Cranial myology
The muscular origin and insertion sites interpreted in the cranium and mandible of each species are identified in Fig. 1; the 3D reconstructed cranial adductor muscles are shown in Fig. 2 (Incisivosaurus and Citipati) and Fig. 3 (Khaan and Conchoraptor).
Locations of reconstructed jaw adductor muscle origin and insertion sites for Incisivosaurus gauthieri (a–c), Citipati osmolskae (d–f), Khaan mckennai (g–i), and Conchoraptor gracilis (j–l). Crania are shown in dorsolateral view (a,d,g,j) with temporal and postorbital bars removed to better show medial regions within supratemporal fenestra. The left sides of the crania are shown in anteroventral view (b,e,h,k) with lower temporal and postorbital bars removed to better show posterior and lateral regions within supratemporal fenestra. Mandibles shown in dorsolateral view (c,f,i,l), lateral muscle insertions sites are shown on the left rami, medial insertion sites on the right rami. Scale bars 50 mm. Muscle abbreviations given in results section.
Reconstructed jaw adductor musculature of Incisivosaurus gauthieri (a–d) and Citipati osmolskae (e–h) shown complete in lateral view (a,e), anterolateral view with mAMES removed (b,f), posterolateral view with mAME complex removed (c,g), and ventral view with only the mPT muscles (mPTv removed on left). Scale bars 50 mm, legend colour coded to identify individual muscles. Muscle abbreviations given in results section.
Reconstructed jaw adductor musculature of Khaan mckennai (a–d) and Conchoraptor gracilis (e–h) shown complete in lateral view (a,e), anterolateral view with mAMES removed (b,f), posterolateral view with mAME complex removed (c,g), and ventral view with only the mPT muscles (mPTv removed on left). Scale bars 50 mm, legend colour coded to identify individual muscles. Muscle abbreviations given in results section.
m. adductor mandibulae externus medialis (mAMEM)
The origin site of the mAMEM is less clear than others of the mAME group31 and we reconstruct it, as others have done, in the posterior portion of the supratemporal fossa12,13,16 where it is constrained anterolaterally and anteromedially by the positions of mAMES and mAMEP (Fig. 1). This region comprises parts of the squamosal and parietal in all four taxa and is generally vertical, concave, and featureless in all apart from Citipati. In this taxon, within the supratemporal fossa, the squamosals and parietals are flattened and orientated to form a deep and concave platform directly perpendicular to the line of action of this muscle (Fig. 1e).
The extent and direction of the mAMEM body are somewhat constrained in all taxa by the anterior, dorsal, and posterior edges of the squamosal, quadrate flange, and epipterygoid respectively.
The insertion sites are typically unclear12,31. The surangular dorsomedially forms a shelf that overhangs the adductor fossa in Citipati, Khaan, and Conchoraptor (potentially taphonomically exaggerated in the latter two). Insertion onto the dorsomedial and posterior margin of the coronoid eminence (along with insertion of the mAMEP onto the eminence) has been suggested for the mAMEM12,13,31,38, but the palatal morphology (especially in the oviraptorids) restricts space around the coronoid eminence so that we do not reconstruct both the mAMEM and mAMEP as inserting in this area. Instead, we reconstruct the mAMEM as inserting on the shelf-like upper part of the surangular’s dorsomedial surface, posterior to the more anterior insertion of the mAMEP, allocating roughly half of the available surface to each (Fig. 1c,f,i,l). This insertion surface is unclear and largely reconstructed in Incisivosaurus where there is less well-defined slight convexity on the upper part of the medial surangular surface (Fig. 1c). This area of the retrodeformed mandible model for Conchoraptor uses material from Khaan and the two are thus similar (Fig. 1i,l).
It is possible the mAMEM and mAMEP merged along their path or did indeed both insert in relation to the coronoid eminence39 but ultimately this would not change reconstructed bite force results significantly.
m. adductor mandibulae externus profundus (mAMEP)
The mAMEP generally has a medial and/or anteromedial origin within the supratemporal fenestra. A vertical crest, similar to that interpreted as the anterior border of the origination site in Carcharodontosaurus and Daspletosaurus31, Allosaurus40, Corythosaurus41, and Erlikosaurus12, is also identified in Citipati19 (Fig. 1d). We interpret it as the boundary between the mAMEP and mPSTs origins. A small sharp prominence, perhaps similar, is present on the lateral surface of the braincase in Incisivosaurus (Fig. 1a). The surface is more featureless in Khaan and Conchoraptor (Fig. 1g,j), so the anterior limit of the mAMEP origin is constrained by the origin area of the mPSTs (in turn based on the extent and position of the laterosphenoid).
