Osteology IX: Maxilla in lateral view

The skull of Albertosaurus libratus with the maxilla highlighted in color, © Dino Pulerà. This is a colorized version of the image that first appeared on the cover issue of JVP in which Carr (1999) was published.

Introduction

Given its importance anatomically and in the literature, I am starting the bone-by-bone osteology series with the maxilla. Structurally this bone forms the most of the lateral surface of the snout, and medially it is also a part of the palate. The maxilla is a source of numerous features that are informative regarding ontogeny, phylogeny and taxonomy. This post will summarize and illustrate the osteology of the maxilla in lateral view as completely as possible, but only brief attention will be given to ontogenetic and phylogenetic variation.

The terminology here draws from the bulk of the literature on tyrannosauroids, but preference is given to the terminology of Witmer (1997) and Witmer and Baumel (1993), given the concerted effort of those authors to standardize the osteological terminology for Archosauria. For reference, terms that have their own descriptive sections in this post are italicized when they are mentioned under headings of different structures. With regard to ontogenetic stages, I will use the terms juvenile, subadult, young adult, and adult in place of the categories “small stage 1”, “large stage 1”, “stage 2” and “stage 3” of Carr (1999). Also, the category “adult” includes “stage 4” of Carr (1999). As per usual, this account does not depart from the literature; since I have two major works on tyrannosaurid ontogeny in progress, I will not add new data here.

Abbreviations: ROM, Royal Ontario Museum, Toronto, Canada.

DESCRIPTION

A. Maxilla en bloc

The maxilla is the primary tooth-bearing bone of the skull and, using the internal antorbital fenestra as a landmark, it can be divided into two primary regions, namely the ascending ramus and the alveolar process (sensu Witmer, 1997). In lateral view, it surrounds most of the internal and external antorbital fenestrae, and among the facial bones it is the most extensively covered by the antorbital fossa. The bone contacts the lacrimal caudodorsally, the nasal dorsally, the premaxilla rostrally, and the jugal caudoventrally. It is deeply notched caudally by the internal antorbital fenestra, and rostrally by the subnarial foramen. The maxilla is penetrated by the large maxillary fenestra, and the bone forms nearly the entire ventral margin of the snout, and part of that of the suborbital region. The coarse subcutaneous surface of the maxilla is continuous with that of the surrounding bones, which is richly perforated by neurovascular foramina at the rostroventral quadrant of the bone.

The maxilla is ontogenetically and phylogenetically variable. During ontogeny in Albertosaurus libratus and Tyrannosaurus rex, the maxilla begins as a narrow and nearly flat bone, and with maturity it inflates laterally in part due to enlargement of the teeth and also inflation of internal pneumatic sinuses (Carr, 1999). The adult condition is also seen in adults of other derived tyrannosauroids, including Bistahiversor, Daspletosaurus, T. bataar, and Zhuchengtyrannus (Carr, 1999; Carr et Williamson, 2010; Hone et al., 2011). In effect, the rostral region of the bone becomes bowed laterally, giving it a sinusoidal contour when viewed from below (Carr, 1999). Specific phylogenetic characters are discussed below.

Maxilla of a subadult Albertosaurus libratus (ROM 1247) in right lateral view, labeled with the primary regions (sensu Witmer, 1997) of the bone.

B. Primary regions

Ascending ramus Witmer, 1997 (=ascending process, nasal process, posterodorsal process): The ascending ramus includes the region of the maxilla above the level of the ventral margin of the internal antorbital fenestra. A useful landmark to define the rostral limit of the ramus is the rostral extent of the joint surface for the nasal, which stops at the caudodorsal limit of the vestibular bulla. The ramus includes the region surrounded by most of the rostrodorsal margin of the bone, above the level of the vestibular bulla, and the rostral and rostrodorsal margins of the internal antorbital fenestra.

The curvature of the ventral margin of the internal antorbital fenestra makes that boundary somewhat variable between specimens, so the vestibular bulla is considered here to be a part of the alveolar process. As such, most of the antorbital fossa and its subordinate openings are located on the ascending ramus.

