The middle ear of the skull of birds :

Transcription

1 /I~ri~liyi~il,/onr,ml 01 the lineon Sociely ( 198 I), 73: The middle ear of the skull of birds : the ostrich, Struthio camelus L. EDWARD I. SAIFF F.L.S. School of Theoretical and Applied Science, Ramapo College of New Jersey, Mahwah, N J , U.S.A. Acceptedfirpublicalim October 1980 The morphology of the middle ear region including the basicranium and quadrate ofsfncchio is very siiidiii. io tlir saiiic region in the orders Procellariiformes. Pelecaniformes. Ciconiiformes and Sphenixifomies. Strufhio though, has some unique middle ear characters such as the lack ofa chorda tympani nerve, the arrangement of the glossopharyngeal and vagus nerve foramina, the structure in the upper neck of the external ophthalmic vein and the position of the Eustachian tube. The articulatory surfaces for the quadrate both on the zygomatic process of the squamosal and the mandible are unique in Strut& when compared to the several orders mentioned above. KEY WORDS : -comparative anatomy- osteology - neurology- angiology - ratites. CONTENTS Introduction... Anatomical descriptions External '2 202 Middle ear region Quadrate and its relation to the middle ear region Discussion. '07 Conclusions Acknowledgements 21 I References I INTRODUCTION The relationship of the ratites to each other and to other birds continues to be a controversial topic. Stresemann ( 1959) allows that a final solution to this problem may never be reached, yet looks forward to further research on the topic particularly in the field of bird anatomy. Bock (1963) notes that while new morphological characters will provide further information it is doubtful whether additional morphology can resolve the problem. What follows is not an attempt to solve once and for all the ratite problem but simply an analysis of middle ear structure of one of the ratites, the ostrich, Slruthio 20 I / I The Linnean Society of London 10

2 202 E. I. SAIFF camelus L. It is hoped that such an analysis will shed some light on this perplexing and interesting problem. The work is grounded on the notion that in similar previous studies (Saiff, 1974, 1976, 1978) the morphology of the middle ear region could be trusted as an indicator of taxonomic relationship on the basis of overall similarity. Whether or not this study will result in better understanding of the ratite problem will not be known until similar analyses are made of other ratites and comparisons are made among ratites and carinates. I have studied several orders of carinate birds (Saiff, 1974, 1976, 1978) and, where appropriate, results of those studies will be mentioned. Parker (18661, Brock (1937), and de Beer (19371, and more recently Frank (1954) and Webb ( 1957) have studied the development of the skull in the ostrich and while each touches upon some middle ear structures none gives as complete an account of middle ear morphology as is presented here. As much as possible, morphological terminology follows that of Baumel et al. (1979). ANATOMICAL DESCRIPTIONS Specimens studied. Struthio camelus. Skeletons: 964, 965, 1503, 1507, 1907, 2732, 2775, 3199, 3869, 4261, 4396, USNM 18218, USNM , USNM , USNM , USNM Dissected: ES 014 (E. Saiff, Private collection, Mahwah, NJ.), USNM External The external auditory meatus (Meatus acusticus externus) is completely covered by feathers (Pennae auriculares) all of which are directed toward the rear of the skull. The opening of the meatus is mm high at the point of the largest opening and 5-9 mm wide at the widest part (four ears). The external meatus on each side is located behind the gape quite near the back end of the head. While the tissue surrounding the external meatus is not pliable enough to constrict it completely, it does appear that the external meatus could be closed by drawing the lateralmost portion of the rim of the meatus mediad. A superficial dissection, though, shows no musculature in the region with which to accomplish this. The external auditory canal is directed anteromediad. Posterior to the meatus and beneath the feather covering is a flattened ovoid area lined with the same type of tissue as that which lines the external auditory canal. This tissue is darkly pigmented and wrinkled. The wrinkles seem to be randomly positioned and may be effects of preservation. Other birds studied had regularly spaced ridges or grooves in the tissue lining the external auditory canal and these too were thought to be possible preservation effects (Saiff, 1974, 1978). The external auditory cavity is extensive and expands beyond the limits of the tympanic membrane (Membrana tympanica). The tympanic membrane forms the anteromedial wall of the base of the external auditory cavity. The tympanum is roughly circular and protrudes in a posterior direction into the external auditory cavity. The tympanic membrane is composed of a tough outer layer that is continuous

