THE ANATOMICAL RECORD 292:12461265 (2009)

New Insights Into Dinosaur JawMuscle Anatomy

CASEY M. HOLLIDAY*

Department of Pathology and Anatomical Sciences, School of Medicine,University of Missouri, Columbia, Missouri

ABSTRACTJaw muscles are key components of the head and critical to testing

hypotheses of soft-tissue homology, skull function, and evolution. Dinosaursevolved an extraordinary diversity of cranial forms adapted to a variety offeeding behaviors. However, disparate evolutionary transformations in headshape and function among dinosaurs and their living relatives, birds and croc-odylians, impair straightforward reconstructions of muscles, and other impor-tant cephalic soft tissues. This study presents the osteological correlates andinferred soft tissue anatomy of the jaw muscles and relevant neurovascula-ture in the temporal region of the dinosaur head. Hypotheses of jaw musclehomology were tested across a broad range archosaur and sauropsid taxa tomore accurately infer muscle attachments in the adductor chambers of non-avian dinosaurs. Many dinosaurs likely possessed m. levator pterygoideus, atrait shared with lepidosaurs but not extant archosaurs. Several major cladesof dinosaurs (e.g., Ornithopoda, Ceratopsidae, Sauropoda) eliminated the epi-pterygoid, thus impacting interpretations of m. pseudotemporalis profundus.M. pseudotemporalis supercialis most likely attached to the caudoventralsurface of the laterosphenoid, a trait shared with extant archosaurs. Althoughmm. adductor mandibulae externus profundus and medialis likely attachedto the caudal half of the dorsotemporal fossa and coronoid process, clear osteo-logical correlates separating the individual bellies are rare. Most dinosaurclades possess osteological correlates indicative of a pterygoideus ventralismuscle that attaches to the lateral surface of the mandible, although the mus-cle may have extended as far as the jugal in some taxa (e.g., hadrosaurs,tyrannosaurs). The cranial and mandibular attachments of mm adductormandibulae externus supercialis and adductor mandibulae posterior wereconsistent across all taxa studied. These new data greatly increase theinterpretive resolution of head anatomy in dinosaurs and provide the anatom-ical foundation necessary for future analyses of skull function and evolutionin an important vertebrate clade. Anat Rec, 292:12461265, 2009. VVC 2009Wiley-Liss, Inc.

Keywords: Dinosaur; functional morphology; jaw muscles

The dinosaur feeding apparatus comprised a compli-cated network of jaw muscles that span an intricateassemblage of intracranial joints that link the bones ofthe skull together. Data from jaw muscles, such as theirhomologies, attachments, and sizes, are important totest hypotheses of cranial function and feeding behaviorssuch as powered cranial kinesis, bite force estimation,chewing behavior, and mechanical optimization. Not sur-prisingly, jaw muscle reconstruction is a common prac-tice among paleobiologists. However, despite a longhistory of muscle reconstruction and soft-tissue infer-

Grant sponsor: NSF; Grant number: IBN-0407735; Grantsponsors: Marshall University School of Medicine, The JurassicFoundation, Ohio University Student Enhancement Award.

*Correspondence to: Casey M. Holliday, Department of Pa-thology and Anatomical Sciences, School of Medicine, Univer-sity of Missouri, Columbia, MO 65211. Fax: 573-882-4612.E-mail: hollidayca@missouri.edu

Received 9 June 2009; Accepted 9 June 2009

DOI 10.1002/ar.20982Published online in Wiley InterScience (www.interscience.wiley.com).

VVC 2009 WILEY-LISS, INC.

ences in dinosaur science, several challenges still impedethe development of precise hypotheses of structure, func-tion, and evolution of the jaw muscles in the group.Major cranial structures including the antorbital cavity(Witmer, 1997; Molnar, 2008), ceratopsid frills (Lull,1908; Dodson, 1996), and buccal emarginations (Galton1973; Knoll, 2008) have only relatively recently beenidentied as non-muscular structures. Regardless, thebasic anatomy of the adductor chamber of dinosaurs hasnot been thoroughly reviewed in a comparative contextand numerous issues still impact the interpretations ofthe regions evolution.Many previous analyses of dinosaur jaw muscle anat-

omy framed their hypotheses on a broadly comparativeframework (e.g., Dollo, 1884; Lull, 1908; Versluys, 1910;Russell, 1935; Janensch, 1936; Ostrom, 1961, 1966;Haas, 1963). With the advent of cladistic methodologies,it is possible to bring increased rigor permitted by phylo-genetically constrained methods such as the Extant Phy-logenetic Bracket approach (Bryant and Russell, 1992;Witmer, 1995a, 1997). In the past, workers reconstructedmuscles based on mammalian anatomy (Dollo, 1884;Russell, 1935) and even included a muscular cheek intheir reconstructions (Lull, 1908). Haas (1955), Ostrom(1961, 1964), and later Norman (1984) re-evaluatedmany earlier descriptions and included their own newinsights on several clades of dinosaurs whereas drawingmore from lepidosaur anatomy.Soft-tissue inferences in fossils carry their own pitfalls

and caution is necessary when reconstructing the mus-culature of extinct animals, particularly when their feed-ing behaviors may differ substantially from their extantrelatives (Haas, 1969; Bryant and Seymour, 1990;Witmer, 1995a,b; Carrano and Hutchinson, 2002;Holliday and Witmer, 2008). Parsimony necessitates con-servative inferences of jaw muscle anatomy. However,because archosaurs are so morphologically diverse andvariation in jaw muscle morphology certainly existsamong sauropsids (Haas, 1973; Schumacher, 1973;Buhler, 1981; Busbey, 1989; Vandenberge and Zweers,1993; Iordansky, 1973; Wu, 2003; Holliday and Witmer,2007), phylogenetic bracketing may still be inadequatefor all soft-tissue inferences and in some cases, compel-ling evidence may override conservative interpretations.Interpretations of muscle scars can be problematic

(McGowan, 1979; Bryant and Seymour, 1990; Bryantand Russell, 1992; Rieppel, 2002) and correspondence ofthe muscle-bone relationship in the head has only beentested in a few cases (e.g., Montanucci, 1989, Witmer,1995b, 1997; Hieronymus, 2002). Osteological correlatescan indicate the presence, attachment site, and to someextent, the size of a jaw muscles attachment. Tendinousor aponeurotic attachments leave more robust musclescars than eshy attachments, though eshy attach-ments can be equally informative (Bryant and Sey-mour, 1990; Bryant and Russell, 1992, Carrano andHutchinson, 2002). In general, osteological correlates ofjaw muscles are common among extant sauropsids,although particular clades appear prone to having morewell-developed correlates than others have. For example,the temporal bones of extant crocodylians offer a richtapestry of fossae and ridges that consistently reect theattachments of particular muscle bellies, their aponeuro-ses, and adjacent neurovasculature (Iordansky, 1973;Holliday and Witmer, in press). However, the temporal

bones of lizards seemingly offer fewer tendinous corre-lates despite the presence of large aponeuroses, such asthe quadrate aponeurosis and the bodenaponeurosis.Osteological correlates are highly susceptible to thevagaries of ontogeny and it is to be expected that juve-nile individuals have fewer osteological correlates thanmore mature individuals do. In addition to these morediscrete correlates, Hutchinson (2001a) introduced theconcept of bone surface homology to refer to the corre-spondence of general osteological regions that are contin-uous through evolution. In the head, examples ofhomologous bone surfaces may include the lateral sur-face of the parietal and dorsal surfaces of the pterygoid,which m. adductor mandibulae externus profundus andm. pterygoideus dorsalis consistently attach to, respec-tively. However, homologous bony surfaces and their cor-responding muscles are more difcult to identify on thequadrate, which underwent signicant morphologicaland myological transformations in different sauropsidclades (Holliday and Witmer, 2007). These evolutionarychanges can prove to be problematic in soft-tissuereconstruction.Caveats aside, reconstructing jaw muscle anatomy

remains an important task necessary to better under-stand cranial function and behavior in extinct animals.Osteological correlates have proven useful in recon-structing soft tissues and tracking their evolution in thecephalic (Witmer 1995a,b, 1997; Snively and Russell;2007) and postcranial anatomy (e.g., Hutchinson,

TABLE 1. List of anatomical abbreviations

aIC Internal carotid arteryaMN Mandibular arteryasp Ascending process of pterygoidaST Stapedial arterycot Cotylecr Crestect Ectopterygoidept Epipterygoidlig Ligamentls Laterosphenoid;mAMEM m. adductor mandibulae externus medialismAMEP m. adductor mandibulae externus profundusmAMES m. adductor mandibulae externus supercialismAMP m. adductor mandibulae posteriormDM m. depressor mandibulaemLPt m. levator pterygoideusmPPt m. protractor pterygoideusmPSTp m. pseudotemporalis profundusmPSTs m. pseudotemporalis supercialismPTd m. pterygoideus dorsalismPTv m. pterygoideus ventralisn,aIM Internal mandibular nerve and arterynCID Nerve to constrictor internus dorsalis musclespal Palatinept Pterygoidqj Quadratojugalqu Quadrateri Rictussh Surangular shelftcr Tensor crestV1 Ophthalmic nerveV2 Maxillary nerveV3 Mandibular nerveVIIhy Hyomandibular ramus of facial nerveVIIpal Palatine ramus of facial nerve

