dorsal silhouette
FIGURE 1.2. Sequential cross-sections through the tail of Tupinambis merianae.
FIGURE 1.3. Lateral view of the dissected tail of Tupinambis
FIGURE 1.4. The anterior end of the M. caudofemoralis, its insertion onto the fourth trochanter of the femur, and the auxiliary tendon
FIGURE 1.5. Lateral view of the M. caudofemoralis termination point of Ornithomimus TMP 1995.11.001
FIGURE 1.6. Lateral view of caudal vertebra 10-17 of Ornithomimus TMP 1995.11.001
FIGURE 1.7. Lateral view of caudal vertebra 13-8 of Gorgosaurus TMP 91.36.500
FIGURE 1.8. Comparison of anterior caudal cross-section reconstructions for Allosaurus (modified from Madsen, 1976) and Caiman
FIGURE 1.9. Tyrannosaurus BHI3033 in dorsal view with M. caudofemoralis musculature reconstructed and in lateral view with full caudal musculature reconstructed
FIGURE 1.10. Modeling sequence for the tail of Tyrannosaurus BHI 3033
FIGURE 1.11. Reconstruction of the lateral margin of the M. caudofemoralis longissimus
FIGURE 1.12. Anterior view of caudal vertebra 1 of Ornithomimus NMNH 2164
FIGURE 1.13. A fully rendered reconstruction of BHI 3033 created by Scott Hartman
Chapter 2
FIGURE 2.1. Typical anterior caudal morphologyCamotaurus of sastrei (MACN-CH 894)
FIGURE 2.2. Select caudal vertebra of Camotaurus sastrei (MACN-CH 894) FIGURE 2.3. Digital model of the tail of Camotaurus sastrei
FIGURE 2.4. Caudal vertebra 4 of Aucasaurus (MCF-PVPH-236)
FIGURE 2.5. Caudal vertebra 1-4 of Aucasaurus (MCF-PVPH-236)
FIGURE 2.6. Cross-section through the tail of Camotaurus sastrei
FIGURE 2.7. The conservatively modeled tail of Camotaurus sastrei (MACN- CH 894)
FIGURE 2.8. The robustly modeled tail of Camotaurus sastrei (MACN-CH 894)
FIGURE 2.9. Hypothesized phylogeny and chronostratigraphy of South American Abelisauridae
FIGURE 2.10. Life restoration of a sprinting Camotaurus sastrei
Chapter 3
FIGURE 3.1. Photograph of the type specimen Khaanof mckennai (MPC 100/1127)
FIGURE 3.2. First caudal vertebra and chevron of the type specimen ofNomingia gobiensis (MPC 100/119) in posterior view, with one half of caudal musculature illustrated
Figure 3.3. Digital models of the caudal osteology and musculature ofKhaan (MPC 100/1127), “ Ingenia” yanshini (MPC 100/30), and Nomingia (MPC 100/119)
FIGURE 3.4. Comparison of the caudal and pelvic skeletons of the primitive deinonychosaurAnchiomis, the primitive bird Archaeopteryx, the pygostyle-bearing birdConfuciusomis, and the oviraptorosaur Khaan
Chapter 4
FIGURE 4.1. Comparison between the mid-caudal osteology of Rhamphorhynchus and Deinonychus
FIGURE 4.2. TMP 2008.041.0001 ( Rhamphorhynchus muensteri) FIGURE 4.3. Dromaeosaurid specimens used in assessing caudal flexibility
FIGURE 4.4. Stages in modeling the tail of Rhamphorhynchus muensteri (TMP 2008.041.0001)
FIGURE 4.5. Stages in modeling the tail of Velociraptor mongoliensis (MPC 100/986)
FIGURE. 4.6. Restored mid-tail cross-section of Deinonychus
FIGURE 4.7. Comparison between the mid-caudal osteology of the early pterosaur Eudimorphodon ranzii, the troodontid Mei long, and the early bird Archaeopteryx lithographica
Chapter 5
FIGURE 5.1.
FIGURE 5.2. Stages in modeling the tail of Coelophysis bauri (AMNH 7229)
FIGURE 5.3. Stages in modeling the tail of Dilophosaurus wetherilli (UCMP 37302)
FIGURE 5.4. Stages in modeling the tail of Limusaurus inextricabilis (IVPP VI5923)
FIGURE 5.5 Stages in modeling the tail of Ceratosaurus nasicomis (USNM 4735)
FIGURE 5.6. Stages in modeling the tail of Camotaurus sastrei (MACN-CH 894)
FIGURE 5.7. Stages in modeling the tail of Allosaurus fragilis (CM 11844 scaled to the size of USNM 4734)
FIGURE 5.8. Stages in modeling the tail of Ornithomimus edmontonicus (TMP4511001)
FIGURE 5.9. Stages in modeling the tail of Gorgosaurus libratus (TMP 1991.36.500)
FIGURE 5.10. Stages in modeling the tail of Tyrannosaurus rex (BHI 3033)
FIGURE 5.11. Stages in modeling the tail of Omitholestes hermanni (AMNH 619)
FIGURE 5.12. Stages in modeling the tail of “Ingenia ” yanshini (MPC 100/30) FIGURE 5.12. Stages in modeling the tail of Nomingia gobiensis (MPC 100/119)
FIGURE 5.14. Stages in modeling the tail of Sinomithoides youngi (IVPP V9612)
FIGURE 5.14. Stages in modeling the tail of Velociraptor mongoliensis (MPC100/986)
Appendix A
FIGURE A.I. Long tail model of Camotaurus
FIGURE A.2. Short tail model of Camotaurus
AppendixB
FIGURE B.l. Alternative 1 model of the tail of Ceratosaurus
FIGURE B.2. Alternative 2 model of the tail of Ceratosaurus INSTITUTIONAL ABBREVIATIONS
AMNH - American Museum of Natural History, New York, New York, USA
BHI - Black Hills Institute of Geological Research, Hill City, South Dakota, USA
FMNH - Field Museum of Natural History, Chicago, Illinois, USA
LACM — Natural History Museum of Los Angeles County, Los Angeles, California, USA
MACN-CH — Museo Argentino de Ciencias Naturales “B. Rivadavia,” Coleccion Chubut, Argentina
MCF-PVPH — Museo Municipal “Carmen Funes”, Paleontologia de Vertebrados, Plaza Huincul, Argentina
MPC — Paleontological Center of the Mongolian Academy of Sciences, Ulaan Baatar, Mongolia
NMNH - Smithsonian Institution National Museum of Natural History, Washington, District of Colombia, USA
TCM -- The Children’s Museum of Indianapolis
TMP — Royal Tyrrell Museum of Palaeontology, Drumheller, Alberta, Canada
UCMP - University of California Museum of Paleontology, California
YPM - Yale Peabody Museum of Natural History, New Haven, Connecticut, USA Introduction
Historically, the study of theropod dinosaurs has progressed posteriorly.
From William Buckland’s original description of the dentary ofMegalosaurus
(Buckland, 1824) onward, the teeth, jaws, and skulls of theropod dinosaurs have been the objects of great scientific fascination and the subjects of much research.
Theropod work has remained definitively front-end heavy, with cranial characters dominating current cladistic analyses and new papers focusing on ever more specific aspects of theropod dentition, jaw mechanics, and cerebral aptitudes emerging at an unrelenting rate. However, segmentally, some attention has shifted from the captivating faces of theropods towards the rear. Theropod necks, forelimbs, dorsal ribs, hips, and hindlimbs are all now established and growing areas of study. The groundbreaking works that initiated each of these posterior shifts in academic focus (such as Romer’s 1923 paper on theropod pelvic musculature) critically broadened the understanding of theropods and swept a wealth of new insight onto theropod physiology, ecology, and evolution. It is the aim of this thesis to take the posterior progression of theropod research to its inevitable extreme.
For reasons discussed in Chapter 1, theropod tails have been examined in few previous studies. A cursory review of modem animals reveals that tails have the potential to evolve into a variety of forms and to serve a wide range of functions, with specific tail adaptations commonly converging when two animals fill similar niches. Nevertheless, as the frequent museum practice of using a copy
1 of the tail of one theropod (even an only distantly related one) to complete the skeleton of another shows, it has been the pervading, if perhaps not fully conscious, assumption of the paleontological community that non-avian theropod tails seldom become specialized for specific functions and had a largely uneventful evolutionary history.
The previous lack of study into theropod tails is especially unfortunate, because a recent flurry of biomechanical research using novel and technologically advanced techniques has endeavored to stretch to the limits what can be learned about theropod locomotion. Without a fundamental understanding of theropod caudal anatomy, many of these attempts have been premature. Tail anatomy has direct bearing on questions of locomotion, because the hindlimb muscle complex of most non-avian theropods was directly bonded to the tail by the caudofemoral musculature.
That most non-avian theropod locomotion was dominated by the caudofemoral muscles (as well as the caudofemoral dominated muscle arrangement of modem crocodilians) was previously established by Gatesy (1990,
1997). It should be emphasized at the onset that, although several of the major conclusions reached by Gatesy (1990) and subsequent publications are here challenged, much of this thesis would not have been possible without the significant knowledge base laid down by Gatsey and colleagues.
Beyond the mere size of the caudofemoral muscles, tails are important to understand because they fundamentally distinguish non-avian theropods from all potential modem locomotive analogues. Birds and large land mammals (the
2 usually preferred analogs) lack long muscular tails. Although lizards and crocodilians have tails with similar proportions to non-avian theropods, most modem reptiles are limited to quadrupedal locomotion and all are limited to a sprawling or semi-sprawling gate and have a primitive pelvic construction.
Theropod tails, therefore, impart a unique anatomy and hinder the ability to make simple comparison with living animals. However, the implications of this anatomical novelty ought to be explored rather than ignored.
As it turns out, the proportions of the caudal musculature are, relative to most other muscles, easy to accurately assess. The epaxial and hypaxial tail muscles are simple in overall shape and have consistent origin and insertion patterns. In the posterior region of the tail, the muscles are almost completely bound on one side by the caudal vertebrae, and in the anterior region of the tail the muscles are almost completely bound on two sides by the caudal vertebrae and the caudal ribs. Based on the anatomy observed and measured firsthand in a variety of dissected reptiles, techniques for digitally modeling each of the major caudal muscle sets overtop of a digital model of the caudal skeleton are here outlined, the accuracy of these techniques are verified on modem reptiles, and the techniques are then applied to fossil theropod specimens.
This thesis is a compilation of work from a three year master’s research project. Its five chapters consist of four previously published or (at the time of writing) currently submitted manuscripts on the particularly intriguing tails of arctometatarsalians, South American abelisaurids, oviraptorosaurs, and dromaeosaurs, plus a final chapter that provides an overview of theropod tail
3 evolution. The accuracy of the digital modeling techniques used throughout this thesis are entirely reliant on the quality of the original fossil specimens. For this reason, the scope of the thesis has been limited to taxa with complete or nearly complete and articulated caudal skeletons. Because the locomotive mechanics of non-avian theropods cannot be well understood without consideration of the caudofemoral muscles, special emphasis has been placed on the reconstructions of the M. caudofemoralis.
Bibliography
Buckland W. 1824. Notice on the Megalosaurus or great fossil lizard of
Stonesfield. Transactions of the Geological Society, second series 1: 390-
396.
Gatesy SM. 1990. Caudefemoral musculature and the evolution of Theropod
Locomotion. Paleobiology 16(2): 170-186.
Gatesy SM. 1997. An electromyographic analysis of hindlimb function in
Alligator during terrestrial locomotion. J Morph 234:197-212.
Romer AS. 1923. The pelvic musculature of saurisehian dinosaurs. Bulletin of the
American Museum of Natural History 48:605-617.
4 Chapter 1 The tail ofTyrannosaurus : reassessing the size and locomotive importance of theM. caudofemoralis in non-avian theropods*
1.1 Introduction
The associations between muscle mass, vertebrae morphology, and function have been well studied in the tails of extant mammals, particularly procyonids and primates, and tail biomechanics are better understood among mammals than any other group of terrestrial vertebrates (Dor, 1937; German,
1982; Lemelin, 1995; Organ et al., 2009). However, in terms of mass and volume,
most fully-terrestrial mammals have unimpressive tails. Large terrestrial
mammals, in particular, tend to have minimalist fly-swatter tails, and our own
species, with nothing but a vestigial stub, is at the furthest extreme. As a result,
when considering the relatively large tails of most non-avian dinosaurs, there has been a misleading tendency to regard tails as predominantly dead weight or, at best, as either defensive lashing weapons or (in bipedal taxa) as mere counterbalances for the crania. The tails of modem reptiles represent the best
modem analogs for the tails of most dinosaurs and demonstrate that large tails
may serve a variety of consequential functions, including femoral retraction
during the locomotive power stroke via the M. caudofemoralis.
* A version of this chapter has been published. Persons and Currie 2011. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 294: 119-131.
5 The M, caudofemoralis is a tail muscle that inserts directly onto the fourth-trochanter of the femur, and acts as a femoral retractor. Extant mammals lack the M. caudofemoralis; instead, the gluteal muscles fill the role of primary limb retractors. Some mammals do have a muscle that is commonly termed the
“M. caudofemoralisbut this muscle is not homologous to the M. caudofemoralis of saurians and birds (Appleton, 1928; Howell, 1938). In modem Aves, knee flexion is more important to locomotion than femoral retraction (Gatesy and
Biewener, 1991; Carrano, 1998; Farlow et al., 2000), and the M. caudofemoralis is greatly reduced in most birds and altogether absent in others (Gatesy, 1990). In crocodilians and the majority of non-serpente squamates, however, theM. caudofemoralis is both the primary and the single largest retractor muscle of the hindlimb (Snyder, 1962; Gatesy, 1990). Electromyographic studies of walking and running crocodiles have shown the M. caudofemoralis to be consistently active at all speeds, whenever femoral retraction occurs (Gatesy, 1997).
The presence of large caudofemoral muscles in non-avian dinosaurs was noted as early as 1833, when Louis Dollo inferred their existence from the large femoral fourth trochanter of the herbivorous dinosaur Iguanodon (Dollo, 1883). In
Gatesy’s 1990 study of theM. caudofemoralis and its reduction in the lineage leading to extant birds, he argued that the gradual shrinkage of the muscle resulted from a push towards overall tail weight reduction and from the tail’s functional shift from locomotion to dynamic stabilization, with both trends relating to the evolution of flight (Gatesy, 1990). Gatesy also argued insightfully that the M. caudofemoralis undoubtedly made the locomotion of most non-avian
6 dinosaurs (perhaps, particularly the bipedal taxa) fundamentally different from what can be observed in any modem mammalian or avian analogue (Gatesy,
1990).
Despite such arguments, the M. caudofemoralis has been undervalued in the majority of dinosaur biomechanical studies, and its contribution to locomotion has not been quantitatively analyzed. Moreover, theM. caudofemoralis has become a point of anatomical confusion, with different authors using different osteological correlates to infer its overall size and shape (Madsen, 1976;
Carpenter et al., 2005; Arbour, 2009; Schwarz-Wings et al., 2009). As a consequence of this confusion, the tails of non-avian dinosaurs are commonly reconstructed with improbable muscle morphology and overly conservative masses, which appear altogether emaciated when compared to the tails of modem reptiles (Fig. 1.1).
FIGURE 1.1. Tyrannosaurus dorsal silhouette (A) previously used in body-mass estimation (image modified from Paul, 1997), compared with a modem Alligator dorsal silhouette (B) (image modified from Cong, 1998). The basal bulge in the tail of the Alligator is primarily the result of a largeM. caudofemoralis.
1 Here, basic caudal musculature of modem reptiles is used for more accurately reconstructing the muscle anatomy of dinosaur tails. The locomotive implications of the reconstructions are considered both qualitatively and quantitatively for non-avian theropods (the primarily carnivorous group of dinosaurs that gave rise to birds and for which the majority of previous locomotive biomechanical research has been done).
1.2 Anatomy
The pelvic and post pelvic musculature of aBasiliscus vittatus (brown basilisk), Caiman crocodilus (spectacled caiman), Chamaeleo calyptratus (veiled chameleon), Iguana iguana (green iguana), and Tupinambis merianae
(Argentinean black and white tegu) were dissected. All specimens had been preserved via deep freezing and showed no signs of desiccation prior to dissection. Immediately followingin situ observations and measurements, individual muscles were removed from each specimen and their mass was measured (Table 1.1). Epaxial muscles that were continuous into the pre-pel vie region were severed in line with the midpoint of the acetabulum.
Three advanced non-avian theropods are considered in this study:
Gorgosaurus libratus (TMP 1991.36.500), Ornithomimus edmontonicus (TMP
1995.11.001), and Tyrannosaurus rex(cast of BHI 3033 currently on loan to the
Smithsonian National Museum of Natural History). The specimens were chosen based on the completeness of the caudal series. Osteological dimensions of the femora, pelvic girdle, and caudal series were taken, and these measurements were
8 later used in modeling digital skeletons. TMP 1991.36.500 is a juvenile. Because
both TMP 1991.36.500 and TMP 1995.11.001 are panel mounts, some
measurements (such as transverse centrum width) could not be made for every
vertebra in the series, and measurements had to be supplemented with those made
on other similarly sized specimens (including AMNH 514, AMNH 5355, TMP
1999.33.1, and NMNH 2164). Likewise, the mounted skeleton of BHI 3033 was
so large and difficult to reach that some measurements were supplemented with those made indirectly from photographs. Whenever possible, previously collected data on the original specimen of BHI 3033 were used to verify the accuracy of
these measurements. Measurements were also made on published illustrations of
other Tyrannosaurus specimens (Paul, 1996; Brochu, 2002) and were used to
supplement portions of the tail that were not preserved in BHI 3033.
9 TABLE 1.1. Caudal muscle mass of theropods and extant reptiles.
M. tendino-articularis M. longissimus M. ilio-ischiocaudalis M.caudo1emoraiis Caiman Crocodilus Mass (g) 1.4 9.6 9 13.8 Spectacled caiman Percent 4.1% 28.4% 26.6% 40.8% Tupinambis merianae Mass (g) 3.9 22.5 12.2 13.3 Black and white tegu Percent 7.5% 43.4% 23.5% 25.6% Iguana iguana Mass (g) 20.8 52.6 70 49.2 Green iguana Percent 18.8% 27.3% 36.3% 25.5% Basiliscus vittatus Mass (g) 0.6 2.4 3 3.4 Brown basilisk Percent 6.4% 25.5% 31.9% 36.2% Chamaeleo calyptratus Mass (g) 0.2 0.6 0.8 0.6 Veiled Chameleon Percent 9.1% 27.3% 36.4% 27.3% Ornithomimus edmontonicus Mass (g) 860 2440 5050 9890 TMP 95.11.001 Percent 4.7% 13.4% 27.7% 54.2% Gorgosaurus ilbratus Mass (g) 3900 6900 10300 17300 TMP 91.36.500 Percent 10.2% 18.0% 26.8% 45.1% Tyrannosaurus rex Mass (g) 65200 154200 159400 522200 BHI 3033 Percent 7.2% 17.1% 17.7% 58.0%
10 1.3 Computer Modeling
Using the modeling software Rhinoceros (McNeel Robert & Associates,
2007), the hips and caudal series of each of the three theropod specimens were digitally sculpted based on the skeletal measurements. Three-dimensional models of the various caudal muscles were then sculpted overtop of the digital skeleton, according to the osteological relations determined from the dissections of extant animals. The volume of each restored muscle was then calculated by the software.
Because muscle is known to have a fairly constant density of 1.06 g em' (Mendez and Keys, 1960), the muscle volume estimates could then be multiplied by this density value to obtain estimates of muscle mass.
To verify the accuracy of the restoration techniques used in sculpting the various theropod caudal muscles, digital skeletons were also made from
measurements taken on three of the dissected reptiles: the Argentinean black and
white tegu, green iguana, and spectacled caiman. Digital skeletons were not made
for the brown basilisk and the veiled chameleon, because these specimens were
too small to measure using the same methods and equipment. The same modeling
techniques were then used to reconstruct the musculature and to estimate muscle
volume and mass for the three extant reptiles, and these muscle mass estimates
were then compared to the true muscle masses as measured during the dissections.
11 1.4 Biomechanics
To evaluate the potential contribution of the M. caudofemoralis to femoral retraction, the digital muscle reconstructions of each theropod were used in combination with a series of standard biomechanical equations. First, M. caudofemoralis mass was calculated using a standard muscle density of 1.06
•j g em' (Mendez and Keys, 1960). Then, the physiological cross-sectional area
(PCSA) of the M caudofemoralis was calculated according to Equation 1 (Sacks and Roy, 1982; Snively and Russell, 2007), wherem is the total mass (the mass of one M. caudofemoralis, not the mass of the total bilaterally symmetric muscle set); a is the pennation angel of the muscle fibers within the M. caudofemoralis and, based on measurements of the dissected specimens, is assumed to be approximately equal to 1.00 (0.95),d is muscle density (again, assumed to be 1.06 g em'3), I is the average fascicle length within the M. caudofemoralis and was calculated for each taxon based on the digital model and close examination of the fascicles in the spectacled caiman specimen:
Equation 1: PCSA = m • cos <7+ d ■ I
Because calculating physiological cross-sectional area requires several assumptions, many authors favor the simpler method of measuring anatomical cross-sectional area (ACSA), which is simply the cross-sectional area through the muscle at its greatest width (Snively and Russell, 2007). Anatomical cross- sectional areas were also measured from the digital models and compared to the
12 calculated physiological cross-sectional areas. In all three instances the two values varied only slightly from one another, as would be expected, given the assumeda value of approximately 1 (Bammanet al. 2000) (Table 1.2).
Specific tension (ST), also sometimes referred to as specific force (Brooks and Faulkner, 1994), is a ratio of the strength of a muscle to its area and has been shown to vary among different muscles and among different taxa. Known ST values for hind limb muscles likely offer the best basis for estimating the ST value appropriate for theM. caudofemoralis of non-avian theropods. An overview of previously reported ST values that might be good analogs for the specific tension of the M. caudofemoralis of non-avian theropods is provided in Table 1.3.
Estimates within the range of 25-35 N-cm' would seem reasonable. Here, ST is assumed to be 25 N cm'2 for all the theropod taxa (certainly a conservative estimate).
The total contractile force (F,) of the M. caudofemoralis was estimated by multiplying the calculatedPCSA by the assumedST (25 N cm'2):
Equation 2: Ft = PCSA ■ ST
While the calculated total contractile force of the M. caudofemoralis is
useful as a comparable factor between taxa, a more accurate measure of its true contribution to locomotion is its capacity to generate torque. As outlined in
Snively and Russell (2007), a muscle’s torque-generating capacity is proportional
to the force the muscle exerts in a direction orthogonal to its moment arm (the
13 moment arm being measured from the joint’s center of rotation to the muscle’s insertion). This orthogonal force is here termed the effective force (Fe). The Fe of the M. caudofemoralis is calculated with the following equation, where 6 is the angle between the vector of line of pull of the M. caudofemoralis and a vector orthogonal to the moment arm (for the M. caudofemoralis, the moment arm is the dorsal-ventral distance from the midpoint of the femoral head to the midpoint of the femoral fourth trochanter), calculated for a femur positioned perpendicular to the ground:
Equation 3: Fe = Ft cos0
Finally, the potential torque generation of theM. caudofemoralis is calculated with the equation:
Equation 4: xm = R F e sin<£
Here, & is the angle between the vectors of the moment arm and the effective force (this angle is assumed to be 90° and the sin<£ is, therefore, equal to
1), and R is the length of the moment arm (again assuming a femur positioned perpendicular to the ground).
14 TABLE 1.2. Cross-sectional area in the M. caudofemoralis amongst theropod taxa. Average Mass fascicle length PCSA ACSA PCSA/ACSA (9) (cm) (cmA2) (cmA2) variation Omithomimus edmontonicus (TMP 95.11.001) 4945 31.423 141.038 127.675 1.105 Gorgosaurus libratus (TMP 91.36.500) 8650 50.585 153.254 144.486 1.061 Tyrannosaurus rex (BHI 3033) 261100 129.697 1804.242 1794.442 1.005
TABLE 1.3. Summary of previously reported ST (specific tension) values forlind limb muscles of extant animals. Animal Muscle(s) ST (N*cmA2) Source Brown et al. Domestic cat Caudofemoralis 31.2 (1997) Storer et al. Human Thigh average 27.3-30.0 (2003) Marx et al. Quarter horse Gluteus medius 25.9 (2005) White Marx et al. rhinoceros Hamstring 34.4 (2005)
15 1.5 Caudal Musculature and Osteological Correlates of Extant Reptiles
The literature is filled with inconsistent and often redundant terminology schemes for the caudal muscles of reptiles. Following the recent scheme established by Arbour (2009), I will acknowledge four major paired muscle sets: the M. spinalis, M. longissimus, M. ilio-ischiocaudalis, and M. caudofemoralis. It should be noted that these four muscles form a good general, but overly simplistic, scheme, and subdivisions are clearly visible within many of these muscles, particularly in the posterior portions of theM. longissimus and M. ilio- ischiocaudalis. Like those of the limb, caudal muscles vary widely in size and relative proportions across reptilian taxa; however, the overall pattern of muscle insertions and positions remains relatively uniform (Fig 1.2 and 1.3). The results presented here are based on the dissections of representatives of five taxa (one
specimen each) and, combined with the previous literature, are intended to offer only a cursory overview of reptilian tail musculature.
Based on the dissections, the arrangement and osteological insertion sites of the caudal muscles are as follows:
M. spinalis—The M. spinalis is the most dorsal of the caudal muscles and is
present along the full length of the tail. The M. spinalis inserts onto the dorsal tips
and the full lateral surfaces of the neural spines.
16 A . Neural spine JM- spinalis
Transverse proces Caudal rib r i i M. longissimus Centrum ^ —IM. caudofemoralis
M. ilio-ischiocaudalis Hemal spine' r y i
M. spinalis
M. spinalis M. longissimus M. longissimus
M.caudofemoralis M. ilio-ischiocaudalis
M. ilio-ischiocaudalis
17 FIGURE 1.2. Sequential cross-sections through the tail of Tupinambis merianae. Tupinambis merianae was chosen to illustrate the anterior/posterior changes in muscle arrangement and morphology, because its tail is relatively unspecialized and its musculature is unremarkable in most respects. The cross-sections are anatomical abstractions, as they depict neural arches and hemal arches in the same vertical plane (these illustrations are similar in this way to those of Schwarz-Wings et al., 2009; Arbour, 2009; and Cong et al. 1998,), but these views are preferable to ones that would omit either hemal or neural arches. A) Caudal vertebra 7; the M. caudofemoralis inserts across the lateral sides of the centrum and across the entire lateral face of the hemal arch. The M. ilio- ischiocaudalis is thin medially, but inserts across the entire ventral surface of the caudal ribs, and only inserts onto the ventral tip of the hemal arch. B) Caudal vertebra 13; the M. caudofemoralis has begun to taper and the M. ilio-ischiocaudalis inserts across a ventral portion of the lateral face of the hemal arch. C) Caudal vertebra 18; the M. caudofemoralis is no longer present. TheM. ilio- ischiocaudalis insets across the entire lateral face of the hemal arch and the lateral sides of the centrum. The caudal ribs are absent. (Note, the posterior portion the tail is also a fat storage location inTupinambis merianae; however, for simplicity, fat deposits have not been shown.)
18 FIGURE 1.3. Lateral view (anterior left, posterior right) of the dissected tail of Tupinambis, with all muscles, except theM. caudofemoralis, removed. Highlighted regions correspond with cross-sections in Figure 1.2.
19 M. longissimus—Composing the primary bulk of the epaxial tail musculature, the
M. longissimus is also present along the full length of the tail and may be difficult to distinguish from the M. spinalis. This distinction becomes more difficult posteriorly, when subdivisions in the two muscles become increasingly independent. The M. longissimus has two strong dorsoventrally stacked subdivisions that are distinguishable in even the most anterior of cross sections.
These two subdivisions are often regarded as separate muscles, with the more ventral subdivision retaining the name M. longissimus, and the more dorsal subdivision occasionally referred to as the M. tendinoarticularis (although this term has also been applied to the M. spinalis). There is no clear osteological indicator of the level at which these two M. longissimus subdivisions meet, and the functional differences between the two are currently unknown. Attempts herein to subdivide the M. longissimus of theropods would, therefore, be both highly speculative and ultimately uninformative.
