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Unlike extant birds and mammals, most non-avian theropods had large muscular tails, with muscle arrangements similar to those of modern reptiles. Examination of ornithomimid and tyrannosaurid tails revealed sequential diagonal scarring on the lateral faces of four or more hemal spines that consistently correlates with the zone of the tail just anterior to the disappearance of the vertebral transverse processes. This sequential scarring is interpreted as the tapering boundary between the insertions of the M. caudofemoralis and the M. ilioischiocaudalis. Digital muscle reconstructions based on measurements of fossil specimens and dissections of modern reptiles showed that the M. caudofemoralis of many non-avian theropods was exceptionally large. These high caudofemoral mass estimates are consistent with the elevation of the transverse processes of the caudal vertebra above the centrum, which creates an enlarged hypaxial region. Dorsally elevated transverse processes are characteristic of even primitive theropods and suggest that a large M. caudofemoralis is a basal characteristic of the group. In the genus Tyrannosaurus, the mass of the M. caudofemoralis was further increased by dorsoventrally lengthening the hemal arches. The expanded M. caudofemoralis of Tyrannosaurus may have evolved as compensation for the animal's immense size. Because the M. caudofemoralis is the primary hind limb retractor, large M. caudofemoralis masses and the resulting contractile force and torque estimates presented here indicate a sizable investment in locomotive muscle among theropods with a range of body sizes and give new evidence in favor of greater athleticism, in terms of overall cursoriality, balance, and turning agility. Anat Rec,, 2010. © 2010 Wiley-Liss, Inc.
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. Modern reptiles represent the best modern 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.
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. caudofemoralis,” but this muscle is not homologous to the M. caudofemoralis of saurians and birds (Appleton,1928; Howell,1938). In modern 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, the M. caudofemoralis is both the primary and the single largest retractor muscle of the hind limb (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's1990 study of the M. caudofemoralis and its reduction in the lineage leading to extant birds, he argued that the muscle's gradual shrinkage 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 dinosaurs (perhaps, particularly the bipedal taxa) fundamentally different from what can be observed in any modern 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, the M. 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 modern reptiles (Fig. 1).
Figure 1. Tyrannosaurus dorsal silhouette (A) previously used in body-mass estimation (Modified from Paul,1997), compared with a modern Alligator dorsal silhouette (B) (Modified from Cong,1998). The basal bulge in the tail of the Alligator is primarily the result of a large M. caudofemoralis.
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Here, basic caudal musculature of modern 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).
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- MATERIALS AND METHODS
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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 of Gorgosaurus (45.1%). However, this discrepancy in relative M. 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 established (Biewener,1989; 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 enlarged M. caudofemoralis estimation indicates that Tyrannosaurus could have achieved the same degree of cursoriality as a juvenile Gorgosaurus or other smaller tyrannosaurids. Indeed, the relatively shorter metatarsals of Tyrannosaurus (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 transverse processes, 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 the M. caudofemoralis was indeed a muscle of fundamental importance to non-avian theropod locomotion. These results have implications for the ongoing discussion of the potential locomotive abilities of non-avian theropods. For instance, in their assessment of the cursoriality of Tyrannosaurus, 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 previously 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).
Considering the results of this study 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 retracts, 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 right M. caudofemoralis' femoral pull. The elongate zygapophyses of Tyrannosaurus 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 beyond what would be estimated based on the limb musculature of most modern 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's2004 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 by Tyrannosaurus to achieve higher speeds and to support its own bulk. Obviously, a larger M. 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 hind limb 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, 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 hind limb, 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 modern 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 tails would 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. 13).
Figure 13. A fully rendered reconstruction of BHI 3033 created by Scott Hartman to illustrate the appearance of a Tyrannosaurus with a tail of appropriate beefiness.
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