Alveolar process Witmer, 1997 (=main body, ventral ramus): The alveolar process is the region of the bone below the ventral margin of the internal antorbital fenestra and the rostral extent of the joint surface for the nasal, which includes the ventral region of the antorbital fossa, the ventral margin of the external antorbital fenestra, the dentigerous (tooth-bearing) region, the vestibular bulla and its associated structures, and the jugal ramus. When the maximum length of the maxilla is measured, it corresponds to the length of the alveolar process.

The depth of the alveolar process in juveniles of T. rex is comparable to that seen in adults of A. libratus, whereas it is significantly deeper in adults (Carr, 1999). The deep condition is also seen in adult Daspletosaurus (Carr, 1999).

Subcutaneous surface Carr et Williamson, 2004 (=lateral face): This term refers to the textured lateral surface that does not extend onto the antorbital fossa, joint surface for the nasal, or narial fossa. Presumably this surface was immediately deep to the cutaneous covering over the periosteum of the bone. This surface is continuous, aside from interruption by several rows neurovascular foramina and their associated sulci. This coarse surface, typified by dorsoventrally trending ridges, is continuous with that seen on the premaxilla, jugal, nasal, and lacrimal. This shared surface is suggestive of an extensive beaklike structure that covered nearly the entire face.

The subcutaneous surface is ontogenetically variable, where its relief is low in juveniles of A. libratus and T. rex, whereas it is coarse in subadults (Carr, 1999; Carr et Williamson, 2004). This sculpturing is taken to an extreme in Daspletosaurus, where the region ahead of the antorbital fossa is much coarser than what is seen in other derived tyrannosauroids (Carr, 1999).

 

C. Secondary structures

I. Secondary structures of the ascending ramus

Maxilla of a subadult Albertosaurus libratus (ROM 1247) in right lateral view showing the secondary structures of the ascending ramus.

Joint surface for the nasal: The joint surface for the nasal extends for nearly the entire length of the dorsal surface of the ramus; only the caudal extremity joins the lacrimal.

In A. libratus, this joint surface is affected by ontogenetic changes to the rostrodorsal region of the bone, where it faces dorsolaterally in juveniles, which expands to displace the joint surface to face dorsally in subadults. In adult Daspletosaurus expansion displaces the joint surface dorsomedially (Carr, 1999). In T. rex, the dorsal to dorsomedial change, from juvenile to adult, is seen (Carr, 1999).

Also, this suture in derived tyrannosaurines (Daspletosaurus, Tyrannosaurus) becomes deeply peg-in-socket in adults, which can be so extreme as to eliminate landmarks such as the maxillary flange.

Joint surface for the lacrimal: The caudodorsal extremity of the ascending ramus splits into a pair of tapering processes, producing a V-shaped notch that receives the rostral end of the lacrimal. The lacrimal extends rostrally ahead of the notch, out of view, onto the medial surface of the ascending ramus. For a short distance, a stout process from the lacrimal overlaps the caudodorsal margin of the maxilla above the notch. Ahead of this, the nasal overlaps the dorsolateral surface of the maxilla.

External antorbital fenestra Witmer, 1997 (=rim of the antorbital fossa): The rostrodorsal extent of the external antorbital fenestra is within the ascending ramus, whereas its ventral margin is below it. The fenestra extends caudodorsally above the internal antorbital fenestra; in some taxa (Albertosaurus spp., Bistahieversor, Daspletosaurus) the margin extends between the internal antorbital fenestra and the joint surface for the nasal, whereas in others (Tyrannosaurus spp.) the fenestra extends to the nasal, and behind this the antorbital fossa extends along the nasal bone (Carr, 1999). As such, the nasal does form part of the dorsal margin of the fenestra on occasion.

Antorbital fossa: The antorbital fossa is the large and smooth depression that covers the caudodorsal region of the bone, which completely surrounds the internal antorbital fenestra. The fossa extends rostrally ahead of the midlength of the dentigerous region of the bone. The fossa is bounded by the external antorbital fossa, the transition point between the fossa and the coarse subcutaneous surface that covers the rest of the lateral surface of the bone. As seen in A. libratus, the fossa is limited to the maxilla, but in derived tyrannosaurines (e.g., Tyrannosaurus), the fossa extends to the joint surface of the nasal where it extends along that bone for some distance (Carr, 1999).