Anteriorly, theM. longissimus inserts onto the full dorsal surfaces of the caudal ribs and to the lateral faces of the neural arches. Posteriorly, after the caudal ribs have terminated, the lateral faces of the neural arches are the only osteological insertion points of the M. longissimus. (Note: The prominent lateral projections of the caudal vertebrae are here referred to as “caudal ribs,” in preference to the term “transverse processes”. Conclusive osteological evidence supporting one terminology scheme over the other is currently lacking among theropods. Although the latter term has become conventional within much of the paleontological literature, the accuracy of the former term has been established in
20 developmental studies on modem sauropsids, including crocodilians (Higgine,
1923; Emelianov, 1937; Romer, 1956; Rieppel 1993).) Throughout its anterior/posterior length, theM. longissimus is separated dorsally from theM. spinalis by a septum that stems from the lateral edges of the pre-zygapophyses and extends lateral at an often strongly dorsally-inclined angle. Both theM. longissimus and M. spinalis are continues into the dorsal region (Organ, 2006).
M. ilio-ischiocaudalis —Consistent with its nomenclature, the M. ilio- ischiocaudalis is composed of two major subdivisions: the m. iliocaudalis and the m. ischiocaudalis, with the former originating from the ilium and the later from the ischium. The M. ilio-ischiocaudalis is relatively thin anteriorly, where it attaches dorsally to the lateral tips and ventral surfaces of the caudal ribs, wraps around the M. caudofemoralis, and attaches ventrally both to the ventral tips of the hemal spines and to the other bilaterally-symmetric half of theM. ilio- ischiocaudalis that wraps around from the other side. Posteriorly, theM. ilio- ischiocaudalis increases in relative thickness as the thickness of the M. caudofemoralis diminishes. After the disappearance of theM. caudofemoralis, the
M. ilio-ischiocaudalis inserts onto the full lateral surface of the centrum and the chevrons.
M. caudofemoralis —Unique among the caudal muscles, the M. caudofemoralis is not partitioned by conical myosepta, and its overall form more closely resembles a limb muscle rather than an axial muscle. The primary caudofemoral tendon
21 attaches the M. caudofemoralis to the fourth trochanter of the femur, and the auxiliary caudofemoral tendon (present in most extant reptiles but absent in birds) also anchors the M. caudofemoralis to the knee joint (Fig. 1.4).
The M. caudofemoralis is composed of the m. caudofemoralis brevis, which fills the brevis fossa and may also insert across the anteriormost caudal vertebra, and the m. caudofemoralis longus. Throughout its anterior/posterior length, the m. caudofemoralis longus inserts medially onto the lateral faces of the caudal vertebrae. However, the insertion of the m. caudofemoralis longus across the lateral faces of the hemal spines varies across the caudal series (Fig. 1.4). The
M. caudofemoralis does not extend down the entire length of the tail (in none of the dissected reptiles did the M. caudofemoralis extend across even half of the tail’s total length). Rather, the M. caudofemoralis extends posteriorly down the caudal series with a gradual reduction in overall size, then reaches a point where it begins to rapidly taper, and, shortly thereafter, terminates (Fig. 1.3).
Prior to the taper point, theM. caudofemoralis' medial insertion extends ventrally across the entire lateral face of the hemal arches. As it tapers, theM. caudofemoralis' medial insertion shrinks dorsally; correspondingly, the ventral insertion of the M. ilio-ischiocaudalis expands dorsally, and theM. ilio- ischiocaudalis begins to insert across an increasing proportion of the lateral faces of the hemal arches. Past the termination point of the M. caudofemoralis, the M. ilio-
22 FIGURE 1.4. The anterior end of the M. caudofemoralis, its insertion onto the fourth trochanter of the femur, and the auxiliary tendon that inserts at the knee joint, seen in (A) Caiman (oblique dorsolateral view, anterior top, posterior bottom) and (B) Tupinambis (oblique posterolateral view, anterior upper right, posterior bottom left).
23 ischiocaudalis inserts across the entire lateral faces of both the chevrons and the centra. As they are no longer needed to provide dorsal insertion points for the M. ilio-ischiocaudalis, the caudal ribs are usually no longer present after theM. caudofemoralis termination. However, because the caudal ribs also serve as lateral insertion points for theM. longissimus, they may (as is the case in the
Argentinean black and white tegu) remain present posterior to the M. caudofemoralis has terminated.
1.6 Evidence for the Posterior Taper Point and Ventral Boundary of theM. caudofemoralis in Non-avian Theropods
Caudal centra 14 is the last caudal rib-bearing vertebra of Omithomimus
TMP 1995.11.001 (Fig. 1.5). The caudal ribs are located at roughly the centrum’s dorsoventral midpoint. Chevron 13 (positioned between caudal vertebra 13 and
14) is displaced slightly, with its posterior end tilted dorsally. A groove or scar is apparent running across its lateral face.
The scar seen on chevron 13 is part of a continuous diagonal sequence of scars that runs anteroventral to posterodorsal across chevrons 10-14 parallel to the axis of the tail (Fig. 1.6). This scar sequence coincides with the rapid decent of the caudal ribs from an elevated height above the centra (a full 19.8 mm above at caudal vertebra 1) to the mid-centrum elevation seen on caudal vertebra 14.
24 FIGURE 1.5. Lateral view (anterior right, posterior left) of the M. caudofemoralis termination point ofOrnithomimus TMP 1995.11.001. Caudal vertebra 14 bears the last caudal ribs, which sit at roughly mid dorsal/ventral height. Hemal arch 13 (between caudal vertebra 13 and 14) is displaced slightly, with its posterior end tilted dorsally. Hemal arch 13 has a strong grove or scar across its lateral face. Photo by V. Arbour and used with permission.
25 FIGURE 1.6. Lateral view (anterior right, posterior left) of caudal vertebra 10-17 of Ornithomimus TMP 1995.11.001. Arrows point to the anterior edges of theM. ilio-ischiocaudalis/M. caudofemoralis septum scarring, visible on hemal arches 11-14 and the posterior end of hemal arch 10. Photo by V. Arbour and used with permission.
26 Together, the descending caudal ribs and chevron scarring are here interpreted as demarcating the boundaries of the tapering M. caudofemoralis. Under this interpretation, the chevron scar is regarded as the insertion point for the skeletogenous septum that divided the M. caudofemoralis from the M. ilio- ischiocaudalis, and the anteroposterior ascent and eventual posterior disappearance of this scar is, therefore, taken to mark the M. ilio-ischiocaudalis’ gradual dorsal intrusion and eventual usurpation of the M. caudofemoralis.
The M. ilio-ischiocaudalis/M. caudofemoralis septum scarring disappears anteriorly, reaching the ventral tip of hemal arch 10. The scar does not reappear on any of the more anterior hemal arches, and this is interpreted as evidence that, prior to the taper point, theM. caudofemoralis inserted across the entire lateral surfaces of the hemal arches. This is in contradiction to some restorations that have shown the M. caudofemoralis of dinosaurs riding high on the caudal series
(see Arbour, 2009, for one example), but is entirely consistent with the structer seen in all of the dissected reptiles.
TMP 1995.11.001 displays theMilio-ischiocaudalis/M. caudofemoralis septum scar sequence more clearly than any of the other fossil specimens examined in this study; however, the scar sequence is by no means a feature unique to TMP 1995.11.001 or to Omithomimus. The scars of TMP 1991.36.500
(Gorgosaurus), which, although faint, are unambiguously present (Fig. 1.7). The
M. ilio-ischiocaudalis/M. caudofemoralis septum scars have not gone unnoticed by previous authors. For instance, although no explanation for the structure is
27 offered, Brochu (2002) notes it existence in his thorough description of the
Tyrannosaurus specimen FMNH PR2081.
28 FIGURE 1.7. Lateral view (anterior right, posterior left) of caudal vertebra 8-13 of Gorgosaurus TMP 91.36.500. The last caudal ribs are present on caudal vertebra 12. Although fainter than TMP 1995.11.001, the M. ilio-ischiocaudalis!M. caudofemoralis septum scarring is visible on hemal arches 11-7. Arrows point to the anterior edges of the scarring. 1.7 Evidence for the Lateral Extent ofM. the caudofemoralis in Non-avian
Theropods
In order to model the M. caudofemoralis of theropods, the muscle’s extent must be defined in all dimensions. The femoral fourth trochanter is the muscle’s anteriormost insertion point. The caudal ribs cap its dorsalmost limit, and the ventralmost margins of the chevrons indicate its ventral extent. Both the M. ilio-
ischiocaudalis/M. caudofemoralis septum scars and the rapid descent of the caudal ribs mark its posterior taper point. What remains is determining the lateral extent of theM. caudofemoralis.
Traditionally, the lateral width of the caudal ribs has been used as a correlate for the girth of the M. caudofemoralis in all saurians. However, this method is without sound anatomical basis. As described here, and contrary to the depictions and descriptions of Caldwell (2006), Arbour (2009), Schwarz-Wings et al. (2009), and various others, the M. caudofemoralis does not attach to the lateral tips or ventral surfaces of the caudal ribs. Rather, both are insertion points of the
M. ilio-ischiocaudalis (the near vertical caudal ribs of some advanced abelisaurids are a possible exception).
When viewed casually in most reptile dissections the caudal ribs are easily
mistaken for an M. caudofemoralis insertion point, because the portion of theM.
ilio-ischiocaudalis that attaches to the caudal ribs are usually quite thin. Adding to
this confusion is the high profile and commonly cited 1923 reconstruction by
Alfred Romer of the hip and hindlimb musculature of Tyrannosaurus, in which
the M. caudofemoralis is clearly, but incorrectly, shown attaching to the lateral
30 tips of caudal ribs (Romer, 1923). Romer does comment in the same manuscript that there is a lack of good tail muscle data available for crocodiles — the analogue on which he most heavily relied — and, four years later, he did correct himself when reconstructing the hip and hindlimb musculature of omithischian dinosaurs (Romer, 1927). Nonetheless, his Tyrannosaurus reconstruction remains the one to which most researchers have paid attention.
The caudal ribs also do not appear to be good indirect indicators of the M. caudofemoralis’ lateral extent. The spectacled caiman, for example, had the relatively largestM. caudofemoralis of any of this study’s extant reptiles, but the lateral widths of its caudal ribs, relative to other aspects of its caudal vertebrae, were only average. In contrast, the dissected Argentinean black and white tegu specimen had among the relatively smallest caudofemoral muscles, but the relatively widest caudal ribs. The dissections also revealed that the width of the
M. caudofemoralis varies relative to the length of the caudal ribs across the caudal series of the same individual, with the caudofemoral muscles extending well beyond the lateral tips of the caudal ribs at the anterior base of the tail, and usually extending well short of the tips at and near the taper point.
Recognizing that the caudal ribs do not bear a M. caudofemoralis insertion and that they are not good indicators of its lateral width is important, because this has dramatic implications for the overall shape of the hypaxial region of the tail.
Figure 1.8A. shows a restored cross-section through the anterior tail base of
Allosaurus from Madsen (1976). Madsen’s reconstruction follows the traditional restoration method, and assumed a M. caudofemoralis that inserted onto the
31 ventral surfaces of the caudal ribs and that did not bulge past their ventral-most tips. As a result, the tail is widest dorsal to its midpoint, at or just below the level of the caudal ribs, producing an inverted tear-drop shaped cross-section. For comparison, the widest portion of the tail of a modem caiman is at roughly mid- hypaxial height (Fig. 1.8B).
FIGURE 1.8. Comparison of anterior caudal cross-section reconstructions for (A) Allosaurus (modified from Madsen, 1976), with greatest width assumed to be roughly equal to the lateral extent of the caudal ribs, and (B)Caiman, reconstructed based on dissection and showing greatest lateral extent to be at roughly mid hypaxial height.
1.8 Muscle Reconstruction
In creating the reconstructions for this study (Fig. 1.9-1.11), the vertical cross-section of the M. caudofemoralis was treated as elliptical in overall shape — consistent with the M. caudofemoralis in all the dissected specimens — and was
32 M. caudofemoralis brevis M. caudofemoralis longus
M.caudofemoralis brevis M. caudofemoralis longus ... I 3 longissimus M. spinalis
M. ilio-ischiocaudalis
FIGURE 1.9. Tyrannosaurus BHI 3033 in dorsal view with M. caudofemoralis musculature reconstructed and in lateral view with full caudal musculature reconstructed. Skeletal image modified from Paul (1989) and used with permission.
33 FIGURE 1.10. Modeling sequence for the tail of Tyrannosaurus BHI3033. A. Skeleton model constructed based of dimensional measurements. B. Model with M. caudofemoralis longissimus sculpted overtop of the skeleton model. C. Full muscle restoration with M. spinalis, M. longissimus, and M. ilio-ischiocaudalis visible.
34 modeled across the caudal series (Fig. 1.11) by tracing an arc from below the medioventral base of the caudal ribs to the ventral tip of the hemal arch.
FIGURE 1.11. Prior to the anterior tapering of the M. caudofemoralis longissimus, its lateral margin was reconstructed at each vertebra, as shown, by tracing a symmetric arch from below the medioventral base of the caudal ribs to the ventral tip of the nearest hemal arch.
Comparisons, based on the dissected reptile specimens, between mass predictions for the M. caudofemoralis derived from digital reconstruction models and the M. caudofemoralis masses actually measured, confirm the accuracy of this restoration technique (see Table 1.4). All predicted M. caudofemoralis masses are within 6% of the true mass and slightly lower than the true value. This is probably because, at the anterior-most base of the tail, the M. caudofemoralis has a more extensive lateral bulge that diverges from the overall shape seen more posteriorly. The mass estimates presented here are, therefore, conservative.
The measured tail muscle masses of the dissected extant reptiles and the estimated tail muscle masses of the three theropods are presented with the
35 percentages of total tail muscle mass (Table 1.1). These percentages offer one
way to quantify the relative size of the different tail muscles across the various
taxa.
TABLE 1.4. True M. caudofemoralis mass vs. estimated mass, based on digital models, in the extant reptiles.______True mass (g) Modeled mass (g) Accuracy Caiman crocodllus 13.8 12.997 -5.8% Tupinambls merianae 13.3 12.692 -4.6% Iguana Iguana 49.2 48.194 -2.0%
Among the extant taxa, the spectacled caiman (the only crocodilian considered in this study) had the highest percentage of its tail muscle mass contributed by the M. caudofemoralis. The brown basilisk had the second highest caudofemoral percentage. Given the caiman’s closer phylogenetic relation and the basilisk’s bipedal running style, the large M. caudofemoralis found in both of
these taxa could be taken as indirect support for a largeM. caudofemoralis in bipedal non-avian theropods.
Among the three extinct taxa,Tyrannosaurus had the largest relative (and absolute) M. caudofemoralis. However, all three theropods were estimated to have substantially larger caudofemoral muscles than any of the modem reptiles.
Given that the M. caudofemoralis is the primary retractile muscle of the hind limb, and given the numerous advanced locomotive adaptations present in non- avian theropods, this high relative investment in caudofemoral mass should, perhaps, not be surprising. But the osteological features associated with this caudofemoral bulk-up do merit special note. Two such features are readily
36 identifiable from this study: the strong dorsally inclined angle of the caudal ribs
and the elevation of the caudal ribs on the neural arch (Fig. 1.12).
The caudal ribs of all the dissected extant reptiles protrude at flat, fully
horizontal angles. Anterior vertebrae with dorsally angled caudal ribs are present
in many theropod taxa, and the angled caudal ribs would have provided an
expanded hypaxial region that M.the caudofemoralis could have filled. However,
angled caudal ribs are not characteristic of all theropod taxa (they are absent in
both Tyannosaurus and Gorgosaurus), and, when present, usually only occur on
the first three or four caudal vertebra.
More important, then, would seem to be the elevation of the caudal ribs on
the neural arch, above the centrum. This too creates a greatly expanded hypaxial region (at the expense of the epaxial region), and theM. caudofemoralis is the
only muscle that is likely to have filled this space. Dorsally-elevated caudal ribs
are found in even primitive theropods, including Coelophysis and Herrerasaurus.
This suggests that a large M. caudofemoralis is a basal characteristic of the group
and appears to have remained present in nearly all non-avian theropod lineages
(the character appears to be absent in the highly derived and specialized tails of
Paraves). Elevated caudal ribs are not only present on the anteriormost tail
vertebra of most non-avian theropods, but remain elevated down the series, until rapidly descending at the taper point.
37 5 cm
FIGURE 1.12. Anterior view of caudal vertebra 1 of Omithomimus NMNH 2164. Note the dorsally-angled caudal ribs, and the dorsal elevation of the caudal ribs above the centrum, which create an expanded hypaxial region.
38 1.9 Biomechanics
Interpreting the results of the biomechanical calculations performed for each of the three theropods (Table 1.5) is hindered by the lack of analogous data
available for modem animals with muscles of equivalent size. The data can most confidently be used to compare different theropod taxa, but it should be noted that
the high torque estimates calculated for all three theropod taxa are consistent with
what would generally be predicted for muscles of their size based on what is
known about the physiology of smaller modem taxa.
1.10 Discussion
Among the three theropods examined here, an intriguing comparison can
be made between the estimated M. caudofemoralis masses of Tyrannosaurus BHI
3033 and the juvenile Gorgosaurus TMP 1991.36.500. As tyrannosaurids, the taxa are closely related, and one might be surprised by the substantially larger tail
mass percentage that the M. caudofemoralis of Tyrannosaurus is predicted to comprise (58.0%) compared with that ofGorgosaurus (45.1%). However, this discrepancy in relativeM. caudofemoralis mass makes sense when considering
the absolute body mass discrepancy between the two tyrannosaurids.
Based on mass estimates of other Gorgosaurus specimens (Paul, 1988),
the body mass of TMP 1991.36.500 can be estimated as roughly 400 kg, and the
mass of BHI 3033 has been estimated as in the range of 3,800-4,500 kg (Stevens
et. al, 2008; but see Bates et al., 2009 for an alternative interpretation). The need
for relatively larger locomotive muscles in absolutely larger taxa has been well
39 .5. Summary of estimated biomec tanical data for theM. caudofemoralis of the theropods. Ornithomimus Gorgosaurus libratus Tyrannosaurus rex (TMP 95.11.001) (TMP 91.36.500) (BHI 3033) Mass (g) 4945 8650 261100 PCSA (cmA2) 141.038 153.254 1804.242 Total Contractile Force (N) 2820.762 3065.082 36084.831 Effective Muscle Pull (N) 2820.480 3064.775 36081.223 Moment Arm (m) 0.081 0.147 0.505 Torque (Nm) 228.459 449.603 18208.028
40 established (Biewener, 1989; and Roberts, 1998). A muscle’s strength is largely a
factor of its cross-sectional area, and locomotive muscles must be strong relative
to the mass of the body they are trying to accelerate. Simple isometric growth of
any animal would result in a three-fold increase in body mass (as mass is largely a function of volume) and only a two-fold increase in the strength of its muscles.
Hence the general rule that larger animals require relatively larger muscles to achieve the same speeds as smaller animals.
That is not to suggest this relatively enlargedM. caudofemoralis estimation indicates that Tyrannosaurus could have achieved the same degree of cursoriality as a juvenileGorgosaurus or other smaller tyrannosaurids. Indeed, the relatively shorter metatarsals ofTyrannosaurus (among other anatomical features) testify that it could not (Holtz, 1995). Nonetheless, it seems likely that the high relative M. caudofemoralis mass of Tyrannosaurus did evolve as partial compensation for its colossal body size, and it is worth noting how this increased
M. caudofemoralis mass was achieved. The higher M. caudofemoralis mass estimation for Tyrannosaurus is not the result of relatively more dorsally angled or elevated caudal ribs, but of more ventrally elongated hemal arches, which means that the hypaxial musculature was increased without decreasing the size of the epaxial musculature.
The expanded masses and high contractile force and torque estimates for all three theropods confirm previous assertions that theM. caudofemoralis was indeed a muscle of fundamental importance to non-avian theropod locomotion.
These results have implications for the ongoing discussion of the potential
41 locomotive abilities of non-avian theropods. For instance, in their assessment of the cursoriality ofTyrannosaurus, Hutchinson and Garcia (2002) assumed a total femoral retractor muscle mass of 297 kg for each leg of a 6,000 kg
Tyrannosaurus. Here, the mass of the M. caudofemoralis alone has been conservatively estimated as 261 kg for each femur of a Tyrannosaurus that was estimated to have weighed as little as 4,500 kg, which implies that the M. caudofemoralis should have a mass of 348 kg in a 6,000 kg individual.
Hutchinson and Garcia (2002) did not provide mass estimates for individual limb muscles, making it difficult to assess how this new M. caudofemoralis data affects their total estimation. However, it can surely be assumed that the mass of the other femoral retractors (the M. adductor femoris, M. puboischiofemoralis externus, and M. ischiotrochantericus) in a 6,000 kg Tyrannosaurus would weigh at least 25 kg. Under this assumption, the 297 kg estimation appears to be off by over 25% (and is conceivably off by as much as 45%). This by no means accounts for the 80% of total body mass that Hutchinson and Garcia (2002) assert must have been invested in the limb retractors, in order for Tyrannosaurus to have been capable of rapid locomotion. Nonetheless, the new M. caudofemoralis data does
suggest that Tyrannosaurus should have fallen towards the higher end of
Hutchinson and Garcia’s (2002) advocated speed range, and the data are consistent with the faster locomotive estimates advocated by other authors using different speed estimating techniques (Bakker, 1986; Paul, 2000; Sellers and Paul,
2005).
42 Considering these results in the context of such biomechanical studies points out the large gaps in our current understanding of how tail muscularity is involved in terrestrial locomotion. The M. caudofemoralis has been treated herein as the only tail muscle involved in femoral retraction, but this is likely a gross oversimplification, and the case can be made for the partial involvement of other caudal muscles in femoral retraction as well. Studies of walking and running alligators demonstrate that during retraction of the right femur, the tail consistently swings to the left, and vice versa (Reilly and Elias, 1998). Given the electromyography evidence showing that during retraction of the right femur, the right M. caudofemoralis contracts, one might instead have predicted the tail to swing towards, not away from, the right side. Pelvic rotation is partially responsible for this tail motion, but the left caudal muscles also retract to pull the tail leftwards and do, thereby, add to the rightM. caudofemoralis’ femoral pull.
The elongate zygapophysesTyrannosaurus of would likely have reduced the overall lateral flexibility of the tail, but the assistance of other caudal muscles in femoral retraction remains plausible, and the recruitment of muscle sets with no direct connections to limb bones has been well documented in extant animals, such as the intercostal muscles in running dogs (Carrier 1996) or neck muscles in galloping horses (Gellman et al., 2002).
Elasticity is another complication likely to have improved the tail’s locomotive contribution. Tails are naturally rich in tendons and septa, which are excellent stores of elastic energy. Elastic elements within the tails of both large and small non-avian theropods may have greatly improved locomotive efficiency
43 beyond what would be estimated based on the limb musculature of most modem birds and mammals.
In addition to considerations of absolute speed, large caudofemoral muscles also have implications for previous estimates of theropod centers of mass and are therefore relevant to Hutchinson and Garcia’s 2002 study and to
Hutchinson’s 2004 follow up, which found via numerous sensitivity analyses that repositioning the axial center of mass more posteriorly had the potential to significantly decrease the estimated muscle mass needed byTyrannosaurus to achieve higher speeds and to support its own bulk. Obviously, a largerM. caudofemoralis mass results in a more posterior position of any center of mass estimation (although the center of mass would also be determined by the dorsoventral angle of the torso and by the amount of curvature in the neck). The similar enlargement of any of the other hindlimb retractors would have a largely neutral effect on the axial center of mass. With its center of mass positioned closer to its hips, a theropod’s leg muscles would be relatively less strained in supporting its weight, and the animal’s overall balance and turning agility would be improved, as it would be less front-end heavy and its rotational inertia would be reduced.
The last point that should be made is primarily an artistic one. The current prevalent fashion among paleoartists is to depict the tails of most dinosaurs, but particularly theropods, as relatively unmuscular and laterally compressed. This is true not only of depictions made strictly for aesthetic purposes but also of those intended to support scientific research, such as estimations of mass (for example,
44 Paul, 1997; Bates et al., 2009). The less-than-robust tail depictions are consistent with the more traditional tail muscle restoration technique described. They are also likely the result of the recent trend towards depicting more lightly built and more fleet-footed theropods, because skinny laterally-compressed tails have a more aerodynamic and superficially more athletic appearance. In reality, skinny tails are not more athletic. Because the M. caudofemoralis is the primary retractor muscle of the hindlimbs, a slim-tailed theropod would be inherently slower than one with a large, muscular tail.
In overall appearance, the tails of most non-avian theropods likely resembled those of their modem crocodilian relatives, with relatively larger hypaxial muscles (and relatively smaller epaxial muscles) but without (in most cases at least) dorsal osteoderms. At the anterior base, the tails of most non-avian theropods would have been as broad or broader laterally as they were tall dorsoventrally. At and near the transition point, the tailswould be laterally compressed, and towards the posterior tip, the tails would, as the neural spines and hemal arches steadily shrunk, return to being roughly round in cross-section
(Fig. 1.13).
45 FIGURE 1.13. A fully rendered reconstruction of BHI 3033 created by Scott Hartman to illustrate the appearance ofTyrannosaurus a with a tail of appropriate beefiness.
46 1.11 Bibliography
Bakker RT. 1986. Dinosaur Heresies. New York: William Morrow.
Bamman, MW, Newcomer BR, Larson-Meyer D, Weisner RL, Hunter DR. 2000.
Evaluation of the strength-size relation in vivo using various muscle size
indices. Med Sci Sport Exer 32: 1307-1313.
Bates KT, Manning PL, Hodgetts D, Sellers WI. 2009. Estimating mass properties
of dinosaurs using laser imaging and 3d computer modelling. PLoS ONE
4(2): e4532.
Biewener, A A. 1989. Scaling body support in mammals: limb posture and muscle
mechanics. Science 245:45-48.
Brochu, CA. 2002. Osteology ofTyrannosaurus rex: insights from a nearly
complete skeleton and high-resolution computer tomographic analysis of
the skull. J Vertebr Paleontol 22: supplement to number 4.
Brooks SV, Faulkner JA. 1994. Skeletal muscle weakness in old age: underlying
mechanisms. Med Sci Sport Exer 26:432-439.
47 Brown IE, Satoda T, Richmond FJR, Loeb GE. 1998. Feline caudofemoralis
muscle Muscle fibre properties, architecture, and motor innervation. Exp
Brain Res 121(1):76-91.
Caldwell MW. 2006. A new species ofPontosaurus (Squamata, Pythonomorpha)
from the Upper Cretaceous of Lebanon and phylogenetic analysis of
Pythonomorpha.Memorie Soc. ital. Sci. nat. Mus. Civ. Stor. Nat. Milano
34:1^42.
Carpenter K, Sanders F, McWhinney LA, Wood L. 2005. Evidence for predator-
prey relationships: example Allosaurusfor and Stegosaurus. In: Carpenter
K, ed. The Carnivorous Dinosaurs. Indianapolis: Indiana University Press,
p 325-350.
Carrano MT. 1998. Locomotion in non-avian dinosaurs: integrating data from
hindlimb kinematics, in vivo strains, and bone morphology. Paleobiology
24(4):450-469.
Carrier DR. 1996. Function of the intercostal muscles in trotting dogs: ventilation
or locomotion? J EXP BIOL 199(7): 1455-1465.
Cong L, Hou L, Wu X, Hou J. 1998. The gross anatomy ofAlligator sinensis
Fauvel. Beijing: Forestry Publishing House. 295.
48 Dollo L. 1883. Note sur le presence, sur les Oiseaux, du "troisieme trochanter"
des Dinosauriens et sur lafonction de celui-ci. Bull Mus Roy Hist Nat Belg
TII, 13.
Dor M. 1937. La morphologie de las queue des mammiferes dans ses rapports
avec la locomotion. These, L‘Universite de Paris.
Farlow JO, Gatesy SM, Holtz TR Jr., Hutchinson JR, Robinson JM. 2000.
Theropod locomotion. Am Zool. 40:640-663.
Gatesy SM. 1990. Caudefemoral musculature and the evolution of Theropod
Locomotion. Paleobiology 16(2): 170-186.
Gatesy SM. 1997. An electromyographic analysis of hindlimb function in
Alligator during terrestrial locomotion. J Morph 234:197-212.