3 SKULL OF OSTRICH 203 with the lining of the external auditory canal. Additionally, there is a thin but elastic inner layer to the tympanic membrane that is continuous with the epithelihm lining the middle ear cavity. The inferior process of the extracolumella (Cartilago extracolumellaris), covered by its ligament, lies embedded within the inner tympanic layer. At this point the tym anic membrane is markedly thickened and this is the apex of the protuberance o P the tympanic membrane into the outer ear cavity. The tympanic membrane separates the external auditory canal from the middle ear cavity. Middle ear region (Figs 1, 2) The middle ear is a large cavity taking up much of the posterolateral region ot' both sides ot' the head. The tissue comprising the middle ear sac is supported anteriorly and dorsally by the quadrate (Quadratum) and squaniosal (Squainosutn), posteriorly by a thin metotic process in the rear, and more anteriorly, the lateral edge of the basitemporal platform (Lamina basiparasphenoidalis). The interior wall of the middle ear cavity is an extensive excavation bounded dorsally by a shallow depression of the skull tilled by Figure I. Slnclhio camrlw ( 4261), oblique vend view of left middle ear region: ATR, anterior tympanic recess; CF, carotid foramen; E, exoccipital; EC, eustachian canal; FV, fenestra vestibularis; H, hypoglossal foramina; LB, lamina basiparasphenoidalis; M, metotic process; OF, occipital vein foramen; P, pneumatic foramen; PA, palatine artery foramen; Q, quadrate; RST, recessus scalae tympani; SF, external ophthalmic (stapedial) arterial foramen; UTR, upper tympanic recess; VCL, exit point for vena capitis lateralis; X, vagus foramen; ZP, zygomatic process of the squamosal.

4 204 Anterior E. I. SAIFF Posterior Figure 2. Struthzo camelus (USNM ), lateral view of the arteries, veins, and nerves of the left middle ear region: C, columella; CA, carotid artery; P, palatine artery; RM, rete mirabile ophthalmicum; SA, external ophthalmic (stapedial) artery; VII, facial nerve foramen; VIIH, hyomandibular ramus of facial nerve; VIIP, palatine ramus of facial nerve; VOE, external ophthalmic vein. musculature, the upper tympanic recess (Foramen pneumaticum dorsale), behind which is located the articular surface of the zygomatic (Proc. zygomaticus) for the otic head of' the quadrate (Proc. oticus quadrati). No portion of the upper tympanic recess extends posterior to the articulatory surface for the otic head of the quadrate. The anterior border of the middle ear cavity is here defined by the anterior border of the foramen for the fifth cranial nerve (Foramen n. maxillomandibularis). The dorsal border of this foramen is continued anterodorsally by a thin ridge of bone which forms the dorsal border of a depression on the outside of the braincase wall. Bellairs 8c Jenkin (1960) refer to the middle ear cavity as the tympanic fossa since it is covered by the tympanic membrane and contains the columella (Basis columellae). The inner wall of the tympanic fossa is made up by the periotic and exoccipital bones at the posterior edge of which is the fenestra ovalis (Fenestra vestibularis) into which is inserted the foot-plate of the columella. Just ventral to the fenestra ovalis is a large recessus scalae tympani. Clearly visible in the dorsal aspect of the recessus scalae tympani is the perilymphatic sac as well as the processus interfenestralis. Just posterior to the fenestra ovalis and slightly dorsal to the recessus scalae tympani there is a pneumatic opening (Foramen pneumaticum caudale). Anterior to the fenestra ovalis and just dorsal to the anteriormost portion of the recessus scalae tympani is a vertical ridge of bone. Just anterior to this ridge is a deep foramen for the seventh cranial nerve (Foramen n. facialis), shared by both the hyomandibular (N. hyomandibularis) and palatine (N. palatinus) rani of that nerve. The palatine nerve branches from the main trunk of the facial immediately on exit from the facial foramen and then turns anteroventrally to enter a thin bony canal, the anterior exit of which is located at the anterior end of the basitemporal platform, medial to the point of the Eustachian tube (Tuba pharyngotympanica) and lateral to the exit point of the palatine artery (A. palatina). For a

