Zoological Journal of the Linnean Society
Functional morphology of neck musculature in the Tyrannosauridae (Dinosauria, Theropoda) as determined via a hierarchical inferential approach
Figure 1. Divisions of amniote neck and craniocervical musculature, superimposed on the cervical vertebrae of Caiman crocodylus. Different shades represent transversospinalis, longissimus, iliocostalis and longus/medial iliocostalis divisions
Figure 2. A, inference of muscle function for turning the head in extant animals. Axes represent levels of corroboration of muscle topological and kinematic morphology, physiology and observed behaviour. The volume subtended by these levels of certainty is the behavioural inference space for the muscle. The muscles m. transversospinalis capitis lateralis and m. complexus, homologous and present in crocodilians and birds, respectively, are depicted as examples with different levels of corroboration along the axes and more or less certain inference of function. Physiological activity is shown as confirmed by electromyography in birds, but only hypothesized in crocodilians. B, inferring the function of m. complexus for turning the head in tyrannosaurids. Axes represent levels of inference (Witmer, 1995) for morphology and physiology, and level of inference for kinematic action of the muscle based on its reconstructed morphology (see text for explanation). Because physiological muscle function during movements is corroborated in only one pole of the extant bracket, and the physiology does not leave osteological correlates, a Level II′ inference is the best possible for the extinct taxon .
Figure 3. Flow chart for extant behavioural interpolation, which enables inference of muscle-modulated behaviours in extinct animals. The certainty of behavioural inference in an extinct taxon is inversely related to the behaviour’s specificity. Behaviour can be inferred by phylogenetic bracketing if similarity of muscle function is established in extant clades by kinematic and physiological considerations, and if these functions correlate with similar behaviours in the extant groups.
Figure 4. Comparison of major sites of muscle attachment on the necks of tyrannosaurids versus crocodilians and birds. A, cervical series of Caiman crocodylus (above; C1–C9) and Tyrannosaurus rex (below; C1–C10), depicting similarities of posterior transverse process morpohology. B, cervical series of Asio flamaeus (above) and Tyrannosaurus rex (below), depicting morphological similarities of epipophysis and the C2 neural spine. In all three groups the anterior transverse processes are smaller than their posterior counterparts (to show this clearly the C2 cerivical rib of T. rex is not pictured). Cervical rib morphology differs markedly among these archosaurs. The specimens are scaled to similar lengths from C1 to C9. The Tyrannosaurus rex is a composite reconstruction of C1 from Osborn (1905), BHI 3033 (C2) and AMNH 5027 (the remaining bones).
Figure 5. Attachments of muscles inserting on the occiput of birds. A, posterior cervical vertebrae of Strutio camelus, showing osteological origin of posterior belly of m. biventer cervicis. B, anterior cervical vertebrae of Haliaeetus leucocephalus, with origins of m. complexus, m. splenius capitis and m. rectus capitis dorsalis (outlined). M. complexus originates from the epipophyses dorsally (as in Haliaeetus leucocephalus), and sometimes the lateral tubercles ventrally. For adjoining origins of m. complexus and m. rectus capitis dorsalis from the lateral tubercles, the latter is the anterior of each pair. C, occiput of Struthio camelus, depicting all insertions. In Struthio camelus and many other birds m. splenius capitis lateralis inserts laterally onto the occiput, but in other birds part of m. complexus inserts here.
Figure 6. Neck muscle origins and insertions in crocodilians. A, muscle attachments on C1–C9 of Caiman crocodylus. B, muscle insertions on the occiput of Caiman crocodylus. m. trans. cap., m. transversospinalis capitis; m. epi.-cap. lat., m. epstropheo-capitis lateralis; m. epi.-cap. med., m. epstropheo-capitis medialis; m. sp.cap. post., m. spinocapitis posticus; m. trans. cerv., m. transversospinalis cervicis; m. long. cerv., m. longissimus cervicis (m. articulares/m. tendinoarticulares); m. long. cap., m. longus capitis; m. long. cap. sup., m. longissimus capitis superficialis; m. long. cap. prof., m. longissimus capitis profundus; m. il. cap., m. iliocostalis capitis; m. il. cerv., m. iliocostalis cervicis.
