Witmer, L. M. 1997. Craniofacial air sinus systems. pp. 151– 159 in The Encyclopedia of , P. J. Currie and K. Padian (eds.), Academic Press, New York.

Craniofacial Air Sinus Systems

LAWRENCE M. WITMER Ohio University Athens, Ohio, USA

n unusual anatomical system pervaded the congested when we have colds and that are involved A heads of dinosaurs. In:sinuated among such in our "sinus headaches." conventional soft tissues as muscles, nerves, blood Paratympanic air sinuses are less common in ar­ vessels, and sense organs was a complicated system chosaurs. In those non-dinosaurian taxa with para­ of air-filled sinuses. These sinuses formed as thin­ tympanic pneumaticity (such as crocodylomorphs walled, epithelial outgrowths (diverticula) of other and ), the bones of the braincase are the air-filled cavities, often invading and resorbing sur­ ones that are usually invaded by air sacs. Among rounding bone and producing foramina and cavities perhaps all , tympanic recesses are best withinthesebones. This process is called pneumatiza­ developed in theropod dinosaurs. As with paranasal tion and the resulting state of having air-filled bones sinuses, humans and most other mammals have a set is known as pneumaticity. Many dinosaurs are highly of sinuses associated with the tympanic cavity, and pneumatic animals indeed, with most of the bony particularly bad middle-ear infections may spread to skull literally riddled with foramina, channels, and our paratympanic air sinuses. cavities. More technical treatments of this topic have In addition to paranasal and paratympanic si­ been published byWitmer (1990, 1995, 1997) and Cur­ nuses, there are other, more poorly known, systems rie and Zhao (1993a,b) and the articles cited therein. pneumatizing the head skeleton. The first may simply represent diverticula from the cervical system of pul­ Pneumatic Systems in Dinosaurs monary air sacs that extend beyond the neck verte­ There are two well-known pneumatic systems in di­ brae into the occipital region of the skull. Some of nosaurs, one arising as outgrowths of the nasal cavity the pneumatic cavities of certain theropod dinosaurs and the other as outgrowths of the tympanic (middle may result from these pulmonary diverticula. The ear) cavity. Not just dinosaurs, but all archosaurs­ second is the median pharyngeal system that forms living and extinct-have at least one main paranasal as a midline outgrowth from the roof of the throat air sinus, known as the antorbital sinus, that forms and invades the base of the skull in the region of as an outgrowth of the main nasal cavity (Fig. 1). The the basisphenoid and basioccipital bones in many antorbital sinus produces a large cavity and opening archosaurs. It is not always demonstrably of pneu­ inthe side of the face known respectively as the antor­ matic origin in many archosaurs but is almost cer­ bital cavity and antorbital fenestra. In many archo­ tainly so in theropod dinosaurs. Although the re­ saurs, the antorbital sinus itself has subsidiary out­ sulting "basisphenoid sinus" is often regarded as a growths that may pneumatize surrounding bones, derivative of a "medianEustachian tube," it is clearly producing so-called accessory cavities. In addition to distinct from the definitive auditory (Eustachian) the nearly ubiquitous antorbital sinus, a few kinds of tubes that, along with the tympanic cavities, have dinosaurs have air sacs deriving from a different part their embryological origins from the paired first pha­ of the nasal cavity, namely, the front-most portion ryngeal (or branchial) pouches; whereas in some ar­ known as the nasal vestibule. Such vestibular sinuses chosaurs the median system eventually connects up tend to pneumatize the bones surrounding the bony with the tympanic cavity, it does not always do so. nostril (i.e., premaxilla and nasal). Humans and most Some have suggested that the median pharyngeal other mammals have similar (but not homologous) pneumatic system results from aeration of the embry­ paranasal sinuses; these are the sinuses that become onic hypophysial pouch (of Rathke)-a precursor of 151 152 Craniofacial Air Sinus Systems

Allosaurus (ragilis Sinraptor dongi lacrimal sUbsidiary diverticula in recess accessory cavities

promaxillary recess

Facial Pneumatic Recesses • Maxillary recesses • Lacrimal recess sinus antorbitalis in • Promaxillary recess • Jugal recess antorbital cavity • Maxillary antrum • Nasal recess • Excavatio pneumatica • Palatine recess