DINOSAUR JAW MUSCLE ANATOMY 1247

2001a,b; Carrano and Hutchinson, 2002; OConnor,2006) of extinct archosaurs. Although many species mayshare numerous features with extant taxa, other derivedgroups, such as hadrosaurs and oviraptorosaurs, presenta number of unique challenges. Numerous studies havefocused on the jaw muscle anatomy of single taxa thoughno study has surveyed jaw muscle anatomy across theentire clade. To allay this gap, this article reviews thehomologies and phylogenetic support of the different jawmuscles with a focus on those of non-avian dinosaurs. Ituses the Extant Phylogenetic Bracket approach (Witmer,1995a) to constrain inferences of soft tissues in fossiltaxa and relies on the archosaur soft-tissue homologiesprovided by Holliday and Witmer (2007). It presentsphylogenetically constrained rules of construction forjaw muscle anatomy and a generalized atlas of dinosauradductor chamber anatomy, including the osteologicalcorrelates and their inferred soft-tissues. Tables 1 and 2list anatomical and institutional abbreviations.

MATERIALS AND METHODS

Anatomical data were analyzed within the frameworkof the Extant Phylogenetic Bracket approach (EPB),which uses the principle of parsimony to infer soft tis-sues in extinct taxa (see Witmer 1995a,b, 1997; Carranoand Hutchinson, 2002). First, the adductor chambers ofextant archosaur and reptile taxa were examined toidentify patterns of topological similarity in jaw musclesand surrounding soft-tissues and to suggest hypothesesof soft tissue homology (Fig. 1). These patterns wereidentied from dissections, computed tomographic (CT)data, and observations of over 100 extant fresh and ske-letonized crocodylian, avian, lepidosaurian, and testu-dine taxa described in Holliday and Witmer (2007).Second, causally associated osteological correlates ofthese soft tissues were identied in the skeletons ofextant taxa (Fig. 1BD). For example, in mammals, par-ticular muscles (e.g., the temporalis muscle) consistentlyleave a fossa or crest on the skull (e.g., temporal fossa)that is used to infer the presence of that muscle whencadaveric specimens are unavailable. Last, presumablyhomologous osteological correlates of jaw muscles and

relevant soft tissues were identied across a largeassemblage of fossil archosaur material including basalarchosaurs, crurotarsans, and non-avian dinosaurs (Fig.1A, Table 3). These osteological data, which are the focusof this article, serve as proxies for the soft tissues in thefossil taxa and thereby form the congruence test ofhomology (Patterson, 1982; Witmer, 1997) used to inferthe positions and homologies of jaw muscles and rele-vant neurovasculature using the phylogenetically basedscoring procedure of the EPB.The EPB relies on drawing anatomical inferences from

not only fossil taxa, in this case non-avian dinosaurs,but also that clades closest-related, extant bracketingtaxa (birds and crocodylians) and nally outgroup taxa(lepidosaurs and testudines) (Fig. 1A). Given the aboveassumption that causally associated osteological corre-lates are homologous among extant and fossil taxa (i.e.,the congruence test is sound), soft-tissue inferences canbe rened further based on the phylogenetic distributionof the osteological correlates among fossil and extantclades. A soft tissue, in this case a muscle, can be inter-preted as a level I, II, or III inference depending on thepresence of the muscles correlate in: both extant brackettaxa and the fossil taxon; one extant taxon plus the fos-sil taxon; or only the fossil taxon, respectively. Addition-ally, the reconstruction of the correlated soft tissue,along with consistent topological patterns recognized inthe extant groups, can subsequently dictate whereneighboring structures should have been (i.e., the maxil-lary nerve, neighboring muscle) and vice versa. If noclear osteological correlates are present among theextant bracket taxa despite the presence of the soft tis-sue, the levels of inference can then be assigned aprime designation (e.g., I0, II0, III0) in which each sub-ordinate prime level is a weaker inference (i.e., it drawsless phylogenetic support) than its predecessor in the hi-erarchy. Following Carrano and Hutchinson (2002), indi-vidual muscle attachments may vary in theirdistribution, therefore, whereas the cranial attachmentof a muscle may have a Level I inference, its mandibularattachment may only be a Level 2 inference.

RESULTSOverview of Adductor ChamberOsteological Correlates

Despite the relative ubiquity of fossae, crests, tuberos-ities, spurs, anges, and other muscle-related bonystructures in the skulls of dinosaurs and other reptiles(Figs. 24), these correlates are quite plastic and canvary among individuals of the same taxon, let aloneamong different taxa. This phenomenon is in part likelydue to ontogenetic differences among individuals of awell-represented taxon. In juvenile Brachylophosaurus,the cranial correlate of m. levator pterygoideus is a fossa(Fig. 2A), whereas in an adult specimen (Fig. 2B), thecorrelate is a long, striated spur. As in Brachylophosau-rus, this spur for m. levator pterygoideus may slightlyoverhang the ophthalmic groove, or as in Lambeosaurus(Figs. 2C and 5B), it may drape ventrally to then fuseonto the basisphenoid, forming a separate ophthalmic fo-ramen. However, many adult individuals may also havedifferent osteological correlates. Among Tyrannosaurusindividuals, only one observed individual (AMNH 5117)possesses a crest in the temporal fossa (Fig. 5C) that

TABLE 2. List of institutional abbreviations

AMNH American Museum of Natural HistoryANS Academy of Natural SciencesBMNH British Museum of Natural HistoryBP Bernard Price InstituteCM Carnegie MuseumCMN Canadian Museum of NatureCMNH Cleveland Museum of Natural HistoryDMNH Denver Museum of Natural HistoryDNM Dinosaur National MonumentFMNH Field Museum of Natural HistoryIGM Mongolian Geological InstituteMCZ Museum of Comparative ZoologyMOR Museum of the RockiesMNN Musee National du NigerROM Royal Ontario MuseumSGM Ministe`re de lEnergie et des MinesTMP Royal Tyrell Museum of PaleontologyUMNH Utah Museum of Natural HistoryUSNM United States National MuseumZG Zigong Dinosaur Museum

1248 HOLLIDAY

Fig. 1. Anatomy and phylogeny of dinosaurs and their extant archo-saur and outgroup relatives.(A) Phylogenetic relationships of dinosaurs,extant bracketing taxa, and outgroups. Extant clades in bold. Numberednodes: 1, Sauropsida; 2, Archosauria; 3, Dinosauria; 4, Ornithischia; 5,Thyreophora; 6, Ornithopoda; 7, Ceratopsia; 8, Saurischia; 9, Sauropoda;10, Theropoda; 11, Coelurosauria; 12, Maniraptora; 13, Aves. (B) Muscle

attachment surfaces in the skull and mandible of the monitor lizard (Vara-nus exanthematicus); (C) Muscle attachment surfaces in the skull andmandible of the chicken (Gallus gallus); (D)Muscle attachment surfaces inthe skull and mandible of the alligator (Alligator mississippiensis). Homolo-gous muscles are similarly color coded throughout gures.

DINOSAUR JAW MUSCLE ANATOMY 1249

marks the separation between m. pseudotemporalissupercialis rostrally, from m. adductor mandibulaeexternus profundus, caudally. Homologous crests areabsent in MOR 555, MOR 1125, CMN 11841, and TMP83.30.1. On the other hand, related taxa such as Nano-tyrannus, individuals of Daspletosaurus (Fig. 3I), as wellas other theropods (Fig. 3C,D) possess these crests.

Finally, different taxa have arguably homologous, butincredibly morphologically dissimilar osteological corre-lates that preclude straightforward ranking systems.This problem is best represented by the coronoid attach-ments of m. adductor mandibulae externus profundus onthe mandible. Among theropods, the correlate variesbetween a shallow depression, a smooth, at area, or asmall, rugose tuberosity, referred to here as the coronoideminence (Fig. 4J,K). On the other hand, the osteologicalcorrelate takes the form of a huge boss in some taxa,such as Panopolosaurus (Fig. 4G). Finally, the coronoidprocesses of derived ceratopsids and hadrosaurs arecharacteristically dorsally elongate, may or may nothave striations on them (Fig. 4). The loss of bony ele-ments also inuences interpretations of muscles andtheir osteological correlates. Several clades of dinosaurslost the epipterygoid (Fig. 6), which is the origin of m.pseudotemporalis profundus. Just because the elementwas lost, does not necessarily mean the muscle was too,because birds also lost the epipterygoid but still havethe muscle. However, epipterygoid loss creates a greaterchallenge when inferring whether the muscle shifted asin Brachylophosaurus (Fig. 2A,B) or if it is absent. Thus,these issues make scoring osteological correlates ofmuscles as a means of character mapping a complicated,if not largely subjective procedure.