Several subordinate structures can be seen within the antorbital fossa, including the interfenestral strut that extends between the internal antorbital fenestra and the maxillary fenestra, the promaxillary strut that separates the maxillary and promaxillary fenestrae, and the maxillary and promaxillary fenestrae. Variable features include accessory pneumatic fossae or fenestrae in the dorsal or ventral regions of the interfenestral strut, and the size of the maxillary fenestra (Carr, 1999; Carr et Williamson, 2004).

In A. libratus juveniles, the rostral margin of the fossa is not overlapped by the subcutaneous surface, whereas the surface is strutlike and covers the leading edge of the fossa in young adults (Carr, 1999).  This difference between juveniles and adults of T. bataar and T. rex is also seen (Carr, 1999). The strut is seen in adult Daspletosaurus, which was presumably absent from juveniles of that taxon (Carr, 1999).

Internal antorbital fenestra Witmer, 1997 (=antorbital fenestra, first antorbital fenestra): The caudodorsally extending margin of the internal antorbital fenestra forms the caudal margin of the ascending ramus, whereas its ventral margin represents the boundary between the ascending ramus and the alveolar process.

Maxillary flange Carr et Williamson, 2004: The maxillary flange is the usually distinct convexity along the dorsal margin of the bone that is situated above the rostral end of the antorbital fossa (Carr et Williamson, 2004). This feature is seen in nearly all specimens, except it can be low and indistinct in juveniles or partly obliterated by the deep peg-in-socket nasomaxillary suture in adults. Also, this structure is so low that it is virtually absent in Alioramus altai (Brusatte et al., 2012). Otherwise, this is a constant feature in derived tyrannosauroids (Carr et Williamson, 2004).

Dorsolateral process Carr et Williamson, 2010: This term refers to the dorsoventrally shallow process located toward the caudal end of the ascending ramus, situated at the boundary of the external antorbital fenestra and the subcutaneous surface. Its dorsal margin extends along the nasal, whereas its ventral surface is separated from the lateral surface antorbital fossa by a narrow groove, its caudal tip may abut the rostroventral process of the lacrimal.

The dorsoventral height of the process is phylogenetically variable, where it is shallow in A. libratus, shallower than the antorbital fossa below it, whereas it is deep – as deep as the fossa below it  - in Daspletosaurus (Carr, 1999). In T. rex, this structure is obliterated by the antorbital fossa (Carr, 1999).

Lateral lamina Witmer, 1997 (=lateral flange): The sheet of bone that is situated lateral to the promaxillary recess and in lateral view is covered by the subcutaneous surface.

Medial lamina Witmer, 1997: The sheet of bone that is produced by the excavation of the antorbital fossa. It is penetrated by the maxillary fenestra, and forms the medial wall of the canal that is expressed caudally as the promaxillary fenestra. As such, the medial lamina forms the partition that separates the maxillary antrum from the promaxillary recess, deep to the lateral lamina. The medial lamina contains the medially extensive (i.e., wide) bony enclosure of the maxillary antrum caudally, and the promaxillary recess rostrally.

Region of the maxillary antrum (=rostrolateral surface): As used here, the region external to the maxillary antrum corresponds to the subcutaneous region ahead of the antorbital fossa. This region is ontogenetically variable in A. libratus, where in juveniles the surface is not expanded or inflated, and a clear ridge can be seen to surround the antorbital fossa rostrally (Carr, 1999). In contrast, this region in young adults is expanded rostrally and dorsoventrally; in adults, it is expanded and inflated owing to enlargement of the teeth and inflation of the maxillary sinus system, eliminating the ridge that encircles the antorbital fossa rostrally (Carr, 1999).  This extreme change distinguishes the juvenile condition in T. rex from that of adults (Carr, 1999). The expanded condition is also seen in adult Daspletosaurus (Carr, 1999).

Maxilla of a subadult Albertosaurus libratus (ROM 1247) in right lateral view, labeled to show the location of the region of the maxillary antrum.