FIGURE 1 Paranasal pneumaticity in theropod dinosaurs. (Left) skull of fragilis in oblique view, showing the antorbital paranasal air sinus and some of its epithelial diverticula (modified from Witmer, 1997, with permission). (Right) skull of Sinraptor dongi in left lateral view with the major paranasal pneumatic accessory cavities labeled (modified from Currie and Zhao, 1994a, with permission). The acces­ sory cavities result from pneumatization by the subsidiary diverticula of the antorbi­ tal sinus. part ofthe pituitarygland-and this is anidea worthy Paranasal pneumaticity, on the other hand, is pres­ of further investigation. ent in probably all ornithischians in that, like all other archosaurs, they possessed an antorbital sinus. This Ornithischian Dinosaurs antorbital air sinus was lodged in a cavity, the antor­ Paratympanic air sinuses are very uncommon in or­ bital cavity, located in front of the orbit and bounded nithischians. The middle ear sac was certainly present by primarily the maxilla and lacrimal, and sometimes (as evidenced by, among other things, the discovery also the jugal, palatine, and nasal. In fact, this descrip­ ofcolumellae-the slender earbones), but apparently tion holds for most dinosaurs (indeed, most archo­ it did not typically send out diverticula that invaded saurs). Pneumatic bony accessory cavities, produced surrounding bones. A few ornithischians, however, by subsidiary diverticula of the antorbital sinus, are such as the basal thyreophoran Scelidosaurus and the relatively rare in ornithischians, although they are ornithopod Hypsilophodon, do seem to have some ex­ present in a few taxa, such as the intramaxillary si­ cavations of portions of the braincase that are best nuses of Protoceratops and its relatives and the maxil­ interpreted as being of pneumatic origin. In these lary recesses of some basal thyreophorans. Higher forms, there is a fairly extensive cavity associated thyreophorans, in particular ankylosaurid ankylo­ with the canal for the major artery supplying the saurians, deserve special mention here in that within brain, the cerebral (or internal) carotid artery. This their highly armored skulls is a maze of pneumatic cavity is directly behind and medially undercuts a sinuses. The precise pattern and arrangement of an­ curving ridge of bone-nearly ubiquitous in archo­ kylosaurid paranasal sinuses remain poorly known, saurs-knownas the otosphenoidal crest, which runs and it is not entirely clear if some are accessory cavi­ from the basipterygoid process to the paroccipital ties of the main antorbital sinus, novel paranasal si­ process and segregates the orbital contents in front nuses, oreven diverticula ofthe nasal vestibule. Pneu­ from the middle ear contents behind. Although such matic evaginations of the nasal vestibule, however, a rostral tympanic recess is, as we will see, fairly are clearly expressed in lambeosaurine hadrosaurids, common in theropod dinosaurs (as well as in a variety such as Corythosaurus. In lambeosaurines, the narial of other archosaurs), it is rather rare in ornithischians. region is greatly enlarged, and the bones enclosing Craniofacial Air Sinus Systems 153