In Citipati, a pneumatic opening in the posterolateral wall of the parietal (visible at the posterior of the mAMEP origin in Fig. 1d), underneath where the squamosal contacts the parietal to form the posteromedial margins of the supratemporal fenestra, seems to limit the mAMEP origin posteriorly, dividing it from the mAMEM. A similar opening is not as large or obvious in the other taxa, but similar limits to the origination sites are constrained by the geometry of the supratemporal fenestra. The dorsal extent of the origin is also clear in Citipati where a sharp lateral edge, running from the frontal-parietal contact posterolaterally to form the posterior boundary of the supratemporal fossa, separates the dorsal surface of the parietals from their lateral surfaces that contribute to the supratemporal fossa (Fig. 1d). This edge may function for muscle attachment similarly as suggested for a parietal ridge in the oviraptorid Osoko2.
We reconstruct the mAMEP inserting more anteriorly than mAMEM on the mandible (Fig. 1c,f,i,l), including around the apex of the coronoid elevation itself, along with the mAMES, specifically on the dorsomedial surface of coronoid prominence31,39.
m. adductor mandibulae externus superficialis (mAMES)
In all taxa, the mAMES can be reliably hypothesised to originate on the supratemporal bar31 (Fig. 1b,e,h,k). In oviraptorosaurs, this is formed by the postorbital and squamosal. The supratemporal bars in all taxa are mediolaterally flattened, with the medial surface directed slightly ventromedially, more so in Citipati than the others (Fig. 1e). The postorbital bars are concave along almost the entire medial surface in Citipati. In the other taxa, only the squamosal contribution is concave, with the postorbital ramus being flat or perhaps weakly convex in Khaan (Fig. 1h). There are no clear osteological signs of the extent of the mAMES origin site so we restrict it to the medial surfaces of the supratemporal bar as the ventral surface is narrow (as the bars are mediolaterally thin) and the medial surface is slightly orientated in the correct muscle direction in all taxa. The mAMES is reconstructed as originating along the full extent of this medial surface with its anterior and posterior limits constrained by the origins of the mPSTs and mAMEM respectively.
The main body of the jugal has a trough-like gently concave medial surface in all taxa (especially so in Conchoraptor where the postorbital process of the jugal also has confluent concavity on its posteromedial surface) that appears like its form would neatly wrap over the exterior of the mAMES as it bulged outwards laterally and followed it anteroventrally on its origin-insertion path.
The mAMES likely inserts onto the dorsolateral edge and lateral surface of the surangular31,39, on a shelf running from the coronoid process to the articular (Fig. 1c,f,i,l). This shelf is more strongly defined in the later diverging taxa, especially Citipati (Fig. 1f) and Khaan (Fig. 1i). The mandibles of the oviraptorids bear apically triangular coronoid eminences, which are anteriorly displaced compared to those of other herbivorous dinosaurs. This has been hypothesized to increase mechanical advantage and attachment area for the temporal musculature as an adaptation for a stronger crushing bite3,8,38. The anteriorly displaced coronoid eminence in oviraptorids has been hypothesized to indicate a more anteriorly extending mAMES (as suggested for some ornithischians39,42). The mAMES is reconstructed thus here. The insertion site is constrained ventrally by the reconstructed extent of the mPTv insertion site, and dorsomedially by the insertions of the mAMEM and mAMEP, which insert onto the dorsomedial surface of the surangular.
m. adductor mandibulae posterior (mAMP)
The mAMP is a well-constrained muscle of the adductor chamber, consistently attaching to the lateral surface of the quadrate in an extant phylogenetic bracket31. We reconstruct the origin site as the lateral surface of the pterygoid flange of the quadrate (Fig. 1), covering most of this broad flat wing but not encroaching on the epipterygoid (where the mPSTp is present) and pterygoids (where the mPTd originates). No clear muscle scar is apparent in any of the studied taxa. The mAMP origin may also have extended posterodorsally onto the confluent lateral surface of the squamosal, where a curved ridge may demark an expanded origin site for the mAMP in Conchoraptor (Fig. 1j)5; Khaan has a similar morphology (Fig. 1g). This expansion is not reconstructed in earnest—the organization of the other muscle volumes, particularly the passage of the mAMEM, would only permit a thin sliver of extra volume to be created on the expanded origin site, not significantly increasing overall volume, direction, or morphology of the mAMP.