Promaxillary fenestra Carpenter, 1992 (=anteriormost fenestra): The promaxillary fenestra, in actuality should be regarded as a foramen, since it is the caudal opening of a short canal that extends caudolaterally from the promaxillary antrum onto the antorbital fossa. This opening is positioned between the lateral and medial laminae of the maxilla.

The lateral exposure of this opening is phylogenetically and ontogenetically informative, where it is either exposed to view or concealed by a strut developed along the rostral margin of the external antorbital fenestra (Russell, 1970). In juveniles and subadults of A. libratus, the opening exposed to view, whereas in young adults the opening is partly or completely concealed (Carr, 1999). Also, the dorsal margin of the fenestra is not recessed in juvenile A. libratus or T. bataar; in contrast, it is recessed in young adults of A. libratus, where the dorsal margin of the fossa that leads into the canal becomes undercut (Carr, 1999).

In A. libratus juveniles the opening is a narrow slit, whereas it is wide in young adults (Carr, 1999). The slit condition is seen in juvenile T. rex, whereas it has the form of a round foramen in adults (Carr, 1999). The round condition is seen in adult Daspletosaurus; presumably the foramen in juveniles was slitlike (Carr, 1999).

Detail of maxilla of a subadult Albertosaurus libratus (ROM 1247) in right lateral view showing the contents of the antorbital fossa, including the interfenestral strut, maxillary fenestra, promaxillary fenestra, and the promaxillary strut.

Promaxillary strut Witmer, 1997: The part of the medial lamina that is interposed between the rostral end of the maxillary fenestra and the promaxillary fenestra.

Maxillary fenestra: The maxillary fenestra is the large opening located between the rostral margins of the external and internal antorbital fenestrae. It is generally round and although variable in size, the caudal margin is always V-shaped with the point of the V extending caudally (Brochu, 1993). The fenestra is the primary lateral opening into the maxillary antrum. In some taxa (A. libratus; Witmer, 1997), an exceedingly shallow fossa extends caudally or caudodorsally from the maxillary fenestra.

This opening is ontogenetically variable; for instance, the fenestra is approximately circular in outline and positioned halfway between the rostral margins of the external and internal antorbital fenestrae in juveniles of A. libratus, T. bataar, and T. rex (Carr, 1999). In contrast, the opening is long in specimens more mature than subadults where it approaches the rostral margin of the antorbital fossa (Carr, 1999). In adults of Daspletosaurus, the maxillary fenestra closely approaches, but does not reach the rostral margin of the antorbital fossa, whereas in Tyrannosaurus adults, and possibly  Zhuchengtyrannus, the fenestra extends past the rostral margin of the fenestra (Carr, 1999; Hone et al., 2011).

Interfenestral strut: This pillar separates the maxillary fenestra from the internal antorbital fenestra. Its dorsoventral height is corresponds to that of the maxillary fenestra.

In A. libratus and T. rex, the lateral surface of the strut is ontogenetically variable, where the ventral half is flat in juveniles, whereas it is concave in adults (Carr, 1999). The concave condition is also seen in Daspletosaurus adults (Carr, 1999). This condition is taken to an extreme in adults of some taxa (e.g., T. rex), where the region is perforated (Carr et Williamson, 2004). Also, the dorsal half of the strut becomes excavated by a deep fossa in old adult T. rex (Carr et Williamson, 2004).

Postantral strut Witmer, 1997: In some specimens, the upper corner of the rostral margin of the internal antorbital fenestra is convex. This bulge represents the relatively caudal position of the caudodorsal part of the postantral strut, the medial branch that bounds the postantral fenestra (=caudal antral fenestra; Witmer, 1997) that otherwise cannot be seen from the side.

II. Phylogenetic characters of the ascending ramus

Maxilla of a subadult Albertosaurus libratus (ROM 1247) in right lateral view labeled with the phylogenetic characters of Brusatte et al. (2010) that pertain to the ascending ramus. Character states that can be seen in the specimen are in boldface.

Illustrated above are the phylogenetic characters that pertain to the ascending ramus, as identified by Brusatte et al. (2010). A detailed description of them will not be given here, but some aspects are worth pointing out.