cavity is relatively tiny and completely closed later­ ~ A ~ ally). A similar phylogenetic trend can be identified ~1 ~~ in thyreophorans. These trends almost certainly relate !!~~-~ to (especially in ornithopods) the expansion and elab­ oration of the feeding apparatus (in particular, the ~ '~ dentition and its bony supports). Thus, as the feeding Heterodontosaurus apparatus expanded phylogenetically, the antorbital Lesothosaurus Iguanodonlia sinus and its bony cavity contracted. Euornithopoda Before concluding the discussion of ornithischian _---"_------' Ornithopoda craniofacial pneumaticity, the supracranial cavities of ceratopsids such as Triceratops need to be considered. These cavities, formed by the folding of the frontal bones, are often referred to as "frontal sinuses" and FIGURE 2 The evolving antorbital cavity of ornithischian are commonly thought to be of pneumatic origin. dinosaurs, especially Ornithopoda. Most clades of ornith­ They are often compared to the frontal air sinuses of ischians, such as Ornithopoda, show marked trends for modem bovid mammals (cattle, sheep, etc.) because reduction and enclosure of the antorbital cavity by laminae inboth ceratopsids and bovids the sinuses form strut­ of the maxilla and lacrimal. Modified from Witmer (1997) and references cited therein with permission. ted chambers that extend up into the base of the hom cores. It is possible that the supracranial cavities of ceratopsids are indeed pneumatic, but the source of the air-filled diverticulum remains obscure. It is not the nasal vestibule (the premaxilla and nasal) are yet clear how an outgrowth from either the nasal folded into a complicated collection of passages and cavity or the tympanic cavity could reach the skull chambers, all of which are perched atop the remain­ roof. Its mode of development is also unusual for a der of the skull. pneumatic recess. Thus, pending further research, the Perhaps the most remarkable aspect of skull pneu­ supracranial cavities of ceratopsids will remain func­ maticity in ornithischians is its recurrent trend for tionally enigmatic. reduction. In other words, ornithischians tend to be­ come relatively less pneumatic when comparing Saurischian Dinosaurs more advanced members of a clade with more basal includes neornithine , the most pneu­ members. For example (Fig. 2), the basal ornithischian matic of all known vertebrates, but not all saurischi­ Lesothosaurus has a more or less primitive-and ans display extensive craniofacial pneumaticity. In hence, fairly large-antorbital cavity; it even has a fact, other than the antorbital cavity itself, sauropodo­ small pneumatic accessory cavity associated with its morphs do not display many pneumatic features in palatine bone. In ornithopodan ornithischians, how­ their skulls, which is ironic because their axial skele­ ever, there is a general trend for reduction of the tons are otherwise often marvels of pneumatization. antorbital cavity and enclosure by lateral sheets of Basal sauropodomorphs (i.e., prosauropods) have rel­ the maxilla and lacrimalbones suchthat the antorbital atively primitive and simple antorbital cavities, al­ cavity becomes a relatively small and completely in­ though a subsidiary diverticulum of the antorbital ternalized space. The broad outlines of this trend can sinus excavates a pneumatic accessory cavity in the be viewed by making a phylogenetic march from a nasal of . The antorbital cavity of most basal ornithopod such as Heterodontosaurus (which sauropods is relatively reduced, being telescoped be­ retains a relatively large antorbital cavity but also tween the orbit behind and the greatly expanded na­ shows the beginnings of the lateral enclosure), sal vestibule infront. As inornithopods, the antorbital through Hypsilophodon (which shows further lateral sinus appears to be, in a sense, "crowded out" by enclosure) and iguanodontians such as Camptosaurus other structures. Paratympanic pneumaticity is also and Iguanodon (which show further reduction and relatively poorly developed in sauropodomorphs. A enclosure), to hadrosaurids (in which the antorbital few basal taxa, such as Anchisaurus and Plateosaurus, 154 Craniofacial Air Sinus Systems have, much as does Hypsilophodon, moderate develop­ lows out the "horns" of theropods such as Allosaurus ment of a rostral tympanic recess (i.e., the cavity asso­ and Ceratosaurus. The nasal, jugal, and palatine bones ciated with the cerebral carotid artery and bounded are less frequently pneumatized, but in some cases by the otosphenoidal crest). Other paratympanic re­ these recesses can result in spectacular structures, cesses i'lPpear to be virtually absent, although a few such as the inflated nasal crest of Monolophosaurus or sauropods (e.g., Camarasaurus) have a deep excava­ the puffed-up palatine bones of . tion in the back surface of the quadrate bone that The phylogenetic distribution of these paranasal could be interpreted as pneumatic in nature. pneumatic accessory cavities can be rather confusing. In contrast to sauropodomorphs, theropod dino­ Some groups, such as tyrannosaurids, tend to be fairly saurs display the most extensive craniofacial pneu­ consistent. Other groups, however, can be more vari­ maticity of all archosaurs with perhaps the exception able. For example, among dromaeosaurids, Deinony­ of some pterosaurs. Not only are the paranasal and chus has all the accessory cavities noted previously, paratympanic systems well developed in theropods but the closely-related form, Velociraptor, has only a but also the median pharyngeal system-for the first few of them. Moreover, a few taxa, such as the basal time in dinosaurs-takes on clearly pneumatic attri­ tetanuran Torvosaurus and the aberrant maniraptoran butes. In virtually all theropods, the antorbital cavity Erlikosaurus, lack many or even all of the accessory is huge, occupying in some cases more than half of cavities that phylogenetics indicates they "should" the total skull length; thus, the enclosed antorbital have. Nevertheless, despite these problems, one point paranasal air sinus must have been very voluminous that emerges is that the facial skeleton of theropods, (Fig. 1). As in other archosaurs, the maxilla and lacri­ as a group, is highly pneumatic; in fact, pneumaticity mal were the major bones housing the air sac, al­ has been recorded in every bone of the facial skeleton though the nasal, jugal, and palatine were also com­ except two (the prefrontal and vomer). monly involved. With the exception of the bizarre A final aspect of the paranasal air sinus system of oviraptorosaurs, which have dramatically compli­ theropods involves a diverticulum of the antorbital cated pneumatic skulls, there is no evidence that the sinus that only very rarely pneumatizes bone. This facial skeleton of theropods was pneumatized by any air sac, the suborbital diverticulum, is almost always air sacs other than the antorbital sinus. present in modern theropods (i.e., birds). It forms as Nevertheless, one of the remarkable aspects of an outgrowth of the back wall of the antorbital sinus paranasal pneumaticity in theropods was the ten­ and expands into the orbit where it often encircles dency for the antorbital sinus to send out subsidiary the eyeball and interleaves with the jaw musculature. diverticula that penetrated into the adjacent facial In at least a few nonavian theropods, there are good bones, often producing large pneumatic accessory reasons to believe that a -like suborbital divertic­ cavities (Fig. 1). Although many other archosaurs ulum was present (Fig. 1). The significance of this have more or less shallow pneumatic depressions suborbital sac is that it provides a mechanism for on various facial bones, it is theropods alone that actively ventilating the antorbital sinus (i.e., pumping routinely exhibit a facial skeleton that is produced air in and out). Movements of the lower jaw-such into an open series of hollowed struts and chambers. as in closing and opening the mouth-will set up The most commonly observed accessory cavities are positive and negative pressures in the suborbital sac those in the maxilla, with the two most consistent because ofits intimate relationship to the jawmuscles. maxillary sinuses being the promaxillary recess and These pressure changes are transferred to the antorbi­ the maxillary antrum. Both these accessory cavities tal sinus and, thus, like a bellows pump, air passes are widely (but not universally) distributed among to and fro between the nasal cavity and antorbital neotetanurans, and many (but again not all) cerato­ sinus. This situationis unique: In other animals with saurians have a single maxillary sinus, which is prob­ paranasal sinuses, such as crocodilians and mam­ ably homologous to the promaxillary recess of higher mals, the sinuses are never actively ventilated but theropods. The lacrimal bone is also commonly pneu­ rather are stagnant, dead-air spaces. What role such matized bya subsidiarydiverticulum ofthe antorbital a paranasal bellows pump plays in the physiology of sinus. It is this lacrimal sinus that invades and hol- birds and probably other theropods is still unknown. Craniofacial Air Sinus Systems 155