The mAMP inserts in the adductor fossa on the medial mandibular surface (Fig. 1c,f,i,l), occupying most of its main extent and posterior and ventral margins31. The adductor fossa in the oviraptorids is large and anteriorly displaced19,38,39 and much more significant than that of Incisivosaurus (Fig. 1c).
m. pseudotemporalis superficialis (mPSTs)
In all four taxa, the mPSTs originates on the anterior and/or anteromedial wall of the supratemporal fenestra. In Citipati, the area is formed predominantly by the capitate process of the laterosphenoid and the posterior portions of the frontal (Fig. 1d). This surface is concave and rugose. The lateral surface of the laterosphenoid is also rugose, indicating a muscle attachment19. The site is bounded laterally by the postorbital, and two ridges may constrain the origin site of the mPSTs 19: a sharp ridge runs posteromedially from the capitate process of the laterosphenoid to the epipterygoid contact, forming the ventral boundary, and a vertical ridge on the medial wall of the supratemporal fossa constrains the origin posteromedially, demarking it from the mAMEM. A triangular anterodorsal-posteroventral sloping surface (where a clear frontoparietal fossa has been lost in derived oviraptorids) extends to the dorsotemporal fossa. The anterodorsal extent of the mPSTs origin site on this surface is unclear. The frontoparietal fossa has been argued as a vascular space in dinosaurs rather than a site of muscle attachment43, and we place the mPSTs similarly (43; Fig. 7 therein), extending into this sloping triangular space but not wholly filling it. We do not reconstruct any attachment of the mPSTs extending onto the frontal processes of the postorbitals.
In Khaan, the origin site is less well preserved (Fig. 1g). The mPSTs origin is placed in a similar position to Citipati and may extend slightly onto the lateral surface of parietals which contribute to the area. Similarly, in Conchoraptor (Fig. 1j), there is more of a contribution of the parietal to the anterior wall of supratemporal fenestra, but very little or no contribution of the frontal. In Conchoraptor, the whole origin site is more anteromedially positioned, and exhibits a large smooth exposure of the laterosphenoid. There are no obvious scars or ridges in the above-mentioned area of Khaan and Conchoraptor. In Incisivosaurus, the anterior corner of the supratemporal fossa is narrow and the mPSTs is more anteromedially positioned (Fig. 1a). The origin site likely comprises the laterosphenoid and small parts of the frontal and parietal.
The insertion of the mPSTs is likely related to the medial aspect of the coronoid elevation and parts of the medial adductor chamber39. As the medial regions of the coronoid elevation are occupied by the mAMEP in our reconstruction we position the mPSTs, as the deepest temporal muscle, inserting into the anterior portion of the medial mandibular fossa31 and its anterodorsal rim (Fig. 1c,f,i,l).
m. pseudotemporalis profundus (mPSTp)
The mPSTp likely attached to the epipterygoid when present in dinosaurs31. When first described in detail, the epipterygoid of C. osmolskae (Fig. 1d) was noted as the largest of any known theropod, with a unique strongly twisted body and dorsal tip hosting robust muscle scars19. We therefore locate the mPSTp origin site on the epipterygoid of each taxon with confidence and reconstruct its origin along the length of the epipterygoid, which is present in all four taxa (though partially reconstructed in Khaan and Conchoraptor) (Fig. 1g,j).
The insertion site is problematic but based on extant taxa the muscle likely inserted along the medial surface of the coronoid process or surangular 31. As the coronoid process is occupied by the insertions of the mAMES and mAMEP, we position the insertion of the mPSTp dorsomedially on the surangular, occupying the dorsal rim of the mandibular adductor fossa, the position being largely constrained dorsally by the insertions of the mAMEM and mAMEP (Fig. 1c,f,i,l).
m. pterygoideus dorsalis (mPTd)
The origin site of the mPTd is reconstructed as the linear dorsal surface of the pterygoid in all oviraptorids where a longitudinal concavity runs anteriorly along their length anterior of the pterygoid flange (Khaan has a convex dorsal surface but the origin site is modelled similarly (Fig. 1h), and possibly the anteriormost dorsolateral surface of the pterygoid flange. The site is limited anteriorly and anterolaterally by the palatines and ectopterygoids, onto which no attachment was modelled as they are relatively small and delicate. In Incisivosaurus, the anterior extent of the origin site is constrained by the level of the jugal ramus of the ectopterygoid anterolaterally and the main body of the ectopterygoid laterally to around a longitudinal concavity on the dorsal surface of the pterygoid (Fig. 1a)—there seems very little/no origination on the palatine.