Overview of Adductor ChamberSoft Tissue Anatomy

In general, jaw muscles are divided into groups basedon their topological relationships with the branches of thetrigeminal nerve (Lakjer, 1926; Holliday and Witmer,2007). These muscle groups include m. constrictor inter-nus dorsalis, and mm. adductor mandibulae internus,externus, and posterior, most of which are then further di-vided into smaller muscle bellies. With a few exceptions,such as extant crocodylians, the muscles maintain thesame topological relationship with numerous other softtissues among tetrapods (Holliday and Witmer, 2007;Holliday and Witmer, in press). It is expected that thesesame topological patterns were present in dinosaurs aswell and there are no data to suggest otherwise. There-fore, if the grooves or foramina for the ophthalmic nerve(V1) and stapedial (aST) and internal carotid (aIC)arteries, which, for example, circumscribe the dorsal andcaudal margins of the origin of m. protractor pterygoideuson the basisphenoid, reasonable inferences of the musclesattachment location can be made, regardless of the pres-ence of a clear osteological correlate (Fig. 5). Similarly, themandibular nerve (V3) and artery (aMN), always passbetween mm. adductor mandibulae externus and poste-rior in the temporal region, and then once they are in themandibular fossa, they pass lateral and rostral to m.adductor mandibulae posterior. The mandibular neuro-vascular bundle then gives off lateral and medial (i.e.,mylohyoid nerve) mandibular branches. Thus, if the posi-tion of the muscle can be inferred (which is consistentlythe medial mandibular fossa), the location of the neuro-vascular bundle can also be inferred regardless if theyleave a groove or foramen. Finally, in all non-crocodyliansauropsids, the maxillary nerve (V2) passes between mm.pseudotemporalis supercialis and adductor mandibulaeexternus profundus before turning rostrally toward thesuborbital region. In the Triceratops braincase, MOR 699,

TABLE 3. List of fossil non-avian dinosaur taxastudied and their identication numbers

Taxon Specimen identication

ThyreophoraScelidosaurus BMNH R1111Stegosaurus CM 41681, DMNH 2818,

USNM 4932, USNM 6645,USNM 2274

Panoplosaurus ROM 20892, ROM 1215Euplocephalus TMP 91.127.1, TMP 97.132.01Edmontonia NMC 8531

CeratopsiaPsittacosaurus IGM 100/1132Leptoceratops CMN 8887, CMN 8889Protoceratops IGM 100/1246Montanaceratops AMNH 5244Arrhinoceratops USNM 15583Triceratops CMN 8528, MOR 699, MOR 1120,

MOR 1157, MOR 1194,UCMP 113697, UCMP137266, USNM 5740,USNM 4286, USNM 24216

Chasmosaurus TMP 79.11.156, TMP 83. 25.1,TMP 85.56.27, TMP87.20.247, TMP 80.18.199,TMP 86.18.11, TMP 86.18.82,TMP 98.68.08, TMP 81.18.86,TMP 96.12.295, TMP 80.16.866,TMP 90.36.390, TMP 89.18.86,TMP 65.12.03, TMP 80.16.866,TMP 90.36.390

Centrosaurus CMN 348, ROM 43214, ROM 767Brachyceratops USNM 7951Einosaurus MOR 456, MOR 492Pachyrhinosaurus TMP 89.55.188, TMP 89.55.1072,

TMP 87.55.101Albertaceratops TMP 2002.69.01

PachycephalosauriaHomalocephale Cast of IGM 100/51Stegoceras AMNH 6788Stenotholus AMNH 25375Pachycephalosaurus USNM 12031

OrnithopodaLesothosaurus BMNH R2477Hypsilophodon BMNH R197Thescelosaurus ROM 8537Parksosaurus ROM 804Orodromeus MOR 1141Zephyrosaurus MCZ 4392Tenontosaurus MOR 682Camptosaurus USNM 5669Brachylophosaurus CMN 8893, MOR 1071Maiasaura MOR 693Edmontosaurus CMN 2288, CMN 2289,

MOR 003, ROM 658,USNM 4737, UCMP 130156

Prosaurolophus ROM 667, MOR 454Kritosaurus AMNH 5204Gryposaurus ROM 873, ROM 44770Tsaagan IGM 100/1015Velociraptor AMNH 6515

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Fig. 2. Osteological correlates of the orbitotemporal and temporalregions. Photos have been standardized to left, lateral views for simplic-ity. White arrows: correlate for m. levator pterygoideus; black arrows,correlate for m. protractor pterygoideus. Scale bar equals 1 cm. (A) Bra-chylophosaurus (juvenile; MOR 1071); (B) Brachylophosaurus (adult;

MOR 1071); (C) Lambeosaurus (CMN 2869); (D) Protoceratops (IGM100/1246); (E) Pachyrhinosaurus (TMP 89.55.188); (F) Triceratops (MOR1120); (G) Plateosaurus (AMNH 6810); (H) Camarasaurus, CM 11378; I,Nigersaurus, MNN GAD 512; (J) Majungasaurus (FMNH PR2100); (K)Daspletosaurus (TMP 94.143.1); (L) Tsaagan, IGM 100/1015.

DINOSAUR JAW MUSCLE ANATOMY 1251

Fig. 3. Osteological correlates of the temporal region and palate.Scale bar equals 1 cm. Braincases in dorsal view: (A) Edmontosaurus(CMN 2289); (B) Leptoceratops (CMN 889); (C) Troodon (TMP82.19.23); (D) Carcharodontosaurus (SGM Din 1; left, lateral view); (E)Herrarasaurus (MCZ 7064); (F) Daspletosaurus (CMN 8506). Palates:

(G) Triceratops (MOR 699; left, lateral view) (H) Same as (G) close upof left, medial view; (I) Brachylophosaurus (MOR 1071; left, lateralview); J, Plateosaurus (AMNH 6810, left, lateral view); (K) Camarasau-rus (CMN 11378 left, lateral view of CT-scan-rendered image); (L) Das-pletosaurus (TMP 2001.36.1; left, lateral view).

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the maxillomandibular foramen is situated directly ven-tral to the laterosphenoid buttress, which is rather rostralto where the foramen is in many dinosaurs (Fig. 5A).However, the foramen is angled caudally and has a longgroove on its caudal edge, suggesting that the maxillary(and mandibular) nerves are pushed caudally by m. pseu-

dotemporalis supercialis, which otherwise has no clearosteological correlate on the braincase. Thus, nerve fora-men morphology can help identify the presence of particu-lar muscles. These examples illustrate how neurovasculartissues, muscles, and their osteological correlates canreciprocally illuminate one another.

Fig. 4. Osteological correlates of the mandible. Scale bar equals 1cm. (A) Thescelosaurus (ROM 3587; left, lateral view); (B) Edmontosau-rus (CMN 2289; right, medial view); (C) indet. hadrosaur (ROM 1949;left, lateral view); (D) Leptoceratops (CMN 8889; left, lateral view); (E)Centrosaurus (ROM 767; left, lateral view); (F) Stegosaurus (CM 41681;

right, medial view); (G) Panoplosaurus (ROM 1215; right, medial view);(H) Plateosaurus (AMNH 6810; right, medial view); (I) Camarasaurus(CM 11378; right, medial view); (J) Dromaeosaurus (AMNH 5356; left,lateral view); (K) Tyrannosaurus (MOR 008, right, medial view); (L) Cae-nognathus (ROM 8776; left, lateral view).

DINOSAUR JAW MUSCLE ANATOMY 1253

In addition to topological patterns, the regions ofattachment can also be used to categorize the differentmuscle groups into the temporal muscles (e.g., mm.pseudotemporalis supercialis and adductor mandibulaeexternus profundus), palatal muscles (e.g., mm. pterygoi-deus and adductor mandibulae posterior), and the jawopening muscle m. depressor mandibulae. Many saurop-sids, including most dinosaurs, also maintain m. con-strictor internus dorsalis muscles that span theorbitotemporal region between the braincase and thepalate (Haas, 1973; Rieppel, 2002; Holliday and Witmer,2008). This organization will be used in the Resultssection later in which each muscle name will be followedby its abbreviation and general levels of inference for itsorigin and insertion in the format: Muscle name (abbre-viation-origin/insertion). Table 4 lists the hypotheses ofmuscle homologies from Holliday and Witmer (2007), themuscles general attachments and their respective EPBinference level for their origin and insertion.