Figure 7. A, dorsal view of m. biventer cervicis (m. biv. c., dark outline) and m. longus colli dorsalis pars cranialis of Aquila chrysaetos. Note the tendon intervening between anterior and posterior bellies of m. biv. c. M. complexus has been removed. B, dorsal view of m. transversospinalis capitis (m. trans. cap., dark outline) of Alligator mississippiensis. Medial and lateral portions of m. trans. cap. in Alligator are not distinguished here. C, lateral view of m. trans. cap. of Alligator mississippiensis (dark outline). D, m. complexus (dark outline) and m. rectus capitis lateralis (light outline) of Pelicanus occidentalis in lateral view. E, m. complexus of Pelicanus occidentalis, outlined in dark grey on the right. This is a dorsal view, with anterior towards the top. F, dorsal view of dissected Alligator mississippiensis, with m. epistrpheo-capitis lateralis, m. spinocapitis posticus and m. transversospinalis cervicis outlined in grey. M. transversospinalis capitis has been removed. G, m. splenius capitis of Anas platyrhynchos, from C2 to the occiput, outlined in grey, in posterior view. M. complexus and m. biventer cervicis have been removed. H, m. epistropheo-capitis medialis/m. altoïdius capitis of Caiman crocodylus, outlined in grey. M. transversospinalis capitis and m. epistropheo-capitis lateralis have been removed.
Figure 8. A, lateral view of m. longus colli dorsalis pars cranialis (m. l.c.d. cranialis), m. longus colli dorsalis pars caudalis (m. l.c.d. caudalis) and mm. intertransversarii (mm. intertrans.) of Cygnus columbianus. Note posterior slips contributing to m. l.c.d. cranialis, ventrally inserting heads of m. l.c.d. caudalis and multiple tendinous divisions of all mm. intertrans. B, left m. transversospinalis cervicis (m. trans. cerv., outlined in grey) of Caiman crocodylus, inserts by a white tendon onto C1. M. spinocapitis posticus (m. sp. cap. post.) and m. longissimus capitis superficialis (m. long. cap. sup., with part of surrounding fascia left on) are also outlined in grey. Superficial muscles have been removed.
Figure 9. A, insertions of (dark grey) m. longus colli dorsalis pars cranialis onto anterior cervical epipophyses of Haliaeetus leucocephalus. B, schematic origin (light grey) of m. longus colli dorsalis pars cranialis, from cervicodorsal region of Struthio camelus. C, schematic origins (dark grey) of m. longus colli dorsalis pars cranialis from epipophyses (processes dorsales) of posterior cervicals in Struthio camelus. Slips from these origins coalasce with the main belly of the muscle, as demarcated by the light-shaded lines. The main belly of the muscle continues dorsally. D, schematic origin and insertions of m. longus colli dorsalis pars caudalis. This muscle subsystem originates from the cervicodorsal region and sends multiple bellies to insert on posterior cervical epipophyses. E, origins of m. longissimus cervicis/m interarticulares of Caiman crocodylus. The gradient-filled slips represent association of origins with the fascia surrounding the muscles. F, anteriormost insertions (dark grey) of m. longissimus cervicis/m. interarticulares, and m. transversospinalis cervicis, of Caiman crocodylus.
Figure 10. A, several muscles of Pelicanus occidentalis, disseted in lateral view. Abbreviations are as in the main text. Several slips of m. rectus capitis dorsalis (m. r.c.d.) converge ventrally, towards tendinous insertions on the basioccipital tuberosities. M. complexus has an unusual lateral, tendinous insertion. B, posterolateral view of m. longissimus capitis superficialis (outlined in dark grey) of Alligator mississippiensis. The posterior origin and the insertion are tendinous. M. iliocostallis capitis (m. il. cap.) is depicted, and m. constrictor colli has not been dissected away. The neck is slightly dorsiflexed in this view .
Figure 11. A, origins (dark shapes) and insertions (lighter outlined shapes) of mm. intertransversarii aponeuroses on posterior cervical vertebrae of Struthio camelus. Origins are from anterior faces of lateral tubercles, and insertions are onto posterior projections of the lateral tubercles. Arrows represent lines of action whereby insertions are drawn towards the origins to effect intervertebral lateroflexion. B, origins (dark) and insertions (lighter) of mm. inclusii on posterior cervical vertebrae of Struthio camelus. Origins are from anterior faces of the costal processes, and insertions are onto the lateral and dorsolateral tubercles. Arrows represent lines of action whereby insertions are drawn towards the origins. C, origins (dark-filled shapes) and insertions (light-filled shapes) of lateral portions of mm. intertransversarii in Caiman crocodylus. Arrows represent lines of action from origin to insertion, by which the muscles would lateroflex the anterior vertebra of each pair relative to the posterior one.
Figure 12. A, origins of m. rectus capitis lateralis (m. r.c.l.) and rectus capitis ventralis (m. r.c.v.) of Corvus brachyrhynchos, from C2 prosessus ventralis. B, all origins of m. r.c.v. from anterior cervicals of another specimen of Corvus brachyrhynchos, and its m. rectus capitis lateralis origin from C2. Both images are ventrolateral views. C, ventrolateral view of m. rectus capitis ventralis (with light outline) of Falco columbarius.