As with the paranasal system, the paratympanic cess./I Perhaps the most commonly encountered tym­ air sinuses are generally very diverse and extensive panic recess is the rostral or lateral tympanic recess in theropods. Most of the sinuses invade the bones noted previously in some other dinosaurs. This recess of the braincase and otic (ear) region, such as the is located just behind the otosphenoidal crest in the prootic, opisthotic, basisphenoid, and basioccipital. area of the cerebral carotid artery foramen. In some Some of these recesses are obviously associated with theropods, such as Syntarsus or , this the middle ear sac, but others, as mentioned pre­ recess resembles that of other archosaurs in being a viously, seem to result from median pneumatic out­ more or less simple but expanded cavity, whereas in growths of the roof of the pharynx and perhaps even others, such as some coelurosaurs, it becomes compli­ from extensions from the pulmonary air sacs in the cated and multichambered. For example, taxa such neck. The pneumatic sinuses of the braincase will be as Deinonychus and Struthiomimus have a discrete p~o­ briefly discussed using a hypothetical form (Fig. 3) otic recess within the rostral tympanic recess just ven­ because no known species has all the air cavities. tral to the facial nerve foramen, and a varied group There are three fairly consistent pneumatic cavities of tetanurans have a more ventral cavity, the subotic that clearly derive from diverticula of the middle ear recess, that excavates the basal tubera. In some forms, sac, and they all aptly bear the name "tympanic re- such as ornithomimids, troodontids, and birds, the

occipital view dorsal left lateral tympanic view recess

suboUc bst recess

Cranial Pneumatic Recesses • Caudal tympanic recess • Subcondylar recess • Dorsal tympanic recess • Quadrate recess • Rostral/lateral tymp. recess • Articulare recess • Prootic recess perhaps: • Subotic recess • SUbsellar recess • Basisphenoid recess • Basipterygoid recess