Orbitotemporal Muscles

M. tensor periorbitae (mTPLevel I/II0). M. ten-sor periorbitae (i.e., m. levator bulbi) attaches to the ros-tral edge of the prootic in lepidosaurs and a prominentcrest on the lateral surface of the laterosphenoid in croc-odylians and birds (Haas, 1973; Elzanowski, 1987). Themuscle then attaches to the rostral portion of the orbitalseptum in birds and lepidosaurs and to the preotic pil-lars in crocodylians, forming a sling under the orbitalcontents in all taxa. All dinosaurs possess the caudalosteological correlate of m. tensor periorbitae: the later-osphenoid buttress, or antotic crest, making its recon-struction a Level 1 inference. This sharp edge of thelaterosphenoid is the attachment of the muscle andclearly separates the temporal region from the orbitalregion (e.g., Fig. 2). In some cases, the muscle creepsonto the rostral surface of the laterosphenoid, as inMajungasaurus (Fig. 2J). On the other hand, correlatesfor the muscles rostral attachment are yet to be found.

M. levator pterygoideus (mLPtIII/III). In lepido-saurs, m. levator pterygoideus originates on the lateralsurfaces of the parietal and prootic (e.g., Lakjer, 1926;Haas, 1973). This small muscle passes ventrally to inserton the ventromedial surface of the epipterygoid and isthought to help modulate movements of the palate dur-ing feeding, particularly in taxa that express cranialkinesis (Holliday and Witmer, 2008). The muscle isabsent in birds and crocodilians, although likely becauseof different phenomena. Both extant archosaur cladeslost the epipterygoid, but crocodilians sutured the palateto the braincase, thereby eliminating the orbitotemporalspace altogether. Some avian taxa occasionally possess ashort ligament between the braincase and thequadrate that may be a rudiment of m. levator pterygoi-deus or the epipterygoid (Dzerzhinsky and Yudin, 1982).M. levator pterygoideus does not leave any consistentosteological correlates on the cranium or palate inlepidosaurs.Reconstructions of m. levator pterygoideuss cranial

and palatal attachments are Level III or III0 inferences,the weakest possible soft-tissue inference (Table 4).Regardless, osteological and topological data, and sup-port from lepidosaurian outgroups, indicate many non-

Fig. 5. Muscle attachments, trigeminal nerves, and arteries of thebraincases of select dinosaurs in left, lateral view. (A) Triceratops; (B)Brachylophosaurus; (C) Tyrannosaurus.

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Fig. 6. Palate anatomy and evolution in non-avian dinosaurs. (A) Palate morphology and homoplasticepipterygoid loss in non-avian dinosaurs; Palates with muscle attachments in left, lateral view of: B, Tri-ceratops; C, Brachylophosaurus; D, Tyrannosaurus.

DINOSAUR JAW MUSCLE ANATOMY 1255

avian dinosaurs likely possessed the muscle. Numerousdinosaur taxa possess clear osteological correlates attrib-utable to this muscle on the laterosphenoid. Cranialosteological correlates of m. levator pterygoideus can beidentied in ceratopsids, ornithopods, some neosauro-pods, and tyrannosaurs (Fig. 3). However, clear corre-lates cannot be easily identied in thyreophorans anddeinonychosaurs (Fig. 2L). The muscles scars are mor-phologically diverse ranging from small fossae (Fig. 2A)to large tuberosities (Fig. 2K). Despite these differencesin shape, the correlates are always found just dorsal tothe ophthalmic groove or lateral to the ophthalmic fora-men when present, and ventral to the epipterygoidcotyle on the laterosphenoid. The only soft tissue thatoccupies this region of the braincase in extant taxa is m.levator pterygoideus. Thus, despite weak phylogeneticsupport from extant bracketing taxa, the topological andosteological support for inferring the presence of themuscle is strong. The levator pterygoideus muscle doesnot leave any robust osteological correlates in most dino-saur taxa. However, in ceratopsids and hadrosaurs, alarge, striated ange arises dorsally from the pterygoidthat suggests the presence of a large, tendinous levatorpterygoideus attachment (Fig. 3GI).

M. protractor pterygoideus (mPPtII/II0). M.protractor pterygoideus attaches to the ventrolateralsurface of the basisphenoid in lepidosaurs or parabasi-sphenoid in birds ventral to the ophthalmic groove androstrolateral to the internal carotid foramen. The muscleonly occasionally leaves a small crest or spur on thebraincase of birds, but in lepidosaurs, the muscle occu-pies the triangular ala basisphenoid, whose border is

excavated by the surrounding neurovasculature such asthe stapedial and internal carotid arteries (Fig. 5). Croc-odyliforms lost m. protractor pterygoideus once the pal-ate was rmly sutured to the braincase (Fig. 1D).However, rauisuchians, such as Saurosuchus, also havean ala basisphenoid suggesting these taxa possessed themuscle (Holliday and Witmer, in press). Reconstructionsof the protractor pterygoideus musculature are Level IIinferences for the braincase origin. Like that of lizards,the dinosaur ala basisphenoid is roughly triangular butvaries in morphology ranging from small tubercles oranges in ankylosaurs and deinonychosaurs (Fig. 2L) tolarge rugose bosses such as those found in tyrannosaurs,hadrosaurs, and ceratopsids (Fig. 2). During manirap-toran evolution, the ala basisphenoid regresses leavingno easily discernable cranial correlate for m. protractorpterygoideus on the braincase, shifting the cranialattachment site inference from a Level II to II0. Whereasthe dromaeosaurs Velociraptor and Tsaagan (Fig. 2L)have a small ala basisphenoid, the troodontid Saurorni-thoides, and basal bird Archaeopteryx both lack the fea-ture. Because extant birds still possess this muscle andsome taxa do have small bony spurs indicative of themuscles attachment, it is reasonable to infer that theirclosest theropod ancestors also possessed the muscle.The protractor muscle attaches along the medial surfa-ces of the pterygoid and quadrate in extant taxa andlikely does the same in dinosaurs. However, the muscledoes not leave any marked scars indicative of its attach-ment to the pterygoid or quadrate making the palatalinsertion a Level II0. The lack of a palatal correlate of m.protractor pterygoideus suggests a eshy attachmentwas present. But because the middle ear cavity, whichdirectly abuts the protractor muscle, also leaves similar

TABLE 4. The jaw muscles of extant and extinct sauropsids coupled with each muscle attachmentsgeneral level of inference in non-avian dinosaurs

Level of inference

Abbreviation Full name Origin Insertion

mTP m. tensor periorbitae Laterosphenoid buttress I Rostral border of orbit II0MLPt m. levator pterygoideus Laterosphenoid dorsal to

ophthalmicforamen/groove

III Medial surface ofpterygoid and epipterygoid

III

MPPt m. protractorpterygoideus

Ala basisphenoid ventral toophthalmic foramen/groove

II Medial surface ofpterygoid and quadrate

II0

MPTd m. pterygoideusdorsalis

Dorsal surface ofrostral portionof pterygoid and palatine

I Medial surface of articular I

MPTv m. pterygoideusventralis

Caudoventralsurface of pterygoid

I Lateral surface ofarticular and surangular

I

mPSTp m. pseudotemporalisprofundus

Lateral surface ofepipterygoid

I0 Medial surface ofsurangular/medialmandibular fossa

I0

mPSTs m. pseudotemporalissupercialis

Rostromedial portion oftemporal fossa

I Medial surface of coronoideminence/rostral medialmandibular fossa

II0

mAMEP m. adductor mandibulaeexternus profundus

Caudomedial portionof temporal fossa

I Coronoid eminence I

mAMEM m. adductor mandibulaeexternus medialis

Caudolateral portionof temporal fossa

I Coronoid eminence/dorsomedialsurface of surangular

I0

mAMES m. adductor mandibulaeexternus supercialis

Medial surface ofupper temporal bar

I Dorsolateral surfaceof surangular

I

mAMP m. adductor mandibulaeposterior

Lateral surfaceof quadrate

I Medial mandibular fossa I

1256 HOLLIDAY

correlates on the medial surface of the quadrate andpterygoid, it remains difcult to determine the expanseand size of either the air sac or muscle. Finally, the alabasisphenoid is often excavated by a neurovasculargroove and is particularly prominent in large taxa suchas Triceratops, Brachylophosaurus, and Tyrannosaurus(Fig. 4). Ostrom (1961) inferred this groove in hadro-saurs to be for the maxillary and mandibular nerves asthey coursed ventrally from the maxillomandibular fora-men. However, when the palate is articulated with thebraincase, this groove lies well medial and ventral to thepterygoid, a position quite different from the positionwhere the nerve is found in other sauropsids. Thesegrooves on the ala basisphenoid are most likely for theneurovascular bundle (nCID) that supplies the protrac-tor muscles and other constrictor internus dorsalismuscles.