The mandibular insertion of the mPTd is commonly regarded to be onto the medial surface of the articular and retroarticular process31. We reconstruct the mPTd in this position (Fig. 1c,f,i,l), inserting in the narrow medial surface of the posterior aspect of the mandibular ramus, under the medial facet of the articular glenoid and posteriorly onto the medial surface of the retroarticular process.
m. pterygoideus ventralis (mPTv)
The mPTv is well constrained through phylogenetic bracketing and we reconstruct it in the oviraptorids as originating along the ventral surface of the pterygoid, probably also extending onto the ventral aspect of the pterygoid flange31 and posteriorly terminating before the contact with the quadrate. The anterior of the origin is reconstructed as the level of the ectopterygoid contact, with the site entering the longitudinal ventral concavity that is anteriorly confluent with the choanae. In Citipati, the pterygoid flange is noted as reduced compared to typically carnivorous theropods, maintaining a roughly consistent width throughout its length (Fig. 1e), as suggested by19 to indicate a relatively small m. pterygoideus. However, the main pterygoid body of oviraptorids is relatively elongate. This may be an adaptation to open space for an expanded mAME group to insert onto the mandible, whilst maintaining volume of the mPT. The pterygoids of Incisivosaurus are also elongate and reduced in width (Fig. 1b), though not as extreme as in the derived oviraptorids 24. The origin of the mPTv on the pterygoid ventral surface is interpreted as running from the posteroventral margin anteriorly into a trough medial to the ectopterygoid, and lateral of a ventral flange termed the accessory ventral flange by Xu et al.22, terminating anteriorly before the palatine contact.
In all taxa, the mPTv wraps around the ventral surface of the mandibular rami and inserts on the broad section of the lateral surface of the mandible (Fig. 1c,f,i,l), predominantly comprising the angular.
Bite force estimates
Measurements of the final volumetric muscle reconstructions are given in Table 1 along with the calculated muscle contraction force, resultant force acting on the mandible, and relative contribution of each muscle. The oviraptorid oviraptorosaurians show greater muscle volumes compared to the earlier diverging Incisivosaurus. This is confirmed by greater muscle CSA values relative to cranial surface area in Citipati (1.80 × 10–2), Khaan (1.77 × 10–2), and Conchoraptor (1.37 × 10–2), compared to Incisivosaurus (1.21 × 10–2). Table 2 shows the inlever and outlever measurements used to calculate bite force resulting from each cranial muscle (and their relative contribution) and the total estimated bite force in each species, for three different bite positions. These range from 349–499 N in Citipati down in order of cranial size to 53–83 N in Incisivosaurus. Complete calculations and values for Tables 1 and 2 along with measurements for the cranial models are documented in SI 2.
The condition of the oviraptorid oviraptorosaurian skull is characterised by an increased volume for adductor musculature and increased mechanical advantage resulting from anteroposterior shortening, compared with the more conventional theropod skull geometry of the earlier diverging Incisivosaurus. Estimated bite forces conserve a greater proportion of the resultant force applied to the mandible (Fbite/Fres) in the oviraptorids compared with Incisivosaurus. This results from greater mechanical advantage in the oviraptorids’ jaw for all bite positions, though the difference relative to Incisivosaurus is greatest anteriorly (see Table 3.) These two factors result in their comparatively stronger estimated bite forces, an increase of 17–84% greater (depending on species and bite position; see Table 2) than would be predicted by scaling by cranial surface area. The increased relative bite force of the oviraptorids is not a result of more beneficial muscle insertion angles; there is no clear difference in the ratio of resultant muscle force acting on the mandible to the actual muscle force produced (Fres/Fmus) between Incisivosaurus (0.894) and the three later diverging taxa (Citipati, 0.856; Khaan, 0.851; Conchoraptor, 0.899).
The relative contribution of the different cranial muscles to bite force is broadly similar in each species (Fig. 4). The mPTv is typically the largest component, followed closely by the mAMES, then the rest of the mAME complex. Citipati differs from the others with a relatively stronger mAMES and mAMEM, and a relatively low value for the mPTv. The width of the Citipati cranium and mandible make the mPTv less vertically orientated and the reconstruction of the mPTv (in all taxa) is less well constrained by bone and other muscle volumes—its volume could be underestimated in all models. No clear difference emerges between Incisivosaurus and the later diverging oviraptorids in the relative contributions of cranial muscles to bite, apart from a slightly relatively weaker mPSTp and mPSTs—reconstructed muscles are proportionally similar but relatively larger in the oviraptorids. The bite force estimates of the four oviraptorosaurians (including Incisivosaurus) are significantly greater than estimates (from similar digital methods) made for other putatively herbivorous theropods of much larger body mass (Fig. 5) both relatively and absolutely.