FIGURE 3 Braincase of a hypothetical theropod showing the diversity of pneumatic recesses. Pneumatization from the middle ear sac produces the dorsal, caudal, and rostral tympanic recesses and the recesses within the quadrate and articular bones (not shown). The subcondylar recesses derive from either the middle ear sac or extensions from the pulmonary air sacs. Pneumatization from a median pharyngeal system produces the basisphenoid recess. The basipterygoid and subsellar recesses are not Clearly pneumatic structures, and the source of the diverticulum, if present, is also uncertain. fo, fenestra ovaHs (or vestibularis) [note: not foramen ovale, which is the maxillary n. foramen in mammals); fpr, fenestra pseudorotundum (or cochlearis); osc, otosphenoidal crest. 156 Craniofacial Air Sinus Systems rostral tympanic recess and part of the main middle Paired openings on the occipital surface of the cra­ ear sac are covered laterally by a thin sheet of bone, nial base below the occipital condyle, known as the the parasphenoid. The caudal tympanic recess is typi­ subcondylar recesses (Fig. 3), are not widely distrib­ cally found in (Troodon being an im­ uted in theropods but are well developed in tyranno­ portant exception) and involves a large air space saurids and ornithomimids. These cavities are obvi­ within the paroccipital process that opens into the ously of pneumatic origin in that they expand within tympanic cavity via an oval foramen on the front the bone and are multichambered. What is uncertain of the base of the paroccipital process. The dorsal is the source of the air-filled diverticulum. The diver­ tympanic recess, a moderate to very deep depression ticulum could indeed derive from the middle ear on the dorsolateral surface of primarily the prootic sac-that is, it is another tympanic recess. Certainly, bone, has a very patchy distribution but is found in the subcondylar recess is close enough to the tym­ ornithomimids, velociraptorine dromaeosaurids, and panic cavity that it would not be a "far reach." An­ all known birds. other idea, however, cannotbe ruled out: The subcon­ In a few groups of nonavian theropods, such as dylar recesses derive from diverticula of the cervical birds, tyrannosaurids, and at least some ornithomi­ division of the air-sac system. The cervical air mids and troodontids, the quadrate and/or articular sacs pneumatize the backbone up to the second cervi­ bones are also invaded by outgrowths of the middle cal vertebra in tyrannosaurids and ornithomimids ear sac. In some respects, such pneumaticity makes and thus are very close to the occiput. Furthermore, good sense in that the quadrate and articular bones they presumably interleaved with neck muscles that have their embryological origins as parts of the first attached to the occiputin the vicinity ofthe subcondy­ pharyngeal (= mandibular) arch; recall that the mid­ lar recesses. Choosing between a tympanic or pulmo­ dle ear sac itself derives from the same pharyngeal nary source is currently very difficult. arch. In fact, it is a mystery as to why more groups A couple of other cavities may be of pneumatic of theropods-especially bird-like forms such as Dei­ origin but are much more uncertain (Fig. 3). The basi­ nonychus that have extensive braincase pneumatic­ pterygoid recess is a depression within the lateral ity-lack mandibular arch pneumaticity. Interest­ surface of the basipterygoid process within the orbit ingly, crocodyliforms, many pterosaurs, and some of theropods such as Allosaurus. If it is pneumatic, other non-dinosaurian archosaurs have pneumatic the source of the diverticulum is unclear. Instead, it quadrates and articulars. may be a site of muscular attachment, perhaps for a The median pharyngeal system, a rudimentary palatal protractor (if indeed such muscles were pres­ blind pit or small foramen between the basioccipital ent in nonavian theropods). The subsellar recess is and basisphenoid in other archosaurs, takes on the a median ventral cavity located just in front of the unmistakable appearance ofaninvasive air-filled cav­ basisphenoid recess at the base of the parasphenoid ity in theropod dinosaurs, in which it is usually re­ rostrum. As its name implies, it resembles the basis­ ferred to as a "basisphenoid sinus" (Fig. 3). Typically, phenoid recess in being directed toward the pituitary the sinus is roughly pyramidal or conical, with its fossa, but obviously both recesses could not result base being a large opening in the midline of the ba­ from a diverticulum tracking along the single embry­ sicranium between the paired basal tubera and basi­ onic hypophysial stalk (if in fact either did). Clearly, pterygoid processes and its apex being directed dor­ both the basipterygoid and subsellar recesses are sally toward the pituitary fossa. Even in basal forms structures that need a good deal more research. such as and Dilophosaurus, the basisphe­ Two more "problem sinuses" need to be consid­ noid sinus is already somewhat expanded. However, ered. Large cavities within both the ectopterygoid in most tetanurans