Palatal Muscles

M. pseudotemporalis profundus (mPSTpI/I).M. pseudotemporalis profundus attaches to the lateralsurface of the epipterygoid in lepidosaurs (Fig. 1B), thelateral bridge of the laterosphenoid in crocodylians, andthe orbital process of the quadrate in birds (Vandenbergeand Zweers, 1993; Holliday and Witmer, 2007). The mus-cle then attaches along the dorsomedial surface of themandible in lepidosaurs and birds. In crocodylians, themuscle is vestigial and variably merges with the bersof the medial surfaces of the temporal muscles. Thereare no clear osteological correlates of the musclesattachment to the mandible, whereas those to the cra-nium are fairly robust. Reconstructions of m. pseudotem-poralis profundus are level I inferences in dinosaursthat have epipterygoids. However, because crocodyliansand birds eliminated the epipterygoid and shifted theposition of the muscle (for reviews see Holliday andWitmer, 2007, 2008, in press) interpretations of dinosauranatomy may not be clear. Among dinosaurs, the musclelikely attached to the lateral surface of the epipterygoid,as in lizards, and the surface of the bony element inlarge theropod taxa occasionally has a fossa suggestingthe attachment of this muscle. However, several cladesof dinosaurs also lost the epipterygoid including hadro-saurs, ceratopsids, and sauropods (Fig. 6). The positionof the origin of m. pseudotemporalis profundus in cera-topsids and sauropods is unclear and it is possible thatthey lost the muscle. However, ornithopods (e.g., Figs.2A,B and 5B) often have a fossa present between theinferred origins of mm. levator pterygoideus and pseudo-temporalis supercialis that may be for m. pseudotem-poralis profundus. Mandibular attachments of themuscle are ill-dened and it is inferred that, like thoseattachments of extant taxa, the muscle likely attachedalong the medial surface of the coronoid process orsurangular.

M. pterygoideus dorsalis (mPTdI/I). M. ptery-goideus dorsalis originates along the dorsal surfaces ofthe pterygoid and palatine bones in lepidosaurs, crocody-lians, and birds (Witmer, 1995b, 1997). The muscle theninserts onto the medial surface of the articular and ret-roarticular process. The rostral extent of the palatalattachments of m. pterygoideus dorsalis can be difcultto discern from the equally smooth and excavated surfa-

ces left by the nasal passages and paranasal air sinusesin dinosaur taxa (Witmer, 1997). Occasionally, a smallcrest on the inner surface of the maxilla or lateral sur-face of the palatine may demarcate the shift from a mus-cle attachment caudally to the caviconchal recess andantorbital cavity rostrally. However, these structures arerare or often distorted in fossil taxa. The mandibularattachments of m. pterygoideus dorsalis are well sup-ported by the common presence of a smooth excavationalong the medial surface of the retroarticular process of

Fig. 7. Mandibular anatomy and m. pterygoideus ventralis attach-ment hypotheses in two derived non-avian dinosaurs. (A) Brachylo-phosaurus: right, conservative, ventral mandibular attachment of m.pterygoideus ventralis; left, osteological correlates suggest a jugalattachment of the muscle; (B) soft-tissue anatomy of the medial por-tion of the mandible of the hadrosaur Edmontosaurus; (C) Nanotyran-nus: right, conservative, ventral mandibular attachment of m.pterygoideus ventralis; left, osteological correlates suggest a jugalattachment of the muscle; (D) soft-tissue anatomy of the medial por-tion of the mandible of the theropod Tyrannosaurus.

DINOSAUR JAW MUSCLE ANATOMY 1257

Fig. 8. Jaw muscle anatomy in three dinosaurs in lateral view. Right, supercial muscles; left, deepermuscles. (A) Edmontosaurus (CMN, 2289; modied with permission from Rybczynski et al., 2008) with ju-gal removed; (B) Diplodocus (CM 3452); (C) Majungasaurus (FMNH PR2100).

1258 HOLLIDAY

the articular in dinosaurs. Therefore, both cranial andmandibular reconstructions of the m. pterygoideus dor-salis are Level I inferences.

M. pterygoideus ventralis (mPTvI/I). M. ptery-goideus ventralis attaches along the caudoventral edgeof the pterygoid in crocodylians and birds. Among croco-dylians, the muscle conspicuously wraps around the ret-roarticular process to attach on the ventrolateral surfaceof the retroarticular process and surangular. The muscleoften attaches along the ventral edge of the retroarticu-lar process but also wraps around the retroarticular pro-cess in some birds to attach to the lateral surface of themandible and even attaches to the jugal in some parrots(Hofer, 1950). It remains unclear if lepidosaurs possess aclear, separate ventral belly of m. pterygoideus. Regard-less, the muscle occasionally also wraps around to thelateral surface of the mandible and in some taxa (e.g.,Uromastix) it attaches to the lower temporal bar.Among dinosaurs, the attachment of m. pterygoideus

ventralis to the ventral edge of the palate is a phyloge-netically supported inference although clear palatal ana-tomical correlates are rare (e.g., Fig. 3G) making theorigin a Level I inference. On the other hand, the man-dibular insertion of m. pterygoideus ventralis is well-supported by a smooth fossa on the ventrolateral surfaceof the mandible making it a clear Level I inference. Likethe muscles attachment in crocodilians and many birds,the muscle also likely wrapped around the retroarticularprocess to attach to the lateral surface of the mandible(Fig. 4). However, the extent of the muscles attachmentacross the mandible is difcult to determine in most di-nosaur taxa. Among most ornithischians and sauropods,there is no clear demarcation between the attachment ofm. adductor mandibulae externus supercialis and m.pterygoideus ventralis, though a few individuals have afossa for the former muscle (Fig. 4C) suggesting it doesnot extend very far ventrally. Among theropods, the ven-tral surface of the mandibular shelf likely marks thedorsal extent of the pterygoid muscle (Figs. 4J and 7C).Interestingly, both derived hadrosaurs and tyrannosaursoften possess anges and bony spurs that descend off ofthe jugal and tend to point toward the retroarticularprocess. In some cases (e.g., Brachylophosaurus), thespurs are rugose and striated suggesting a tendinousattachment. These morphologies suggest that m. ptery-goideus ventralis may actually have attached to the ju-gal, rather than simply the mandible (Fig. 7).

M. adductor mandibulae posterior (mAMPI/I). M. adductor mandibulae posterior is the most phyloge-netically and anatomically consistent muscle in theadductor chamber. Among extant taxa, the muscleattaches across the lateral surface of the quadrate. Incrocodylians, the muscle leaves a number of crests andfossae (Iordansky, 1973; Holliday and Witmer, 2007)marking its aponeurotic and eshy attachments whereasamong birds and lizards, correlates are rare (Fig. 1).Osteological correlates of the muscle on the quadrate arealso rare among dinosaurs (Fig. 3). Regardless, data fromextant bracketing and outgroup taxa suggest that themuscle also attached to the quadrate in these fossil taxa.M. adductor mandibulae posterior consistently attachesto Meckels cartilage within the medial mandibular fossain lizards, crocodylians, and birds, other than anseri-

forms, where it attaches to the lateral surface of the man-dible. All data from dinosaurs suggest that m. adductormandibulae posterior also lled the medial mandibularfossa making it a Level I inference (Fig. 4).

Temporal Muscles

The temporal region is dominated by the vertically ori-ented jaw closing muscles including m. pseudotemporalissupercialis, which is a division of m. adductor mandi-bulae internus and bellies of m. adductor mandibulaeexternus including mm. adductor mandibulae externusprofundus, medialis, and supercialis. Signicantchanges occurred in the organization of the temporalmuscles during archosaur evolution and the musclesrelationships with the skull in crocodilians, birds, andnon-avian dinosaurs are not necessarily similar to thoseof lepidosaurs. As will be discussed thoroughly later, theorganization of the temporal muscles changed in theskull roof as well as on the mandible in archosaurs.These changes create challenges when identifyinghomologies as well as determining the attachments,function, and evolution of the muscles in fossil taxa. Thefollowing passages will document the temporal musclesfrom supercial (i.e., m. adductor mandibulae externussupercialis) to deep (i.e., m. pseudotemporalis super-cialis; Figs. 2, 3, 8).