Gatesy S M, Biewener A A. 1991. Bipedal locomotion: effects of speed, size and
limb posture in birds and humans. J Zool, Lond 224:127-147.
Gellman KS, Bertram JEA, HermansonlJW. 2002. Morphology, Histochemistry,
and Function of Epaxial Cervical Musculature in the Horse(Equus
caballus). J Morph 251:182-194.
49 German RZ. 1982. The functional morphology of caudal vertebrae in new world
monkeys. Am J Phys Anthropol 58(4):453-459.
Howell AB. 1938. Muscles of the avian hip and thigh. Auk 55: 71-81.
Holtz TR Jr. 1995. The arctometatarsalian pes, an unusual structure of the
metatarsus of Cretaceous Theropoda (Dinosauria: Saurischia). J Vertebr
Paleontol 14:480-519.
Hutchinson JR. 2004. Biomechanical Modeling and Sensitivity Analysis of
Bipedal Running Ability. II. Extinct Taxa. J Morph 262:441-461.
Lemelin P. 1995. Comparative and functional myology of the prehensile tail in
new world monkeys. J Morph 224(3): 351-368.
Madsen JH. Jr. 1976. Allosaurus fragilis: a revised osteology. Utah Geological
and Mineral Survey. Bulletin 109.
McNeel Robert & Associates. 2007. Rhinoceros NURBS modeling for Windows
4.0. Seattle, Washington, USA.
50 Mendez J, Keys A. 1960. Density and composition of mammalian muscle.
Metabolism 9: 184-188, 1960.
Organ CL. 2006. Thoracic epaxial muscles in living archosaurs and omithopod
Dinosaurs. AR 288A:782-793.
Organ JM, Teaford MF, Taylor AB. 2009. Functional correlates of fiber
architecture of the lateral caudal musculature in prehensile and
nonprehensile yails of the Platyrrhini (Primates) and Procyonidae
(Carnivora). Anat Rec 292:827-841.
Paul GS. 1988. Predatory Dinosaurs of the world. Simon and Schuster. New
York, New York, p 327-337.
Paul GS. 1997. Dinosaur models: the good, the bad, and using them to estimate
the mass of dinosaurs. In: Wolberg, D. L., Stump, E., Rosenberg, G. D.
(eds.). Dinofest International: Preceedings of a Symposium Held at
Arizona State University. The Academy of Natural Sciences. Philadelphia,
p 129-154.
Paul GS. 1998. The complete illustrated guide to dinosaur skeletons. Gakken Co.
Ltd., Japan. 22.
51 Paul GS. 2000. Limb design, function and running performance in ostrich-mimics
and tyrannosaurs. Gaia 15:257-270.
Roberts TR, Chen MS, and Taylor CR. 1998. Energetics of bipedal running. II.
Limb design and running mechanics. J Exp Biol 201:2753-2762.
Romer AS. 1923. The pelvic musculature of saurischian dinosaurs. Bull Amer Nat
Hist 48:605-617.
Romer AS. 1927. The pelvic musculature of the omithischian dinosaurs. Acta
Zool, Stockholm 8:225-275.
Romer AS. 1956. Osteology of the Reptiles. The University of Chicago Press.
Chicago & London. 268-273.
Sacks RD, Roy RR. 1982. Architecture of the hindlimb muscles of cats:
functional significance. J Morphol 173:185-195.
Schwarz-Wings D, Frey E, Martin T. 2009. Reconstruction of the bracing system
of the trunk and tail in hyposaurine dyrosaurids (crocodylomorpha;
mesoeucrocodylia). J Vert Paleo 29(2):453-472.
52 Sellers WI, Paul GS. 2005. Speed potential of giant tyrannosaurs. Artif Intell
Study Behav Q. 121, 3.
Snively E, Russell AP. 2007. Craniocervical feeding dynamics ofTyrannosaurus
rex. Paleobiology 33(4):610-638.
Snyder RC. 1962. Adaptations for bipedal locomotion of lizards. Am Zool 191-
203.
Thomas WS, Magliano L, Woodhouse L, Lee ML, Dzekov C, Dzekov J, Casaburi
R, Bhasin S. 2003. Testosterone dose-dependently increases maximal
voluntary strength and leg power, but does not affect fatigability or
specific tension. J Clin Endocrinol Metab 88(4): 1478-1485.
53 Chapter 2 Dinosaur Speed Demon: the Caudal MusculatureCarnotaurus of and Implications for the Evolution of South American Abelisaurids*
2.1 Introduction
When first described by Bonaparteet al. in 1990, the holotype of
Carnotaurus sastrei (MACN-CH 894) revealed many puzzling adaptations in both the appendicular and axial skeleton that were previously unseen in theropods. Carnotaurus established Abelisauridae as a unique clade of carnivorous dinosaurs, evidently separated from all other known theropod groups by a large evolutionary rift (Bonaparteet al., 1990). Abelisauridae is best known for the small horns and other cranial ornamentations common to most of its members. Carnotaurus is the most advanced member of Abelisauridae, with a pair of robust conical horns that extend devilishly from the frontals. However, the most unusual skeletal adaptations of Carnotaurus and its close relatives occur not in the skull, but in the tail.
The preserved tail vertebrae of MACN-CH 894 have caudal ribs that are dorso-posteriorly inclined and often exceed the neural spines in absolute height
(Bonaparte et al., 1990). The tips of the caudal ribs are flattened and expanded with anteriorly-projecting half-crescent-shaped anterior edges and rounded posterior edges (Figs. 2.1, 2.2). Since the initial description ofCarnotaurus, many aspects of this bizarre caudal morphology have been reported in other South
American abelisaurids, including Aucasaurus (Coria et al., 2002),
* A version of this chapter has been submitted for publication. Persons 2012. PLOS One.
54 Caudal rib Neural spine Caudal rib
Neural spine
Prezygap- ophysis Postzygap- Prezygap- ophysis ophysls
Centrum Centrum
4 cm
Postzygap- Neural spine ophysis
Caudal rib
Prezygap- Centrum ophysis
FIGURE 2.1. Typical anterior caudal morphologyCarnotaurus of sastrei (MACN-CH 894). Restored illustration of caudal vertebra 6 in (A) left lateral view, (B) anterior view, and (C) dorsal view.
55
FIGURE 2.2. Select caudal vertebrae of Carnotaurus sastrei (MACN-CH 894). (A, B, C) Caudal vertebra 1 in right lateral, anterior, and dorsal view, respectively - note: caudal rib tips not fully preserved. (D, E, F) Caudal vertebra 2 in right lateral, anterior, and dorsal view, respectively - note: caudal rib tips not fully preserved. (G, H, I) Caudal vertebra 5 in right lateral, anterior, and dorsal view, respectively - note: centrum and caudal rib tips not preserved. (J, K, L) Caudal vertebra 6 in right lateral, anterior, and dorsal view, respectively; note: centrum not preserved.
57 Ilokelesia (Coria and Salgado, 1998), and Skorpiovenator (Canale et al., 2009).
Similarly, the discoveries of abelisaurids in Madagascar and Southern Asia have consistently shown an absence of this unusual morphology. In the Malagasy genus Majungasaurus, for which a largely complete caudal series is known, the general proportions of the caudal osteology do not differ dramatically from those of most other large-bodied non-coelurosaurian theropods. The anterior caudal ribs of Majungasaurus project predominantly transversely, with only a slight ventral inclination, and lack specialized caudal rib tips (O’Connor, 2007). [Note: As here used, the term “caudal rib” should also not be confused with the arguments made by Caronoet al. (2011) (later discussed), which suggests that both caudal ribs and caudal transverse processes were present in some abelisaurids.)
Beginning with the original description ofCarnotaurus, the potential athleticism of abelisaurids has been the subject of speculation and debate. Based on the proportions of the hindlimbs, Bonaparteet al. (1990) suggested that
Carnotaurus was among the most cursorial of the large-bodied theropods, and
Mazzetta et al. (1998) supported this inference. However, the subsequent discovery of complete hindlimbs in the type specimen of the closely related
Aucasaurus showed that the length ratio of the tibia/femur was likely not a high as
Bonaparte et al. (1990) anticipated (Coria et al., 2002). InMajungasaurus, the total tibia-femur length is notably short compared to other similarly sized theropods (Carrano, 2007), suggesting that Majungasaurus was comparably slow.
The hindlimbs of the Indian abelisaurid Rajasaurus and the South American abelisaurid Ekrixinatosaurus were proportioned similarly toMajungasaurus,
58 while the legs of Carnotaurus and Aucasaurus were relatively longer and more gracile (Novas et al., 2004; Carrano, 2007; Juarez Valieri et al., 2010).
Consideration of the novel caudal osteology ofCarnotaurus and its South
American relatives is potentially relevant to the discussion of abelisaurid cursoriality, because the tails of most non-avian theropods, like the tails of modem saurians, were the origin sites for the primary hind-limb retractor muscle: the M. caudofemoralis (see Chapter 1). Here, the same digital modeling techniques described in Chapter 1 are applied to a digital reconstmction of the caudal skeleton of Carnotaurus (with posterior portions modeled after those of more complete closely related theropods).
2.2 Reconstruction Method and Assumptions
Digital skeletal and muscle models of Carnotaurus were created following procedures shown to be accurate for modem taxa (see Chapter 1). All models were created using the digital modeling program Rhinoceros® (McNeel Robert &
Associates, 2007).
Skeleton
MACN-CH 894 includes only the first six caudal vertebrae and an isolated fragment interpreted by Bonaparteet al. (1990) as possibly belonging to caudal vertebra 12. In the digital model, the first six caudal vertebrae were sculpted based on measurements made on LACM 127704 (a cast of MACN-CH 894). To ensure accuracy, measurements of LACM 127704 were compared to those
59 published in Table 2 of Bonaparte et al. 1990, and were found to be reliable (see
Table 1 in Appendix A).
The remaining vertebrae had to be digitally sculpted based on published measurements and illustrations of other abelisaurid material and scaled to fit.
Caudal vertebrae 7-13 were modeled based on MCF-PVPH-236, the holotype of
Aucasaurus (Coria et al., 2002). The anterior caudal vertebrae of Aucasaurus show a morphology similar in most respects to that ofCarnotaurus (although the caudal ribs of Aucasaurus are not as dorsally inclined and lack the distinctive crescent shape), and the two theropods are considered by most authors to be sister taxa (Coria et al., 2002; Coria, 2007, Canale et al., 2009). Thus, the posterior portion of the created “Carnotaurus” model may be more representative of a generalized camotaurine, but the model does include all the known advanced caudal morphology ofCarnotaurus, with the region modeled after Aucasaurus modified to fit the proportions of the anterior sequence and scaled to conform to the large body size ofCarnotaurus.
Deducing the shape of the more posterior vertebrae requires greater speculation. Fortunately, beyond caudal vertebra 13, the vertebrae and associated muscles are so diminished in size that reasonable variation in their shape and total number can only have minimal effects on the calculations of muscle mass (see
Table A.2 in Appendix A). Caudal vertebrae 14-25 were based on those of
Majungasaurus (FMNH PR 2100) - the only abelisaurid for which a reasonably good series of posterior caudals has been described. Based on the trend of vertebral size reduction observed in the more anterior vertebrae, the series is
60 estimated to have ended at caudal vertebra 42, and the remaining 17 vertebrae
were based on those of Ceratosaurus (USNM 4735). It is assumed that in the
more posterior vertebrae the caudal ribs gradually had a more typical, horizontal
orientation. This assumption seems reasonable, given that in other theropods with
slightly dorsally oriented caudal ribs on the anterior caudal vertebrae (such as
Allosaurus and Ceratosaurus) the caudal ribs of the posterior caudals lose all
dorsal inclination.
In the description of the type specimen, the chevrons ofCamotaurus were
reconstructed with strong posterior angles (Bonaparteet al., 1990). This was
based on the morphology of the chevron articular facets and the alignment of the
haemal canals. The chevrons of most non-avian theropods show some degree of posterior orientation, but none are as extreme as those depicted forCamotaurus
(Fig. 38 of Bonaparte et al., 1990). The articulated caudal series preserved for
Aucasaurus shows chevrons with posterior angulations relative to the axis of the caudal vertebrae, but the chevrons are still less posteriorly inclined than in the original depiction. In the digital model, the anterior chevrons have been inclined to angles consistent with those seen in Aucasaurus. This more conservative
chevron orientation is also consistent with the angles of the chevron indentations preserved with the skin impressions of MACN-CH 894. There is a possible explanation for the discrepancy between the chevron angulations proposed here
and those proposed by Bonaparteet al. (1990). The one well preserved chevron of
MACN-CH 894 was tentatively identified by Bonaparteet al. (1990) as chevron number four, whereas it was in fact chevron number one or two. The first two
61 chevrons of crocodiles and many modem reptiles are more strongly inclined posteriorly than the other chevrons in the series, and this is also the case in numerous theropod genera (Brochu, 2002), includingAucasaurus (see Fig. 2 in
Coria et al., 2002).
The digital reconstruction assumes that the total number of caudal vertebrae in the tail of Camotaurus was 42, that the posterior caudal ribs became gradually less dorsally inclined and terminated at caudal vertebrae 26, and that the orientations of the chevrons were similar to those seen in Aucasaurus (see Fig.
2.3).
Musculature
Gatesy (1990) argued that the posterior tip of theM. caudofemoralis was correlated with the termination of the caudal ribs. A scar on the haemal spines of
some well preserved theropod specimens demarks the insertion of the septum that
separated theM. ilio-ischiocaudalis from the M. caudofemoralis (see Chapter 1).
This scar could, therefore, could be used to identify the posterior tip of theM. caudofemoralis. However, well preserved haemal spines from the region of the tail where the posterior terminus of the M. caudofemoralis would be expected have yet to be described for Camotaurus or any of its close relatives. In
Camotaurus, the position of the posterior tip must be inferred, based on the point of caudal rib termination, which must in turn be inferred from the general trend in caudal rib reduction seen in the anterior vertebrae and from the caudal rib
termination point of the distantly relatedMajungasaurus.
62 FIGURE 2.3. Digital model of the tail of Camotaurus sastrei. Blue vertebrae modeled after Camotaurus sastrei (MACN-CH 894), red vertebrae modeled after Aucasaurus garridoi (MCF-PVPH-236), purple vertebrae modeled after Majungasaurus crenatissimus (FMNH PR 2100), and green vertebrae modeled after Ceratosaurus nasicomis (USNM 4735).
63 As described in Chapter 1, anterior to its posterior termination, the M.
caudofemoralis of dinosaurs inserted across the full lateral surfaces of the centra and chevrons. Contrary to numerous depictions (e.g. Romer, 1923; Arbour, 2009), the M. caudofemoralis did not insert onto the ventral surfaces of the caudal ribs
(which are strictly insertions of theM. ilio-ischiocaudalis). However, the nearly
vertical caudal ribs of some advanced abelisaurids are possible exceptions. The
well preserved anterior caudal series of Aucasaurus offers strong evidence that
this was indeed the case, and that the caudal ribs of advanced South American
abelisaurids were insertion surfaces for both the M. ilio-ischiocaudalis and the M.
caudofemoralis. The ventral surface of each caudal rib of Aucasaurus shows a
narrow anteriorposteriorly directed scar (Figs. 2.4,2.5) that strongly resembles the
haemal spine scar interpreted as the insertion of a septum in other theropods.
Carrano et al. (2007) interpreted the caudal rib scars of Aucasaurus as
sutures between caudal ribs and transverse processes. This interpretation is here
disfavored, because the scars do not form continuous rings around the caudal ribs,
but are instead pronounced only on the ventral surfaces. The scars are also
morphologically dissimilar to typical sutures, being substantially distended from
the surrounding bone surface and tapered to form central keels. These caudal rib
scars are here interpreted as marking the dorsal insertion of the M. ilio-
ischiocaudalis/M. caudofemoralis septum. Using these scars as a guide, it is
possible to reconstruct how far dorsally theM. caudofemoralis extended across
the caudal ribs of Aucasaurus, and, by analogy, approximately how farM. the
caudofemoralis extended across the caudal ribs of Camotaurus (Fig. 2.6).
64 FIGURE 2.4. Caudal vertebra 4 of Aucasaurus (MCF-PVPH-236) in (A) lateral, (B) dorsal, and (C) anterior view. Arrows indicate the M. ilio-ischiocaudalis!M. caudofemoralis septum scars.
65 FIGURE 2.5. Caudal vertebra 1-4 of Aucasaurus (MCF-PVPH-236) in right lateral view. Arrows indicate the sequence of M. ilio- ischiocaudalis! M. caudofemoralis septum scars.
66 M. spinalis M. longissimus
ilio-ischiocaudalis
M. caudofemoralis
FIGURE 2.6. Cross-section through the tail of Camotaurus sastrei showing caudal vertebra 6 and accompanying musculature. Note: the cross-section is an anatomical abstraction and depicts the neural arch and heamal arch in the same vertical plane.
67 Following similar methods as Arbour (2009), Allen et al. (2009), and
Mallison (2011), two muscle reconstructions were created. One is a conservative reconstruction that is comparable with those created in Chapter 1,3,4,5. The other is a robust reconstruction.
In the conservative model: the whole of the epaxial musculature was reconstructed by extending an arc in dorsoventral cross-section from the tips of the neural spines to the tips of the caudal ribs; anterior to its tapering, the M. caudofemoralis was reconstructed by extending an arc in dorsoventral cross- section from its attachment site on the ventrolateral surface of the caudal ribs to the ventral tip of the chevrons; and the M. ilio-ischiocaudalis was reconstructed, anterior to the taper point of theM. caudofemoralis, by extending an arc in dorsoventral cross-section from the lateral tips of the caudal ribs to below the ventral tips of the chevrons, and, posterior to the taper point of theM. caudofemoralis, by extending an arc in dorsoventral cross-section from the ventral boundaries of the neural arches to the ventral tips of the chevrons.
Anteriorly, the arc of theM. ilio-ischiocaudalis maintained a consistent thickness equal to the distance between the reconstruction of the M. caudofemoralis and the ventrolateral edge of the caudal ribs. Note, this method of conservative reconstruction is not synonymous with the “traditional elliptical” reconstruction method described in Allen et al. (2009), and in this model the dimensional extents of the caudal musculature greatly exceeds that of caudal osteology.
In the robust model: the epaxial musculature arc was assumed to extend beyond the neural spines and caudal ribs by 125% and 175 %, respectively; theM.
68 caudofemoralis was reconstructed with a laterally oblong shape; and theM. ilio- ischiocaudalis was thickened such that the lateral extreme of its arch extended beyond that of the anterior caudal ribs by 500%. Like the conservative model, the robust model assumes that no large fat deposits were present in the tail, although in modem sauropsids the tail is a common site of fat storage. In modem crocodilians, a thick layer of fat is often deposited between theM. caudofemoralis and the M. ilio-ischiocaudalis (Cong et al., 1998). The proportions used in the robust model conform to those observed in the girthy anterior-most caudal regions of modem reptiles (Cong et al., 1998; Allen et al., 2009; Mallison, 2011), with fat deposits removed.
The portion of the M. caudofemoralis reconstructed in both the conservative and the robust model corresponds to the m. caudofemoralis longus.
The m. caudofemoralis brevis was not modeled. Instead, the mass of the m. caudofemoralis brevis was estimated by measuring the volume of the brevis fossa.
Because the m. caudofemoralis brevis is completely capped by the brevis fossa, the size of the m. caudofemoralis brevis is far less speculative, and its contribution to the final mass estimations was not varied between the robust and conservative results.
2.3 Reconstruction Results
That the insertion of the M. caudofemoralis onto the lateral surfaces of the caudal ribs and the dorsal tilt of the caudal ribs permitted the dorsal expansion of the M. caudofemoralis, even past the point of mediolateral overlap with theM.
69 longissimus, is apparent from simple observation of the fossil specimens of both
Camotaurus and Aucasaurus. The results of the digital modeling are summarized in Table 2.1 and indicate a substantial investment in hypaxial vs. epaxial musculature (Figs. 2.7,2.8). The calculated mass of the M. caudofemoralis is particularly large, estimated to range from 111-137 kg for each hindlimb. In
Chapter 1, the conservative muscle modeling methods used here were tested on a range of modem long-tailed sauropsids and were found to consistently underestimate true M. caudofemoralis mass, but to within 1-6% of the true value.
The overall muscle to bone proportions of the robust model exceed the typical range reported by Allenet al. (2009) for a variety of modem lizards. The true mass of the M. caudofemoralis of Camotaurus, therefore, likely lies within this range, but probably not at either extreme. Compared with the other muscles, the estimated mass of the M. ilio-ischiocaudalis varied the most between the conservative and robust models. This is because, in the robust reconstruction, both the absolute thickness of M. ilio-ischiocaudalis was increased and, because the M. caudofemoralis was expanded laterally, the elliptical path of theM. ilio- ischiocaudalis was also increased.
Comparisons of the conservative muscle mass estimations with those obtained using the same methods for other theropods are give in Table 2.2, and confirm that Camotaurus had an exceptionally large investment in theM. caudofemoralis - estimated to be greater relative to overall body size than that previously calculated for any other theropod.
70 FIGURE 2.7. The conservatively modeled tail of Camotaurus sastrei (MACN- CH 894). (A) Digital reconstruction of the caudal and pelvic skeleton with M. caudofemoralis longus (red). (B) Complete digital reconstruction, with epaxial musculature (gold) and M. ilio-ischiocaudalis (pink) added.
71 FIGURE 2.8. The robustly modeled tail of Camotaurus sastrei (MACN-CH 894). (A) Digital reconstruction of the caudal and pelvic skeleton with M. caudofemoralis longus (red). (B) Complete digital reconstruction, with epaxial musculature (gold) and M. ilio-ischiocaudalis (pink) added.
72 TABLE 2.1. Mass estimation results from the conservative and robust models of Camotaurus sastrei (results are presented for left and right muscle sets combined). M. spinalis Al. longissimus Al. ilio-ischiocaudalis Al. caudofemoralis Conservative Model 7000 g 15000 g 63000g 222000 g Total tail muscle mass: 307000 g 2.3% 4.9% 20.5% 72.3% Total body mass: 1500000 g 0.5% 1.0% 4.2% 14.8% Robust Model 11000g 24000 g 106000g 273000 g Total tail muscle mass: 414000 2.7% 5.80% 25.6% 65.9% Total body mass: 1500000 g 0.7% 1.6% 7.1% 18.2%
TABLE 2.2. Estimated conservative caudal muscle masses of Camotaurus and other theropods (results are presented for left and right muscle sets combined). Camotaurus body mass estimation form Mazzetta et al. ( 998). Al. spinalis Al. longissimus Al. ilio-ischiocaudalis M.caudofemoralis Camotaurus sastrei MACN-CH 894 7000 g 15000 g 6 3 0 0 0 g 222000 g Total tail muscle mass: 307000 g 2.3% 4.9% 20.5% 72.3% Total body mass: 1500000 g 0.5% 1.0% 4.2% 14.8% Omithomimus edmontonicus TMP 95.11.001 860 g 2440 g 5050 g 9890 g Total tail muscle mass: 18240 g 4.7% 13.4% 27.7% 54.2% Total body mass: 150000 g 0.6% 1.6% 3.4% 6.6% Gorgosaurus libratus TMP 91.36.500 3900 g 6900 g 1 0 3 0 0 g 1 7 3 0 0 g Total tail muscle mass: 38300 g 10.2% 18.0% 26.9% 45.2% Total body mass: 400000 g 1.0% 1.7% 2.6% 4.3% Tyrannosaurus rex BHI3033 65200 g 1 5 4 2 0 0g 1 59400g 522200 g Total tail muscle mass: 901000 g 7.2% 17.1% 17.7% 58.0% Total body mass: 5622000 g 1.2% 2.7% 2.8% 9.3%
73 2.4 Functional Implications
As previously described, the models created in this study are largely based on both Camotaurus and Aucasaurus. For the sake of simplicity, and because
Camotaurus shows the most extreme caudal morphology, in this section, the results are discussed primarily as they relate to the paleobiologyCamotaurus. of
Nonetheless, the functional implications of this study are relevant, to varying degrees, to most known South American abelisaurids.
The arguments made by Bonaparteet al. (1990) and Mazzetta et al.
(1998) that Camotaurus was a more cursorial form than other large-bodied theropods is partially supported by this study. The large size ofM. the caudofemoralis of Camotaurus would impart great force to the power strokes of the hindlimbs, however the ridged nature of the caudal series likely reduced turning performance.
The flattened, half-crescent-shaped tips of the caudal ribs ofCamotaurus overlapped with those directly anterior and posterior in the series, with those of the first caudal vertebra articulating with the ilium (Coria et al., 2002). This appears to create a highly inflexible anterior tail, in terms of both lateral and dorsoventral maneuverability. Recent biomechanical analyses of theropod turning performance have commented on the large rotational inertia that the elongate body-plans of most theropods would impart (Carrier et al., 2001; Henderson and
Snively 2004). Such studies have likely underestimated the turning abilities of most theropods, because they have assumed that the sum total of a theropod’s rotational inertia had to be overcome all at once. Theropods were not laterally
74 stiff, and it is likely that most theropods turned with a more serpentine motion - turning first their heads and necks, then torsos, then hips, and finally, in a sinuous motion, their tails. In the case of Camotaurus and the other abelisaurids that
shared the interlocking caudal rib morphology, the hips and most of the caudal mass would have been forced to rotate as one unit, and sinuosity would have been minimized. This suggests that Camotaurus and its close relatives had a diminished ability to make rapid tight turns, relative to other equivalently sized theropods.
However, the results of the digital muscle reconstruction suggest that what
Camotaurus lacked in turning ability it may have made up for in overall speed and acceleration. In a sensitivity analysis of bipedal dinosaur running, Bates etal.
(2010) found that locomotive muscle mass and cross-sectional area were the most important factors in estimations of top running speeds. Because theM. caudofemoralis was the primary femoral retractor, the large relative mass and corresponding large relative cross-sectional area of the M. caudofemoralis of
Camotaurus would impart exceptional strength to the backwards strokes of the hindlimbs. Such a large investment in caudofemoral mass would translate into enhanced locomotive force generation. For an animal as massive as Camotaurus, overcoming its own inertia would pose a considerable hindrance to rapid acceleration. The enlarged M. caudofemoralis may have providedCamotaurus with the raw power necessary for sudden straight-forward sprints and charges.
This investment in locomotive power required a tradeoff in muscle masses. Dorsal tilting of the caudal ribs allowed for a larger M. caudofemoralis,
75 but, because the neural spines are observably no more elongated than those of most other similarly sized theropods, it also left relatively less space available to be filled by the M. spinalis and M. longissimus. Both the M. spinalis and M. longissimus function in mediolateral and dorsoventral tail movement and in maintaining tail stability. While overall tail maneuverability was lost, the interlocking tips of the caudal ribs served to compensate for the diminished epaxial musculature by enhancing tail stability and were perhaps key to allowing the dorsal expansion of theM. caudofemoralis. The increased relative stiffness of the anterior portion of the tail likely aided in providing a rigid framework for the large caudofemoral muscles to pull against and likely mitigated energy loss that would have resulted from any lateral or dorsal swing of the tail towards the contracting muscle.
On its own, increased maximum femur retraction force has positive implications for the cursorial potential ofCamotaurus overall. However, it should be noted that the effect the rigidity of the anterior caudal vertebrae had on locomotive endurance is unclear. On the one hand, in computer simulations of
Allosaurus, Manning (2008) found that a stiff trunk had the potential to store significant elastic energy during dinosaur locomotion. The stiff tail of
Camotaurus may, therefore, have translated to more spring in its step. On the other hand, undulations of dinosaur tails while walking and running could have facilitated preload stretching of the M. caudofemoralis, which also had the potential for great energetic efficiency. The enhanced rigidity in the tail of
76 Camotaurus may have limited or altogether prevented anterior tail undulations and the resulting energetic benefits.
2.5 Evolutionary Context
Camotaurus, of Campanian-Maastrichtian age, is currently the youngest known South American abelisaurid and is generally regarded as the most derived in its morphological features (Coria et al., 2002; Coria, 2007). In recent years, a series of older South American abelisaurids have been found and help reveal the rough evolutionary sequence that led to the caudofemoral-dominated tail morphology ofCamotaurus. Ekrixinatosaurus and Ilokelesia (from the lower
Cenomanian Candeleros Formation, and the upper Cenomanian Huincul
Formation, respectively) are the oldest known South American members of the
Abelisauridae (Coria, 2007; Calvo et al., 2004). Anterior caudal vertebrae are not known for Ilokelesia, but in Ekrixinatosaurus they have caudal ribs with slight dorsal inclinations and expanded tips (Coria, 2007). The mid-caudal vertebrae of both Ekrixinatosaurus and Ilokelesia have caudal ribs with generally similar morphology. The main difference is that the mid-caudal ribs ofEkrixinatosaurus are more posteriorly inclined (Coria, 2007). In both taxa the mid-caudal ribs extend laterally with slight dorsal inclinations and have strong posterior and anterior projections on the tips, giving them a “T-shape” in dorsal view. While these ‘T-shaped” caudal ribs lack the overlapping and interlocking morphology of
Camotaurus, the anterior and posterior projections nearly abutted with the next tips in the series and were likely connected by ligaments or other more sturdy tissue. In the caudal vertebrae of Ilokelesia, the neural spines appear to be reduced
77 in relative dorsoventral height (however, this observation is tenuous, because the incompleteness of the caudal series makes determining the exact position of each vertebra difficult), and indicates that the epaxial muscle mass was somewhat reduced, but with no strong evidence of increased relative hypaxial muscle mass.