Figure 18. Topological appearance of (A) m. splenius capitis (medial part) and (B) m. longus colli dorsalis/ transversospinalis cervicis, on anterior vertebrae and skull of Tyrannosaurus rex skeleton (AMNH 5027). Note that the parietals are probably closer to the axial neural spine than in neutral life posture, and m. splenius capitis would be longer than shown here. C, topological appearance of m. splenius on another specimen of Tyrannosaurus rex (BHI 3033). M. complexus is also represented, and m. transversospinalis capits is depicted as though reflected back. D, E, appearance of m. longissimus capitis profundus (large anterior muscle), and cervical mm. intertransversarii (bands between transverse processes), on skeleton of Tyrannosaurus rex (AMNH 5027). A′–E′, functional inference strengths of muscles after visualization of inference space in Figure 2. A′, strength of functional inference for m. splenius capitis of tyrannosaurids, for head dorsiflexion and stabilization. The large inference space is possible by morphological and physiological bracketing between homologous muscles in birds and crocodilians. B′, strength of functional inference for m. transversospinalis cervicis of tyrannosaurids, for neck dorsiflexion. Inference strengh is particularly high for this muscle. D′, Level II′ inference for ventroflexion by m. longissimus capitis profundus. E′, inferernce for lateroflexion by mm. interntransversarii, with poor, Level III′ support from physiological data; EMG has been uninformative about mm. intertrans. lateroflexion in extant archosaurs .
› Figure 13. A, the posteriormost subdivision of m. longus colli ventralis of Leptoptilos crumeniferus, depitcted in ventrolateral view. The outlined bellies originate deep in the thoracic region, and insert on light-coloured tendons to the posterior cervical ribs. The inset shows the morphology without highlighting. B, C, anteroventral views of the anterior vertebrae of Asio flammeus, depicting origins (B) and insertions (C), in dark shading, of m. longus colli ventralis. In B arrows represent schematic action of multiple slips of m. l.c.v. converging on an anterior insertion. D, ventral view of insertions (light shading) of m. iliocostalis cervicis onto the cervical ribs of Caiman crocodylus, with arrows representing schematic ventroflexive action. E, cervical vertebrae and ribs of Caiman crocodylus in oblique ventral view, depicting origins (dark shading) of m. rectus capitis ventralis and m. longus capitis, and m. iliocostalis cervicis (lighter shading), from the ventral centra and ventral spinous processes.
Figure 14. Mm. intercristales and mm. cervicales accendentes of birds. A, mm. intercristales shaded dark on the posterior cervicals of Leptoptilos crumeniferus. Inset to left depicts mm. intercristales in context on more of the neck. Recoil of the elastic ligament dorsiflexed the neck in this dissection specimen. B, mm. ascendentes cervicales on the posterior neck of Aquila chrysaetos (light outline). Most of m. transversospinalis capitis has been removed. C, origins and insertions of mm. intercristales (dark shapes), and cervicales ascendentes (lighter shapes), on the posterior cervicals of Struthio camelus. Arrows represent lines of action pulling the insertion towards the origin. In mm. intercristales, origins are from the anterior part of the attachment overlain in blue, and insertions from the posterior part of this area on the next anterior vertebra. For mm. cervicales ascendentes, several slips from posterior vertebrae converge upon a common insertion.
Figure 15. Photographic-style representation of Tyrannosaurus rex (AMNH 5027) neck muscles, with definitive osteological correlates, visible in lateral view. A–C represent successively deeper layers. Varying hues represent transversospinalis, longissimus, iliocostalis and longus derivatives derivatives, respectively. Some muscles are omitted for clarity, including mm. interspinales between neural spines, and m. iliocostalis cervicis that inserted medially on the cervical ribs. M. transversospinalis capitis and cervicis, and m. longissimus capitis superficialis, are drawn as gradients to show tendinous anterior insertions. M. transversospinalis capitis is depicted as reflected downwards to show epipophyses of several vertebrae, to which it would insert and/or posterior parts of M. complexus would originate. M. iliocostalis capitis is rendered as having individual slips that arose from heads of the cervical ribs, one interpretation of this muscle’s osteological origins. M. rectus capitis ventralis originates from the ventral surfaces of the anterior cervicals, and is restored here as passing medial to the anterior cervical ribs. The skull has been displaced slightly anteriorly, to compensate for an anteroposteriorly compressed C1 in this specimen.
Figure 16. Schematic diagram of major neck muscles of Tyrannosaurus rex in dorsal view. A–C represent successively deeper layers, and other conventions are as in Figure 15. M. complexus inserts dorsally on the squamosal, and m. iliocostalis capitis inserts along the ventral edge of the paroccipital process. M. longissimus capitis superficialis inserts between these on the lateral edge of the paroccipital process. In C a probable lateral part of m. spinalis capitis is signified by a ‘? ’ .