the basisphenoid sinus becomes and squamosal bones are clearly pneumatic. The a large expansive cavity, invading back into the basi­ source of the diverticula, however, remains unclear. occipital bone, sometimes even into the occipital con­ The ectopterygoid recess is an almost ubiquitous fea­ dyle. Sometimes a median septum is preserved ture of theropods. It usually takes the form of a sim­ within the sinus, partially dividing it into left and ple, smooth-walled ventromedial "pocket" in the right sides. bone, although in some tyrannosaurids it becomes a Craniofacial Air Sinus Systems 157 multichambered affair. However, did the diverticu­ lum come from the middle ear sac, the antorbital .c, sinus, or from some unknown source (perhaps yet " ~ another pharyngeal outgrowth!)? All these ideas are ..... f;;r.~ possible buthave problems. Likewise, the large recess do....tympan~~~Tc;.... within the squamosal bones of tyrannosaurids and diverticulum ~ ornithomimids could have been produced by subsid­ iary diverticula of either the antorbital sinus or the middle ~,-:? middle ear sac, and we currently have little strong ear sac ",1\ .;' -'. _ Within an evolutionary sequence; --.../" .oJ \ .Conformatio~alchang~si~gross evidence that allows us to make a reasoned choice. ---.J anatomlcalorgamzatlon In summary, theropod dinosaurs obviouslyexhibit '~,- """""~~ -Resultantdiverticulachanges in pneumatic ~ _ Potentially large changes in an extraordinary-often bewildering-diversity of ) \ bony pneumatic recesses air-filled sinuses. Without question, pneumaticity is ---.J v' the single most important anatomical system shaping theropod skull morphology. Interestingly, however, FIGURE 4 A transgression-regression model for homo­ it seems fraught with high levels of homoplasy (the plasy in pneumatic systems. Hypothetical evolutionary transformation series of theropod braincases depicting the evolutionary loss and/ or convergent acquisition of changing status of a dorsal tympanic diverticulum of the a feature). Certainly, there are some very consistent, middle ear sac and, hence, the variable presence or absence phylogenetically informative pneumatic characters, of the bony recess. As the anatomical conformation of the such as the presence of the two main maxillary si­ whole region changes, the possibility for a diverticulum to nuses in neotetanurans or the caudal tympanic recess evaginate changes. Thus, the mechanism for pneumatic homoplasy is easily envisioned, with an apt analogy being in coelurosaurs. However, many of the pneumatic the fluctuating sea levels associated with transgression characters seem to have been evolved or been lost and regression. repeatedly-often yielding a morphology so similar that the only hint ofhomoplasy comes through phylo­ genetic analysis. The dorsal tympanic recess of coelur­ osaurs is a good, but by no means the only, example. conformational change might prevent evagination of This recess is found in Mesozoic birds, such as Hesper­ this diverticulumor cause it to shift its position, which ornis and Archaeopteryx, as well as the dromaeosau­ would appear to us as a reversal. Subsequent changes rids Deinonychus and Velociraptor. So far, so good, but could permit the diverticulum to evaginate once it is absent in the dromaeosaurid Dromaeosaurus. It is again, perhaps resulting in a bonyrecess thatis identi­ also absent in the bullatosaur Troodon but is clearly cal to the second species, which then would represent present in the bullatosaur Struthiomimus. The addi­ convergence. The point is that these epithelial air sacs tion of other taxa onlycomplicates the picture further. are highly labile structures, the position (or even the When the workings of pneumatic systems-that presence) of which is easily affected by surrounding is, the soft tissue systems that literally produces the anatomical structures. Thus, given this almost capri­ bony recesses-are understood, morphogenetic cious ebb and flow of pneumatic diverticula, perhaps mechanisms for phylogenetic reversal and conver­ it is unreasonable even to expect these bony cavities gence become rather easy to envision. For example, to fall out neatly on a cladogram. in the diagram in (Fig. 4) showing a hypothetical ancestor-descendant sequence of species, the ances­ Functions of Sinuses tral form has a relatively simple middle ear sac with It is somewhat ironic that, despite air-filled sinuses no dorsal tympanic diverticulum. A descendant spe­ being very prominent components of head anatomy cies might evolve some anatomical change in the con­ in not justbirds and other dinosaurs but also in mam­ formation of the general region (in this case, a higher mals, the function of pneumaticity has remained ob­ and shorter braincase) that, for some reason, permits scure. Numerous ideas have been proposed over the evagination of a diverticulum, and this diverticulum years, including sinuses acting as shock absorbers, excavates a pneumatic cavity on the prootic. A further flotation devices, vocal resonators, thermal insula- 158 Craniofacial Air Sinus Systems