5 SKULL OF OSTRICH 205 portion ot its length, this canal tor the palatine nerve is contiguous with the canal carrying the palatine artery,and thus represents a true parabasal canal. The hyomandibular ramus of the facial nerve, on leaving its foramen, continues laterally, su ported by a thin strip of bone which is a continuation of the rim of the bony facial P oramen. The hyomandibular ramus continues dorsal to the columella to the rear of the middle ear cavity, running along the lateral surface of the vena capitis lateralis (V. ophthalmica external with which it exits from the middle ear cavity through a large foramen in the lower portion of the metotic process. There is 110 chorda tympani nerve. Webb ( 1957) also notes the lack of chorda tympani in struthio. The vena capitis lateralis leaves the middle ear as a single vessel which subsequently breaks up into individual venous branches and lower down in the neck reunites to form a single vessel (Fig. 2). The carotid artery (A. carotis interna) is found in the upper neck just below the middle ear region wrapped in a bundle of veins all ofwhich are branches of the vena capitis lateralis. The venous bundle and its enclosed carotid artery are surrounded by a tough membrane. The carotid artery enters the middle ear from below by a carotid foramen in the Fossa parabasalis. The artery travels in the ventral portion of the middle ear cavity in a bony carotid canal (Canalis caroticus). Approximately halfway along the length of the carotid canal is a carotid entrance foramen through which the carotid artery enters the braincase. A branch of the carotid artery, the palatine artery, continues forward in the parabasal canal to exit adjacent to the Eustachian tube. Just prior to entering the middle ear region from the neck, the carotid artery gives off a dorsal branch, the external ophthalmic (stapedial) artery (A. ophthalmica external. The external ophthalmic artery enters the middle ear region through a foramen in the metotic process. The foramen continues as a canal running in the same plane as the metotic process to a position just below the recessus scalae tympani. The external ophthalmic artery continues to run first posterior then dorsal to the columella in a deeply excavated groove in the medial wall of the tympanic fossa. The anterior edge of this groove forms the ventral and then the posterior edge of the recessus scalae tympani. Running lateral and dorsal to the external ophthalmic artery is the vena capitis lateralis which leaves the middle ear cavity through the foramen that it shares with the hyomandibular nerve adjacent to the external ophthalmic arterial foramen in the metotic process. Together the stapedial artery and vena capitis lateralis form a rete mirabile ophthalmicum medial to the quadrate and quite a distance posterior to the fifth nerve foramen. The medial wall of the external ophthalmic arterial canal is perforated by a foramen which leads into a groove which courses dorsolaterally to the foramen magnum. A small occipital vein is carried in this groove. The foramen for the fifth nerve is large in Strulhio and separated from the facial foramen by a large, anteriorly directed, conical concavity, the anterior tympanic recess (referred to as the presphenoid sinus in Saiff, 1974, 1976, 19781, theanterior end of which is highly pneumatic. The fifth nerve foramen is found on the lateral wall at the outer surface of the anterior tympanic recess. Much of the anterior tympanic recess extends posterior to the fifth nerve foramen. Several shallow grooves emanate from the foramen for the fifth nerve and carried in them may be slips of V, described by Lakjer ( 1926) for the levator pterygoideus muscle complex. None of the branches of the fifth nerve complex traverses the middle ear region. The glossopharyngeal and vagus nerves exit together from the skull by a foramen medial to the external ophthalmic arterial foramen. In several of the