Phylogenetically informative characters of the ramus are not localized to one region, where they are instead distributed among (1) the nasomaxillary joint, (2) the maxillary fenestra and interfenestral strut, (3) the promaxillary fenestra, (4) the external antorbital fenestra, (5) the antorbital fossa, (6) the size of the ascending ramus, and (7) the form of the rostrodorsal margin of the bone.

III. Secondary structures of the alveolar process

Maxilla of a subadult Albertosaurus libratus (ROM 1247) in right lateral view, labeled with the secondary features of the alveolar process.

  Narial fossa: The narial fossa is a depression that extends caudodorsally from the subnarial foramen that is pinched out between the subcutaneous surface and the joint surface for the premaxilla. The fossa covers the lateral and rostrolateral surfaces of the vestibular bulla, whereas its dorsal surface is covered by the joint surface. Although the fossa does extend caudodorsally into the basal region of the ascending ramus, the fossa and its contents are here treated as a part of the alveolar process, given that its subordinate features and association with the subnarial foramen are located there.

The narial fossa is smooth relative the coarse subcutaneous surface and in many cases it is depressed relative to that external surface. The texture and inset nature of the fossa indicates that it is a continuation of the narial fossa that depresses much of the external surface of the premaxilla. Doubtlessly, it is an osteological correlate of soft tissue associated with the external naris, and not the subcutaneous surface. The former presence of a specific blood supply to that tissue is indicated by distinct foramina that open into the fossa, which have a stable occurrence in derived tyrannosauroids.

The narial fossa of the maxilla has a notable concentration of neurovascular openings at its caudoventral corner, namely one or two rostral foramina and the subnarial foramen. This occurrence indicates that the soft tissue associated with the external naris required a substantial blood and nervous supply. The fossa wraps around the rostral edge of the bone at the margin of the subnarial foramen.

Vestibular bulla Witmer, 1997 (=premaxillary process): This flange-like structure that extends from the rostromedial surface of the bone, situated between the subnarial foramen ventrally and the joint surface for the premaxilla dorsally. It is smooth and lies within the narial fossa. It is delimited by the rostral end of the promaxillary sinus rostrally, the joint surface for the premaxilla dorsally, the narial fossa laterally, and the margin of the subnarial foramen ventrally. Anatomically, the bulla is a swelling of the promaxillary sinus that extends rostrally into view, ahead of the external surface of the bone.

The bulla is almost certainly ontogenetically variable, where its lateral surface relatively flat in juveniles and subadults of A. libratus, whereas it is swollen and convex in adult Daspletosaurus and T. rex (Carr, 1999). Presumably this structure was not swollen in juveniles of the tyrannosaurines.

Joint surface for the premaxilla: In lateral view, the joint surface for the premaxilla excavates the dorsal surface of the vestibular bulla. The joint surface faces more dorsally than laterally, it is triangular in outline, and it tapers caudodorsally, pinched out between the bulla medially and the rostral end of the joint surface for the nasal laterally. The joint surface is coarse and concave, and rostrally it widens rostromedially toward the intermaxillary process, the free rostral end of the palatal process of the maxilla. This contact with the premaxilla is separated rostroventrally from the premaxillary buttress the gap formed by the margin of the subnarial foramen.

Margin of the subnarial foramen (=narial foramen): In all tyrannosaurids, the margin of the subnarial foramen is a shallow or deep notch in the rostral margin of the alveolar process that is separated from the ventral margin of the bone by a dorsoventrally deep joint surface for the premaxilla, the premaxillary buttress. The foramen opens into the narial fossa between the maxilla and premaxilla, producing a narrow gap or a large foramen. This foramen does not correspond to the alveolar or circumferential row, and almost certainly not to one of the rows that occur between them. The large size of the subnarial foramen indicates a substantial blood and nerve supply to the presumably cavernous soft tissue of the external naris.

Detail of the narial fossa of the maxilla of a subadult Albertosaurus libratus (ROM 1247) in right lateral view, labeled to show several of its subordinate structures, including the dorsal rostral foramen, joint surface for the premaxilla, margin of the premaxillary buttress, margin of the subnarial foramen, the ventral rostral foramen, and the vestibular bulla.