Skorpiovenator (Canale et al., 2009) is a slightly younger abelisaurid
(from the Huincul Formation, Late Cenomanian - Early Turonian). The morphology of the caudal ribs ofSkorpiovenator closely resembles those of
Ekrixinatosaurus and Ilokelesia, but the ribs have notably stronger dorsal inclinations and the anterior projections of the tips of the caudal ribs are more pronounced than the posterior projections (Canale et al., 2009). The next youngest
South American abelisaurid for which good caudal material is known is
Aucasaurus from the Campanian Rio Colorado Formation (Coria et al., 2002).
Aucasaurus is regarded by many to be the sister taxon toCamotaurus (Coria et al., 2002; Coria, 2007; Canale et al., 2009) (but for an alternative interpretation see Carrano and Sampson, 2008). The caudal ribs of Aucasaurus have a strong dorsal orientation with interlocking tips. Aucasaurus still has “T-shaped” caudal ribs, but the posterior projections are smaller in relation to the anterior projections.
The phylogeny of the Abelisauridae has been the subject of much analysis, debate, and uncertainty. Based on the caudal morphology and the chronology of taxa, the overall evolutionary sequence of South American abelisaurids seems to have been: 1) slight dorsal inclining of the caudal ribs and the development of anterior and posterior projections on the tips of the caudal
78 ribs, which increased rigidity in the caudal series and diminished the need and functional value of the caudal epaxial musculature (seen inEkrixinatosaurus and
Ilokelesia); 2) the gradual increase in the dorsal inclination of the caudal ribs
(Skorpiovenator) and corresponding dorsal expansion and increase in total mass of the M. caudofemoralis; 3) a further increase in rigidity accomplished through true interlocking caudal ribs ( Aucasaurus) and continued caudofemoral dorsal expansion; and, 4) the maximized rigidity through crescent-shaped, tightly interlocking rib morphology (Camotaurus). The possible evolutionary sequence is summarized in Figure 2.9.
This phylogeny should not be misinterpreted as a well substantiated cladistic conclusion. It is instead a tentative hypothesis derived solely from two lines of evidence (caudal morphology and chronological sequence). It is offered here with the hope that it will be validated or invalidated by future studies, and with the encouragement that subsequent cladistic analyses of Abelisauridae
(which have previously been heavily reliant on cranial characters) take into more thorough consideration the morphology of the caudal vertebral series.
Regardless of the true phylogeny, increasedM. caudofemoralis mass and caudal rigidity appear to be characteristic of later South American abelisaurids.
This result, and its inferred relation to relative cursoriality, is consistent with previous consideration of South American abelisauride limb proportions (Ju&rez
Valieri et al., 2010), which reported longer and more gracile limbs in
Camotaurus, Aucasaurus, and Skorpiovenator than in earlier genera. These results also show a strong contrast between the late abelisaurids of South America
79 and those from the rest of Gondwana — which have primitive caudal morphology and short, stocky hindlimb proportions (Calvo et al., 2004; Novas et al., 2004;
to
71 - -
t o
LU
to - o__ LU OC
•9 4 --
100
FIGURE 2.9. Chronostratigraphy and hypothesized phylogeny of South American Abelisauridae with representative caudal vertebrae for each in anterior and dorsal views. Note: although each taxa is demarked by a separate branching event, it is probable, given the close geographic and temporal proximities of these taxa, combined with the unlikelihood that multiple other as-yet-unknown large-bodied carnivorous abelisaurids were coexistent, that some of these taxa have a direct anagenic relationship with others.
80 Carrano 2007). In particular, these results conflict with previous conclusions that the Malagasy abelisaurMajungasaurus and Camotaurus were more closely related to each other than ether were to any of the other South American taxa
(Sereno 1998; Sampson et al., 2001; Wilson et al., 2003).
2.6 Conclusion
In his examination of theM. caudofemoralis of theropod dinosaurs,
Gatesy (1990) posited a general trend of relative caudofemoral muscle size reduction throughout the whole of theropod evolution. As shown by Gatsey
(1990a, 1990b) a strong trend toward reduced caudofemoral mass can be seen in the lineage leading to modem birds. However, the unique caudal vertebrae morphology ofCamotaurus and its close relatives offers a dramatic counterexample. The development of interconnecting caudal ribs, each with a
strong dorsal inclination, enabled an exceptionally largeM. caudofemoralis. This would have made Camotaurus a powerful sprinter -- perhaps among the fastest of the large bodied theropods (see Fig. 2.10). Consideration of these morphological differences in a stratigraphic context indicates a pattern of increased caudofemoral
mass and cursorial potential throughout the evolutionary history of the
Abelisauridae of South America. During at least the early portion of this history,
abelisaurids coexisted with another clade of predatory dinosaurs:
carcharodontosaurids. The carcharodontosaurids of South America (including
Giganotosaurus, Mapusaurus, and Tyrannotitan) were among the largest of all
81 theropods, and obtained body sizes much greater than that of any known abelisaurid (Juarez Valieri et al., 2010). It has been argued that the extreme size of these carcharodontosaurids allowed them to hunt the even larger South American titanosaur sauropods (Coria and Salgado, 1995). The cursorial tail morphology of
South American abelisaurids may have arisen to help in avoiding potential carcharodontosaurid predators and/or supported niche partitioning by allowing abelisaurids to specialize in the pursuit and capture of smaller prey (such as omithopods).
82 FIGURE 2.10. Life restoration of a sprinting Camotaurus sastrei, by Lida Xing and Yi Liu. Dlustration shows laterally expansive and appropriately large caudal musculature.
83 2.7 Bibliography
Arbour VM (2009) Estimating impact forces of tail club strikes by ankylosaurid
dinosaurs. PLoS ONE. 4(8): e6738.
Brochu CA (2002) Osteology ofTyrannosaurus rex: insights from a nearly
complete skeleton and high-resolution computer tomographic analysis of
the skull. J Vertebr Paleontol 22: supplement to number 4.
Bonaparte JF, Novas FE, Coria RA (1990) Camotaurus sastrei Bonaparte, the
homed, lightly built, camosaur from the middle Cretaceous of Patagonia.
Contributions in Science 416:1-42.
Calvo JO, Rubilar-Rogers D, Moreno K (2004) A new Abelisauridae (Dinosauria:
Theropoda) from northwest Patagonia. Ameghiniana 41:555-563.
Canale JI, Scanferla CA, Agnolin FL, Novas FE (2009) New carnivorous
dinosaur from the Late Cretaceous of NW Patagonia and the evolution of
abelisaurid theropods. Naturwissenschaften 96:409-414.
Carrano MT, Loewen MA, Sertich Joseph JW (2011) New materials of
Masiakasaurus knopfleri Sampson, Carrano, and Forster, 2001, and
84 implications for the morphology of the Noasauridae (Theropoda:
Ceratosauria). Smithsonian Contributions to Paleobiology 95.
Carrano MT, Sampson SD (2008) The phylogeny of Ceratosauria (Dinosauria:
Theropoda). Journal of Systematic Palaeontology 6(2): 183-326.
Carrier DR, Walter RM, Lee DV (2001) Influence of rotational inertia on turning
performance of theropod dinosaurs: clues from humans with increased
rotational inertia. J Exp Biol 204:3917-3926.
Coria RA, Chiappe LM, Dingus L (2002) A new close relative ofCamotaurus
sastrei Bonaparte, 1985 (Theropoda: Abelisauridae) Naturwissenschaften
(2009) 96:409-414 413 from the Late Cretaceous of Patagonia. J Vert
Paleontol 22:460-465.
Coria RA, Salgado L (1998) A basal Abelisauria Novas, 1992 (Theropoda-
Ceratosauria) from the Cretaceous of Patagonia, Argentina. GAIA 15:89-
102.
Corio RA (2007). Nonavian Theropods. In: Gasparini Z, Salgado L, Coria RA,
editors. Patagonian Mesozoic reptiles. Bloomington and Indianapolis:
Indiana University Press, pp. 229-256.
85 Coria RA, Salgado L. 1995. A new giant carnivorous dinosaur from the
Cretaceous of Patagonia. Nature 377:224-226.
Gatesy SM. 1990. Caudefemoral musculature and the evolution of Theropod
Locomotion. Paleobiology 16(2): 170-186.
Gatesy SM. 1997. An electromyographic analysis of hindlimb function in
Alligator during terrestrial locomotion. J Morph 234:197-212.
Henderson DM, Snively E. 2004. Tyrannosaurus en pointe: allometry minimized
rotational inertia of large carnivorous dinosaurs. Proc Biol Sci 271(suppl
3): S57-S60.
Juarez Valieri RD, Porfiri JD, Calvo JO. 2010. New information on
Ekrixinatosaurus novasi Calvo et al 2004, a giant and massively-
constructed Abelisauroid from the “Middle Cretaceous” of Patagonia. In:
Calvo J, Porfiri J, Gonzalez Riga B, Dos Santos D, editors. Paleontologfa
y Dinosaurios en America Latina, pp. 161-169.
Mazzetta GV, Farina RA, Vizcaino. 1998. On the palaeobiology of the South
American homed theropod Camotaurus sastrei Bonaparte. GAIA 15:185-
192.
86 McNeel Robert & Associates. 2007. Rhinoceros NURBS modeling for Windows
4.0. Seattle, Washington, USA.
Romer AS. 1923. The pelvic musculature of saurischian dinosaurs. Bull Amer Nat
Hist 48:605-617.
Romer AS. 1956. Osteology of Reptiles. Krieger Publishing Company. Malabar,
Florida.
Paul GS. 1988. Predatory Dinosaurs of the World. Simon and Schuster. New
York, New York.
87 Chapter 3 Oviraptorosaur Tail Forms and Functions*
3.1 Introduction
Oviraptorosaurs are a group of maniraptoriform theropod dinosaurs, characterized by numerous synapomorphies, including: a crenulated ventral margin of the premaxilla, a U-shaped mandibular symphysis, an edentulous dentary, pneumatized caudal vertebrae, an anteriorly concave pubic shaft and a posteriorly curved ischium (Osmolska et al., 2004). Although absent in several genera, prominent cranial crests are common and emblematic features within the group. Oviraptorosaurs ranged in size from the 0.69 meter long
Protarchaeopteryx to the 8 meter long Gigantoraptor (Xu et al., 2007). At present, all confirmed oviraptorosaur material is limited to Cretaceous sediments of Asia, Europe, and North America. The absence of teeth and the inferred presence of a non-hooked homy beak in advanced forms, along with the incisciform teeth of the basal genus Incisivosaurus (Xu et al., 2002a) and the in situ gizzard stone masses preserved in specimens ofCaudipteryx (Ji et al., 1998), suggest that the group was predominantly herbivorous. Although all known forms are definitively flightless, direct proof of feather integument is preserved in specimens ofCaudipteryx, Protarchaeopteryx (Ji et al., 1998), and
Similicaudipteryx (Xu et al., 2010b). Structures tentatively identified as quill knobs are present on the ulna of Avimimus (Kurzanov, 1987).
* A version of this chapter has been submitted for publication. Persons 2012. Acta Palaeontologica Polonica.
88 The tail of an oviraptorosaur is remarkable for its reduced length. In the genera Nomingia and Similicaudipteryx, the last few caudal vertebrae are fused.
These fused vertebrae formed a pygostyle that probably supported a fan of tail feathers (Barsbold et al., 2000; Xu et al., 2010b). The similarities between the tails of oviraptorosaurs and modem birds have been cited as support for a close relationship between the two groups (Lii et al., 2002; Maryahska et al., 2002), as evidence that oviraptorosaurs were secondarily flightless (Maryahska et al., 2002;
Paul, 2002), and as a correlate for bird-like knee-flexion-dominated locomotion
(Maryahska et al., 2002).
In this study, the caudal osteology and inferable caudal musculature of oviraptorosaurs is considered with the aim of critically reevaluating claims of avian affinities and similarities. Particular attention is paid to three genera of advanced oviraptorosaurs for which nearly complete and articulated caudal material is known: “Ingenia” yanshini (MPC 100/30), Khaan mckennai (MPC
100/1127), and Nomingia gobiensis (MPC 100/119).
3.2 Caudal Osteology
The tail of any oviraptorosaur is reduced compared to those of most other non-avian theropods, both in terms of length relative to body size and in the total number of caudal vertebrae (which ranges from 22 vertebrae in Caudipteryx zoui to 32 in Conchoraptor gracilis). Typically, caudal centra in a non-avian theropod increase in relative anteroposterior length down the caudal series. A centrum near
89 the base of the tail in most non-avian theropods is subequal in height, width, and
length, and those near the tail tip are many times longer than they are tall or wide.
The tails of oviraptorosaurs also follow this pattern of progressive centrum elongation, but the trend is more subtle. As a result, the caudal centra of oviraptorosaurs remain dimensionally symmetrical farther down the tail, and the caudal vertebrae are therefore more densely packed. Barsbold et al. (1990) briefly noted a similar morphological pattern in oviraptorosaur caudal prezygapophyses.
Usually, the prezygapophyses of non-avian theropods increase in relative
anterior/posterior length down the caudal series - eventually developing into
long, finger-like projections that may equal or exceed the centra in length and that
flank the lateral sides of the preceding vertebrae. Among advanced coelurosaurs,
the prezygapophyses of the posterior caudal vertebrae tend to be particularly
elongate. In oviraptorosaurs (although Gigantoraptor may be an exception), the
prezygapophyses of all but the most posterior caudal vertebrae remain short
anteroposteriorly, maintain wide articular surfaces for the postzygapophyses, and
maintain a dorsal (not lateral) position relative to the preceding vertebrae. Both
the reduced lengths of centra and the short broad articular surfaces of the
prezygapophyses suggest a relatively high degree of tail flexibility per unit of
length. MPC 100/1127 (the type specimen ofKhaari) supports this inference. It
includes a nearly complete and articulated caudal series (Fig. 3.1) that is
preserved in a sinuous S-shaped curve (Clark et al., 2001).
90 FIGURE 3.1. Photograph of the type specimen Khaanof mckennai (MPC 100/1127). The nearly complete and articulated caudal series shows a graceful S- shaped curve. The anterior caudal ribs of oviraptorosaurs have greater lateral widths,
relative to the widths of their associated centra, than those of any other theropod
group. As remarked by Barsbold (1986), the caudal ribs are persistent far down
the caudal series. Anteriorly, the caudal ribs are slightly lobate and have strong posterior inclinations - roughly 65°. The relative elevation of an oviraptorosaur caudal rib is variable, but the most anterior caudal ribs are more ventrally positioned than in most other non-avian theropods. Posteriorly, the caudal ribs become gradually reduced in size, extend roughly perpendicular to the vertebral midline, and have an increasingly more ventral position. In many oviraptorosaurs,
including “Ingenia” and Khaan, the most posterior caudal ribs are T-shaped with
lateral tips that are nearly as long anteroposteriorly as the centra, and these elongated tips nearly abut with those adjacent in the series.
The chevrons of oviraptorosaurs are morphologically variable. In
Caudipteryx, the anterior chevrons are dorsoventrally tall and anteroposteriorly
narrow, while the posterior chevrons are dorsoventrally short with anteroposteriorly expanded ventral tips (overall, the posterior chevrons of
Caudipteryx are similar to those of other coelurosaurs). The chevrons of more advanced oviraptorosaurs are blade-shaped, with haemal spines that are mediolaterally compressed but anteroposteriorly broad, and that taper to a ventral point. The posterior chevrons of advanced oviraptorosaurs are present until the last few caudal vertebrae, and they are notably longer anteroposteriorly than they are tall dorsoventrally.
92 The neural spines have what is perhaps the only truly typical shape in the caudal series. They are dorsoventrally tall on the anterior vertebrae, gradually become reduced in height, and are absent on the posterior vertebrae.
3.3 Caudal Musculature
The laterally extensive and lobate caudal ribs of oviraptorosaurs indicate that the M. ilio-ischiocaudalis and M. longissimus were both greatly expanded.
The elevation of the caudal ribs (relative to other non-avian theropods) also implies a large M. longissimus. The unexceptional neural spines suggest that the
Af. spinalis was moderate in size (Fig. 3.2). The elongate lower leg bones of most oviraptorosaurs indicate a moderate degree of cursoriality, particularly in caenagnathids. Key to understanding the group’s locomotive style is assessing the size of oviraptorosaur caudofemoral musculature.
Although oviraptorosaurs lack a pronounced fourth trochanter crest, they do show marked bone rugosity at the fourth trochanter (similar to the condition in some omithomimids), which attests to the insertion of a large caudofemoral tendon. Anteriorly, the distance from the ventral surfaces of the caudal ribs to the ventral tips of the haemal spines are predictive of the overall size of the M. caudofemoralis. In oviraptorosaurs, the height of the anterior chevrons indicates a large anterior M. caudofemoralis. Many authors have commented that oviraptorosaurs lack a clear caudal “transition point” (Barsbold et al., 1990;
Osmolska et al., 2004). The caudal transition point is the region where the M. caudofemoralis is presumed to have tapered out, and is usually identified by the
93 M. spinalis Neural spine
M. longissimus
Caudal rib
M. caudofemoralis
Centrum
Haemal arch i \ M. ilio-ischiocaudalls
Haemal spine
FIGURE 3.2. First caudal vertebra and chevron of the type specimen ofNomingia gobiensis (MPC 100/119) in posterior view, with one half of caudal musculature illustrated. termination of the caudal rib series, and by an abrupt shift in the shape of the chevrons (Russell, 1972; Gatsey, 1990a). It is true that oviraptorosaur caudal ribs persist until very near the tip of the tail; however, a transition point is generally recognizable prior to the final vertebrae. In Nomingia (MPC 100/119), the last caudal rib set is present on caudal vertebra 18, caudal vertebrae 14-17 show a
94
Figure 3.3. Digital models of the caudal osteology and musculature ofKhaan (MPC 100/1127) (A), “Ingenia” yanshini (MPC 100/30) (B), and Nomingia (MPC 100/119) (C). Three stages of each reconstruction are shown: the caudal skeleton modeled based on specimen measurements; the m. caudofemoralis longus (in red) modeled over the digital skeleton; and the full muscle reconstruction (with M. spinalis, M. longissimus, M. ilio-ischiocaudalis visible) modeled over both the digital skeleton and the m. caudofemoralis longus reconstruction.
96 TABLE 3.1. Estimated caudal muscle masses of oviratorosaurs and other non-avian coelurosaurs. M. spinalis M. longissimus mass M. ilio-ischiocaudalis M. caudofemoralis “Ingenief' yanshlni MPC 100/30 89 a 660a 1220 g 1504 a Total tail muscle mass: 3473 g 2.56% 19% 35.1% 43.3% Total body mass: 17000(Paul, 2010a) 0.52% 3.88% 7.18% 8.85% Khaan mckennai MPC 100/1127 25 a 161 a 500a 569 a Total tall muscle mass: 1255 g 1.99% 12.83% 39.84% 45.34% Total body mass: 4500(Paul, g 2010b) 0.55% 3.58% 11.11% 12.64% Nomingia gobiensls MPC 100/119 145a 541 a 1299 a 2353 a Total tail muscle mass: 4338 g 3.34% 12.47% 29.64% 54.24% Total body mass: 20000(Paul, g 2010a) 0.73% 2.71% 6.50% 11.77%
Other Non-avian Theropods Gorgosaums libratus TMP 91.36.500 3900 a 6900 a 10300 a 17300 a Total tail muscle mass: 38300 g 10.2% 18.0% 26.9% 45.2% Total body mass: 400000 g 0.98% 1.73% 2.58% 4.33% Omithomimus edmontonlcus TMP 95.11.001 860 a 2440 a 5050 a 9890 g Total tail muscle mass: 18240g 4.7% 13.4% 27.7% 54.2% Total body mass: 150000 g 0.57% 1.63% 3.37% 6.59% Tyrannosaurus rex BHI3033 65200 a 154200 a 159400 a 522200 a Total tail muscle mass: 901000 g 7.2% 17.1% 17.7% 58.0% Total body mass: 5622(Paul, kg 2010b) 1.16% 2.74% 2.84% 9.29% Veloclraptor mongoliensis MPC100/986 108a 210 g 318 g 202.4 a Total tail muscle mass: 838.4 g 12.9% 25.1% 37.9% 24.1% Total body mass: 15000(Paul, g 1988) 0.7% 0.1% 2.1% 1.4%
97 pattern of rapid descent of the caudal ribs, and the associated chevrons become markedly shorter and anteroposteriorly broader. In bothKhaan and “Ingenia,” the final ribs are found on the 25th caudal vertebrae. This leaves five post-transition- point vertebrae in Nomingia, three in Khaan and four in “Ingenia”. Nevertheless, it is clear that the M. caudofemoralis of oviraptorosaurs was present through most of the caudal series.
To quantify the muscle proportions and absolute masses, the osteological muscle insertion correlates, and digital muscle modeling techniques described in
Chapter 1 were applied to the caudal series of MPC 100/30, MPC 100/119, and
MPC 100/1127 (Fig. 3.3, Table 3.1).
3.4 Discussion
Based on a suite of morphological characters, Paul (2002) argued that oviraptorosaurs are most parsimoniously interpreted as secondarily flightless.
Based on the findings of a cladistic analysis, Maryahska et al. (2002) concluded that oviraptorosaurs were not only secondarily flightless, but true members of the
Avialae. The phylogenetic position of oviraptorosaurs and the possibility that some major lineages of Mesozoic theropods were secondarily flightless are unresolved issues, and both merit serious consideration and further research.
However, the results of this study do not support the interpretation of oviraptorosaurs as secondarily flightless or as members of the Avialae.
Both oviraptorosaurs and modem aves have caudal series that can be described as “reduced”, but citing this general similarity as compelling evidence
98 for close kinship is unwarranted. The caudal anatomy of oviraptorosaurs is fundamentally dissimilar to that of modem birds and to that observed at any stage during avian evolution. Oviraptorosaurs achieved their reduced tails through the
loss of the terminal caudal vertebrae and through reduction in vertebral length
throughout the caudal series. The evolutionary sequence leading to the reduced
state observed in the tails of modem birds has been previously described (Gatesy,
1990b; Gatesy and Dial, 1996; see Chapter 4). The general sequence in avians
appears to have been: (1) reduction in the total number of caudal vertebrae
(accomplished by the loss of distal vertebrae and by the incorporation of anterior
vertebrae into the sacrum), considerable elongation of the posterior caudal
vertebrae (which, combined with the loss of caudal vertebrae, resulted in only a
slight shortening in overall caudal length), a reduction in epaxial musculature (as
indicated by a reduction in caudal rib and neural spine proportions), and a
substantial reduction in the mass of the hypaxial musculature, particularly M.the caudofemoralis (as indicated by a reduction in chevron height and the total
number of caudal rib sets) - this condition is observed in troodontids, including
the basal form, Anchiomis; (2) continued loss of caudal vertebrae and reduction in
caudal musculature - as seen in Archaeopteryx', (3) complete loss of the elongate
posterior caudal vertebrae and development of a pygostyle - as seen in
Confuciusomis and later birds (Fig. 3.4).
Oviraptorosaurs do not fit neatly into any stage of this sequence. If
oviraptorosaurs are interpreted to have a shared non-avian ancestor that is more
99 closely related toArchaeopteryx than the shared non-avian ancestor of
Deinonychosauria (as suggested by Kurzanov, 1987; Elzanowski, 1999), it must be assumed that oviraptorosaurs secondarily lost the elongate morphology of the posterior caudal vertebrae. If oviraptorosaurs are instead interpreted to have a shared avian ancestor between Archaeopteryx and Confuciusomis (as suggested by Maryahska et al., 2002), then it is necessary to assume that most oviraptorosaur genera secondarily increased the total number of caudal vertebrae.
Further, both scenarios require oviraptorosaurs to have re-evolved extended posterior caudal ribs and chevrons, along with the corresponding increases in associated muscle mass. Considered at the level of the Maniraptoriformes and based solely on the morphology of the tail, it is most parsimonious to regard oviraptorosaurs as having no close avian affinities.
The lack of a close avian relationship is not intrinsically irresolvable with the suggestion that oviraptorosaurs were secondarily flightless, especially given recent findings that show arboreal and potentially gliding/flying forms were prevalent among non-avian Maniraptoriformes (Xu et al., 2002b; Zhang et al.,
2002; Xu and Zhang, 2005; Zhang et al., 2008; Xu et al., 2010a). The reduced caudal series of birds is generally accepted to be an adaptation for flight that helped to reduce excess posterior weight. In particular, the reduction of theM. caudofemoralis was a direct loss of hind-limb locomotive musculature that coincided with increased emphasis and reliance on forelimb-powered flight. The
M. caudofemoralis of pterosaurs was similarly reduced (see Chapter 4).
Maryahska et al. (2002) asserted that oviraptorosaurs had greatly reduced caudal
100 1 cm
B
1 cm
C.
1 cm
D.
10 cm
FIGURE 3.4. Comparison of the caudal and pelvic skeletons of the primitive deinonychosaurAnchiomis (A), the primitive bird Archaeopteryx (B), the pygostyle-bearing birdConfuciusomis (C), and the oviraptorosaur Khaan (D).
101 masses, a resulting center of mass positioned well anterior to the hips, and a terrestrial locomotive style similar to that of modem cursorial birds that placed greater emphasis on knee-flexion than on femoral retraction. The results of the digital muscle reconstructions indicate the opposite.
Most oviraptorosaurs did not have a M. caudofemoralis that was proportionately small. Muscle mass reduction in oviraptorosaur tails was limited to the region posterior to the caudal transition point. Despite the reduced lengths of the anterior caudal vertebrae, robust caudofemoral musculature was supported by additional posterior caudal ribs and extended chevrons. This suggests that the mass of the M. caudofemoralis was being selectively maintained during oviraptorosaur tail evolution. Retention of powerful femoral retractor muscles is inconsistent with the morphology predicted by the secondarily flightless hypotheses. The digital modeling results also confirm that, anteriorly, both theM. longissimus and M. ilio-ischiocaudalis were exceptionally large in oviraptorosaurs. Overall, oviraptorosaur tails appear to have been short but stocky, and it is likely that most oviraptorosaurs had a center of mass that was only slightly more anterior than those of most other non-avian theropods. Based on these results, there is no reason to suspect most oviraptorosaurs diverged from the standard femoral-retraction-dominated locomotive style, or to evoke a flying ancestor as an explanation for the uniqueness of the caudal morphology.
That said, however, it must be pointed out that the tail of the primitive oviraptorosaur Caudipteryx is far more reduced than that of other oviraptorosaurs and is likely a partial exception to the previously described general structure.
102 While the caudal reduction observed in Caudipteryx is highly disparate from the deinonychosaurian condition andCaudipteryx does have deep anterior chevrons, the reduction in tail length is so extreme that the size ofM. caudofemoralis must have been affected. As argued by Jones et al. (2000), the proportions of the hindlegs of Caudipteryx are also consistent with greater relative emphasis on knee flexion and less emphasis on femoral retraction. It does, therefore, remain a possible alternative that early oviraptorosaurs diverged from an arboreal flying/gliding maniraptorian ancestor, which was not close to the deinonychosaurian linage and which had only just begun caudofemoral muscle reduction, and that, after becoming secondarily terrestrial, later oviraptorosaurs secondarily re-enlarged theM. caudofemoralis. The exact phylogenetic position of Caudipteryx is not clear, and evaluation of this highly speculative scenario must await additional fossil evidence.