6 206 E. I. SAIFF skulls studied a thin bridge of bone partially divides the vagus-glossopharyngeal foramen into regions for each of the two nerves and in one specimen ( 4396) there seems to be a separate foramen tor the glossopharyngeal nerve. Brock ( has described a single foramen for the glossopharyngeal and vagus nerves in the ostrich embryo. The hypoglossal nerves exit by several small foramina located in the region between the posterior portion of the exoccipital and the occipital condyle. Beneath the floor of the anterior tympanic recess and dorsal to the carotid foramen is the entrance to the Eustachian canal. The membranous Eustachian tube is completely encased in the bony Eustachian canal. The Erzstachian tubes of both sides exit from above the basitemporal platform by a pair dkidely separated foramina in the dried skull. The tube from each side runs along the ventral surface of the basipterygoid process (McDowell, 1948) also called by Bock (1963) the basitemporal process, and each opens into the hind portion of the palate as a small slit located within a larger vacuity found posterior to the opening of the internal nares at the rear end of the mouth. Just anterior to the dorsal articulation of the quadrate with the zygomatic process is the upper tympanic recess from which originates the M. pseudotemporalis superficialis. This is not so extensive as in other forms studied by me (Saiff, 1974, 1976, 1978) although the cavityinextendingdorsallyand mediallyfills much of the zygomatic squamosal region of the skull. At its internal end it has many pneumatic openings. Posterior to the dorsal quadrate - zygomatic articulation are several pneumatic foramina, the cavities of which are continuous with each other through foramina in their side walls. Quadrate and its relation to the middle ear region The head of the quadrate articulates with the cranium in two places, by an internal (Condylus prooticus) and an external capitulum (Condylus squamosus). The capitula are not separated by a capitular groove (Incisura intercondylaris). A shallow capitular groove has been observed in Procellariiformes (Saiff, 19741, Spheniscitbrmes (Saif f, 1976) and Pelecaniformes and Ciconiiformes (Saiff, 1978). The facets that receive the capitula are not separated from each other by a bony ridge. Such a ridge has been observed in the above-mentioned orders (Saiff, 1974, 1976, 1978). No nerves or blood vessels run between the facets. A line drawn through these facets intersects the long axis of the skull at an angle of approxiiriately sixty degrees. The zygomatic process extends nearly halfway down the length ofthe quadrate on the lateral side of the quadrate but it does not contact the quadrate lateral ro the capitular articulation. The head of the quadrate, as seen in lateral view, forms an angle of approximately ninety degrees to the long axis of the head. Just in front of the articulation of the head of the quadrate with the temporal region of the skull is the entrance to the upper tympanic recess. Projecting anteriorly and medially toward the orbit from the shaft of the quadrate is the orbital process (Processus orbitalis quadrati; metapterygoid process of Parker, 1870). Ventral and medial to the orbital process is the pterygoid condyle (Condylus pterygoideus) which is the articulatory surface on the quadrate for the pterygoid bone. It is an extensive area taking up most of the medial surface of the quadrate shaft ventral to the orbital process. Dorsal to the pterygoid condyle, at the junction of the quadrate shaft with the orbital process, is

7 SKULL OF OSTRICH Table 1. Quadrate pneumatic foramina 20 7 Specimen Left side Right side ES USNM USNM USNM USNM USNM I I Quadrate lacking Smooth surface Smooth surface Not examined Not examined Deprgssion Quadrate lacking Not examined Not examined Not examined a pneumatic opening. At the same horizontal level on the quadrate shaft but on its rear surface some of the quadrates examined had an additional pneumatic foramen. In several specimens one side had this additional opening while it was lacking on the opposite side, although a slight depression may be present (Table 1 ). At the base of the quadrate shaft on its lateral aspect, just above the mandibular articulatory surface, is the articular surface for the quadratojugal (Cotyla quadratojugalis) which is referred to by Walker (1888) as the quadratojugal cup. The articular surface for the mandible consists of two long condyles separated by a trochlear groove (Sulcus intercondylaris). The medial condyle is ovoid. The lateral condyle is elongate, running almost parallel with the long axis of the skull. DISCUSSION Anterior tympanic recess (Anuum pneumaticum rostrale). Little mention of this structure