M. adductor mandibulae externus supercialis(mAMESI/I). M. adductor mandibulae externus super-cialis invariably attaches across the upper temporalbar in lepidosaurs via a eshy attachment that does notleave any specic osteological correlate. The muscle thenattaches to the dorsolateral surface of the mandible andonly occasionally leaves a smooth, ovate region that maybe bordered laterally by a faint ridge marking the tran-sition from muscle to integument attachment. In crocodi-lians, the muscle attaches along the ventral surface ofthe quadratojugal by means of a eshy attachment later-ally and aponeurotic attachment medially, which leavesa rostroventrally oriented ridge that it shares with m.adductor mandibulae posterior (Iordansky, 1973; Schu-macher, 1973). The mandibular attachment of the croco-dylian m. adductor mandibulae externus supercialis iswell-emarginated by a smooth region on the dorsal sur-face of the surangular that is bounded rostrally by thecoronoid eminence left by m. adductor mandibulae exter-nus profundus. Because birds lost the upper temporalbar, m. adductor mandibulae supercialis generallyattaches across the lateral surface of the squamosal andwhen present, the ventral surface of the postorbital pro-cess (e.g., Anas), but also across the suprameatal shelfin many others (e.g., Gallus, Larus, Phalacrocorax; Fig.1B). In ratites (e.g., Struthio), m. adductor mandibulaeexternus supercialis is greatly reduced and attachesalong the temporal fascia and only slightly to the lateraledge of the postorbital process. The muscle often leavessmall crests marking its aponeurotic attachments on thecranial surface in most birds.As in extant taxa, the temporal bar is arguably the

best indicator for the attachment of m. adductor mandi-bulae externus supercialis. Taxa with long upper tem-poral bars likely had rostrocaudally broader muscles;those with shorter bars have smaller muscles. Despitethis basic anatomical relationship with the skull, the

DINOSAUR JAW MUSCLE ANATOMY 1259

muscle does not leave clear osteological correlates. Intaxa that have rugose bone textures on the skull surface(e.g., tyrannosaurs, abelisaurids), the muscle attachmentis easily recognizable because of its contrasting smoothtexture. Thus, its reconstruction is a well-supported,Level I inference. However, the medial, or deep, extentof the muscle is difcult to estimate because it does notusually attach to bony structures that mark its bounda-ries with deeper muscles such as mm. adductor mandi-bulae externus medialis or profundus caudomedially, orm. pseudotemporalis supercialis rostromedially.The most problematic concern of reconstructions of m.

adductor mandibulae externus supercialiss origin isthat despite the muscles likely attachment across themedial surface of the squamosal and postorbital, basi-cally all of the medial surfaces of the postorbital, post-frontal, squamosal, jugal, and quadratojugal are smoothbecause of the numerous soft-tissues that emarginatethe region including fascia, neurovascular bundles, peri-orbital structures, and pneumatic diverticulae. Haas(1963) interpreted m. adductor mandibulae externussupercialis to attach along the postorbital bar, ratherthan the upper temporal bar in Diplodocus based on hisevaluation of the smooth, slightly grooved medial surfaceof the bone. However, this groove is more likely exca-vated by postorbital or jugal vessels from the stapedialartery that pass along the medial surfaces of the postor-bital and jugal. Among theropod dinosaurs that have aprominently excavated squamosal recess, the interfacebetween the pneumatic sinus and muscle on the squa-mosal may mark the muscles caudal boundary (Witmerand Ridgely, 2008). However, it is also possible that m.adductor mandibulae externus supercialis simplyenclosed the medial portions of the sinus, which likelyderives from the suborbital diverticulum (Witmer andRidgely, 2008). In taxa that do not have well-developeddiverticular correlates, although their phylogenetic rela-tionships support the structures reconstruction, the in-ference of a muscle attachment versus pneumaticstructure is equivocal. Finally, many lepidosaurs alsohave a small supercial muscle belly, m. levator angulioris, which is often associated with m. adductor mandi-bulae externus supercialis (Haas, 1973). The muscleoriginates on the pretemporal and lateral temporal fas-ciae and then inserts on the rictus (i.e., corner of themouth; Haas, 1973). Extant archosaurs do not possessthis muscle nor does the muscle leave osteological corre-lates on the skeleton. Thus, the reconstruction of m. le-vator anguli oris is a Level III0 inference in dinosaurs.In most lepidosaurs, the m. adductor mandibulae

externus supercialis attaches along the dorsolateralsurface of the surangular, caudal to the coronoid process.The muscle is typically a eshy, parallel-bered bellyand occasionally leaves a fossa or a slight bony ridge(Fig. 1B). In crocodylians, the muscle occupies the major-ity of the dorsal surface of the surangular, caudal to thecoronoid eminence and leaves a faint ridge marking itsextent laterally. The muscles mandibular attachmentvaries among birds and generally attaches along the lat-eral surface of the mandible between the jaw joint cau-dally, the attachment of m. adductor mandibulaeexternus profundus rostrally and the attachment of m.pterygoideus ventralis ventrally.As in extant taxa, the dorsolateral surface of the sur-

angular is the most likely attachment of m. adductor

mandibulae externus supercialis among non-avian di-nosaur taxa and the muscle does not lend many specicidentiable correlates other than a smooth region of thesurangular. Haas (1955) reconstructed the muscle inProtoceratops attaching across the lateral surface of thesurangular based on the smooth, shallow fossa on theelement and this is a reasonable inference. In basal(e.g., Leptoceratops, CMN 8889) and derived ceratopsids(e.g., Styracosaurus CMN 344), the smooth surangularbecomes incorporated into the caudal portion of thelarge, rugose coronoid process suggesting a marked dif-ference in muscle attachment type between the twostructures (Fig. 4G). The caudal, smooth surface is mostlikely the attachment for m. adductor mandibulae exter-nus supercialis (e.g., Ostrom, 1964). The dorsal surfaceof the surangular forms the caudal portion of the coro-noid process in basal ornithopods such as Thescelosaurus(ROM 3587; Fig. 4A) and Dryosaurus (CM 3392), andthere is occasionally a slight shallow fossa long the dor-sal surface of the element that is the correlate for m.adductor mandibulae externus supercialis. However, inderived ornithopods, the attachment of m. adductormandibulae externus supercialis is rarely demarcated(e.g., Fig. 4C), but still most likely attaches along caudo-dorsal surface of the surangular, just rostral to the jawjoint (e.g., Ostrom, 1961; Rybczynski et al., 2008). Insauropods, the dorsal edge of the surangular is oftensmooth and acutely angled suggesting a very thin man-dibular attachment of m. adductor mandibulae externussupercialis. There are no clear, consistent osteologicalcorrelates of the muscle on the lateral surface of themandibulae in Camarasaurus or Diplodocus (Fig. 5B).Non-avian theropods have the most clearly dened man-dibular attachments for m. adductor mandibulae exter-nus supercialis because the surangular has aprominent shelf on its lateral edge marking the lateralextent of the muscle (Figs. 5 and 8).

M. adductor mandibulae externus medialis(mAMEMI/I0). M. adductor mandibulae externusmedialis is the most problematic of the temporal musclesin several ways. For reasons discussed later in Discus-sion section, it is difcult to interpret in the adductorchamber of extant reptiles and its reconstruction in fos-sil taxa is equally ambiguous. The muscle is large andwell-differentiated in lepidosaurs and attaches to the lat-eral surface of the large temporal aponeurosis, the bode-naponeurosis (Haas, 1973). The muscle attaches alongthe caudal surface of the dorsotemporal fossa and mayleave a shallow fossa on the surface of the posttemporalbar, lateral to the spur often left by the bodenaponeuro-sis. However, its attachment to the mandible is unclearbecause it may share a common attachment with mm.pseudotemporalis supercialis and adductor mandibulaeexternus profundus. In birds and crocodylians, the mus-cle is often anatomically and always topologically indis-tinguishable from mm. adductor mandibulae externusprofundus and supercialis (Holliday and Witmer, 2007).In crocodylians, m. adductor mandibulae externus medi-alis is a small, quadrangular muscle that occupies asmooth region of the quadrate between the trigeminalforamen and m. adductor mandibulae posterior, withwhich it shares aponeurotic attachments. However, themuscle melds with parts of mm. adductor mandibulae

1260 HOLLIDAY

externus profundus and supercialis as it attaches tothe mandible leaving no specic osteological correlate.Among birds, many of which have divided m. adductormandibulae externus into more than three, simple bel-lies, a discrete m. adductor mandibulae externus medi-alis is difcult to separate from deep or supercialportions without corroborating developmental evidence.That said, these intermediate bellies of m. adductormandibulae externus typically attach to the temporalfossa, or to fasciae or aponeuroses of the other temporalmuscles cranially and then to the coronoid region of themandible.Reconstructions of the cranial and mandibular attach-

ments of m. adductor mandibulae externus medialis areLevel I0 inferences among non-avian dinosaurs. However,these inferences are problematic, because interpretationsof attachments of m. adductor mandibulae externusmedialis depend on interpretations of where the sur-rounding muscles attach, which typically leave corre-lates that are more consistent. The mandibles ofhadrosaurs and ceratopsids (Fig. 4B, D, E) occasionallyhave shallow fossae that pass between the coronoid pro-cess and the jaw joint, a region that was certainlybounded by mm. adductor mandibulae externus profun-dus and supercialis, respectively. It could be expectedthat m. adductor mandibulae externus medialis occupiedthis intermediate position. However, this inference isequal to the hypothesis that the muscle attached to thecoronoid process with m. adductor mandibulae externusprofundus.