Dorsal rostral foramen Carr, 1999: This is a relatively large foramen located toward the lateral edge of the narial fossa at the level of the dorsal margin of the subnarial foramen; it is dorsal to the ventral rostral foramen, if that opening is present (Carr, 1999). This foramen does not correspond to the alveolar or circumferential row, or to any of the rows that are scatted between those primary rows. The relatively large size of this foramen indicates a substantial blood and nerve supply to the presumably cavernous soft tissue that supported the external naris and produced the narial fossa.

This opening is ontogenetically variable in A. libratus, where the foramen is slit-like in juveniles, whereas it is large and round in young adults (Carr, 1999). The round condition is also seen adults of Daspletosaurus and T. rex (Carr, 1999). In adult Daspletosaurus, expansion of this region is so great that the subcutaneous surface separates this opening from the ventral rostral foramen (Carr, 1999).

Ventral rostral foramen Carr, 1999: This small foramen is located toward the lateral edge of the narial fossa rostroventral to the dorsal rostral foramen, at the level of the ventral margin of the subnarial foramen; it is not present in all tyrannosauroids (Carr, 1999). This foramen does not obviously correspond to the alveolar or circumferential row, or to any of the rows that occur between them.

This opening is ontogenetically variable in A. libratus, where it is smaller then the dorsal rostral foramen in juveniles, whereas it is larger then the dorsal foramen in young adults (Carr, 1999). This difference is also seen between the juveniles and adults of T. rex, and the large condition is seen in adult Daspletosaurus (Carr, 1999). In adult Daspletosaurus, expansion of this region is so great that the subcutaneous surface separates this opening from the dorsal rostral foramen (Carr, 1999).

Premaxillary buttress Carr, 1999: This structure is located below the margin of the subnarial foramen. The buttress proper faces rostrally and it is an abutting joint surface for the maxilla below that foramen. In the articulated skull the buttress forms the maxillary contribution to the maxillopremaxillary suture below the subnarial foramen.

Dentigerous region (=alveolar region): In lateral view, this region makes up the bulk of the alveolar process. Although the dorsal limit of the alveoli cannot be seen from the side, they approximately line up with (slightly above) the ventral margin of the external antorbital fenestra. The dentigerous region begins at the rostral end of the bone, and stops caudally at the caudal end of the last tooth socket, in the vicinity of the caudalmost foramen of the alveolar row of neurovascular foramina. The dentigerous region occupies at least two thirds of the length of the entire bone.

The dentigerous region is ontogenetically variable, where it increases in dorsoventral depth with maturity (Carr, 1999). Also, in juveniles a distinct ridge extends along the ventral margin of the external antorbital fenestra and around its rostral margin (Carr, 1999). Expansion of the teeth makes this ridge indistinct in subadults (Carr, 1999). This is taken to an extreme in adult Daspletosaurus, where alveolar expansion completely eliminates the ridge (Carr, 1999).

In Daspletosaurus, the dentigerous region is so dorsoventrally expanded that its dorsal and ventral margins only gradually converge caudally toward the jugal ramus (Carr, 1999).

Circumfenestral ridge: This structure encircles the ventral and rostral margins of the external antorbital fenestra. In T. rex it is distinct in juveniles, whereas it is absent from adults; its presence is seen in A. libratus juveniles, and it is absent from adults of Daspletosaurus (Carr, 1999). Carr et Williamson (2004) have found that loss of the ridge is seen late in T. rex ontogeny, in the transition between young and old adults.

Ventral margin: The ventral margin of the maxilla in derived tyrannosauroids has a distinct profile, where the margin below the dentigerous region is ventrally convex. The margin of the dentigerous region is distinct from that of the jugal ramus in that the ventral margin of the jugal ramus is straight, or it is convex and extends at an angle caudoventrally from the dentigerous margin. Even in species where the dentigerous region is shallow and its ventral margin is nearly straight (e.g., Alioramus altai), an angulation separates it from the jugal ramus (Brusatte et al., 2012).