is made in the early anatomical literature. Watson ( 1883) figured it in his work on penguins and Parker (1870, 18751, Shufeldt (1888) and Pycraft (1898a, b, 1899) mentioned it. Only Shufeldt (1888) discussed it comparatively. There seems little doubt that the anterior tympanic recess is pneumatic. The lateral rim of the anterior tympanic recess aperture in Struthio fuses to the outside edge of the lamina basiparasphenoidalis and offers protection to the carotid artery, palatine artery and nerve, and Eustachian tube. The Procellariiformes, except the Diomedeidae (albatrosses), have a well developed anterior mpanic recess (Saiff, 1974). This region in the Pelecaniformes (Saiff, 1978) varies 7 rom a very extensive structure in several of the Pelecanidae (pelicans) to a fav medially directed pneumatic foramina located anterodorsal to the carotid entrance foramen in the Sulidae (gannets). The sphenisciform (penguins) anterior tympanic recess is shallow and poorly developed (Saiff, 1976). Its lateral wall, though, does fuse with the lamina basiparasphenoidalis as seen here in the ostrich. All Ciconiiformes (herons, storks, ibises, etc.) examined by me (Saiff, 1978) have an extensive anterior tympanic recess but not all have the lateral edges fused with the lamina basiparasphenoidalis.

8 208 E. I. SAIFF Upper tympanic recess. The relationship between the upper tympanicrecess and the zygomatic facet for the head of the quadrate has been used as a character in the classification of some groups of birds by Lowe (1925). Lowe suggested that the Procellariiformes fall into a primitive group having the entrance to the upper tympanic recess between the facets for the head of the quadrate, and a specialized group with a large, conspicuous upper tympanic entrance anterior to the paired quadrate facets. I have found the entrance to the upper tympanic recess anterior to the paired quadrate facets in the Procellariidae and the Diomedeidae of the Procellariiformes, the Pelecaniformes, Sphenisciformes (Saiff, 19 74, , ) and Struthio. But in the two latter the upper tympanic recess could not be considered conspicuous either in size or location. Furthermore in Struthio there are several small pneumatic openings located posterior to the quadrate zygomatic articulatory site. The Hydrobatidae of the Procellariiformes have the primitive condition according to Lowe (1925) (Saiff, 1974) as do the Ciconiiformes (Saiff, 1978). Facial foramen. Struthio has a facial foramen located anterior to the fenestra vestibularis and posterior to the fifth nerve foramen, an arrangement typical of' most birds (e.g. Saiff, 1974, 1976, 1978) save the penguin genus Aj~tenodyles described in Saiff( 1976) which lacks a facial foramen opening within the middle car region. The Procellariiformes, Sphenisciformes, Ciconiiformes and Pelecaniformes are quite variable with respect to the presence of single or separate foramina for the palatine and hyomandibular rami of the facial nerve. Further variability is found regarding whether or not these rami travel through the middle ear in grooves, canals or without impression on the bone. Metotic process. A cartilaginous plate typically, in birds, becomes attached to the occipital arch, the outer edge of the basal plate and the auditory capsule. This plate, the metotic cartilage, separates the glossopharyngeal (if present) foramen from the vagus foramen, provides a floor for the recessus scalae tympani (de Beer, 1937 ; de Beer & Barrington, 1934; Bellairs 8c Jenkin, 1960) and forms at least part of the posterior and ventral point of attachment for the tympanic membrane. Sonies (1907) recognized the importance of this structure, referred to by Parker ( 189 1) as the paroccipital process and by Shushkin ( 1899) as the occipital wing. de Beer (1937) homologized the metotic cartilage or its ossification as used here (metotic process) with the paracondylar process (usually called the paroccipital process) in inaininals. Medially in the exoccipital near the occipital condyle are the hypoglossal foramina, the number of which varies among different forms and at different developmental stages (de Beer, 1937; Crompton, 19531, and in some instances on the two sides of the head. Among my material there is much variability with up to six hypoglossal foramina on each side of the skull. In Struthio the metotic process is perforated by a large foramen shared by the vagus and glossopharyngeal nerves and a foramen for the stapedial artery. There is also a foramen shared by the v. ophthalmica externa and the hyomandibular nerve as well as a foramen for the carotid artery. I 11 general, the metotic process of the Procellariiformes, Spheniscifbmmes, Ciconiiformes and Pelecaniformes (Saiff, 1974, 1976, 1978) is similar to that of Struthio although some groups of these orders are characterized by a weak or even absent metotic process, particularly the Diomedeidae of the Procellariiformes, the