M. adductor mandibulae externus profundus(mAMEPI/I). Musculus adductor mandibulae exter-nus profundus is the deepest portion of the adductormandibulae externus muscle group. In lepidosaurs, it isrelatively small compared with the other temporalmuscles and attaches to the caudomedial corner of thedorsotemporal fossa and a portion of the prootic, some-what deep to mm. pseudotemporalis supercialis andadductor mandibulae externus medialis. It attaches lat-erally to the bodenaponeurosis and then prominentlyattaches to the coronoid process. In crocodylians, m.adductor mandibulae externus profundus is the onlymuscle that occupies the dorsotemporal fossa, thoughtemporal osteological correlates of basal crocodylomorphsshow evidence of there being multiple muscles in thefossa (Holliday and Witmer, 2007, in press). In crocodyli-ans, the muscle attaches to the caudomedial corner ofthe dorsotemporal fossa and then attaches as a tendonto a characteristic rugosity on the dorsal surface of thesurangular rostral to m. adductor mandibulae externussupercialis. In ratites and anseriforms, the muscleattaches to the postorbital process and in galliforms andmost other birds, the muscle attaches to the temporalfossa. The muscle then consistently attaches to the coro-noid process in all birds.Among dinosaurs, m. adductor mandibulae externus

profundus most likely occupied most of the caudomedialportion of the dorsotemporal fossa and likely attached tothe sagittal and nuchal crests when present. However,as noted earlier, its caudolateral border, which wouldhave been shared with mm. adductor mandibulae exter-nus medialis or supercialis, is unclear. The musclesrostral bony attachment is occasionally marked by a

small spur or vertical crest in a few taxa (e.g., Carcharo-dontosaurus, Daspletosaurus; Fig. 3D,F), or a subtleshift in curvature of the dorsal edge of the fossa (e.g.,Herrerasaurus, Hypsilophodon, Brachylophosaurus;Figs. 2 and 3). However, in most taxa, there are no de-nable osteological correlates other than the dorsotem-poral fossa itself that indicate the rostral extent of m.adductor mandibulae externus profundus. In Edmonto-saurus (CMN 2289; Fig. 3A), there is a shallow fossa onin the ventral portion of the temporal fossa that maycorrespond to this muscle, which would then suggestthat m. adductor mandibulae externus medialis mayextend across the dorsal edge of the dorsotemporal fossa,as in lizards. However, this is the only specimenobserved that bears this feature. That said, cranialreconstructions of the m. adductor mandibulae externusprofundus are Level I inferences. Most non-avian dino-saurs also possess mandibular osteological correlates ofthe muscle including coronoid processes in most ornithi-schians and smaller coronoid eminences in theropodsand thus, these the muscles mandibular attachmentsare also Level I inferences.

M. pseudotemporalis supercialis (mPTsI/I0).The deepest and most rostral temporal muscle is m.pseudotemporalis supercialis. In lepidosaurs, m. pseu-dotemporalis supercialis attaches to the medial surfaceof the dorsotemporal fossa. The muscle then attaches tothe medial portion of the coronoid region. During croco-dyliform evolution, m. pseudotemporalis supercialisshifted from a position similar to that present in lepido-saurs to the caudal surface of the laterosphenoid anddoes not attach within the dorsotemporal fossa proper inextant crocodylians (Holliday and Witmer, 2007, inpress). The muscle then inserts on the rostral portion ofthe medial mandibular fossa where it is compressed bythe pterygoid buttress and develops a sesamoid carti-lage, the cartilago transiliens. In ratites other thanApteryx, m. pseudotemporalis supercialis solely occu-pies the dorsotemporal fossa and also attaches in themedial mandibular fossa via an intertendon. In virtuallyall other birds, the muscle is miniscule relative to otherjaw muscles and attaches along caudoventral edge of thelaterosphenoid buttress of the temporal region and thento the medial surface of the coronoid region of themandible.Reconstructions of m. pseudotemporalis supercialis

are Level I or I0 inferences (Table 4). Despite this strongphylogenetic support, the position of m. pseudotempora-lis supercialis is difcult to clearly identify amongmany dinosaurs. Drawing from the muscles position inlepidosaurs, many early studies considered it to be thedominant muscle of the dorsotemporal fossa. Lull (1908)reconstructed the muscle on the rostral surface of thelaterosphenoid, inside of the orbit, in Protoceratops.However, as noted by Haas (1955) this was a novel, andunsupported interpretation and the muscle likely occu-pied part of the dorsotemporal fossa. Several authorshave suggested that m. pseudotemporalis supercialisattached to a large excavation on the dorsal surface ofthe frontal in many theropod taxa (e.g., Coria and Cur-rie, 2002; Molnar, 2008). However, the shape, horizontalorientation, surrounding bony structures, and the phylo-genetic distribution of this structure suggest that a

DINOSAUR JAW MUSCLE ANATOMY 1261

muscle did not likely attach to it (Holliday, 2008; unpub-lished data) and phylogenetic bracketing further sup-ports that m. pseudotemporalis supercialis more likelyattached within the dorsotemporal fossa proper. How-ever, like m. adductor mandibulae externus profundus,m. pseudotemporalis supercialis does not commonlyleave specic osteological correlates on the skull otherthan the characteristic smooth area of rostrolateral por-tion of the dorsotemporal fossa (Fig. 3). As noted in theearlier section, some individuals may have a crest orcurvature shift on the temporal fossa that indicates theseparation between m. adductor mandibulae externusprofundus and m. pseudotemporalis supercialis (Fig 3).The rostral extent of the muscle is bounded by the later-osphenoid buttress and the attachment of m. tensorperiorbitae.The mandibular attachment of m. pseudotemporalis

supercialis is difcult to infer. The extant bracketingtaxa suggest that the muscle probably attached to therostral portion of the medial mandibular fossa in ankylo-saurs, stegosaurs, pachycephalosaurs, and basal ceratop-sids and iguanodontians. However, m. pseudotemporalissupercialis likely attached to the medial surface of thecoronoid process in many derived iguanodontians andceratopsids. The derived ornithischian conditiona coro-noid attachmentis hypothesized to be similar to thatpresent in lepidosaurs because in hadrosaurs and cera-topsids, the medial mandibular fossa is very small andsignicantly caudal to the coronoid process thereby giv-ing the muscle a rostral moment, rather than the caudo-vertical moment it provides in other taxa. Furthermore,the coronoid processes of these taxa tend to have differ-ent domains of striations on them, which suggest thepresence differently oriented muscle attachments (Fig.4B,E). In theropods and sauropods, which have large,rostrally extended medial mandibular fossae that arevery similar to those found in crocodylians and ratites,inferring the muscle to attach in the rostral portion ofthe fossa is a Level I inference.

DISCUSSION

Jaw muscle inferences offer a potential wealth ofphylogenetic, anatomical, and functional information.However, there are a number of vagaries associated withthem and the distribution of osteological correlates on theskull can differ among individuals as well as clades. On theother hand, specic osteological correlates, and their soft-tissue inferences, may be phylogenetically robust. Forexample, with the exception of extant crocodylians, whichhave signicantly reorganized their jaw muscles, m. adduc-tor mandibulae posterior is a relatively simple, parallel-bered muscle among extant sauropsids. Therefore, from aphylogenetic standpoint, it is reasonable to infer that themuscle was also parallel-bered among non-avian dino-saurs. This inference is anatomically supported by the lackof crests and other osteological correlates that would sug-gest tendinous attachments on the quadrates. The tempo-ral muscles are more pinnate than m. adductormandibulae posterior, and thus, a pinnate m. adductormandibulae externus profundus or m. pseudotemporalissupercialis is a relatively strong inference that is sup-ported by the extant phylogenetic bracket as well as atleast a few individuals that have crests suggesting strongaponeuroses. However, these inferences also rely on a con-

sistent distribution of correlates, which given the fragmen-tary nature of skull specimens, is still a challenge. Theseissues aside, there are several trends in dinosaur jaw mus-cle anatomy and evolution that can be explored.