The relative contribution of each cranial muscle to total estimated bite force by species. Note that the condition of Citipati appears the most dissimilar to all others in its comparatively stronger mAMEM, mAMES and weaker mPTv.
Comparison of the estimated bite forces in multiple positions of Incisivosaurus and three oviraptorid oviraptorosaurians with other likely herbivorous theropod taxa that have had estimates made using similar digital volumetric methods12,13 show the oviraptorosaurians (oviraptorids especially) are capable of much stronger bite forces both relative to body mass and absolutely. Body mass values from Zanno and Makovicky11.
Gape analysis
The early diverging oviraptorosaurian Incisivosaurus showed the highest estimates of optimal (25.0°) and maximum gape limit (49.5°) compared with the oviraptorid oviraptorosaurians, though not by much; estimates for gape limit in Khaan were lowest (20.5° and 40.0°), marginally less than Citipati (21.0° and 41.0°). Values for Conchoraptor (23.0° and 46.0°) lie between Incisivosaurus and the others. Figure 6 shows these estimates along with charts of the muscle cylinder strains that they are derived from. The anteriormost cylinder representing the mPTv constrains optimal and maximum gape in all but Citipati, in which it is constrained by the anteriormost regions of the mAMES. In this taxon the postorbital half of the skull is particularly low, sloping posteriorly, and the relatively low upper temporal bar directs the strong mAMES ventromedially to a prominent coronoid process of the surangular of the mandible. This leads to a shorter resting length for this muscle, causing its extension during jaw opening to exceed our tension limits just before the mPTv (which is the next most extended). The mAMEM is also relatively more extended in Citipati. The other three species are more similar in relative muscular strain, reinforcing the finding that relative muscle strength and arrangement in Citipati has more differences compared with other oviraptorids, than between some oviraptorids (Khaan and Conchoraptor) and earlier diverging oviraptorosaurians (Incisivosaurus).
Estimates of the gape angle limit of optimal tension and the maximum limit of gape for muscle tension in Incisivosaurus gauthieri (a), Citipati osmolskae (b), Khaan mckennai (c), and Conchoraptor gracilis (d) from a muscle resting length at a gape angle of 5°. Bar charts show the strain factors of individual modelled muscle cylinders at optimal and maximum tension limit; anteriormost muscle cylinders suffixed ‘1’, posteriormost suffixed ‘2’. Muscle cylinders (and corresponding bars) are colour coded yellow and red when exceeding 130% and 170% of resting length respectively, otherwise green. Note that the anterior mPTv constrains gape in all species apart from Citipati which is constrained by the anterior mAMES. Scale bars 50 mm. Muscle abbreviations given in results section.
Acting antagonistically to the jaw closing muscles is the m. depressor mandibulae (mDM), primarily responsible for jaw depression (opening). It originates from around the paroccipital processes of the cranium, inserting onto the dorsal aspect of the retroarticular process of the mandible31,39. During the gape analysis, we checked mDM length change (from a shorter state at the maximum and optimal estimated gape angles to an elongated state at the 5° resting jaw angle) was not unrealistic. Strain values of the mDM were all calculated to be below the maximum strain limit (1.7) we modelled for the jaw adductors. From its shortest (maximum gape limit) the mDM in Incisivosaurus was extended by a factor of 1.08 at the estimated optimal gape limit and 1.20 the 5° resting jaw angle, Citipati reached 1.11 and 1.33 respectively, Khaan reached 1.16 and 1.48, and Conchoraptor reached 1.19 and 1.67.
The oviraptorosaurians show estimated gape limits much lower than those of carnivorous theropods tested by Lautenschlager12, more like herbivorous theropod Erlikosaurus (optimal tension limit 24.0°; maximum tension limit 49.0°; resting gape of 6°). It is noted that herbivorous species exhibit lower gape angles than carnivorous species23,44, and thus our estimates of gape angle may be further support for a herbivorous diet among oviraptorosaurians (when considered against other theropods). Lautenschlager 12 notes that experimental results document gape angle in modern birds can reach angles up to around 40°. The maximum gape angles estimated for these oviraptorosaurians are similar to experimental results of gape angle in birds among passerines and Galliformes, which can reach around 40°45,46,47,48 (though this can be greater in parrots49)—a functional similarity between the crania of birds and oviraptorids which, beyond superficial beaked appearance, are quite dissimilar.
Source: Ecology - nature.com