9 SKULL OF OSTRICH 209 Phaethontidae (tropic birds) of the Pelecaniformes and the Scopidae and Phoenicopteridae (flamingos) of the Ciconiiformes. Ently ofcircdution into the head. In Struthio the carotid artery and v. ophthalmica externa enter the head from the neck without altering their dorsoventral direction. In the Procellariiformes (Saiff, 1974) and Sphenisciformes (Saiff, 1976) these blood vessels curve rostrad in order to enter the head from the neck. The path taken by the v. ophthalmica externa and carotid artery is dependent on two things: first, the position of the foramen magnum, which is indicative of the relationship between the head and the neck; and second, the metotic process-its presence, location and whether or not it is perforated by these vessels. In the adult ostrich there is an a proximate 110 degreeangle between the plane of the foramen magnum and the p P ane of the lamina basiparasphenoidalis. Parker (1866) notes that this angle in his 2i inch embryo is essentially a right angle. Furthermore, the metotic process is perforated by a sta edial arterial foramen, a carotid foramen and a v. ophthalmica externa-hyoman d! ibular foramen. The situation in the ostrich is similar to that in most of the Pelecaniformes and Ciconiiformes (Saiff, 1978) where the foramen magnum is in the posterior wall of the braincase and almost at right angles to the basitemporal platform. The long axis of the head is thus a forward continuation of the long axis of the neck, obviating the need for the carotid artery and v. ophthalmica externa to bend in order to enter the head. Middle ear blood vessel^. The common carotid artery in Struthio passes through a bundle of veins (part of the jugular) prior to entering the middle ear. After emerging from the venous bundle but just ventral to the metotic process the common carotid gives off the external ophthalmic artery. In none of the forms previously studied by me was there any indication of a venous bundle wra ping round the common carotid artery. Procellariiformes (Saik, 1974) does the external ophthalmic artery branch On? rom in the common carotid within the middle ear proper. Struthio has a carotid canal which complete1 encases the internal carotid artery (carotid after external ophthalmic is given o as in the Sphenisciformes (Saiff, 1976) and several of the Ciconiiformes (Saiff, 1978). Such a canal is lacking in the Procellariiformes (Saiff, 1974) and Pelecaniformes (Saiff, 1978). Struthio has the external ophthalmic artery travel naked laterally in the middle ear region (once it passes through the metotic) as is the case in Procellariiformes (Saiff, 1974) but not in Sphenisciformes (Saiff, 19761, and many of the Pelecaniformes and Ciconiiformes (Saiff, 1978) where some lateral bony protection is given to the external ophthalmic artery. In Struthio though, the external ophthalmic artery does travel in a deeply excavated groove on the dorsal wall of the tympanic fossa. Rete mirabile oph&lmkurn. An extensive rete mirabile has been found in Struthio and its structure has been confirmed by histology. The position of the rete is not the same as in the other avian forms I have described (Saiff, 1974, 1976, 1978). In the ostrich the rete is posterior to the fifth nerve foramen; in other forms which I have studied it is lateral to the foramen for the fifth nerve. The function of the rete mirabile and its relationship with the middle ear, if any, continues to elude me. As far as I can determine, there is no physiological or behavioural feature which distinguishes the forms possessing a rete mirabile from those which lack one. Recent work in my laboratory on Gdlw shows a well developed rete mirabile in the 19- day-old embryo. Further work on earlier embryos is in progress. Whether or not the interesting arrangement of the jugular vein, venous bundle