Undulations Lambe, 1917: The ventral margin of the dentigerous region is not an uninterrupted continuous curve, it is broken up by undulations that in turn are made up of two parts: a series of notches in the margin corresponds to each interalveolar septum (mediolaterally oriented partition of bone that separates adjacent tooth sockets) that are separated from each other by convexities that flank the base of each tooth. It appears that the notches are the donut (downward growth inhibited by the septa), whereas the convexities are the donuts (growth that extends the alveolus ventrally) that presumably limited lateral displacement of teeth under the loadings of a bite.

Alveolar skirts Carr, 1999: These structures are short flanges that extend ventrally from the convex undulations that flank the alveoli. They are only seen in adult derived tyrannosaurines, including Daspletosaurus (Carr, 1999).

Neurovascular foramina: Two primary rows of neurovascular foramina penetrate the lateral surface of the bone (Brochu, 1993). The circumferential row is the dorsalmost of the two rows, which extends close to – and around – the ventral and rostroventral margins of the external antorbital fenestra (Brochu, 1993). The alveolar row extends just above – and parallel to – the ventral margin of the dentigerous region (Brochu, 1993). The alveolar row extends uninterrupted onto the premaxilla where it splits into two or three rows, whereas it stops caudally in the vicinity of the last (i.e., caudalmost) alveolus of the tooth row. Several rows of foramina are scattered between the primary rows, especially rostrally.

These openings are the external exits of canals that extended within the interior of the maxilla that in life housed the branch of an artery, vein, and nerve. The openings continue onto the lateral surface of the bone as branching grooves termed neurovascular sulci. In the living animal, the neurovascular bundle would have extended toward the overlying dermis to (1) deliver nutrients and oxygenated blood to the cells of the dermis and periosteum, (2) receive metabolic waste and depleted blood to be sent to the lungs and kidneys, and (3) transduce the tactile sensations stimulated by the physical contact between the epidermis and the immediate environment into a charge difference for transmission along the membranes of nerve cells to the brain for processing and response.

The sulci of the alveolar row extend to the ventral edge of the bone, indicating that the nerves brought sensations stimulated along the external oral margin to the brain. The large size of these foramina suggests that this was an area of active remodeling that required a higher blood supply than the lateral surface of the bone situated away from the tooth row.

In contrast, the sulci of the circumferential row - and those between it and the alveolar row - generally extend ventrally, but they also have a dorsally extending component. This arrangement transforms the rostral end of the alveolar process into a massive, and presumably highly sensitive, tactile surface. Presumably, cutaneous sensations replaced the sense of sight during activities that engaged the power of the jaws during killing and feeding.

The foramina and sulci are ontogenetically variable in A. libratus, where the foramina are small and the sulci shallow in juveniles (Carr, 1999). In contrast, the openings are large and the grooves are deeply incised in young adults (Carr, 1999). This difference is also seen between juvenile and adult T. rex (Carr, 1999). Carr et Williamson (2004) later found that this change occurs relatively late in T. rex ontogeny, between subadults and adults. The large foramina and deep sulci are seen in adult Daspletosaurus, presumably the small and shallow condition is in juveniles (Carr, 1999).

External antorbital fenestra: In A. libratus, the rostroventral margin of the fenestra is ontogenetically variable, where the distinction between the fenestra and antorbital fossa is sharp in juveniles, whereas these surface grade into each other in more mature individuals (Carr, 1999).

In A. libratus, the ventral margin of the fenestra is ontogenetically variable, where it is straight or concave in juveniles, whereas it is sigmoid or dorsally convex in young adults (Carr, 1999). The margin is also convex in adult Daspletosaurus, and alveolar expansion (enlargement of teeth) expands the dentigerous region such that the ventral margin of the antorbital fossa extends laterally like a ledge (Carr, 1999). In T. rex the ventral margin is straight, and both the straight and concave conditions are seen in adults (Carr, 1999).

 

Detail of the jugal ramus (indicated by dotted line) of the maxilla of a subadult Albertosaurus libratus (ROM 1247) in right lateral view, labeled with its subordinate features, including the breach of the sulcus of the last foramen, the dorsal jugal process, the joint surface for the jugal, the last foramen of the alveolar row, the sulcus of the last foramen, and the ventral jugal process.