tors, weight-reducing air bubbles, and the list goes or the diverticula of the middle ear sac? The answer on. Many of these ideas at first may seem absurd but is probably, at its base, no particular function whatso­ still may apply to some animals in some cases. For ever. That ,is not to say that any of these air sacs example, the sinuses within the crests of lambeosau­ could notbe secondarily pressed into service for some rine hadrosaurids are thought to have functioned as positive function, subsequently honed by natural se­ resonating chambers. However, these functions obvi­ lection. Such is likely the case for the resonating cham­ ously cannot apply broadly across all animals that bers of hadrosaurs and, additionally, aspects of the possess the sinus. In fact, because almost all the ideas expanded tympanic cavities of theropod dinosaurs, that have been proposed fail because of limited appli­ which enhance hearing due to certain acoustic prop­ cability, the problem of the general function of pneu­ erties. However, at the same time, positive functions matic sinuses has been regarded as one of the great need not be sought for every pneumatic recess in mysteries of craniofacial functional morphology. every species that has them. Again, they are simply It is significant that virtually all the suggestions intrinsic properties of pneumatic systems. hinge on the empty space within the sinuses being This new view on the function of pneumaticity that which provides the suggested functional bene­ helps explain certain trends in various dinosaur fits. With regard to the lambeosaurine example dis­ groups. For example, the reduction of the antorbital cussed previously, the empty space would provide cavity in ornithopod ornithischians that was dis­ the chamber in which sound resonates. It now seems cussed previously (Fig. 2) clearly reflects a situation that it is this focus on the enclosed volume of air that in which bone deposition "won out" over pneumati­ has led us astray. Sinuses are not truly "empty," but cally-induced resorption of bone. The evolution and rather they contain the air sac itself-that is, the thin refinement of chewing in ornithopods required exten­ epithelial balloon that lines the bony recess. It turns sive bony buttressing and reinforcement, and so out that the epithelium-not the empty space-may expansion of the antorbital sinus was severely lim­ be the key. Pneumatic epithelium (and its associated ited. On the other hand, skull pneumatization in ther­ tissues) appear to have the intrinsic capacity to ex­ opods appears to have progressed with few con­ pand and to pneumatize bone. Therefore, these air straints and was clearly opportunistic. Although sacs may simply be opportunistic pneumatizing ma­ carnivory may involve fairly large bite stresses (force chines, expanding as much as possible-but within per unit area), the stresses and strains that a theropod certain limits. These limits are provided by the local skull as a whole underwent were minimalincompari­ biomechanicalloading regimes (i.e., the stresses and son with the repetitive masticatory forces to which strains within the bone substance). Bone is sensitive chewing animals such as ornithopods were subject. to and responsive to its local stress environment, such Thus, in theropods, sinuses were generally free to as the forces involved in chewing or biting or laying expand. It is significant, however, that the remaining down new bone to maintain sufficiently strong and bony struts in theropod skulls are positioned in me­ stiff structures. Thus, there are two competing tend­ chanically advantageous locations, giving the appear­ encies, one involvingexpanding air sacs and the other ance of exquisite design. It is also worth mentioning involving mechanically mediated bone deposition. A that Tyrannosaurus rex, a theropod that secondarily compromise is struck ensuring that pneumatization became adapted for particularly hard biting, in­ does not actually jeopardize the strength of the whole creased the dimensions of some bony buttresses and structure. An interesting consequence of this "battle" bars to resist the stresses, yet it maintained pneuma­ is that mechanically"optimal" structures will result ticity-and even expanded some sinuses-by pneu­ as a secondary and completely incidental by-prod­ matizing the bones internally, yielding a skull com­ uct-in other words, there is no reason to invoke posed of a series of hollow, often truly tubular bars natural selection to act directly to produce structures and plates. of maximal strength but minimal materials. Put sim­ ply, architecturally "elegant" structures are auto­ matic outcomes of these two intrinsic, but opposite, See also the following related entries: processes. BRAINCASE ANATOMY. POSTCRANIAL PNEUMA­ Thus, what is the function of the antorbital sinus TICITY • SKULL, COMPARATIVE ANATOMY Cretaceous Period 159