The large sizes of the M. caudofemoralis in most oviraptorosaurs are consistent with the high degree of cursoriality inferred for the group. However, the M. longissimus and M. ilio-ischiocaudalis function in controlling tail motion rather than femoral retraction, and the large anterior size of both these muscles
still merits functional explanation. Barsbold (1977,1983) previously recognized the highly muscular nature of oviraptorosaur tails, and speculated that they may have been adapted for aquatic sculling. A swimming explanation is consistent
with both a robust M. longissimus and M. ilio-ischiocaudalis, which are responsible for laterally swinging the tail and are large in many modem aquatic reptiles, and with the highly flexible nature of the oviraptorosaur caudal series.
103 However, as later pointed out by Barsbold et al. (1990), the cursorial hindlimbs of oviraptorosaurs were inconsistent with an aquatic lifestyle. Moreover, the reduced tail length, un-heightened neural spines, and lack of lateral compression strongly contradict the notion that oviraptorosaur tails were adapted for swimming.
Furthermore, the majority of oviraptorosaurs are associated with arid to semi-arid environments (Longrich et al., 2010).
An alternative explanation is that the tails of oviraptorosaurs served to facilitate effective cursoriality but were also highly specialized to serve as visual display structures. Specimens of the primitive oviraptorosaursCaudipteryx (Ji et al., 1998) and Similicaudipteryx (Xu et al., 2010b) include preserved fans of feathers on the terminal tail tips. As in birds, Similicaudipteryx has a specialized pygostyle to serve as an anchor for the feather fan, whileCaudipteryx has a feather fan but lacks a pygostyle. The advanced oviraptorosaurNomingia also has a terminal pygostyle that presumably supported tail feathers of its own and suggests that caudal feather fans were prevalent throughout oviraptorosaurs.
Short, muscular, and highly-flexible tails would have been well suited to flaunt these fans. Oviraptorosaurs would have been capable of twisting and swinging their tails laterally and dorsally to strike and hold the posterior tail feathers in desired poses. Such dexterous caudal displays could have been used in intraspecific communication, including courtship rituals — a common function of caudal plumage in modem birds. It follows that the caudal morphology of oviraptorosaurs may prove to be sexually dimorphic, although, at present, the sample size for any oviraptorosaur species is insufficient to test this prediction.
104 The results of the digital modeling confirm that oviraptorosaurs had muscularly robust tails. Unlike the condition observed in the avian lineage, oviraptorosaurs maintained large caudofemoral tail muscles, which suggests the anterior tail region never lost its primary function in terrestrial locomotion throughout the evolutionary history of the group. In addition, muscles responsible for controlling tail motion were proportionately larger in oviraptorosaurs than in other theropods, and oviraptorosaur tails were also exceptionally flexible. A terminal tail-feather fan appears to have been a common feature among oviraptorosaurs, and the muscular and flexible tails would have permitted these fans to be flaunted in dynamic displays. This new functional interpretation, combined with the prevalence of cranial crests among the oviraptorosaurs, suggests the group had a propensity for visual exhibition.
3.5 Bibliography
Arbour, V.M. 2009. Estimating impact forces of tail club strikes by ankylosaurid
dinosaurs. PLoS ONE 4(8): e6738.
Barsbold, R. 1977. Kinetism and peculiarity of the jaw apparatus of oviraptors
(Theropoda, Saurischia). Soviet-Mongolian Paleontological Expedition,
Turdy 4: 37-47 (in Russian with English summary).
105 Barsbold, R. 1983. Carnivorous dinosaurs from the Cretaceous of Mongolia.
Soviet-Mongolian Paleontological Expedition, 19: Turdy 1-117 (in
Russian with English summary).
Barsbold, R. 1986. Raubdinosaurier Oviraptoren. In E.I. Vorobyeva (ed.)
Herpetologische Untersuchungen in der Mongolischen Volksrepublik,
210-223. Nauk S.S.R. Inst. Evolyucionnoy Morfologii I Ekologii
Zhivotnykh im. A.M. Servertsova, Moskva (in Russian).
Barsbold, R., Currie P.J., Myhrvold, N.P., Osmolska, H., Tsogtbaatar, K, and
Watabe, M. 2000. A pygostyle from a non-avian theropod.Nature 403:
155-156.
Barsbold, R., Maryahska, T., Osmolska, H. 1990. Oviraptorosauria. In D.B.
Weishampel, P. Dodson, and H. Osmolska (eds.), The Dinosauria (first
edition), 249-258. Berkeley: University of California Press.
Clark, J.M., Norell, M.A., and Barsbold, R. 2001. Two new oviraptorids
(Theropoda: Oviraptorosauria), Upper Cretaceous Djadokhta Formation,
Ukhaa Tolgod, Mongolia. Journal of Vertebrate Paleontology 21(2): 209-
213.
Elzanowski, A. 1999. A comparison of the jaw skeleton in theropods and birds,
with a description of the palate in the Oviraptoridae. In: Olson ST (ed.),
106 Avian Paleontology at the Close of the 20th Century: Proceedings of the 4th
International Meeting of the Society of Avian Paleontology and Evolution,
Washington D.C., 4-7 June 1996. Smithsonian Contributions to
Paleobiology 89 (14): 311-323.
Gatesy, S.M. 1990a. Caudefemoral musculature and the evolution of theropod
locomotion. Paleobiology 16(2): 170-186.
Gatesy, S.M. 1990b. The evolutionary history of the theropod caudal locomotor
module. In J. Gauthier and L.F. Gall (eds.), New Perspectives on the
Origin and Evolution of Birds, 333-346. Connecticut: Peabody Museum of
Natural History.
Gatesy, S.M. 1997. An electromyographic analysis of hindlimb function in
Alligator during terrestrial locomotion. Journal of Morphology, 234:197-
212.
Gatesy, S.M., and Dial, K.P. 1996. From frond to fan:Archaeopteryx and the
evolution of short-tailed birds. Evolution 50(5): 2037-2048.
Ji, Q., Currie, P.J., Norell, M.A., and Ji, S.-A. 1998. Two feathered dinosaurs
from northeastern China. Nature 393:753-761.
107 Kurzanov, S.M. 1987. Avimimidae and the problem of the origin of birds.
Transactions of the Joint Soviet-Mongolian Paleontological Expedition 32:
5-92.
Longrich, N.R., Currie, P.J., and Dong Z.-M. 2010. A new oviraptorid
(Dinosauria: Theropoda) from the Upper Cretaceous of Bayan Mandahu,
Inner Mongolia. Palaeontology 53: 945-960.
Lii, J., Dong, Z., Azuma, Y., Barsbold, R., and Timida, Y. 2002. Oviraptorosaurs
compared to birds. In: Z. Zhou and F. Zhang (eds.), Proceedings of the th5
Symposium of the Society of Avian Paleontology and Evolution, Beijing, 1-4
June 2000. Beijing, China: Science Press.
Maryanska, T., Osmdlska, H., and Wolsam, M. 2002. Avialan status for
Oviraptorosauria. Acta Palaeontologica Polonica (1): 97-116.
Osmdlska, H., Currie, P.J., Barsbold, R. 2004. Oviraptorosauria. In: D.B.
Weishampel, P. Dodson, H. Osmolska (eds.), The Dinosauria (second
edition). Edited by. Berkeley: University of California Press, 7-19.
Paul, G.S. 1988. Predatory Dinosaurs of the World. New York: Simon and
Schuster.
Paul, G.S. 2002. Dinosaurs of the Air. Baltimore and London: The Johns Hopkins
University Press.
108 Paul, G.S. 2010b. Dinosaur Mass Estimate Table [online]. Available from
http://gspauldino.com/data.html [cited 1 December 2010].
Paul, G.S. 2010a. The Princeton Field Guide to Dinosaurs. New Jersey: Princeton
University Press.
Russell, D.A. 1972. Ostrich dinosaurs from the late Cretaceous of western
Canada. Canadian Journal of Earth Sciences 9: 375-402.
Snyder, R.C. 1962. Adaptations for bipedal locomotion of lizards.American
Zoologist 191-203.
Xu, X., Cheng, Y.-N., Wang, X.-L., and Chang, C.-H. 2002a. An unusual
oviraptorosaurian dinosaur from China. Nature 419: 291-293.
Xu, X., Ma, Q.Y., and Hu, D.Y. 2010a. Pre-Archaeopteryx coelurosaurian
dinosaurs and their implications for understanding avian origins. Chinese
Science Bulletin 55: 1-7, doi: 10.1007/sll434-010-4150-z.
Xu, X., Tan, Q. Wang, J., Zhao, X., and Tan, L. 2007. A gigantic bird-like
dinosaur from the Late Cretaceous of China. Nature 447: 844-847.
Xu, X. Zhang F, 2005. A new maniraptoran dinosaur from China with long
feathers on the metatarsus. Naturwissenschaften 92(4): 173-177.
Xu X., Zheng, X., and You, H. 2010b. Exceptional dinosaur fossils show
ontogenetic development of early feathers.Nature 464: 1338-1341.
109 Xu, X., Zhou, Z., Wang, X., Kuang, X., Zhang, F., and Du, X. 2002b. Four
winged dinosaurs from China. Nature 421: 335-340.
Zhang, F., Zhou, Z., Xu, X., and Wang, X. 2002. A juvenile coelurosaurian
theropod from China indicates arboreal habits. Naturwissenschaften 89(9):
394-398.
Zhang, F., Zhou, Z., Xu, X., Wang, X., and Sullivan, C. 2008. A bizarre Jurassic
maniraptoran from China with elongate ribbon-like feathers. Nature 455:
1105-1108.
110 Chapter 4 Dragon Tails: Convergent Caudal Morphology in Winged
Archosaurs*
4.1 Introduction
The remarkable morphological convergence between the caudal osteology of dromaeosaurid dinosaurs and rhamphorhynchid pterosaurs was first noted by
John Ostrom in his classic description ofDeinonychus antirrhops (Ostrom, 1969).
Ostrom recognized that a similar morphology is found in no other living or extinct group, and he expressed an intention to study this parallel adaptation further.
Regrettably, Ostrom never followed through with these plans. Here, the caudal osteology and inferred musculature of both dromaeosaurids and rhamphorhynchoids is considered in terms of functional morphology, and an effort is made to place each in broader evolutionary context. Note: as used here, the term “rhamphorhynchoids” refers to all caudal rod-bearing non-pterodactyloid pterosaurs more closely related toRhamphorhynchus than to Dimorphodon.
Dromaeosaurids have long been recognized as among the most bird-like of the non-avian dinosaurs, although the exact relationship between dromaeosaurids and birds remains unclear (Ostrom, 1973; Bakker, 1975; Gauthier, 1986; Padian and
Chiappe, 1998; Norell et al., 2001). Considered at the scale of overall archosaur evolution, rhamphorhynchids and dromaeosaurids are only distantly related.
*A version of this chapter has been submitted for publication. Persons 2012. Acta Geologica Sinica 86(1).
I ll Although the magnitude of this distance varies considerably depending on the choice of phylogenetic scheme, with the position of pterosaurs potentially shifting from the sister group of Dinosauromorpha (as argued by Gauthier, 1984,
1986; Padian, 1984; Sereno, 1991; Benton, 2004) to amongst more basal archosauromorphs (as argued by Bennett, 1995,1996; Wellnhoffer 1991).
Regardless, the evolutionary expanse separating dromaeosaurids and rhamphorhynchids makes the strong morphological similarities between the unusual caudal osteology of both groups all the more extraordinary.
Both dromaeosaurids and rhamphorhynchids have a lengthy caudal series
(generally accounting for no less than 50% of the total length of the animal). The most anterior vertebrae of both groups support caudal ribs that are positioned dorsoventrally low on the centrum and that become rapidly reduced in size down the caudal series (along with the neural spines and chevrons). The more posterior caudal vertebrae (starting at anywhere from the sixth to the twelfth vertebra, depending upon the species) have no neural spines, no caudal ribs, elongate centra, and chevrons that are short dorsoventrally with anteroposteriorly elongate ventral tips (Fig. 4.1). As Ostrom noted, the most striking similarities are the rod like extensions that originate from the tips of the posterior prezygapophyses and the anterior tips of the posterior chevrons (Ostrom, 1969). The lengths of these rod-like prezygapophysis and chevron extensions, hereafter referred to as “caudal rods”, varies along the caudal series, but the caudal rods often span more than six vertebral centra in length. In both dromaeosaurids and rhamphorhynchids, each prezygapophysis rod bifurcates posteriorly. In dromaeosaurids the chevron rods
112 1 cm
FIGURE 4.1. Comparison between the mid-caudal osteology ofRhamphorhynchus (A lateral view, B dorsal view, C lateral view) and Deinonychus (D lateral view, E dorsal view, F lateral view). Images based on Wellmhofer (1991) and Ostrom (1969). Abbreviations:
113 ce - centrum; ch - body of the chevron; chr - chevron rod; po - body of the postzygapophysis; pr - body of the prezygapophysis; prr - prezygapophyseal rod.
114 also bifurcate. The result is a bilaterally symmetrical dorsal and ventral quiver of caudal rods extending in parallel along the tail, with the dorsal quiver tightly flanking the neural arches and the ventral quiver tightly flanking the haemal arches. It should be noted that caudal rods are also present in the tails of the dimorphodontid pterosaurs but are absent in the greatly reduced tails of the
Anurognathidae (Bennett, 2007), and recent work has shown the rods are absent in several of the earliest non-pterodactyloid pterosaurs, includingAustriadactylus,
Eudimorphodoti, and Preondactylus (Dalla Vecchia, 2001, 2003).
Functional theories proposed to explain the evolution of this odd caudal morphology have generally focused on the possible role the caudal rods served in increasing overall tail stiffness. In the case of dromaeosaurids, the posterior portion of the tail has been compared to the balancing pole of a tightrope walker
and argued to have aided in maintaining balance during irregular movements
involved in pursuing and subduing prey (Ostrom, 1969). The tails of caudal-rod- bearing pterosaurs have been interpreted as flight stabilizers (Unwin, 2006) and/or
as aerial rudders useful for steering, especially in taxa with diamond-shaped flaps
of skin at the posterior tail tips (Wellnhofer, 1991; Frey et al., 2003).
Such theories are faced with what seem to be inherent functional contradictions. The caudal rods of both groups overlap multiple vertebrae, and
must, therefore, have impeded tail flexibility (past the most anterior caudals, even moderate inter-vertebral flexing would require multiple caudal rods to be physically bent). However, the caudal vertebrae are not fused to one another as would be expected of a “truly” rigid tail, and the articular facets of the
115 zygapophyses are suited to permit reasonable mobility. To resolve these contradictions, it has been suggested that the caudal rods of dromaeosaurids and rhamphorhynchids might have provided “elastic” rigidity so that the tails could be flexed in any direction but would then spring back to their original straight shape
(Wellnhofer, 1991; Unwin, 2006). It has also been suggested that the stiffening effect of the caudal rods was controlled by tail muscles that when contracted held the caudal rods tightly against the vertebral column to increase rigidity but, when relaxed, permitted a reasonable degree of flexibility (Ostrom, 1969).
4.2 Materials and Methods
Detailed measurements were taken of the caudal, hind limb, and pelvic osteology of MPC100/986 (Velociraptor mongoliensis) and TMP 2008.041.0001
(Rhamphorhynchus muensteri) (Fig. 4.2). Each of these specimens includes a pristinely preserved and articulated caudal series with undisturbed caudal rods in their natural positions, and each has a tail morphology that is typical of its respective group. The caudal series of TMP 2008.041.0001 is complete; however,
MPC 100/986 lacks the distal tip of the caudal series, and measurements of
MPC 100/986 had to be supplemented with those taken from the slightly larger
Velociraptor specimen MPC 100/25 and scaled to fit. These data were used as the basis for creating two digital skeletal models.
To assess the relative and absolute mass of the caudal musculature of
Velociraptor and Rhamphorhynchus, the primary caudal muscle sets (M.spinalis,
M. longissimus, M. ilio-ischiocaudalis, and M. caudofemoralis) were digitally
116 FIGURE 4.2. TMP 2008.041.0001 (Rhamphorhynchus muensteri)
sculpted over the skeletal models, following the osteological correlates and
technique outlined in Persons and Currie (2011), which were shown to be
accurate for a range of modem reptilian taxa. The volume of each digital muscle
model was then determined and, assuming a standard muscle density of 1.06
g em'3, the mass of each independent muscle was calculated. All digital models
were created using the modeling software Rhinoceros® (McNeel Robert &
Associates, 2007).
The small size and intrinsic delicacy of most rhamphorhynchid skeletons
makes the fossil specimens prone to vertical compaction. This problem is
compounded because only one side of the caudal series is usually prepared and
117 available for examination. However, the larger and more robust bones of dromaeosaurids are more resistant to taphonomic deformation, and in rare
instances the caudal series is undistorted and three-dimensionally prepared. Such
specimens most commonly have an unbent caudal series, but some show evidence of a strong natural flexure. MPC100/986, MPC100/25, and AMNH001 (Fig. 4.3) each includes an articulated and three-dimensionally preserved caudal series.
These specimens were examined to assess the degree of apparent flexibility and to verify that the caudal rods of each had conformed to any flexure without injury.
TMP 1982.26.1 and TMP 1988.121.39 (Fig. 4.3) are partially disarticulated caudal series of Sauromitholestes, and provide evidence of the degree of individual caudal rod flexibility.
The stiffening effect of the caudal rods was not necessarily uniform in all directions. While any bending at a particular point along the posterior tail region would require an equal number of caudal rods to bend, the cumulative thickness of the rods would vary with respect to their arrangement and to the orientation of the bend. To test for a difference in lateral vs. dorsoventral flexibility, the maximum lateral and dorsoventral caudal rod thicknesses were measured from three cross-sections made through the articulated tail of YPM 5202 (Deinonychus antirrhopus). These cross-sections were originally described by Ostrom, 1969.
The right side of the tail of YPM 5202 is better preserved than the left, and it was assumed that the number and arrangement of the caudal rods was bilaterally symmetrical.
118 The measured thicknesses were averaged to obtain an average lateral and an average dorsoventral thickness. The area moment of inertia is a cross-sectional property that expresses the ability of a beam to resist bending. Using Equation 1 and Equation 2, the average area moment of inertia was calculated for tail flexure in both the lateral and dorsoventral dimensions, where Ix is the lateral area moment of inertia, Iy is the dorsoventral area moment of inertia, x is the average lateral thickness, and y is the average dorsoventral thickness.
3 Equation 1. Ix = yx /12
Equation 2. Iy = xy /12 '
119 10 cm
FIGURE 4.3. Dromaeosaurid specimens used in assessing caudal flexibility: Velociraptor MPC 100/25 in left lateral views (A, B); Velociraptor MPC 100/986 in dorsal view (C); Bambiraptor AMNH001 in ventral view (D); Sauromitholestes TMP 1988.121.39 overview (E) and close-up of chevron rods in flexed position (F).
120 4.3 Results
The results of the digital muscle modeling (Fig. 4.4,4.5) are compared with the estimated muscle masses to those previously calculated for other theropod taxa and measured in modem reptiles (Table 4.1). The results indicate that both dromaeosaurids and rhamphorhynchids have relatively light caudal musculature and particularly small caudofemoral muscles.
The degree of tail flexibility observed in MPC 100/25, MPC 100/986, and
AMNH 001 is not the result of a damaging or disruptive taphonomic history, as evidenced by the pristine condition of the many delicate portions of the caudal osteology. Whether or not each tail was curved prior to or shortly following death is unknown. In all cases, the vertebral series are still intact, with all zygapophysial facets in correct articulation. Although some of the caudal rods do show dorsoventral hairline fractures, all breaks in the caudal rods appear to have occurred post-fossilization and many of the caudal rods remain unbroken. The most strongly bent caudal rods are those on the disarticulated series of TMP
1988.121.39. As described in Norell and Makovicky (1999), MPC100/986 shows the greatest degree of articulated tail flexure, and demonstrates unequivocally that the tail of Velociraptor was capable of simultaneously bending in multiple directions at different points. That the sinuous tail shape of MPC 100/986 was retained postmortem suggests that the caudal rods were not as elastic as some previous speculation assumed. Similarly, the caudal rods of all the articulated specimens are preserved in tight contact with the neural and haemal arches,
121 regardless of the degree of tail curvature. This casts doubt on the notion that the positions of the rods could be slackened by muscle action.
The results of the moment of inertia calculations (Table 4.2) show that the tail of Deinonychus was roughly seven times more resistant to dorsoventral than lateral bending.
122 FIGURE 4.4. Stages in modeling the tail of Rhamphorhynchus muensteri (TMP 2008.041.0001) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (C).
123 s i j a u t
FIGURE 4.5. Stages in modeling the tail of Velociraptor mongoliensis (MPC 100/986) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (C).
124 TABLE 4.1. Results of caudal muscle mass reconstructions for Velociraptor and Rhamphorhynchus. M. spinalis M. longissimus M. ilio-ischiocaudalis M.caudofemoralis Velociraptor mongollensis MPC100/986 108 a 210 g 318 a 202 a Total tail muscle mass: 838.4 g 12.9% 25.1% 37.9% 24.1% Total body mass: 24000 g (Paul, 2010) 0.5% 0.9% 1.3% 0.8% Rhamphorhynchus muensteri TMP 2008.041.0001 0.4 a 1-2 a 2.7 g 0.3 g Total tail muscle mass: 4.6 g 8.7% 26.1% 58.9% 6.5% Total body mass: 280 g (Prondvai et a!., 2008) 0.1% 0.4% 0.9% 0.1%
TABLE 4.2. Mid-caudal cross-section measurements of YMP 5202 (Deinonychus antirrhopus). Average thickness Average moment of inertia (mm) (mm4) Lateral 20 30000 Dorsoventral 53 250000
125 4.4 Muscle Mass and Flexibility
The caudal muscle masses of Velociraptor and Rhamphorhynchus are estimated to be relatively much lower than all other taxa presented in Table 4.1.
This is primarily due to the abrupt reduction of the caudal ribs, neural spines, and chevrons that occurs down the anterior caudal vertebrae. This morphology is consistent in all known dromaeosaurids and rhamphorhynchids. While both groups have lengthy caudal series, the vertebrae beyond the first 5-11 caudal vertebrae are narrow and gracile. Given that most caudal muscle sets function primarily in swinging, curling, straightening, or stiffening the tail, it is not surprising that the lightweight tail osteology of dromaeosaurids and rhamphorhynchids required proportionately lean tail musculature. However, the similarity in the reduced size of theM. caudofemoralis in both groups merits particular consideration.
The M. caudofemoralis originates on the most anterior caudal vertebrae and inserts onto the femur (usually the fourth trochanter is the insertion site, however a true forth trochanter is absent in many birds and pterosaurs and is reduced to a simple rugosity in many dromaeosaurs) and functions primarily in femoral retraction, but not in controlling tail motion. In most saurian taxa, the M. caudofemoralis is the primary and largest hindlimb muscle (Snyder, 1962;
Gatesy, 1990, 1997). Gatesy (1990,1999) concluded that the rapid reduction in caudal rib width indicated a reduced M. caudofemoralis in dromaeosaurids, but argued that caudofemoral muscle reduction was a trend throughout the evolution of coelurosaurian theropods. However, recent assessments of the M.
126 caudofemoralis in some advanced coelurosaurs (Persons and Currie, 2011)
indicate that no such general trend was prevalent and affirm that reduced
caudofemoral muscle mass was more the exception than the rule. The position of
the most anterior caudal ribs of dromaeosaurids on the lateral faces of the centra is
also noteworthy. Caudal ribs positioned high on the neural arches of anterior caudal vertebrae are present in basal theropod dinosaurs, and this elevated position provided extra room for relatively large caudofemoral muscles (Persons
and Currie, 2011). The low elevations of dromaeosaurid caudal ribs are indicative of a reduced M. caudofemoralis, which is a reversion to the primitive archosaur condition. Regardless of their exact phylogenetic placement, early pterosaurs (as saurians) must have also descended from an ancestor with substantial caudofemoral muscle mass.
Why, then, did both groups so radically reduce the size of what had been the dominant locomotive muscle set? For rhamphorhynchids, the answer seems obvious: it was probably because ancestrally the group’s primary means of locomotion shifted to forelimb-powered flight. Large caudofemoral muscles would have been of no use to rhamphorhynchids while in the air, and the extra rear-positioned weight of these muscles could have been a severe hindrance. The aerial lifestyle of rhamphorhynchids also explains the overall gracile and lightweight morphology of the more posterior caudal vertebrae. Explaining why
such a caudal muscle reduction is seen in dromaeosaurids, a group composed largely of terrestrial (and in many cases highly cursorial) animals is more difficult.
127 All bones have a degree of flexibility, and it is clear that an individual caudal rod of a dromaeosaurid was flexible along its length and entirely capable of bending without breaking. Nevertheless, the results of this study suggest that the classic interpretation of the caudal rods as tail stiffeners is correct, but the rigidity afforded by the rods was highly anisotropic. Lateral tail flexing remained possible down the entire caudal series, but dorsoventral tail flexibility was severely hampered in the posterior portion of the tail. The caudal rods of dromaeosaurids were not bundled together in an irregular mass along the tail.
Rather, the rods were stacked in parallel dorsoventrally (Fig. 4.5). This arrangement is responsible for the higher calculated dorsoventral vs. lateral moment of inertia. Relatively greater lateral flexibility is also suggested by the articulated dromaeosaurid specimens with tails. As noted respectively by Norell and Makovicky (1999) and Burnham (2003), the tails of MPC 100/986 and
AMNH 001 show clear evidence of having assumed lateral curvature prior to fossilization and attest that the caudal rods were little hindrance to lateral
movement. Only MPC 100/25 is curved dorsally, and most of the dorsal curvature is the result of a strong bend in the first five caudal vertebrae, which lack
overlapping caudal rods. Past the fifth caudal vertebra, the degree of tail curvature
is suddenly and dramatically reduced.
Hwang et al. (2002) argued that the tail of CAGS 20-8-004 ( Microraptor)
lacked the same degree of flexibility observed in MPC 100/986, because broken
and displaced caudal rods surrounded a posterior bend in the tail of CAGS 20-8-
004. Hwang et al. (2002) suggested that, due to allometry, the smaller caudal rods
128 of Microraptor imparted proportionately greater caudal stiffness. It may well be true that allometric properties caused the stiffening effect of the caudal rods to be proportionately greater in smaller dromaeosaurids (although the high degree of caudal rod flexibility observed in the tail of tinyBambiraptor AMNH 001 is evidence against this), but more important is the observation that the bend in the tail of CAGS 20-8-004 is ventral, not lateral. The uniformly rigid balancing pole of a tight-rope walker is a deceptive analog for the tail of a dromaeosaurid. A better analogy would be a slat of bamboo or a thin wooden meter-stick, which may be bent with moderate force, but only perpendicular to the broadest plane.
Caution is warranted in using the articulated caudal series of dromaeosaurid specimens to infer the degree of flexibility possible in the tails of rhamphorhynchids. Rhamphorhynchid specimens that show unbroken and laterally flexed caudal series have not been documented. As described earlier, this may be the result of preservational bias, or it may be that the caudal rods of rhamphorhynchids were intrinsically less flexible than those of dromaeosaurids.
However, rhamphorhynchids did have the same dorsoventrally stacked caudal-rod arrangement as dromaeosaurids, and this does indicate a similarly greater degree of dorsoventral stiffness.
In considering the function of the caudal rods, the question should be changed from “why did both groups evolve stiffened tails?” to “why did both groups evolve preferentially dorsoventrally stiffened tails?” Again, prescribing a functional explanation is easier in the case of rhamphorhynchids. For a flying vertebrate, a long and lightly muscled tail poses a potential problem. While
129 FIGURE. 4.6. Restored mid-tail cross-section of Deinonychus. Abbreviations: ce - centrum; ch - body of the chevron; chr - chevron rod; nc - neural chanal; pr - body of the prezygapophysis; prr - prezygapophyseal rod.
130 airborne, such a tail would be inclined to slacken and become ventrally deflected by the constant pull of gravity. A limp tail would disrupt the otherwise
streamlined body-posture and create unwanted drag. The evolution of caudal rods in rhamphorhynchids would have prevented the tails from sagging while still allowing the tails to bend and swing laterally - movements that would have been important for maneuverability, particularly if the terminal tail flaps were dorsoventrally oriented and were able to serve as rudders. In a terrestrial animal, the need to reduce posterior tail slacking (beyond preventing the tail tip from dragging the ground) would not be as great, as the absence of caudal rods in the wide range of other long-tailed terrestrial archosaur taxa suggests.