Jugal ramus: The jugal ramus includes the entire region of the alveolar process (including the antorbital fossa) that is caudal to the dentigerous region. The ramus is approximately a third of the length of the entire bone. The ramus is tightly interleaved with the jugal along several mostly vertical connections (see joint surface for the jugal). The ramus splits caudally into a pair of processes, the short dorsal jugal process and the long ventral jugal process. The ramus often, but not always, extends at a caudoventral angle from the dentigerous region; in contrast, the ramus extends nearly directly caudally from the dentigerous region in juveniles and subadults (Carr, 199).

In the disarticulated bone, the split between the dorsal and ventral processes occurs far caudal to where the rostral tip of the jugal is situated. However, the rostral end of the joint surface of the jugal is a useful landmark as the point of separation between the two processes when making comparisons between articulated skulls and disarticulated bones.

Joint surface for the jugal: In lateral view, the joint surface covers the region caudal to the antorbital fossa, bordered above by the dorsal margin of the dorsal jugal process, and from there it extends caudally onto the dorsomedial surface of the ventral jugal process. The joint surface rostrally is vertically oriented and flat, which extends laterally onto the dorsal surface of the ledge of the external antorbital fenestra that extends below and along the antorbital fossa. The ventral part of the joint surface is generally flat.

In contrast, the joint surface on the ventral jugal process is coarsened by rostrocaudally extending grooves and ridges. This widely exposed joint surface extends rostrally medial to the vertical flange that is overlapped by the jugal. As such, the maxilla is gripped from both sides of the antorbital fossa by the jugal.

Dorsal jugal process (=upper process): In lateral view, the dorsal jugal process is located entirely within the antorbital fossa, and so it is medially inset relative to the wide, laterally extending ventral jugal process. The overlapping lateral maxillary process of the jugal covers most of the lateral surface of the dorsal jugal process, but a slip of the process always extends above that bone. In effect, the maxilla excludes the tip of the jugal from contributing to the caudoventral part of the margin of the internal antorbital fenestra. In the disarticulated maxilla, the joint surface for the jugal on the process is a flat and inset facet, relative to the ridge that extends above the tip of the jugal.

Ventral jugal process Carr et Williamson, 2004 (=lower process): The ventral jugal process corresponds to the tapering caudoventral extremity of the bone caudal to the dentigerous region that is covered by the subcutaneous surface. Its rostral end is penetrated by the last foramen of the alveolar row of foramina, and it is scoured by the long sulcus that extends caudoventrally from the opening.

In A. libratus, the sulcus is shallow in juveniles, and it extends parallel to the ventral margin of the process; in contrast, the sulcus of young adults is short, deeply incised, and breaches (i.e., notches) the ventral margin of the process (Carr, 1999). The juvenile and mature conditions are also seen in the juveniles and adults of T. rex, respectively (Carr, 1999). In adult Daspletosaurus, the sulcus breaches the ventral margin of the process (Carr, 1999).

In the illustration of Albertosaurus libratus skull above, it can be seen that the ventral jugal process extends far caudally, below the level of the orbital fenestra. In derived tyrannosauroids, the tip of the process extends onto the medial surface of the jugal, so the bone in actuality extends a short distance further caudally before it stops.

IV. Phylogenetic characters of the alveolar process

Maxilla of a subadult Albertosaurus libratus (ROM 1247) in right lateral view labeled with the phylogenetic characters of Brusatte et al. (2010) pertaining to the alveolar process. Character states that can be seen in the specimen are in boldface.

 Several phylogenetically informative characters pertain to the lateral surface of the alveolar process, which are shown in the accompanying diagram. The characters are not dominated by a single structure or region, where they pertain to (1) the rim around the antorbital fossa, (2) the texture of the subcutaneous surface, (3) the primary row of foramina, (4) the ventral margin of the external antorbital fenestra, (5) the dorsoventral height of the antorbital fossa, and (6) the dorsoventral depth of the dentigerous region.

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