Protractor Muscles

Protractor muscles are key structures involved in cra-nial kinesis, or the ability of an animal to move the pal-ate independent of the braincase and mandible.However, to what extent dinosaurs could display thiscomplicated behavior remains debatable (Holliday andWitmer, 2008). Regardless as to whether the protractormuscles are functional or evolutionary relics, they areubiquitous among dinosaurs. For example, comparedwith those of basal ornithopods, the ala basisphenoid ofhadrosaurs have a greatly expanded tripartite morphol-ogy suggesting an enlarged and modied muscle thathad pronounced tendinous attachments to the braincasethat radiated not only caudoventrally, but also rostrolat-erally onto the palate. These data suggest m. protractorpterygoideus may have become hypertrophied to resistlaterally oriented forces generated by the medially insetdental batteries that derived ornithopods evolved(Rybczynski et al., 2008). Similarly, the alae basisphe-noid of many non-coleurosaurian theropods, such as Her-rerasaurus, Allosaurus, and Majungasaurus are smooth,triangular pendants that are attachments for a modest,eshy, pinnate m. protractor pterygoideus. However,those of large tyrannosaurs become dorsoventrally elon-gate, highly textured, and covered with numerous creststhat point ventrally or caudoventrally suggesting anincrease in aponeurotic attachment for m. protractorpterygoideus.These changes in morphology of the ala basisphenoid

may be functionally adaptive, but they may also simplybe the results of the evolution of large head size intyrannosaurs, ceratopsids and hadrosaurs. Similarly, thedisappearance of the ala basisphenoid during manirap-toran evolution may be associated with trends in minia-turization displayed in the clade [e.g., Sinosauropteryx,(Currie and Chen, 2001); Bambiraptor, (Burnham,2004); Sinovenator (Xu et al., 2002); Microraptor, (Xu etal., 2003); Mei, (Xu and Norell, 2004), and Mahakala,(Turner et al., 2007)]. Whereas adductor muscles areknown to scale positively with body size in lizards (Her-rel and OReilly, 2005; Herrel et al., 2007), it remains tobe determined if protractor muscles scale similarly withother parts of the feeding apparatus among extant andfossil taxa. Neosauropods attained huge body sizes with-out the accompanying increase in head size and reducedtheir alae basisphenoid to thin anges of bone that sug-gest they had a simple soft-tissue septum that separatedthe orbit from the ear. However, these taxa possess alsosome of the most extreme head and feeding structuresfound in dinosaurs (e.g., Nigersaurus, Diplodocus).Thus, teasing out the differences between allometry andfunctional signicance in the system is challenging, butit offers numerous new directions to explore.

Temporal Muscles

Muscles that directly attach to the bony surfaces ofthe temporal region, such as mm. pseudotemporalissupercialis and adductor mandibulae externus

1262 HOLLIDAY

profundus, are more likely to leave discernable osteologi-cal correlates that support anatomical inferences. How-ever, muscles that instead primarily attach to softtissues such as skin that covers the lateral temporal fen-estrae, such as m. levator anguli oris, or large aponeuro-ses, such as m. adductor mandibulae externus medialis,will not leave bony evidence of their attachments. Thispresents a major problem with reconstruction of struc-ture in the temporal region because m. adductor mandi-bulae externus medialis was likely an important musclein the temporal region of dinosaurs. Despite these ratherrobust inferences, the anatomical and phylogenetic vaga-ries of the muscle preclude estimations of the locationand potential size of the muscle in fossil archosaurs.Whereas lepidosaurs have prominent m. adductor man-dibulae externus medialis bellies, extant archosaurs donot. This is problematic because, like all tetrapods, non-avian dinosaurs probably had at least rudimentary ver-sions of this muscle and phylogenetic bracketing is sup-portive of the muscles reconstruction. However, from ananatomical perspective, it is simply unclear where andto what extent the muscle attached on the dorsotemporalfossa or the coronoid region of the mandible.The identication of evolutionary patterns of jaw

muscles is clouded by the difculties in diagnosinghomologies of specic bellies among fossil taxa. Althoughall dinosaurs had temporal muscles, exactly whichmuscles occupied the dorsotemporal fossa are difculthypotheses to test. The most consistent inferences arethat m. adductor mandibulae externus supercialisattached to the upper temporal bar and m. pseudotem-poralis supercialis attached to the caudal surface of thelaterosphenoid. The regions organization in extant taxabrackets inferences to a point: lepidosaur temporal fos-sae have three muscles (mm. pseudotemporalis super-cialis, adductor mandibulae externus profundus andmedialis); crocodylians and neognath birds have one (m.adductor mandibulae externus profundus). However, itis clear that the extant conditions in crocodylians andbirds are highly derived and numerous data suggest fos-sil crocodylomorphs and maniraptoran dinosaurs cer-tainly had multiple muscles in the dorsotemporal fossa.The few osteological correlates of temporal muscles thatdo exist among non-avian dinosaurs indicate that themm. adductor mandibulae externus profundus/medialiscomplex was the dominant muscle of the dorsotemporalfossa whereas m. pseudotemporalis supercialis was lim-ited to the caudal surface of the laterosphenoid. How-ever, if one considers that ratites (e.g., Struthio,Eudromia) may represent the primitive avian condition,rather than a secondarily derived clade, then one wouldinfer that m. pseudotemporalis supercialis was thedominant temporal muscle among, at least, theropoddinosaurs. Clear data that indicate shifts in muscleattachments among different clades of non-avian dino-saurs, such as the envisioned muscle shifts between ba-sal and derived ceratopsians and ornithopods, wouldcertainly benet systematic analyses.Inferences of jaw muscles reciprocally illuminate infer-

ences of other cranial soft tissues. As they exit the brain-case, the mandibular, and more often, the maxillarynerves excavate portions of the laterosphenoid andprootic. It is assumed that non-avian dinosaur jawmuscles and nerves follow the same topological patternsas other sauropsids, thus if a groove for the maxillary

nerve is identied on the laterosphenoid, marking itscourse rostrally, it can be inferred that m. pseudotem-poralis supercialis, which lies medial to the nerve wassmall or attached rostrally on the braincase. In hadro-saurs, the maxillomandibular nerves exit directly later-ally and a bit caudally, often leaving a shallow groove orlip on the prootic (Figs. 2 and 5). This suggests that m.pseudotemporalis supercialis did attach to the rostralportion of the dorsotemporal fossa even though there areno direct correlates that indicate the muscles attach-ment. Therefore, given adequate knowledge of jaw mus-cle anatomy and using neurovascular topological rules, aportion of the other soft tissues of the adductor chambercan be reconstructed with relative condence. Interest-ingly, in hadrosaurs, when the temporal muscles arereconstructed from the temporal fossa to the coronoidprocess, around the laterosphenoid buttress, the musclespass through much of the orbit. Therefore, interpreta-tions of muscle anatomy may directly impact inferencesof eyeball size. Thus, as in other vertebrates, orbit sizemay not be a complete index of eyeball size (Ross andKirk, 2007). These packing issues can be furtherexplored not only in the orbit, but also the nasal cavity,pharynx, and middle ear cavities, which are bounded bylarge portions of the pterygoideus dorsalis and ventralismuscles, and protractor muscles, respectively.Finally, feeding behavior and connective tissue adapt-

ive plasticity are major factors involved in the structureand function of jaw muscles and the skull (Ravosa et al.,2007). These phenomena make interpreting jaw musclefunctional anatomy extremely difcult over ontogenies ofanimals and may even manifest themselves among dif-ferent populations of the same taxon (Erickson et al.,2004). These anatomical features must be well-under-stood before the testing of functional and systematichypotheses. The best solution to investigating feedingbehaviors, such as chewing or bite force, among non-avian dinosaurs may be to test hypotheses using grossas well as more exact muscle inferences (i.e., temporalmuscles versus specic muscle bellies) while also testinga variety of virtual physiological cross-sectional areas,recruitment levels, and other behavioral or biomechani-cal parameters (e.g., Rayeld, 2005; Wroe et al., 2005;Rayeld and Milner, 2008). Anatomical inferences canonly form a general framework for functional analysiswhen dealing with soft tissues such as jaw muscles.In conclusion, jaw muscles offer a variety of bony

structures that support inferences of their reconstructionin fossil taxa such as non-avian dinosaurs. Even individ-uals of the same taxon may have more or fewer osteolog-ical correlates that support one muscles inferenceversus another. When anatomy does not offer necessaryinsight for soft-tissue reconstruction, phylogenetic brack-eting may lend inferential support. Among the musclesdescribed above, the orbitotemporal muscles have theweakest phylogenetic support, but generally have thestrongest anatomical support: m. levator pterygoideus isa Level III inference, but has excellent osteological cor-relates that support its reconstruction. On the otherhand, temporal muscles such as m. adductor mandibulaeexternus medialis or m. pseudotemporalis supercialishave strong phylogenetic support, and it is likely all fos-sil reptiles had the muscle bellies, but anatomical struc-tures that explicitly support identications of theirattachments are rare. It is relatively easy and

DINOSAUR JAW MUSCLE ANATOMY 1263

straightforward to make conservative interpretations ofjaw muscles and caution is suggested when using muscledata in evolutionary and functional analyses. Regard-less, jaw muscles are a critical component to under-standing head anatomy, function, and evolution in non-avian dinosaurs.

ACKNOWLEDGMENTS

Many thanks to Lawrence Witmer, Natalia Rybczyn-ski, David Dufeau, Tobin Hieronymus, Ryan Ridgely,Emily Rayeld, Mark Young, and others for providingadvice and assistance during the development of thisproject. Thanks to numerous staff and curators at muse-ums for access to specimens. Comments from Peter Dod-son and two anonymous reviewers greatly improved themanuscript.

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