4.5 Evolutionary Context
The striking similarity in form between the odd caudal osteology and musculature of dromaeosaurids and rhamphorhynchids strongly indicates a similarity in function. A thin light-weight tail with reduced caudofemoral musculature that preferentially retains lateral flexibility while increasing dorsoventral rigidity is well suited for a flying or gliding animal. That many of the oldest known pterosaurs lacked caudal rods indicates that rhamphorhynchoid caudal rods evolved in the context of an aerial lifestyle, and not prior to the evolution of pterosaur flight. This suggests the possibility that the caudal rods and overall caudal morphology of dromaeosaurids also evolved as adaptations to life on the wing. That the majority of known dromaeosaurids were secondarily flightless has been previously proposed (Paul, 1988, 2002; Olshevsky, 1994;
131 Mayr, 2005), and a number of other unusual features of some dromaeosaurids have been interpreted as evidence of a flying ancestor, including a U-shaped furcula, a well developed acromion process, retroverted coracoids, ossified uncinate processes, a large ossified sternum, and ossified sternal ribs (Paul, 2002).
Recent discoveries of theropod specimens with impressions of long feathers behind the arms have strengthened this case. (Note: arguments made explicitly favoring the interpretation of some dromaeosaurids and other deinonychosaurs as secondarily flightless should not be confused with advocacy for the now archaic notion that modem birds lack a definitively dinosaurian ancestry.)
Microraptor from the Jiufotang Formation (minimally aged at 120 Ma) is currently among the oldest known dromaeosaurid (He et al., 2004). The elongate fore- and hindlimb feathers of Microraptor are strong evidence that it had an aerial lifestyle, although debate continues regarding whether it was capable of tme powered flight or only tree-to-tree gliding (Xu et al., 2003; Chatterjee and
Templin, 2006; Alexander et al., 2010). The oldest currently known member of the Deinonychosauria (Dromaeosauridae and Troodontidae) isAnchiornis from the Tiaojishan Formation (approximately 161-151 Ma) (Hu et al., 2009). Like
Microraptor, a specimen ofAnchiornis includes direct evidence of long feathers that are indicative of flying or gliding capabilities. However, whereas
Microraptor has the typical dromaeosaurid caudal morphology, the tail of
Anchiornis has no caudal rods, although the tail osteology ofAnchiornis is lightweight and does show clear signs of reduced caudofemoral muscle mass.
Anchiornis has been classified as a troodontid (Hu et al., 2009; Xu et al., 2010),
132 but if it is taken to represent the basal deinonychosaur condition, the most
parsimonious reconstruction of dromaeosaurid tail evolution would place the
development of caudal rods somewhere between Anchiornis and Microraptor,
with the rods simply being retained in later secondarily more terrestrial forms.
The pterosaurDarwinopterus has been interpreted as a transitional form
between the rhamphorhynchids and the Pterodactyloidea (Lii et al., 2010). As
such, the presence of caudal rods in the tail ofDarwinopterus is evidence that the
rods were secondarily lost in pterodactyloids (presumably this loss coincided with
the overall reduction of the caudal series). Given the close relationship between
dromaeosaurids and birds, this raises the question: did the avian lineage also
progress through a caudal-rod-bearing stage prior to the reduced caudal series
observed in modem forms? The answer to this question appears to be a decisive
“no.” The oldest known bird, Archaeopteryx has a caudal series of moderate
length, but with no evidence of caudal rods. Overall, the caudal osteology of
Archaeopteryx closely resembles that ofAnchiornis or other troodontids (Fig.
4.7). Caudal rods help to confirm the phylogenetic placement of dromaeosaurids
near, but not directly ancestral to, modem Aves.
The reduction of the M. caudofemoralis was taken to an extreme in
advanced pterosaurs, with pterodactyloids, likePterodactylus and Pterodaustro
having a caudal series only 13 and 22 vertebrae long, respectively, and with no
caudal ribs (Wellnhofer, 1991; Codomiu and Chiappe, 2004). In modem birds,
the M. caudofemoralis is often absent entirely, as is the case in many ratites and
vultures (Gatesy, 1990). However, the two archosaur lineages differed in how
133 FIGURE 4.7. Comparison between the mid-caudal osteology of the early pterosaurEudimorphodon ranzii (A), the troodontid Mei long (B), and the early bird Archaeopteryx lithographica (C) (images not to scale).
they compensated for a reduction in what had been the primary locomotive muscle set. Pterosaurs largely abandoned the terrestrial usefulness of the hind limbs, which became reduced in overall mass and were tethered to the body by the wing patagium (Elgin et al., 2011). In birds and deinonychosaurs, the hind limbs remained relatively large and long, and more anteriorly positioned muscle
sets became enlarged. Birds and deinonychosaurs developed the “Groucho running” style (McMahon et al., 1987), which required less femoral retraction and placed greater emphasis on knee flexors (Gatesy, 1990a, 1990b, 1999; Farlow et
al., 2000). Although it has been recently proposed that many pterosaurs were able to predominantly rely on their stronger forelimbs for terrestrial locomotion (Habib
2008; Witton and Naish, 2008), the lack of well-developed hind limbs may, as previously proposed by Unwin (1997), have limited the group’s ability to later
134 invade terrestrial and aquatic niches (something birds were repeatedly successful at).
After the reduction of the caudofemoral musculature, the tails of birds remained important to locomotion. The evolution of a pygostyle, which supported a fan of caudal feathers, allowed caudal muscles to aid in aerial maneuverability
(Gatesy 1990b, 1999; Gatesy and Dial, 1996). The tails of most pterodactyloids appear to have been largely vestigial; however, the unique tail of the advanced omithocheiroid Pteranodon may be an exception. As described by Bennett (1987,
2001) the caudal series of Pteranodon consists of an anterior vertebral segment that is highly flexible dorsoventrally and highly inflexible laterally, and of posterior vertebrae that are anteroposteriorly elongate and fused. Bennett (1987) argued that this strange tail may have been an attachment site for the wing membrane. Most probably, the tail supported a small uropatagium, which could have been raised and lowered independently of the cruropatagium, giving the tail subtle control over posterior drag. If this was the case, the cruropatagium- supporting, fused caudals ofPteranodon may be thought of as a pterosaurian pygostyle.
4.6 Bibliography
Alexander, D.E., Gong E., Martin, L.D., Burnham, L.D., and Falk, A.R., 2010. Model tests of gliding with different hindwing configurations in the four winged dromaeosaurid Microraptor gui. PNAS, 107 (7): 2972-2976.
Bakker, R.T., 1975. Dinosaur renaissance. Scientific American, 232: 58-78.
Bennett SC. 1987. New evidence on the tail of pterosaur Pteranodon (Archosauria: Pterosauris). In: Currie, P.J., and Koster E.H. (eds), Fourth
135 Symposium on Mesozoic Terrestrial Ecosystems, Short Papers. Occasional Papers of the Tyrrell Museum of Paleontology, 3: 18-23.
Bennett, SC. 1995. An arboreal leaping origin of flight and the relationships of pterosaurs. Journal of Vertebrate Paleontology, 15: 19A.
Bennett SC. 1996. The phylogenetic position of the Pterosauria within the Archosauromorpha. Zoological Journal of the Linnean Society, 118: 261— 308.
Bennett SC. 2001. The osteology and functional morphology of the Late Cretaceous pterosaur Pteranodon. Palaeontographica, A 260:1-153.
Bennett SC. 2007. A second specimen of the pterosaurAnurognathus ammoni. Palaontologische Zeitschrift, 8: 376-398.
Benton MJ.,2004. Origin and interrelationships of dinosaurs. In: Weishampel, D.B., Dodson, P., and Osmolska, H. (eds.), The Dinosauria (second edition). Berkeley: University of California Press, 7-19.
Bumham DA. 2003. New information on Bambiraptorfeinbergi (Theropoda: Dromaeosauridae) from the Late Cretaceous of Montana. In: Currie, P.J., Koppelhus, E.B., Shugar, M.A. and Wright, J.L. (eds.),Feathered Dragons. Bloomington: Indiana University Press, 67-111.
Chatterjee S. Templin RJ. 2006. Biplane wing planform and flight performance of the feathered dinosaur Microraptor gui. PNAS, 104 (5): 1576-1580.
Codomiu L, Chiappe LM. 2004. Early juvenile pterosaurs (Pterodactyloidea: Pterodaustro guinazui) from the Lower Cretaceous of central Argentina. Canadian Journal of Earth Sciences. 41: 9-18.
Dalla Vecchia FM. 2001. A caudal segment of a Late Triassic pterosaur (Diapsida, Pterosauria) from northeastern Italy.Gortania, 23: 5-36.
Dalla Vecchia FM. 2003. New morphological observations on Triassic pterosaurs. Geological Society, London, Special Publications, 217: 23-44.
Elgin RA, Hone DWE, Frey E. 20011. The extent of the pterosaur flight membrane. Acta Palaeontologica Polonica, 56: 99-111.
Farlow JO, Gatesy SM, Holtz TR Jr, Hutchinson JR, Robinson JM. 2000. Theropod locomotion. American Zoology, 40:640-663.
136 Frey E, Tischlinger H, Bushy MC, et al. 2003. New specimens of Pterosauria (Reptilia) with soft parts with implications for pterosaurian anatomy and locomotion. Geological Society, London, Special Publications, 217: 233- 266.
Gatesy SM. 1990a. Caudefemoral musculature and the evolution of Theropod Locomotion. Paleobiology, 16(2): 170-186.
Gatesy SM. 1990b. The evolutionary history of the theropod caudal locomotor module. In: Gauthier, J., and Gall, L.F. (eds.), New Perspectives on the origin and evolution of birds. Connecticut: Peabody Museum of Natural History, 333-346.
Gatesy SM. 1999. Guineafowl hind limb function. I: Cineradiographic analysis and speed effects. Journal of Morphology, 249: 115-125.
Gatesy SM, Dial KP. 1996. From frond to fan:Archaeopteryx and the evolution of short-tailed birds. Evolution, 50 (5): 2037-2048.
Gauthie JA. 1984. A cladistic analysis of the higher systematic categories of the Diapsida. Unpublished Ph.D. Dissertation, University of California at Berkeley.
Gauthier J. 1986. Saurischian monophyly and the origin of birds. In: Padian, K. (ed.), The origin of birds and the evolution of flight.Memoirs of the California Academy of Sciences, 8:1-55.
Habib MB. 2008. Comparative evidence for quadrupedal launch in pterosaurs. Zitteliana B28: 161-168.
He HY, Wang XL, Zhou ZH, Wang F, Boven A, Shi GH, Zhu RX. 2004. Timing of the Jiufotang Formation (Jehol Group) in Liaoning, northeastern China, and its implications. Geophysical Research Letters, 31: L12605.
Hu, D.Y., Hou, L., Zhang, L., and Xu, X., 2009. A pre-Archaeopteryx troodontid theropod from China with long feathers on the metatarsus. Nature, 461: 640-643.
Hwang SH, Norell MA, Ji Qiang, Gao Keqin. 2002. New specimens of Microraptor zhaoianus (Theropoda: Dromaeosauridae) from northeastern China. American Museum Novitates, 3381: 1-44.
Lii J, Unwin DM, Jin X, Liu Y, Ji Q. 2009. Evidence for modular evolution in a long-tailed
137 pterosaur with a pterodactyloid skull. Proceedings of the Royal Society B, 277: 383-389. [Published online before print, 2009, doi: 10.1098/rspb.2009.1603]
McMahon TA, Valiant G, Frederick EC. 1987. Groucho running. Journal of Applied Physiology, 62:2326-2337.
McNeel Robert & Associates. 2007. Rhinoceros NURBS modeling for Windows 4.0. Seattle, Washington, USA.
Norell MA, Makovicky PJ. 1999. Important features of the dromaeosaur skeleton II: information from newly collected specimens ofVelociraptor mongoliensis. American Museum Novitates, 3282: 1-45.
Olshevsky G. 1994. The birds first? A theory to fit the facts — evolution of reptiles into birds. Omni, 16(9): 34-86.
Ostrom JH. 1969. Osteology ofDeinonychus antirrhops, an unusual theropod from the Lower Cretaceous of Montana. The Peabody Museum Bulletin, 30: 1-165.
Ostrom JH. 1973. The ancestry of birds. Nature, 242: 136.
Padian K. 1984. The origin of pterosaurs. In: Reif, W-E, and Westphal, F. (eds.), Third Symposium on Mesozoic Terrestrial Ecosystems. Tubingen: Attempto Verlag, 163-168.
Paul GS. 1988. Predatory Dinosaurs of the world. Simon and Schuster. New York, New York.
Paul GS. 2002. Dinosaurs of the Air. Baltimore and London: The Johns Hopkins University Press.
Paul GS. 2010. “Dinosaur Mass Estimate Table.” Offical Website of Gregory S. Paul - Paleoartist, Author, and Scientist. December 1, 2010. http://gspauldino.com/data.html
Sereno PC. 1991. Basal archosaurs: phylogenetic relationships and functional implications. Society of Vertebrate Paleontology Memoir 2, Journal of Vertebrate Paleontology, 11 (Supplement to #4), 1-53.
138 Unwin DM. 1997. Pterosaur tracks and the terrestrial ability of pterosaurs. Lethaia, 29: 373-386.
Unwin DM. 2006. The Pterosaurs from Deep Time. New York: Pi Press.
Wellnhofer P. 1991. The Illustrated Encyclopedia of Pterosaurs. London: Salamander Books.
Witton MP, Naish D. 2008. A reappraisal of azhdarchid ptrerosaur functional morphology and paleoecology. PloS ONE 3(5): e2271. doi: 10.137 l/joumal.pone.0002271.
Xu X, Ma QY, Hu DY. 2010. Pre-Archaeopteryx coelurosaurian dinosaurs and their implications for understanding avian origins. Chinese Science Bulletin, 55: 1-7.
Xu X, Zhou Z, Wang X, Kuang X, Zhang F, Du X. 2002. Four-winged dinosaurs from China. Nature, 421: 335-340.
139 Chapter 5 An Overview and Reanalysis of Theropod Tail Morphology,
Function, and Evolution
5.1 Introduction
Previously, the only attempt to examine the evolution of caudal morphology across the entirety of the Theropoda was a study by Gatesy (1990a).
In it, the vertebra bearing the most posterior caudal rib (“transverse process”) was used to infer the posterior termination point of theM. caudofemoralis and thereby assess the total M. caudofemoralis length in a variety of extinct theropods. This inferred M. caudofemoralis length, combined with the prominence of the femoral fourth trochanter, was taken as a general gauge of the overall size of the M. caudofemoralis in each taxon. Based on these assessments of the relative size of the M. caudofemoralis, it was argued that throughout the evolution of theropods there was a general trend towards caudofemoral muscle reduction and a gradual progressive shift in locomotive style that placed decreasing emphasis on femoral retraction and increasing emphasis on knee flexion (Gatesy, 1990a). Specifically, a functional shift in the role of the tail from locomotion to dynamic stabilization was described within coelurosaurs. It was argued that this shift began prior to (but ultimately served as a pre-adaption for) the evolution of avian flight (Gatesy,
1990a). This theory was discussed in more depth by later works (Gatesy, 1990b;
Gatesy and Dial, 1996).
Since the groundbreaking study (Gatesy 1990a) was published, the understanding of caudal morphology, including the osteological correlates for the
140 shape and size of the M. caudofemoralis, of both modem reptiles and theropods has advanced extensively. Great strides have also been made in understanding theropod phylogeny, and many previously glaring gaps within the theropod family tree have been filled, particularly with regard to the origin of birds (Fig.
5.1). Here, a new (though by no means all encompassing) synthesis is offered on the functional morphology and emergent patterns of theropod caudal evolution.
141 Dibphosaurus
Coeksphysis
Limusaurus
Majungasaurus
Spinosauridae
Altosaurus
Caicharodontosauridae
Gorgosaurus AntonwUlim lli Tyrannosaurus
Therizinosauroldea
Nomingia
'Ingenta‘ Ovtnptorouurla Anchiomis
Sinomithoides
Microraptor
Velociraptor Deinonychosauria Dromaaosaurtdaa Archaeopteryx
Modern Birds
FIGURE 5.1 Theropod phlogeny, including all genera and major groups considered in this study. Doted line shows the possible postion ofAnchiomis at the base of deinonychosauria. Based with modification on Holtz 1998b and Hu et al., 2009.
142 5.2 Musculature Reconstruction Methodology and Results
The reconstruction of non-avian dinosaur caudal musculature based on caudal osteology and comparisons with modem reptiles has been discussed in depth by several recent studies (Allen et al., 2009; Arbour, 2009; Mallison, 2011).
A general consensus of caudal muscle origination and insertion patterns has been reached, and it has been recognized that, when fully fleshed, the tails of most dinosaurs likely exceeded the dimensional boundaries of the caudal skeleton, with muscles budging well past the lateral tips of the caudal ribs and well below the ventral tips of the chevrons (see Chapter 1).
Caudal muscle mass estimations for seven theropod taxa described in the preceding chapters has been compiled, and the results of new digital reconstructions, utilizing the same methodology, are presented for an additional seven taxa. Together, they provide comparative data from 14 theropod taxa for which reasonably complete caudal material was available (Table 5.1).
In Chapter 1, based on the digital modeling results of three non-avian coelurosaurs, it was argued that most non-avian theropods had relatively larger
143 TABLE 5.1. Compilation of caudal muscle mass estimations for 5 extant reptiles and 14 non-avian theropods.
Modern Reptiles M. spinalis M. longissimus M. ilio-ischiocaudalis M. caudofemoralis Caiman crocodiius 1.4 g 9.6 a 9 g 13.8 a Total tail muscle mass: 33.8 g 4.1% 28.4% 26.6% 40.8% Total body mass: 578 g 0.2% 1.7% 1.6% 2.4% Tupinambis merianae 3.9 g 22.5 a 12.2 a 13.3 a Total tail muscle mass: 51.9 g 7.5% 43.4% 23.5% 25.6% Total body mass: 539.3 g 0.72% 4.17% 2.26% 2.47% Iguana iguana 20.8 g 52.6 a 70 g 49.2 a Total tail muscle mass: 192 g 18.8% 27.3% 36.3% 25.5% Total body mass: 2357.6 g 0.9% 2.2% 3.0% 2.1% Basiliscus vittatus 0.6 a 2.4 a 3 a 3.4 a Total tail muscle mass: 9.4 g 6.4% 25.5% 31.9% 36.2% Total body mass: 112.6 g 0.5% 2.1% 2.7% 3.0% Chamaeieo calyptratus 0.2 a 0.6 a o .8 a 0.6 a Total tail muscle mass: 2.2 g 9.1% 27.3% 36.4% 27.3% Total body mass: 121.15 g 0.2% 0.5% 0.7% 0.5%
144 Non-coelurosaurian Theropods M. spinalis M. longissimus M. ilio-ischiocaudalis M. caudofemoralis Coelophysis bauri AMNH 7229 21.3Q 71.4 g 114.4g 398.5 g Total tail muscle mass: 605.6 g 3.5% 11.8% 18.9% 65.8% Total body mass: 5700 g 0.4% 1.3% 2.0% 7.0% Dttophosaurus wetherilli UCMP 37302 2987 fl 5696 g 17920 g 22062 g Total tail muscle mass: 48665 g 6.1% 11.7% 36.8% 45.3% Total body mass: 283000 g (Paul, 1988) 1.1% 2.0% 6.3% 7.8% Ceratosaurus nasicornis USNM 4735 19210g 26527 g 51401g 61572g Total tail muscle mass: 158710 g 12.1% 16.7% 32.4% 38.8% Total body mass: 524000 g (Paul, 1988) 3.7% 5.1% 9.8% 11.8% Umusaurus inextricabilis IVPP V15923 45 g 289 g 482 g 1073 g Total tail muscle mass: 1889 g 2.4% 15.3% 25.5% 56.8% Total body mass: 15000 g (Paul, 2010) 0.3% 1.9% 3.2% 7.2% Carnotaurus sastrei MACN-CH 894 8000 g 18000 g 74000g 222000 g Total tail muscle mass: 322000 g 2.5% 5.6% 23.0% 68.9% Total body mass: 1500000 g (Mazzetta et al., 1998) 0.5% 1.2% 4.9% 14.8% Allosaurus fragilis USNM 4734 13745 g 15540g 79470 g 140028g Total tail muscle mass: 248783 g 5.5% 6.2% 31.9% 56.3% Total body mass: 1700000 g (Paul, 1988) 0.8% 0.9% 4.7% 8.2%
145 Coelurosaurs M. spinalis U. longlssimus M. ilio-ischiocaudalls M. caudofemoralis Ornitholestes hermanni AMNH 619 79 a 166 a 840 a 1241 a Total tail muscle mass: 2326 g 3.4% 7.1% 36.1% 53.4% Total body mass: 12600 g (Paul, 1988) 0.6% 1.3% 6.7% 9.8% Omithomimus edmontonicus TMP 95.11.001 860 g 2440 a 5050 a 9890 a Total tail muscle mass: 18240g 4.7% 13.4% 27.7% 54.2% Total body mass: 150000 g 0.6% 1.6% 3.4% 6.6% Gorgosaurus libratus TMP 91.36.500 3900 a 6900 a 10300 a 17300 a Total tail muscle mass: 38300 g 10.2% 18.0% 26.9% 45.2% Total body mass: 400000 g 1.0% 1.7% 2.6% 4.3% Tyrannosaurus rex BHI3033 65200 a 154200 a 159400 a 522200 a Total tail muscle mass: 901000 g 7.2% 17.1% 17.7% 58.0% Total body mass: 5622000g (Paul, 2010) 1.2% 2.7% 2.8% 9.3% “Ingenia" yanshini MPC 100/30 89 a 660 a 1220 a 1504 a Total tail muscle mass: 3473 g 2.6% 19.0% 35.1% 43.3% Total body mass: 17000 0.5% 3.9% 7.2% 8.9% Nomingia gobiensis MPC 100/119 145 a 541 a 1319a 1795 a Total tail muscle mass: 3800 g 3.8% 14.2% 34.7% 47.2% Total body mass: 20000 g 0.7% 2.7% 6.6% 9.0% Sinornithoides youngi IVPP V9612 9.5 a 25.2 a 50.1 g 78.0 a Total tail muscle mass: 162.8 g 5.8% 15.5% 30.8% 47.9% Total body mass: 2500 g 0.4% 1.0% 2.0% 3.1% Velociraptor mongoliensis MPC100/986 108 a 210 a 318 g 202.4 a Total tail muscle mass: 838.4 g 12.9% 25.1% 37.9% 24.1% Total body mass: 15000 g (Paul, 1988) 0.7% 0.1% 2.1% 1.4%
146 caudofemoral muscles than extant saurians. The increased dataset of this study
strongly supports that general assertion. The calculated large relative size of the
M. caudofemoralis of most non-avian theropods is primarily the result of a greater relative distance from the ventral base of the caudal ribs to the ventral tips of the chevrons in the anterior region of the tail. Following the modeling methodology used here, changes in this distance have a more than exponential effect on the calculated volume of the M. caudofemoralis. As discussed in Chapter 1, most non-avian theropods have anterior caudal ribs that are positioned high on the neural arch, often well above the neural canal. In comparison, the anterior caudal ribs of modem lepidosaurs are positioned level with the dorsal edge of the centra.
The elevated anterior caudal ribs of most non-avian theropods greatly increased the relative caudal-rib-base-to-chevron-tip distances, and are, therefore, assumed to have allowed an increase in the relative M. caudofemoralis mass.
5.3 The Caudofemoral Complex and the Origin of Archosaur Bipedality
Of the modeled taxa, Coelophysis is the oldest and represents the most basal form. The estimated relative M. caudofemoralis mass of Coelophysis is
substantially greater than that documented in any modem sauropsid, and the anterior caudal ribs of Coelophysis are positioned well above the centra. The same is true of the anterior caudal ribs of more primitive theropods, including
Herrerasaurus and Eodromaeus. In modem crocodilians, the ribs of the first three anterior caudal vertebrae are usually slightly elevated. It appears, then, that while
147 the morphology was exaggerated in basal theropods, expanded caudofemoral muscles were primitive to the group.
Previous authors have argued that the presence of long and robust tails was an influential factor in the evolution of bipedal locomotion within archosaurs
(and, similarly, that the absence of long robust tails may have limited the evolution of bipedality within mammals) (Snyder 1967; Tarsitano, 1983;
Hutchinson and Gatesy, 2001). Such arguments have usually focused on the effect tails had on the center of mass. With robust tails, most early archosaurs had centers of mass positioned posteriorly, such that the hindlimbs naturally bore more weight than the forelimbs, and, thus, reliance on only the hindlimbs was easier to achieve. It should be recognized that the presence of a large M caudofemoralis also likely favored the hindlimbs to support bipedal locomotion.
Similar arguments can also be made based on the larger size and greater rigidity of the pelvic, as compared to the pectoral, girdle. However, while such arguments help to explain why archosaurs may have evolved hindlimb based bipedality instead of forelimb based bipedality and why bipedality has been more widespread and successful in archosaurs than in mammals, they do not explain the more fundamental question of why some archosaurs abandoned quadrupedality in favor of bipedality.
One causal explanation for archosaur bipedality has focused on the forelimbs rather than the hind. This explanation has garnered the most widespread acceptance, and suggests that archosaur bipedality was encouraged by the benefits associated with freeing the hands to serve in dexterous activities, most
148 significantly in grappling with prey (Hutchinson and Gatesy, 2001). This explanation is supported by the fused clavicles and grasping hands of early theropods, although many modem predators, such as varanids and felines, make
good use of their forelimbs when subduing prey, despite being obligate quadrupeds. Additionally, while the earliest dinosaurs and obligatorily bipedal dinosauromorphs have relatively long forelimbs (as would be expected, given the only recent loss of the forelimbs’ locomotive function) (Sereno, 1993), the forelimbs of most later forms are greatly reduced in their maximum anterior reach. In many Triassic and Jurassic theropods, the forelimbs are so short that it is difficult to envision them grappling with any prey that had not already been
seized by the jaws or, in the case of many theropods (such asCoelophysis), with prey that was not already more than a quarter of the way down the throat. This reduction in forelimb length, seen even in many early theropods, suggests that the forelimbs did not play a vital role in predation (but see Carpenter, 2002 for a different interpretation).
As an alternative to the “forelimb freeing” explanation (though by no means a mutually exclusive one), archosaur bipedality (and particularly that of theropod dinosaurs) may have arisen to support increased cursoriality. This is not to suggest that, all other considerations being equal, bipedal locomotion is
intrinsically faster than quadrupedal locomotion. Indeed, it is not (Coombs, 1978).
However, as in modem crocodilians and most lizards, the size and potential force generation of the M. caudofemoralis was without equal in the forelimb
musculature of early archosaurs. This would have translated into more powerful
149 and more rapid retraction of the hindlimbs compared to the forelimbs. While running, the forelimbs of some early archosaurs may, therefore, have had difficulty keeping pace with the hindlimbs, and the expansion of theM. caudofemoralis would have magnified this difference. In the interest of reaping the greatest cursorial benefits, lengthening of the hindlimbs would have increased stride length, but would have required either the adaption of a bipedal stance or the proportionate lengthening of the forelimbs (which would have yielded proportionately less cursorial benefits). Additionally, lengthening of the limbs would potentially have caused an overlap in strides and brought the stronger and faster motions of the hindlimbs into conflict with the weaker and slower motions of the forelimbs. This is a known problem in modem lizards with hind limbs that are longer than the forelimbs (Irschick and Jayne, 1990), and may have been an even greater concern when combined with a parasagittal gait. Thus, raising the forelimbs to attain a bipedal stance would have permitted the unencumbered extension of the hindlimbs, and a switch from quadrupedal to bipedal locomotion would have cursorial benefits, at least in terms of maximum sprint speed. Further reduction in the size and length of the forelimbs would have lessened weight, and eventually true obligate bipedality could arise.