Figure 17. A, topological appearance of m. transversospinalis capitis on anterior vertebrae and skull of Tyrannosaurus rex (AMNH 5027). The insertion is inferred as strongly tendinous, and is rendered as white. B, topological appearance of m. longissimus capitis superficialis restored on the same skeleton. The posterior origin was tendinous, and its morphology is depicted as white. C, D, topological appearance of (C) m. complexus and (D) m. iliocostalis capitis on anterior axial skeleton of Tyrannosaurus rex skeleton (AMNH 5027). A′–D′, functional inference strengths of muscles after visualization of inference space in Figure 2. A′, strength of functional inference for m. transversospinalis capitis (m. trans. cap. strong Level I′ inference of dorsiflexion). B′, weaker, Level II′ inference of lateroflexion in m. longissimus capitis superficialis. C′, D′, Level II′ strengths of functional inference for m. complexus (m. compl.) and m. iliocostalis capitis (m. il. cap.).
Figure 23. A, topological appearance of m. rectus capitis ventralis (anterior muscles) and m. iliocostalis cervicis (posteroventrally originating muscles) on anterior axial skeleton of Tyrannosaurus rex (BHI 3033), ventral view. The moment arm for lateral flexion by m. iliocostalis cervicis is superimposed. B, m. r.c.v.: origins of m. rectus capitis ventralis from ventral spinous processes of Tyrannosaurus rex (BHI 3033) with arrow showing course of the muscle. m. il. cerv.: origin from ventral centra and insertions onto ventral fascia of cervical ribs of m. iliocostalis cervicis, with arrow showing course of the muscle. C, insertion of m. rectus capitis ventralis onto basioccipital of Daspletosaurus torosus (CMN 8506; the specimen is incomplete and the image partly mirrored), showing moment arms. Because the tyrannosaurid occiput slopes anteroventrally, the ventroflexion moment arm is somewhat longer than depicted in this view. D, strength of functional inference for head ventroflexion by m. rectus capitis ventralis in Tyrannosaurus rex. E, strength of functional inference for neck lateroflexion by m. iliocostalis cervicis of Tyrannosaurus rex.
Figure 19. A, origins of m. transversospinalis capitis (C2–C9), m. complexus (C2–C5) and m. splenius capitis from C2 and possibly C3, of Tyrannosaurus rex (BHI 3033). B, rugose scarring of m. transversospinalis capitis insertion on parietals of Tyrannosaurus rex (AMNH 5029). C, insertion of m. transversospinalis capitis onto parietals of Daspletosaurus torosus (CMN 8506; the specimen is incomplete and the image partly mirrored), with moment arms for lateral and dorsiflexion. D, insertions and moment arms for m. complexus (two dorsal) and m. iliocostalis capitis (ventral) on occiput of Daspletosaurus torosus (CMN 8506; the specimen is incomplete and the image partly mirrored for clarity).
Figure 20. A, origin scar of m. splenius capitis from C2 of Tyrannosaurus rex (BHI 3033), in anterodorsal view. B, area of possible insertions of m. splenius capitis (medial part) on the occiput of Daspletosaurus torosus (CMN 8506; the specimen is incomplete and the image partly mirrored), with moment arms shown for dorsiflexion and lateroflexion. C, insertions of m. longus colli dorsalis/m. transversospinalis cervicis onto posterior and dorsal surfaces of epipophyses, from C2 to C5. The most prominent insertion is a posteriorly concave scar on the C2 epipophysis. D, centres of rotation (white circles) and moment arms (lines) for insertions of m. longus colli dorsalis/m. transversospinalis cervicis, on cervical vertebrae of Tyrannosaurus rex (BHI 3033). Centres of rotation are estimated to be at positions similar to those Selbie, Thomson & Richmond (1993) determined for intervertebral flexion in cats.
Figure 21. A, origin scars of m. longissimus capitis superficialis (C7–D1 parapophyses) and m. longissimus capitis profundus (C6–C3 parapophyses) of Tyrannosaurus rex (AMNH 5027). B, short moment arm of m. longissimus capitis superficialis for neck plus head dorsiflexion. C, paroccipital process insertions and moment arms of m. longissimus capitis superficialis on Daspletosaurus torosus (CMN 8506). D, basioccipital insertions and moment arms of m. longissimus capitis profundus on Daspletosaurus torosus (CMN 8506; the specimen is incomplete and the images are partly mirrored).
Figure 22. A, origins and insertions of mm. intercristales (top, light-fill shapes), mm. intertransversarii (dark-fill shapes) and an interpretation of dorsal, rib head origins (large light-filled shapes) of m. iliocostalis capitis, of Tyrannosaurus rex (AMNH 5027). B, moment arms for lateroflexion by mm. intertransversarii on C6–C8 of Tyrannosaurus rex (BHI 3033, ventral view).