References ------­ Once divided into three epochs, the Cretaceous Currie, P. J., and Zhao, X.-J. (1993a). A new carnosaur of Europe is now divided into the Early and Late (Dinosauria, ) from the Jurassic of Xinjiang, Cretaceous, which are further subdivided into 12 People's Republic of China. Can. J. Earth Sci. 30,2037­ stages. These were all defined on the basis of strata 208l. in the Anglo-Paris-Belgian area. In North America, Currie, P. J., and Zhao, X.-J. (1994b). A new troodontid the period is also divided into Early (Comanchean) (Dinosauria, Theropoda) braincase from the Dinosaur and Late (Gulfian) Cretaceous. Park Formation (Campanian) of Alberta. Can. J. Earth Sci. 30,2231-2247. The earth's climate was generally warm in the Cre­ taceous. Early in the period, conditions were becom­ Witmer, L. M. (1990). The craniofacial air sac system of Mesozoic birds (Aves). Zool. J. Linnean Soc. 100, ing more humid and seasonal, which favored explo­ 327-378. sive diversification of the floras and the animals that Witmer, L. M. (1995). Homology of facial structures in ex­ fed on them. By the end of the Cretaceous, global tant archosaurs (birds and crocodilians), with special cooling led to a drop in diversity of plants and ani­ reference to paranasal pneumaticity and nasal conchae. mals in the higher latitudes. J. Morphol. 225, 269-327. Throughout the Cretaceous, the continents drifted Witmer, L. M. (1997). The evolution of the antorbital cav­ apart to approach their currentpositions. The Atlantic ity of archosaurs: A study in soft-tissue reconstruction Ocean opened up, India reached Asia, and extensive in the fossil record with an analysis of the function of inland seas subdivided the continental masses. pneumaticity. Mem. Soc. Vertebr. Paleontol (I. Vertebr. Pa­ leontol.) 17(Suppl.), 1-75. Cretaceous rocks are widely distributed and ex­ posed, and it is not surprising that almost half of the known dinosaurs have been found at this level. Hadrosaurs and ceratopsians in particular are com­ mon in the Late Cretaceous of the Northern Hemi­ Crests sphere. It was a time of great diversification, and dinosaurs shared their world with many other verte­ see ORNAMENTATION brate groups that have changed little since the Creta­ ceous. Placental mammals, birds, snakes, and many other animals established the bauplans that are famil­ iar to us today. Insects and other invertebrates were taking on a more modern appearance. It was a time Cretaceous Extinction when the terrestrial floras changed from being en­ tirely dominatedbypteridophytes and gymnosperms see EXTINCTION, CRETACEOUS in the early part of the Cretaceous to angiosperms in the Late Cretaceous. The floral assemblages from the Late Jurassic persisted into the Early Cretaceous inthe lower latitudes, whereas angiosperms became more prominent in the higher latitudes. By the early Late Cretaceous Period Cretaceous, there was a dramatic change into assem­ blages dominated by angiosperms. Four floral prov­ EVA B. KOPPELHUS inces based on pollen have been recognized in the Geological Survey of Denmark and Greenland Cenomanian: northern Laurasia, southern Laurasia, Copenhagen, Denmark northern Gondwana, and southern Gondwana (Bren­ ner, 1976). By Santonian-Campanian times, angio­ The Cretaceous is the last period of the Mesozoic. sperm pollen assemblages have been used to divide It lasted for approximately 80 million years, ending Laurasia into a southern Normapolles province and a 65 million years ago. The name is derived from the northern Aquilapollenites province (Batten, 1984). The Latin word "creta," which means "chalk," and refers Cretaceous is a mostinterestingperiod from anevolu­ to the thick beds of Cretaceous chalk that are charac­ tionary point of view. teristic of parts of Europe. Toward the end of the period, however, things Witmer, L. M. 1997. Craniofacial air sinus systems. pp. 151-159 in The Encyclopedia of Dinosaurs, P. J. Currie and K. Padian (eds.), Academic Press, New York.

Figure 1 a i l a h a r p o e h c p o o n

i Hypsilophodon Edmontosaurus e g r r y a h T M

Heterodontosaurus Iguanodon Lesothosaurus Iguanodontia Euornithopoda Ornithopoda

Ornithischia Figure 2 Witmer, L. M. 1997. Craniofacial air sinus systems. pp. 151-159 in The Encyclopedia of Dinosaurs, P. J. Currie and K. Padian (eds.), Academic Press, New York.

Figure 3 Witmer, L. M. 1997. Craniofacial air sinus systems. pp. 151-159 in The Encyclopedia of Dinosaurs, P. J. Currie and K. Padian (eds.), Academic Press, New York.

Figure 4