Unlike the “forelimb freeing” explanation, the “cursorial” explanation of archosaur bipedality is well supported by comparisons to modem analogues and to other presumed bipedal taxa within the fossil record. Many modem lizards
(including Basiliscus, Chlamydosaurus, Dipsosaurus, and Callisaurus) assume a bipedal stance when fleeing at top speed from perceived threats (Irschick and
150 Jayne, 1990). The gait and pelvic morphology of modem lacerta is fundamentally different from that of archosaurs and particularly that of dinosaurs, so caution is warranted in comparing the two. However, modem lizards are generally regarded to assume a bipedal running posture for the same reasons here outlined for some early archosaurs (Snyder 1949, 1952,1954, 1962; Irschick and Jayne, 1990;
Chrustian et al., 1994; Fieler and Jayne, 1998), and they are likely representative of an early intermediate stage in the development of true obligatory bipedality.
These lizards have a well developed M. caudofemoralis and hindlimbs that are substantially longer than their forelimbs. Based on the relatively lengthened hindlimbs, several non-archosaur fossil taxa have been identified as facultative bipedal runners, including the bolosaurid Eudibamus, which is also thought to have been digitigrade with a nearly vertical limb position while running (Berman et al., 2000) and the prolacertiformes Langobardisaurus and Macrocnemus
(Renesto et al., 2002). These taxa affirm that bipedality for the sake of cursorial benefits has evolved independently multiple times in lineages with well developed caudofemoral muscles.
5.4 Tails of Non-coelurosaurian Theropods
In general, the tails of non-coelurosaurian theropods are long and deep.
The anterior centra are roughly equal to those of the dorsal series in anteroposterior length, but gradually become increasingly elongate down the series. The centra of the terminal two or three caudal vertebrae are often reduced in anteroposterior length, but in all other posterior caudal vertebrae the centra are
151 many times longer than they are wide or tall. The caudal ribs extend strongly posterolaterally with a slight dorsal inclination (although caudal rib dorsoventral inclination is often difficult to judge, given that caudal ribs are prone to being taphonomically flattened towards the midline). The neural spines of the anterior caudal vertebrae are tall (equaling or exceeding the heights of the centra) and posteriorly inclined. Posteriorly, the neural spines become gradually reduced in height, are anteroposteriorly narrower, more posteriorly inclined, and more posteriorly positioned - such that the bases of the neural spines are posterior to the midpoints of the centra. The neural spines persist beyond the termination of the caudal ribs, but usually for only 4-5 additional vertebrae. The zygapophyses of the posterior caudal vertebrae are proportionately longer and oriented more dorsally than those of the anterior caudal vertebrae, but both the anterior and posterior tail regions appear to have been highly flexible in the lateral plane. The anterior chevrons are deep and finger-like, curve slightly posteriorly, and have simple unexpanded ventral tips. Posteriorly, the depths of the chevrons diminish gradually, but the simple and primitive chevron morphology is maintained well past the caudal transition point. In the most posterior region, the chevrons often develop posteriorly extended ventral tips.
The caudal series of Coelophysis bauri (Fig. 5.2) includes an estimated 40 vertebrae, and the last caudal rib is present on caudal vertebra 19. The anterior neural spines are unusually short, which suggests relatively weak epaxial musculature. The digital muscle reconstruction reveals that the post transition- point region of the tail was remarkably long and narrow. The posterior
152 FIGURE 5.2. Stages in modeling the tail of Coelophysis bauri (AMNH 7229) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio- ischiocaudalis (pink) (C).
153 zygapophyses are more developed than in modem crocodilians and most modem
lepidosaurs, but whether this was sufficient to hold the tail stiff and prevent
ventral sagging, as is commonly depicted, is unclear.
The caudal series of Dilophosaurus wetherilli (Fig. 5.3) includes an estimated 46 vertebrae, and the last caudal rib is present on caudal vertebra 17.
The anterior chevrons are unusually short dorsoventrally; however, the chevrons do not become rapidly reduced in depth after the termination of the caudal ribs.
Rather, the chevrons remain proportionately deep throughout much of the posterior tail region. In the digital muscle reconstruction, this gives the posterior portion of the tail a dorsoventrally deep and laterally compressed shape.
The caudal series of Limusaurus inextricabilis (Fig. 5.4) includes an estimated 49 vertebrae, and the last caudal rib is present on caudal vertebra 17.
The anterior caudal ribs are anteroposteriorly broad. The anterior chevrons are strongly curved posteroventrally. The chevron series is uniquely displaced posteriorly, with the first chevron located between caudal vertebrae three and four and with chevron number four having the greatest dorsoventral depth.
The caudal series of Ceratosaurus nasicornis (Fig. 5.5) includes an estimated 50 vertebrae, and the last pair of caudal ribs is present on caudal vertebra 33. The neural spines are exceptionally tall, the chevrons are exceptionally deep, and the caudal ribs are unusually wide (although, owing to their strong posterior inclination, the absolute lateral width of the caudal ribs is less, relative to centrum width, than those of some oviraptorosaurs). A prominent ridge extends nearly halfway up the anterior edges of the more anterior neural
154 FIGURE 5.3. Stages in modeling the tail of Dilophosaurus wetherilli (UCMP 37302) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (C).
155 A. 10 cm
B. 10 cm
10 cm C.
FIGURE 5.4. Stages in modeling the tail of Limusaurus inextricabilis (IVPP V15923) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (C).
156 B. 1 m
/# i i f
FIGURE 5.5. Stages in modeling the tail of Ceratosaurus nasicomis (USNM 4735) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (C).
157 spines. There are more caudal ribs than in any other theropod. The most posterior
chevrons are relatively shorter dorsoventrally than the anterior caudals, but
maintain a narrow finger-like morphology - without posteriorly expanded tips.
The digital muscle reconstructions suggest Ceratosaurus had a more
massive tail, compared to total body mass, than any other theropod here
considered. However, Ceratosaurus poses a unique set of challenges to the digital
modeling methodology. Gatsey (1990a) assumed that theM. caudofemoralis of all
theropods extended to all vertebrae with caudal ribs. This assumption was not
unreasonable, and the termination of the caudal ribs does correlate with the taper
point of the M. caudofemoralis of modem crocodilians and of some modem
lizards. Additionally, the termination of the caudal ribs of some non-avian
coelurosaurs corresponds with a strong morphological change in the chevrons.
Furthermore, an anteroposteriorly directed scar on the lateral faces of the
chevrons directly demarcates the ventral boundary of the taperingM.
caudofemoralis (see Chapter 1). This relationship between the posterior extent of
the M. caudofemoralis and the caudal ribs presumably exists because a major
function of the caudal ribs is to provide a dorsal insertion site for the M. ilio-
ischiocaudalis, and this function is no longer necessary once theM.
caudofemoralis has tapered out and the M. ilio-ischiocaudalis is free to insert
directly onto the lateral faces of the centra.
However, in many modem lizards (includingTupinambis) no correlation
between the termination of the caudal ribs and the posterior extent of the M. caudofemoralis exists (see Chapter 1). The caudal ribs also serve as a ventral
158 insertion surface for the M. longissimus, and a large M. longissimus often requires the caudal ribs to persist posteriorly beyond theM. caudofemoralis. In
Ceratosaurus, the proportions of the caudal ribs and neural spines suggest the presence of sizable epaxial musculature, and the digital models predict a relatively large M. longissimus. Given that, if the M. caudofemoralis of Ceratosaurus did extend to caudal vertebra 33, the relative length of the muscle would vastly exceed that of any other theropod or any other sauropsid and would have an unusually narrow posterior morphology, it seems more likely thatM. the
caudofemoralis of Ceratosaurus ended well prior to the last caudal rib set. Based
on other theropods, the most likely position of theM. caudofemoralis taper-point
would be between caudal vertebrae 17 and 20. Unfortunately, complete chevrons
are not known from this region of the tail and potentially confirming evidence of a
M. caudofemoralis /ilio-ischiocaudalis septa scar cannot be evaluated.
In the model used to generate the data (Table 5.1), it was assumed that,
unlike all other theropods, the M. caudofemoralis of Ceratosaurus ended before
the final caudal rib set, and, to maintain a consistent M. caudofemoralis shape,
that the M. caudofemoralis did not reach the ventral tip on many of the chevrons.
These assumptions constitute a “most likely”Ceratosaurus tail reconstruction
(see Appendix B for two alternative models).
Functionally, the unique caudal morphology Ceratosaurusof merits
special consideration. Bakker and Bir (2004) argued that Ceratosaurus had a deep
and laterally compressed tail that was adapted for swimming. This, along with a
reported frequent association between the shed teeth of Ceratosaurus and the
159 teeth of large lungfish (including “Ceratodus” robustus), was interpreted as evidence of a partially piscivorous diet. The muscular tails of most non-avian
theropods would have made them all potentially proficient swimmers, but the
digital modeling results do support the claim thatCeratosaurus had an unusually deep and laterally compressed tail. The muscle mass estimates also show that the
M. longissimus and M. ilio-ischiocaudalis of Ceratosaurus were unusually large.
Both these muscles function in swinging the tail laterally, and would have been
important if the tail was specialized for aquatic sculling.
As in Ceratosaurus, modem reptiles that are highly adapted for swimming
(such as crocodilians and the marine iguana Amblyrhynchus cristatus) have tails
that are deep and laterally compressed overall, with extended neural spines and
chevrons. These modem swimmers also have posterior tail tips that are deep and
laterally compressed, and that serve as paddles while swimming. The skeleton and
muscle reconstructions show that the tail of Ceratosaurus had a more uniform
morphology, with no evidence of a specialized posterior paddle. However, in
crocodilians this paddle region is largely attributable to a heightened row of
mediodorsal osteoderms, whereas in Amblyrhynchus cristatus the function is
served by the tall mediodorsal row of scale-spines. It is worth noting, therefore,
that Ceratosaurus is the only theropod for which a mediodorsal row of
osteoderms has been reported (Gilmore, 1920), although the osteoderms are
currently known only from the anterior caudal region.
A partially piscivorous diet and aquatic lifestyle has been proposed for
various other non-avian theropods, including Dilophosaurus (Paul 1988) and
160 spinosaurids. As previously described, the tail ofDilophosaurus is not particularly deep overall, but it does have a deep and laterally compressed posterior region, which could have served effectively in aquatic locomotion. Based on stomach contents (Charig and Milner, 1997), the morphology of the jaws and teeth (Charig and Milner, 1997; Holtz 1998a), and isotopic studies (Amiot et al., 2010), spinosaurids are the best candidates for piscivory and a semi-aquatic lifestyle among non-avian theropods. Unfortunately, good caudal material for any spinosaurid has yet to be described, and it is currently impossible to evaluate the question of whether or not spinosaurid tails were specialized for swimming.
The caudal series of Carnotaurus sastrei (Fig. 5.6) includes an estimated
35-45 vertebrae, and the position of the last pair of caudal ribs is unknown. The anterior caudal ribs of Carnotaurus are more morphologically complex than those of any other theropod. The caudal ribs are angled above the horizontal by more than 60 degrees, and inclined slightly posteriorly. The tips of the caudal ribs are broad and flat with anteriorly-projecting half-crescent-shaped anterior edges and rounded posterior edges. The caudal rib tips interlock sequentially, with the first rib-set embracing the posterior edge of the ilium. The bizarre caudal rib morphology ofCarnotaurus, along with that of other South American abelisaurids, is discussed in depth in Chapter 2. The unique form of the caudal ribs permitted the expansion of theM. caudofemoralis to a greater relative size than that of any other theropod - hypothesized to be an adaptation for sprinting.
161 FIGURE 5.6. Stages in modeling the tail of Carnotaurus sastrei (MACN-CH 894) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (C).
162 FIGURE 5.7. Stages in modeling the tail of Allosaurus fragilis (CM 11844 scaled to the size of USNM 4734) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (C).
163 The caudal series of Allosaurus fragilis (Fig. 5.7) includes an estimated 42 vertebrae, and the last caudal rib set is present on caudal vertebra 18. The majority of specimens show that both the left and right caudal ribs of the anterior vertebrae are slightly inclined dorsally, indicating that this was the true orientation of the ribs in life, and is not due to taphonomic distortion. As in Ceratosaurus, a prominent anterior ridge or shelf is present on the neural spines of the more anterior vertebrae. The prezygapophyses of the posterior vertebrae are long and laterally embrace the postzygapophyses of the adjacent vertebra.
5.5 Tails of Non-deinonychosaurian Coelurosaurs
Compared to those of non-coelurosaurs, the tails of non- deinonychosaurian coelurosaurs are generally reduced in total length and in total vertebral count. However, the anterior caudal centra tend to be proportionately more elongate (oviraptorosaurs are an exception). The caudal transition point is dramatic, with chevron depth and neural spine height reduced posteriorly.
Posterior caudal vertebrae are stiffly held together by elongate, laterally positioned prezygapophyses (again oviraptorosaurs are a notable exception). The chevrons are morphologically variable throughout the tail. The anterior chevrons have anteroposteriorly broader hemal spine shafts, the hemal spine tips of the posterior chevrons have anterior and posterior elongated tips extensions, and, in the vicinity of the caudal transition point, overall chevron shape often progresses through a short series of unique morphologies not seen elsewhere in the tail.
164 The caudal series of Omithomimus edmontonicus (Fig. 5.8) includes 33
vertebrae, and the last caudal rib is present on caudal vertebra 14. The anterior
chevrons are curved posteroventrally. The specimen TMP 95.11.001 is preserved
in a classic “death pose” and likely records the maximum possible dorsal tail
flexion. In TMP 95.11.001 the anterior portion of the tail has a strong dorsal bend,
but posterior to the transition point the tail is straight. This lack of posterior
curvature is a testament to the dorsoventral rigidity of the rear half of the tail.
The caudal series of Gorgosaurus libratus (Fig. 5.9) includes an estimated
37 vertebrae, and the last caudal rib is present on caudal vertebra 12. In
Gorgosaurus, the ventral ends of the chevrons develop anteroposteriorly
elongated morphology early in the series. In some specimens, a prominent
posterior extension is present as early as the third chevron, and a prominent
anterior extension is present as early as the fifth chevron. However, larger
specimens tend to have less prominent chevron extensions, so this morphology
may vary ontogenetically.
The caudal series of Tyrannosaurus rex(Fig. 5.10) includes an estimated
42 vertebrae, and the last caudal rib is present on caudal vertebra 17. In large
Tyrannosaurus specimens (such as FMNH PR2081), the anterior neural spines have multiple short prongs and prominent rugosities on both the anterior and posterior edges. These structures suggest that, in life, sequential neural spines were probably connected by ligaments, cartilage, or other soft tissues. (Similar structures are also present in large specimens of the Asian tyrannosaurid
165 FIGURE 5.8. Stages in modeling the tail of Omithomimus edmontonicus (TMP4511001) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (C).
166 FIGURE 5.9. Stages in modeling the tail of Gorgosaurus libratus (TMP 1991.36.500) (juvenile) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (C).
167 FIGURE 5.10. Stages in modeling the tail of Tyrannosaurus rex(BHI3033) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio- ischiocaudalis (pink) (C).
168 Tarbosaurus.) The anterior chevrons of Tyrannosaurus are proportionately deeper than those of Gorgosaurus, and anteroposteriorly elongated tips do not develop until further down the series.
The tails of tyrannosaurids and omithomimids are similar in overall form and share several morphological characteristics that are unique among theropods.
In both groups, the neural spines are elongated anteroposteriorly. Even on posterior vertebrae the tops of the neural spines always overlap the anteroposterior midpoints of the centra; the neural spines have wide anterior and posterior ends and are pinched medially, such that they are hourglass-shaped in dorsal view; and multiple ventrally bowed neural spines are present immediately posterior to the caudal transition point. Although not entirely unique to tyrannosaurids and omithomimids, both groups also have posterior vertebrae with laterally positioned and elongated prezygapophyses that equal or exceed the centra in length and that tightly interlock with the postzygapophyses. Combined with short anteroposteriorly elongate chevrons, this creates a rigid and inflexible tail distally. The similarities of the tails of tyrannosaurids and omithomimids may be the result of convergence related to a high level of cursoriality, but it seems much more likely - given that cladistic analysis usually finds the two groups to have close phylogenetic proximity (Holtz 1998b; Sereno 1999) — that these traits are indicative of a shared common ancestor.
The caudal series of Omitholestes hermanni (Fig. 5.11) includes an estimated 36-40 vertebrae, and the position of the last caudal rib set is unknown but was likely between caudal vertebrae 16-20. Though the tail of Omitholestes is
169 A. 10 cm — — -- y\
FIGURE 5.11. Stages in modeling the tail of Omitholestes hermanni (AMNH 619) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, withM. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (C).
170 incompletely known, in most respects it seems to adhere to the typical coelurosaur morphology. At least two of the chevrons are laterally forked, with a large projection of the haemal spine that extends ventrally and at a slight posterior angle, and a smaller projection of the haemal spine that extends ventrally and at a stronger posterior angle. Based on size, these forked chevrons must have been positioned in sequence at, or just posterior to, theM. caudofemoralis taper point.
Laterally forked chevrons are also present at the taper point in dromaeosaurids
(but the position of the dromaeosaurid taper point, and thus the forked chevrons, is more anterior.)
The caudal series of “lngenia” yanshini (Fig. 5.12) includes an estimated
28 vertebrae, and the last caudal rib is present on caudal vertebra 25. The anterior chevrons are blade-shaped. The tips of both the chevrons and caudal ribs are rugose and bulge slightly, indicating that they may have been attachment cites for large muscle-septa or ligaments. There is no evidence of a pygostyle.
The caudal series of Nomingia gobiensis (Fig. 5.13) has an estimated 23 vertebrae, and the last caudal rib is present on caudal vertebra 18. The tail is short anteroposteriorly, but the muscle reconstructions indicate it was relatively stout.
The caudal ribs are laterally extensive and lobate. The anterior chevrons are blade-shaped, and the posterior chevrons are rectangular. The last four vertebrae are fused into a pygostyle.
The tails of “lngenia” and Nomingia, like all oviraptorosaurs, are highly derived. They have greatly reduced vertebral counts and, differing from most non- avian coelurosaurs, the individual centra are reduced in length. However, the
171 FIGURE 5.12. Stages in modeling the tail of “lngenia” yanshini (MPC 100/30) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio- ischiocaudalis (pink) (C).
172 FIGURE 5.13. Stages in modeling the tail of Nomingia gobiensis (MPC 100/119) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M ilio-ischiocaudalis (pink) (C).
173 caudal ribs persist until almost the end of the tail, and, as a result, the relative pre
transition point length is largely unaffected. The caudal ribs are more laterally
extensive (relative to centrum width) than in any other theropod group. Near the
transition point, the caudal ribs are positioned anterior to the midpoint of the centrum and the tips of the caudal ribs have anterior and posterior expansions.
The zygapophyses become prominently elongate only on the most posterior
vertebrae and maintain a horizontal articulation. This combination of
anteroposteriorly reduced centra and zygapophyses implies greater relative tail
flexibility per unit of length. The chevrons are deep and anteroposteriorly broad.
The digital reconstructions indicate that oviraptorosaurs had relatively largeM.
caudofemoralis and robust overall tail musculature. Pygostyles and tail-tip feather
fans were widespread among oviraptorosaurs, and, as argued in Chapter 3, the
muscular and flexible tails of oviraptorosaurs were well equipped to dexterously
flaunt the caudal plumage.
The conclusion reached by Gatesy (1990a) that theM. caudofemoralis was
diminishing in size throughout coelurosaurs is not supported by the results of this
study. Gatesy’s 1990 assessment of the tail morphology of non-coelurosaur
theropods was, by necessity, based largely on incomplete specimens, and his
assessment of the size of the M. caudofemoralis relied particularly on the extent
of the caudal ribs in Allosaurus and Ceratosaurus. As previously discussed, the
tail of Ceratosaurus is exceptional and was likely specialized for swimming.
Although Gatesy (1990a) used the tail ofCeratosaurus to illustrate the primitive
theropod condition, the extent of the caudal ribs and the total number of caudal
174 vertebrae in Ceratosaurus exceed those of all more advanced and of all more primitive theropods. The caudal count is probably related more to the size of the
M. longissimus than to the size of the M. caudofemoralis. In the case of
Allosaurus, Gatesy (1990a) relied on Madsen’s (1976) conclusion that the tail of
Allosaurus included 50+ vertebrae with 25 sets of caudal ribs, but Madsen based this estimate on incomplete and disarticulated material. The better preserved tail of CM 11844 shows that the true number of caudal vertebrae in the tail of
Allosaurus is roughly 42, and that caudal ribs are present on only 18 vertebrae.
Outside of the deinonychosaurs, a proportionally largeM. caudofemoralis was maintained throughout most coelurosaurs. Some forms, such as Gorgosaurus, did evolve an M. caudofemoralis that was proportionately smaller than theM. caudofemoralis of most non-coelurosaur theropods. However, other coelurosaurs, such as Tyrannosaurus and most oviraptorosaurs, evolved an M. caudofemoralis that was proportionately larger.
5.6 Tails of Deinonychosaurian Coelurosaurs and the Origin of Dinosaur
Flight
The relationship between the three major groups of deinonychosaurs
(aves, dromaeosaurids, and troodontids) is a hotly debated topic. Among modem birds, the caudal vertebral series is greatly shortened, all caudal centra are reduced in length, a large pygostyle is present, theM. caudofemoralis is greatly reduced or altogether absent, and knee flexion dominates femoral retraction during terrestrial locomotion (Tarsitano, 1983; Gatesy, 1990a, 1990b). In primitive birds, such as
175 Archaeopteryx and Jeholomis, the anterior caudal region is proportionally similar to those of modem birds, but the posterior region, although it is reduced in length, is composed of more elongate vertebrae. As would be expected, the tails of non- avian deinonychosaurs are similar to those of primitive birds, but with higher total vertebral counts and proportionately larger chevrons. The post-transition-point regions of dromaeosaur tails have characteristic bifurcating caudal rods that extend from the prezygapophyses and from anterior projections of the chevrons, and haemal spines that are anteroposteriorly long and form thin plates at their ventral tips. In troodontids, the post-transition-point tail region lacks caudal rods, but the haemal spines do form ventral plates. Jeholomis has chevrons with ventral plates with short anterior projections (showing that this was the primitive condition for birds), but no bird is known to possess true caudal rods. In terms of caudal morphology, troodontids are definitively the most primitive of the deinonychosaurs, and it is likely that aves and dromaeosaurs descended separately from troodontid ancestors.
The caudal series of Sinomithoides youngi (Fig. 5.14) includes an estimated 30 vertebrae, and the last caudal rib is present on caudal vertebra 11.
The neural spines rapidly diminish in size and disappear even before the caudal ribs do. The most anterior chevrons are deep and anteroposteriorly broad. By the transition point, the chevrons are dorsoventrally short, anteroposteriorly extended, and ventral plates have begun to form. Posteriorly, the chevrons become narrower mediolaterally. The ventral plates of the middle chevrons bridge the centra immediately anterior and posterior in the series, and likely limited the ability of
176 the tail to flex ventrally. The digital models show that the tail ofSinomithoides was narrow in life, with relatively reduced musculature.
The caudal series of Velociraptor mongoliensis (Fig. 5.15) totals an estimated 30 vertebrae, and the last caudal rib is present on caudal vertebra 11.
Prior to the transition point, the haemal spines progress through a number of distinctive morphologies. The most anterior ones are deep and laterally compressed, whereas more posterior ones become dorsoventrally short with anteroposteriorly broad extensions. More posteriorly, they are first laterally forked, then become boot-shaped with long posterior projections, and finally assume the ventral plate morphology with two anterior projections that exceed the single posterior projection in length. The tail ofVelociraptor is known from several articulated and nearly complete specimens. MPC100/986 preserves the tail in a sinuous S-shaped curve and shows that the caudal rods were flexible and that the tail was capable of substantial bending in the lateral plane. Similarly, in
MPC 100/25 the anterior caudal region is preserved in a strong dorsally curved arch, but the posterior region is preserved at a straight unbending angle. As discussed in Chapter 4, this suggests that the caudal rods kept the tail more ridged dorsoventrally. The digital models indicate the tail ofVelociraptor was reduced in overall muscle mass, with caudofemoral muscles that were small even relative to many modem crocodiles and lizards.
177 A. 10 cm
B. 10 cm
10 cm
FIGURE 5.14. Stages in modeling the tail of Sinomithoides youngi (IVPP V9612) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, withM. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (C).
178 10 cm
FIGURE 5.15. Stages in modeling the tail of Velociraptor mongoliensis (MPC 100/986) in lateral and dorsal views. Digital reconstruction of the caudal skeleton (A). Digital reconstruction including the M. caudofemoralis longus (red) (B). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (C).
179 Gatesy (1990b) argued that the extreme reduction of theM. caudofemoralis seen in birds relates to the specific biomechanical demands of flight. Caudofemoral muscle reduction logically benefits flight, because it reduces overall weight, repositions the center of mass more anteriorly, and reduces rotational inertia - potentially important for aerial maneuverability. However, regardless of what branch of the deinonychosaur family tree Aves descended from, it is clear that the avian ancestor already possessed a substantially reduced
M. caudofemoralis. Because the terrestrial dromaeosaur Deinonychus has a caudal morphology similar toArchaeopteryx, including clear evidence of a reduced M. caudofemoralis, Gatesy (1990a, 1990b) concluded that, while flight-related benefits may have taken caudofemoral muscle reduction to the extreme in modem birds, the reduction had begun prior to the evolution of dinosaur flight. To explain
why, Gatesy suggested that the function of the tails of dromaeosaurs (and some
theropod groups that came before them) was undergoing a functional shift from primarily serving in locomotion to primarily serving in dynamic stabilization - a
function originally proposed for the tail ofDeinonychus by Ostrom (1969).
Since Gatesy’s original study (1990a) was published, the understanding of
the sequence and timing of dinosaur flight was greatly advanced by the discovery
of two key early deinonychosaurs:Microraptor and Anchiomis. Microraptor is
among the oldest and most primitive known dromaeosaurs (Xu et al., 2002).
Anchiomis is a troodontid and among the oldest known deinonychosaurs (Xu et al
2010). Both taxa had long asymmetrical feathers on both the fore and hindlimbs
and were clearly adapted for some degree of aerial locomotion, either limited
180 gliding or true powered flight (Xu et al, 2002; Chatterjee and Templin, 2007;
Alexander et al., 2010; Xu et al 2010). These two early, primitive forms raise the
possibility that later deinonychosaurs, such asDeinonychus, were obligatorily
terrestrial secondarily and share a gliding/flying ancestor. If this is true,
adaptation to aerial locomotion is a sufficient explanation for the reducedM.
caudofemoralis of all deinonychosaurs. Prior to the description ofAnchiomis, the
possibility that advanced non-avian deinonychosaurs secondarily lost an aerial or
semi-aerial lifestyle was advocated based on numerous lines of morphological
evidence (Paul, 2002).
As pointed out in Chapter 4, reduction in overall tail size and particularly
in caudofemoral muscle mass similar to that seen in deinonychosaurs also
occurred in the first archosaur lineage to develop flight: the pterosaurs. Many of
the earliest known pterosaurs (including Austriadactylus, Eudimorphodon, and
Preondactylus) have caudal morphologies strikingly similar to those of
troodontids and Archaeopteryx. In all three groups, caudal ribs are present on only
the most anterior caudal vertebrae, the non-caudal-rib-bearing vertebrae are
greatly elongated anteroposteriorly with no neural spines and low but long
zygapophyses, and posterior- and mid-chevrons are short, with long posterior and
anterior projections. The tails of dromaeosaurids are even more similar to those of
some rhamphorhynchoid pterosaurs. Both dromaeosaurids and
rhamphorhynchoids independently evolved elongate caudal rods (see Chapter 4).
Microraptor has well developed caudal ribs, while Anchiomis does not, and
together these taxa phylogeneticaly bracket the evolution of caudal rods between
181 two gliding/flying forms. Although caudal rods were not likely present at any point in the linage that led directly to birds, the caudal rods of dromaeosaurs enhanced the potential of the tail to serve as an aerial rudder and to maintain aerodynamic shapes by preventing ventral tail sagging. The numerous convergences in the tails of deinonychosaurs and pterosaurs support the interpretation that deinonychosaur tails were originally adapted for flight/gliding.
The recognition that deinonychosaurs had a reducedM. caudofemoralis also has bearing on the long-standing “trees down vs. ground up” debate over the origin of dinosaur flight. This debate has raged within the scientific literature since the late 1870’s. In brief, the “trees down” theory suggests that true powered flight evolved in arboreal dinosaurs, and gradually arose to extend air time between tree-to-tree or tree-to-ground leaps (Marsh, 1880; Heilmann, 1926; Bock,
1986; Norberg, 1990; Chatteijee, 1997; Chatteijee and Templin, 2004). In opposition, the “ground up” theory postulates that flight evolved in highly cursorial dinosaurs, with many of the aerodynamic properties of flight feathers evolving to improve terrestrial maneuverability, and with true flight ultimately deriving to benefit increased vertical leaping ability, perhaps to help in pursuing flying insect prey or in predator avoidance (Williston, 1879; Nopsca, 1923;
Ostrom, 1979,1986; Gauthier and Padian, 1985; Padian and Chiappe, 1998). A more recent revision of the “ground up” theory, argues that flight evolved to facilitate the speed and ease that cursorial theropods could ascend steep inclines, particularly tree trunks (Bundle and Dial, 2003; Dial, 2003).
182 The “trees down” theory is supported by the many modem tree-to-tree
gliders (such as the “flying lemur”Cynocephalus, the “flying lizard”Draco, the
“flying squirrel”Hylopetes, the “sugar glider” Petaurus, and “the flying gecko”
Ptychozoon), which potentially represent functional intermediaries. The “trees down” theory is also strengthened by the general acceptance that in both bats and pterosaurs (the only other tetrapod lineages to evolve true flight) a “ground up” scenario appears to have been impossible, because in bats and pterosaurs the wing membranes unite the fore and hindlimbs and would have hampered (rather than helped) terrestrial locomotion. Given that the “trees down” theory applies unopposed to bats and pterosaurs, both lineages offer support and a conceptual validation of the “trees down” theory as it might apply to the dinosaur lineage.
Historically, the “ground up” theory has drawn support from the recognition that the non-avian theropods (the deinonychosaurs), which share the most synapomorphies with birds, were terrestrial cursors (Ostrom, 1979, 1986).
The incline running reinterpretation of the “ground up” theory is additionally strengthened from the observation of wing-assisted incline running in many ground-living modem birds (Dial, 2003). These modem analogs show that forelimb wings (even poorly developed ones), combined with rapid flapping action, can significantly enhance running performance up steep inclines and vertical surfaces.
The apparent reduction of theM. caudofemoralis represents a fundamental challenge to the “ground up” theory. Although many modem birds are capable of rapid terrestrial and incline running, despite having caudofemoral muscles that are
183 far more reduced than those of non-avian deinonychosaurs, the running abilities
of modem birds are achieved through a complexly reengineered hindlimb
locomotive system that places much greater emphasis on knee-flexion than on
femoral retraction. The impetus for this hind-limb reengineering is easily explained in the context of direct flight evolution, but not in the context of cursorial evolution. Early reduction of the primary hindlimb retractile muscle would be detrimental to terrestrial cursors and is counterintuitive to the suggestion that proto-flyers were adapting to be rapid terrestrial predators. The reduction of the M. caudofemoralis is therefore, inconsistent with the “ground up” and incline running theories. M. caudofemoralis reduction is, however, an entirely consistent
adaptation for arboreal gliding.
Similarly, the presence of long hindlimb feathers on early deinonychosaurs, which have been shown to have dragged on the ground when in a standard walking or running pose (Xu et al, 2002), suggests reduced terrestrial locomotive function in the hindlimbs. It has been argued that the long hindlimb feathers of Microraptor do not pose a challenge to the “ground up” theory, because Microraptor is younger thanArchaeopteryx and has several derived characteristics not seen in birds, and is not, therefore, representative of the avian
ancestral condition. This argument is certainly correct in its phylogenetic and
temporal placement ofMicroraptor at a distance from the direct avian lineage.
However, it requires either the assumption that the hindlimb wings of
Microraptor evolved under an altogether different set of selective pressures than the forewings or else that both sets of wings evolved under an altogether
184 independent set of selective pressures than those of the direct avian lineage. This
must be regarded as improbable, given the close morphological similarities of the
Microraptor forewing feathers, the Microraptor hindwing feathers, and the forewing feathers of birds. At the very least, Microraptor is evidence that some early deinonychosaurs were arboreal and employed feathery wings in gliding.
Moreover, Anchiomis now provides proof of a four-winged deinonychosaur that
predatesArchaeopteryx and (while still not likely a direct avian ancestor) likely has a phylogenetic position closer to the point of avian divergence (Hu et al.,
2009; Xu et al., 2010).
Lastly, the long forelimbs, grasping hands, and hooked claws of basal deinonychosaurs appear amply suited for arboreal scaling (Chatterjee and
Templin, 2004), and pose a particular problem for proponents of the incline- running hypothesis. Simply providing a slight advantage in running up tree trunks
or other steep inclines is not sufficient to explain the development of wings and
the flight stroke in deinonychosaurs. The advantage gained from proto-wings and
accompanying flapping motion would have to outweigh the advantage that would be gained from simply extending the forearms and climbing - and that is less
likely.
In light of these morphological challenges and the wealth of information provided by the new record of early deinonychosaurs, it may be appropriate to critically reexamine the historic origins of the “trees down” vs. “ground up” debate. The issue was originally fueled by the larger debate over whether dinosaurs were the true ancestors of birds. Opponents to a dinosaur-bird ancestry,
185 argued vehemently in favor of the simplistic “trees down” theory of avian flight.
Proponents of a dinosaur-bird ancestry were compelled to develop a “ground up”
theory of flight evolution, not because the “ground up” theory had by itself greater conceptual merits than the “trees down” theory, but because no convincingly
arboreal dinosaurs were known. The “trees down” theory was, therefore,
seemingly inapplicable to even the most bird-like of dinosaurs. That birds are indeed descended from theropod dinosaurs is now supported by overwhelming evidence, and a dinosaur origin of birds is widely accepted. Moreover, with the recent recognition of numerous deinonychosaurs (not onlyAnchiomis and
Microraptor, but also such forms as Jinfengopteryx, Pedopenna, and
Sinomithosaurus) and other advanced bird-like taxa (such as Scansoriopteryx and
Yixianosaurus) that appear well suited to arboreal or semi-arboreal lifestyles, evoking a “ground up” explanation for theropod flight is no longer strictly necessary. Instead, applying the “trees down” theory of flight evolution to theropod dinosaurs is most consistent with the latest fossil evidence and resolves a long-standing point of paleontological contention.
5.7 Conclusions and Discussion
Previous arguments supporting a broad trend towards caudofemoral mass reduction and a functional shift towards dynamic stabilization throughout the evolution of theropod tails are drastic oversimplifications, and the result of a limited set of examined taxa. The role of theM. caudofemoralis as the primary femoral retractor was retained or even exaggerated in the majority of advanced
186 theropod groups. Moreover, theropod tails are morphologically diverse and show evidence of divergent adaptations that were specialized to serve a variety of additional functions, from swimming to courtship displays. Two overarching, or at least frequently recurring, trends can be indentified (although Ceratosaurus is an exception to both): an increase in tail stiffness, and the reduction in the length of the post-transition-point tail region.
Tails that are relatively stiffer than the ancestral condition have long been recognized as characteristic of the Tetanurae (Gauthier, 1986), and the interlocking caudal ribs and accompanying extreme caudal rigidity of advanced
South American abelisaurids shows that stiffened tails evolved independently in another major early branch of the theropod linage. In non-oviraptorosaur coelurosaurs, the increase in average relative centrum length, in combination with a reduced number of total tail vertebrae, resulted in increased overall tail rigidity.
The highly inflexible posterior tail regions of tyrannosaurids and omithomimids, the lengthened centrum and bracing hemal spine plates of deinonychosaurs, and the caudal rods of dromaeosaurs are additional advanced morphologies that appear to stiffen the tails
The primitive total number of caudal vertebrae seems to have been 45-50 in theropods. The total number of caudal vertebrae is currently unknown for abelisaurids, though, as noted by Coria et al. (2002), the tail tapers more abruptly than in more primitive theropods (as can best be inferred from what is preserved of the caudal series of Aucasaurus). In most non-avian coelurosaurs, the caudal vertebra count is significantly less. At an estimated 42 caudal vertebrae,
187 Tyrannosaurus has a high count for a coelurosaur. Although oviraptorosaurs increased rather than decreased caudal flexibility, outside of birds, oviraptorosaurs reduced the post-transition point region more than any other group. A decreased caudal series also evolved in deinonychosaurs and was taken to the extreme in Aves.
Again, it should be emphasized that in all lineages, other than the deinonychosaurs, the reduction in the relative length of the tail was concentrated posterior to the M. caudofemoralis. Reduction in the post-transition-point region probably served to reduce the total weight of the tail, without negatively affecting the function of the caudofemoral muscles. It has also been argued that the long tails of theropods imparted substantial rotational inertia (Carrier et al., 2001;
Henderson and Snively, 2004) and, thus, reduced total tail length may have also benefitted maneuverability.
The relatively stiff tails of deinonychosaurs can be explained in terms of flight/gliding related benefits, but for other groups the benefits of increased tail rigidity are not as apparent. Indeed, loss of caudal flexibility would seem to have obvious disadvantages. Increased tail rigidity may simply have made it easer on
the epaxial tail muscles to hold the entirety of the tail straight and off the ground.
Alternatively, stiffened tails may have provided an advantageously less giving framework for the caudofemoral muscles to pull against or may have prevented
large unbalanced motion waves, resulting from one-sided muscle contractions,
from being carried down the tail while walking and running.
188 To facilitate future tail research, I offer as a final commentary the
recommendation that new published descriptions of theropod specimens change
their emphasis in reporting caudal material. Chevrons and caudal vertebrae
morphology seem like afterthoughts in the majority of specimen descriptions.
This thesis has shown that there is a wealth of potential information that can be
gained from careful consideration of the caudal osteology, and more ink ought to
be spilled on describing tail anatomy. However, it is unlikely, given the scope and
spatial limitations of most specimen descriptions, that lengthy sections devoted to
tails will become a hallmark of specimen descriptions anytime in the foreseeable
future. Nonetheless, a few more practical and specific changes would greatly
increase the usefulness of specimen descriptions and alleviate for future tail
researchers some of the frustrations that arose recurrently while conducting this
research.
First, caudal vertebrae descriptions should not be limited to simply
classifying vertebrae based on centrum concavity. This information is not
especially useful for functional or polygenetic concerns, and it is easily
observable from figures. What is especially useful (when the completeness of the
specimen allows) is a description of how the proportions of the caudal vertebrae
change down the caudal series, and at what vertebra the caudal transition point
occurs. With regard to figures, providing illustrations or photographs of multiple
sequential and well preserved vertebrae (except perhaps those vertebrae that
surround the caudal transition point) is less useful that providing an image of a
single vertebra from one region of the tail and one image of a single vertebra from
189 another region (even if one of the vertebra is poorly preserved). It is also significantly more informative to figure anterior caudal vertebrae in anterior or posterior view than in dorsal or ventral view. Lastly, there is a need for greater continuity between descriptions of caudal vertebrae and chevrons. Chevron descriptions ought to be included in the same descriptive section as the caudal vertebrae or else in a separate section that immediately follows. The helpfulness of figuring chevrons in articulation with the caudal vertebrae cannot be overstated. More than any other measurement, the distance from the ventral tip of the chevrons to the ventral edge of the caudal ribs is the most telling indicator of the size of the M. caudofemoralis, and images of disarticulated chevrons, with unknowable hemal facet articulation angles, cannot be used to assess this distance.
5.8 Bibliography
Allen V, Paxton H, Hutchsinson JR. 2009 Variation in center of mass estimates
for extant sauropsids and its importance for reconstructing inertial
properties of extinct archosaurs. Anatomical Record 292:1442-1461.
Amiot R, Buffetaut E, Lecuyer C, Wang X, Boudad L, Ding, Z, Fourel F, Hutt S,
Martineau F, Medeiros A, Mo J, Simon L, Suteethom V, Sweetman S,
Tong H, Zhang F, Zhou Z. 2010. Oxygen isotope evidence for semi-
aquatic habits among spinosaurid theropods. Geology 38: 139-142.
190 Arbour VM. 2009. Estimating impact forces of tail club strikes by ankylosaurid
dinosaurs. PLoS ONE 4: e6738.
Alexander DE, Gong E, Martin LD, Burnham DA, Falk AR. 2010. Model tests of
gliding with different hindwing configurations in the four-winged
dromaeosaurid Microraptor gui. Proceedings of the National Academy of
Science, USA, 107: 2972-2976.
Bakker RT, Bir G. 2002. Dinosaur crime scene investigations: theropod behavior
at Como Bluff, Wyoming, and the evolution of birdness. In: Currie PJ,
Koppelhus EB, Shugar MA, Wright JL (eds.),Feathered Dragons.
Bloomington, Indiana: Indiana University Press, p.301-342.
Berman DS, Reisz RR, Scott D, Henrici AC, Sumida SS, Martens T. 2000. Early
Permian bipedal reptile. Science 290: 969-972.
Bundle MW, Dial KP. 2003. Mechanics of wing-assisted incline running (WAIR).
The Journal of Experimental Biology 206: 4553-4564.
Bock WJ. 1985. The arboreal theory for the origin of birds. In: Hecht MK,
Ostrom JH, Viohl G, and Wellnhofer (eds.), The Beginnings of Birds.
Eichstatt: Freunde des Jura Museums, Eichstatt. p. 199-207.
Carpenter K. 2002. Forelimb biomechanics of nonavian theropod dinosaurs in
predation. Palaeobiodiversity and Palaeoenvironments 82: 59-75.
191 Carrier DR, Walter RM, Lee DV. 2001. Influence of rotational inertia on turning
performance of theropod dinosaurs: clues from humans with increased
rotational inertia. Journal of Experimental Biology 204: 3917-3926.
Charig AJ, Milner AC. 1997. Baryonyx walkeri, a fish-eating dinosaur from the
Wealden of Surrey. Bulletin of the Natural History Museum, Geology
Series 53: 11-70.
Chatterjee S, Templin RJ. 2004. Feathered coelurosaurs from China: new light on
the arboreal origin of avian flight. In: Currie PJ, Koppelhus EB, Shugar
MA, Wright JL (eds.), Feathered Dragons. Bloomington, Indiana: Indiana
University Press, p.251-281.
Chatteijee S, Templin RJ. 2007. Biplane wing planform and flight performance of
the feathered dinosaur Microraptor gui. Proceedings of the National
Academy of Sciences, 104(5): 1576-1580.
Christian A, Horn HG, Preuschoft H. 1994. Biomechanical reasons for bipedalism
in reptiles. Amphibia-Reptilia, 15: 275-284.
192 Coria RA, Chiappe LM, Dingus L (2002) A new close relative ofCarnotaurus
sastrei Bonaparte, 1985 (Theropoda: Abelisauridae) from the Late
Cretaceous of Patagonia. Journal of Vertebrate Paleontology 22: 460-465.
Coombs WP Jr. 1978. Theoretical Aspects of cursorial adaptations in dinosaurs.
The Quarterly Review of Biology, 53: 393-418.
Dial KP. 2003. Wing-assisted incline running and the evolution of flight. Science,
299: 402-404.
Fieler CL, Jayne BC. 1998. Effects of speed on the hindlimb kinematics of the
lizard Dipsosaurus dorsalis. The Journal of Experimental Biology, 201:
609-622.
Gatesy SM. 1990a. Caudofemoral musculature and the evolution of Theropod
Locomotion. Paleobiology, 16(2): 170-186.
Gatesy SM. 1990b. The evolutionary history of the theropod caudal locomotor
module. In: Gauthier, J., and Gall, L.F. (eds.), New Perspectives on the
origin and evolution of birds. Connecticut: Peabody Museum of Natural
History, 333-346.
193 Gatesy SM. 1997. An electromyographic analysis of hindlimb function in
Alligator during terrestrial locomotion. J Morph 234:197-212.
Gauthier J A. 1986. Saurischian monophyly and the origin of birds. In: Padian K
(ed.) The Origin of Birds and the Evolution of Flight. Memoirs of the
California Academy of Sciences. 8. California Academy of Sciences,
pp. 1-55.
Gilmore CW. 1920. Osteology of the carnivorous dinosauria in the United States
National Museum, with special reference to the generaAntrodemus
(Allosaurus) and Ceratosaurus. Smithsonian Institution United States
National Museum Bulletin 110.
Gauthier J, Padian K. 1985. Phylogenetic, function and aerodynamic analysis of
the origin of birds and their flight. In: Hecht MK, Ostrom JH, Viohl G,
and Wellnhofer (eds.), The beginnings of birds. Eichstatt: Freunde des
Jura Museums, Eichstatt. p. 185-187.
Heilmann G. 1926. The origin of birds. London: Witherby.
Henderson DM, Snively E. 2004. Tyrannosaurus en pointe: allometry minimized
rotational inertia of large carnivorous dinosaurs. Proceedings of the Royal
Society - Biological Sciences 271(suppl 3): S57-S60.
194 Hu DY, Hou L, Zhang L, Xu X. 2009. A pre-Archaeopteryx troodontid theropod
from China with long feathers on the metatarsus. Nature, 461: 640-643.
Hultz TR Jr. 1998a. Spinosaurs as crocodile mimics. Science 282: 1276-1277.
Hultz TR Jr. 1998b. A new phylogeny of the carnivorous dinosaurs. GAIA 15: 5-
61.
Hutchinson JR, Gatesy SM. 2001. Bipedalism. eLS.
Irschick DJ, Jayne BC. 1990. Comparative three-dimensional kinematics of the
hindlimb for high-speed bipedal and quadrupedal locomotion of lizards.
Journal of Experimental Biology 202: 1047-1065.
Mallison H. 2011. Defense capabilities of Kentrosaurus aethiopicus Hennig,
1915. Paleontologica Electronica 14 (2): 1-25.
Marsh OC, 1880. Odontomithes: a monograph on the extint toothed birds of
North America. Report of the geological exploration of the fortieth
parallel 7: 1-201.
Nopsca F. 1923. On the origin of flight of birds. Proceedings Zoological Society
of London 1907: 223-235.
195 Norberg UM. 1990. Vertebrate flight. Berlin: Springer-Verlag.
Ostrom JH. 1979. Bird flight: how did it begin? American Scientist 67: 46-56.
Ostrom JH. 1986. The cursorial origin of avian flight. In: Padian K (ed.), The
origin of birds and the evolution of flight. California Academy of
Sciences, San Francisco, California, p.73-81.
Ostrom JH. 1969. Osteology ofDeinonychus antirrhops, an unusual theropod
from the Lower Cretaceous of Montana. The Peabody Museum Bulletin,
30: 1-165.
Padian K, Chiappe LM. 1998. The origin of birds and their flight. Scientific
America 278: 38-47.
Paul GS. 1988. Predatory Dinosaurs of the world. Simon and Schuster. New
York, New York.
Paul GS. 2002. Dinosaurs of the Air. Baltimore and London: The Johns Hopkins
University Press.
196 Persons WS, Currie PJ. 2011. The tail of Tyrannosaurus: reassessing the size and
locomotive importance of the M. caudofemoralis in non-avian theropods.
The Anatomical Record, 294: 119-131.
Renesto S, Dalla Vecchia FM, Peters D. 2002. Morphological evidence for
bipedalism in the Late Triassic prolacertiform reptileLangobardisaurus.
Palaeobiodiversity and Palaeoenvironments 82: 95-106
Sereno PC. 1999. The evolution of dinosaurs. Science 284: 2137-2147.
Snyder RC. 1949. Morphological evidence for bipedal locomotion of the lizard
Basiliscus basiliscus. Copeia 1949: 129-137.
Snyder RC. 1952. Quadrupedal and bipedal locomotion of lizards. Copeia 1952:
64-70.
Snyder RC. 1954. The anatomy and function of the pelvic girdle and hindlimb in
lizard locomotion. American Journal of Anatomy 95: 1-45.
Snyder RC. 1962. Adaptations for bipedal locomotion of lizards. Am Zool 191-
203.
197 Snyder RC. 1967. Adaptive values of bipedalism. American Journal of physical
Anthropology 26: 131-134.
Tarsitano S. 1983. Stance and gait in theropod dinosaurs. Acta Palaeontologica
Polonica 28: 251-264.
Williston SW. 1879. Are birds derived from dinosaurs? Kansas City Review of
Sciences 3: 456-460.
Xu X, Ma QY, Hu DY, 2010. Pre-Archaeopteryx coelurosaurian dinosaurs and
their implications for understanding avian origins. Chinese Science
Bulletin, 55: 1-7, doi: 10.1007/sll434-010-4150-z.
Xu X, Zhou Z, Wang X, Kuang X, Zhang F, Du X. 2002. Four-winged dinosaurs
from China. Nature, 421: 335-340.
198 Conclusion
Like the head, forelimbs, hindlimbs, and other significant components of the anatomy, theropod tails had a complex and dynamic evolutionary history.
While the rest of the body evolved and progressed, tails did not remain in an anatomically primitive state, but instead kept pace. Nor was the evolution of theropod tails dictated by a single selective pressure or follow a single adaptive path. Across different lineages, tails became specialized for an array of different functions in both subtle and dramatic ways, such that by the end of the Cretaceous the caudal vertebrae and chevrons of all major theropod groups had become morphologically diagnostic. In some theropod groups, the caudal osteology shows strong evidence of adapting for tail-specific functions, such as aquatic sculling in
Ceratosaurus and courtship displays in oviraptorosaurs, which imply behaviors not inferable from the rest of the skeletal anatomy. In others, such as the caudal- rod-braced tails of early dromaeosaurs, tail form changed in tandem with many other features to facilitate a dramatic shift in lifestyle.
If it is true that the presence of a large M. caudofemoralis was paramount in the evolution of archosaur bipedality, then, for theropods, caudal anatomy was destiny. The impact that bipedality had on the whole of theropod evolution is impossible to calculate but would be difficult to overestimate. In all but the avian lineage, hindlimb-based locomotion with caudofemoral dominated femur retraction was maintained, and bipedality may have been essential to the attainment of forelimb-powered flight within the Aves. The caudofemoral
199 muscles bound non-avian theropod tails to basic terrestrial movement in a way that defies simple comparison with all modem animals. Based on the estimated sizes of the M. caudofemoralis, this bond was strengthened over time in many theropod groups and was stronger than all previous works have assumed.
It is hoped that this thesis will influence how theropod tails are commonly depicted and thought of. There is an overarching need for more robust theropod tail depictions and for greater appreciation of the variability in tail form across theropod groups. More importantly, the results and techniques presented in this thesis should serve as a helpful guide and foundation for future research into theropod tails and the tails of archosaurs in general. Much remains to be done. For simple logistical reasons, many taxa with good caudal material were not examined in this study, and the tails of many more taxa remain altogether undiscovered.
200 Appendix A
TABLE A. 1. Measurements of LACM 127704 (a cast of Camotaurus sastrei MACN-CH 894). Direct measurements of MACN-CH 894 form Bonaparte et al (1990) included for comparison.______Caudal Vertebra Number 1 2 3 4 5 6
Spinous Process Maximum Height (from neural arch) 110 109 104 112 113 105 Dorsal Run (from neural arch) 142 135 125 135 138 123 Basal Length 74 73 77 81 75 70 Basal Width 21 21 15 12 19 10 Middle Length 61 60 47 48 43 43 Tip Length 51 45 43 48 38 33 Tip Width 26 23 29 24 28 14
Caudal Rib/Transverse Process Maximum Height Centrum 215 180 210 230 205 200 Maximum Lateral Width (from Neural Arch) 129 136 90 111 127 118 Lateral Run (from centrum to tip) 225 215 240 245 220 215 Basal Length 59 83 75 82 74 80 Basal Thickness 46 40 24 23 38 28 Middle Length 56 54 51 54 34 32 Tip Thickness 10 12 11.7 10 10 15 Tip Length 101 106 112 120 118 112
C entrum Maximum Length 127 114 116 ??? 92 96 Maximum Length (Bonaparte et al., 1990) 128 122 120 136 ?????? Width Anterior 140 143 121 ??? 91 98 Width Anterior (Bonaparte et al., 1990) 140 144 ??? 104 ??? ??? Height Anterior 120 115 118 ??? 103 100 Height Anterior (Bonaparte et al., 1990) 126 118 120 117 ??? ??? Width Posterior 127 134 87 82 93.2 104 Height Posterior 110 105 116 100 79 103 Height Middle 67 68 72 79 63 69 Width Middle 88 78 65 53 64 69
Post Zygapophyses Articulation Surface Width 10.4 16.9 ??? 16.8 12.7 14 Articulation Surface Length 17.4 ??? ??? 22.2 26.5 29.4
Pre Zygapophyses Articulation Surface Width 19.2 10.9 ??? ??? 19.1 14.1 Articulation Surface Length 29.8 29.2 42.2 ??? 36.4 40.9
201 Left Ilium Side Greatest Length 950 Greatest Length (Bonaparte et al., 1990) 970 Posteriori Height 230 Brevis Length 350 Brevis Width 77 Brevis Depth 103
202 FIGURE A.I. Long tail model of Camotaurus sastrei (MACN-CH 894) reconstructed to test for muscle mass variation resulting from uncertain posterior tail form. Reconstruction assumes five additional posterior vertebrae and posterior chevrons and caudal ribs that decrease in size more gradually. Muscle reconstruction follows the conservative method. (A) Digital reconstruction of the caudal and pelvic skeleton with M. caudofemoralis longus (red). (B) Complete digital reconstruction, with epaxial musculature (orange) andM, ilio- ischiocaudalis (pink) added.
203 A
FIGURE A.2. Short tail model of Camotaurus sastrei (MACN-CH 894) reconstructed to test for muscle mass variation resulting from uncertain posterior tail form. Reconstruction assumes five fewer posterior vertebrae and posterior chevrons and caudal ribs that decrease in size more rapidly. Muscle reconstruction follows the conservative method. (A) Digital reconstruction of the caudal and pelvic skeleton with M. caudofemoralis longus (red). (B) Complete digital reconstruction, with epaxial musculature (orange) andM. ilio-ischiocaudalis (pink) added.
204 TABLE A.2. Comparison of mass estimations from the test of muscle mass variation resulting from uncertain posterior tail form. Results indicate total tail muscle mass is potentially effected by less than 7%. M. spinalis M. longissimus M. ilio-ischiocaudalisM. caudofemoralis Long Tail Model 8000 q 18000 a 75000 a 225000 Total tail muscle mass: 326000 g 2.5% 5.5% 23.0% 69.0% % Deviation from Conservative Model 14% 17% 16% 1%
M. spinalis M. longissimus M. ilio-ischiocaudalis M.caudofemoralis Short Tail Model 6000 14000 a 58000 a 210000 a Total tail muscle mass: 288000 g 2.1% 4.9% 20.1% 72.9% % Deviation from Conservative Model 14% 7% 8% 5%
205 Appendix B
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FIGURE B.l. Alternative 1 model of the tail of Ceratosaurus nasicomis (USNM 4735) reconstructed using the standard methodology and osteological correlates in lateral and dorsal views (model assumes that the M. caudofemoralis longus extended to the ventral tips of the chevrons and extended posteriorly to the last caudal rib set). Digital reconstruction including the M. caudofemoralis longus (red) (A). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio-ischiocaudalis (pink) (B).
206 FIGURE B.2. Alternative 2 model of the tail of Ceratosaurus nasicomis (USNM 4735) in lateral and dorsal views (model assumes that the M. caudofemoralis longus extended posteriorly to the last caudal rib set but did not extend ventrally to the tips of the anterior chevrons). Digital reconstruction including the M. caudofemoralis longus (red) (A). Complete digital reconstruction, with M. spinalis and M. longissimus (gold), and M. ilio- ischiocaudalis (pink) (B).
207 TABLE B.l. Alternative caudal muscle mass estimations for Ceratosaurus nasicomis (USNM 4735) M. spinalis M. longissimus M. ilio-ischiocaudalis M. caudofemoralis "Best guess" model 19210 a 26527 a 51401 a 61572 a Total tail muscle mass: 158710 g 12.1% 16.7% 32.4% 38.8% Total body m ass: 524000 g (Paul, 1988) 3.7% 5.1% 9.8% 11.8% Alternative 1 19210 a 26527 a 57068 a 123806 a Total tail muscle mass: 226611 g 8.5% 11.7% 25.2% 54.6% Total body m ass: 524000 g (Paul, 1988) 3.7% 5.1% 10.9% 23.6% Alternative 2 19210 a 26527 a 46450 a 94188 a Total tail muscle mass: 186375 g 10.3% 14.2% 24.9% 50.5% Total body m ass: 524000 g (Paul, 1988) 3.7% 5.1% 8.9% 18.0%
208