10 210 E. I. SAIFF and carotid artery in the upper neck region functions in a manner similar to the middle ear rete is a matter of conjecture. Obviously, further study on both these structures is in order. Eustachian tube. The usual arrangement in birds is for this structure to run from the anteroventral region of the middle ear cavity to a median opening in the rear of the palate which is shared with its fellow from the other side of the head. While Struthio shares this arrangement in general it is interesting to note that the entrance to the Eustachian tube is nearer to the posterior portion of the middle ear than in any other form which I have studied. Furthermore, the bony openings of the Eustachian canals on both sides of the rear of the palate are separated by a much greater (relative to skull size) distance than in any of the forms previously studied by me. In Struthio the Eustachian tubes are, for part of their length, completely encased in bony canals. Such protection is present in all Sphenisciformes (Saiff, 1976) but is generally absent or present for only a short distance in Procellariiformes (Saiff, 1974), Pelecaniformes and Ciconiiformes (Saiff, 1978). Quadrate. Walker (1 888) wrote a comparative analysis of avian quadrate structure but did not study the ostrich. She did, though, figure Rhea americanus as an example of a ratite, and pointed out that no other quadrate studied approaches that of Rhea in character. More generalized descriptions of the avian quadrate were given by Newton (1893), Coues (19031, de Beer (19371, Portmann (19.50) and Bcllairs 8c Jenkin (1960). Lowe (1926) and Cottam (1957) have used quadrate IIiorphology as a taxonomic character. My own studies (Saiff; 1974, 1976, 1978) include an analysis of quadrate structure. The quadrate of Struthio in general form appears similar to that of the other groups of birds that I have studied (Procellariiformes, Sphenisciformes, Pelecaniformes, and Ciconiiformes) although in some areas significant differences are to be found. In particular, the ostrich lacks a capitular groove on its articular surface with the zygomatic process. The mandibular articulatory surface, too, is different from those which I have studied. In the ostrich, as in other birds, a trochlear groove separates the articular surface into two condylar surfaces, with the anterior surface medial to the posterior surface. In the Procellariiformes (Saiff, 1974), Sphenisciformes (Saiff, 1976) and Ciconiiformes and Pelecaniformes (save Phaethon and Fregata) (Saiff, 1978) each of the condylar surfaces is paired to some degree. In Phaethon there is no pairing in the posterior condyle and in Fregata neither of the condylar surfaces are paired. In the ostrich the mandibular condyles of the quadrate are not paired. Additionally, the orbital process of Struthio is massive, suggesting an extensive point of attachment for the protractor quadrati muscle (Bellairs, 1964). Furthermore, the variability in the number of pneumatic foramina seen in the ostrich has not been observed in other avian forms which I have studied. CONCLUSIONS Slruthio cnrnelus shares numerous middle ear characters with Procellariiformes, Sphenisciformes, Pelecaniformes and Ciconiiformes. There are similarities in several of the foramina for the cranial nerves that open into the middle ear region, the presence and morphology of the anterior tympanic recess and upper tympanic recess, as well as the paths taken by the major blood vessels of the region, and the presence of a rete mirabile ophthalmicum. Not only do these orders share middle

11 SKULL OF OSTRICH ear characters, but they also share numerous other anatomical and embryological characteristics as reviewed by Sibley & Ahlquist ( 1972). These include pterylosis of the wing, intestinal convolutions, hallux morphology and function, and general featuies of skull embryology. At the same time Struthio retains some unique middle ear structures which clearly distinguish it from the flying forms on which I have previously reported. There is the interesting arrangement of a single foramen shared by the glossopharyngeal and vagus nerves (but apparently not constant) and the lack of a chorda tympani nerve. There is a unique structure in the upper neck just below the middle ear for the jugular vein, as well as a Eustachian tube that opens near the posterior end of the middle ear and continues forward completely encased in bone to open at the rear of the palate in a manner unlike that seen in the carinates so far examined. Further, there is the position of the rete mirabile ophthalmicum which in Struthio is in a more posterior location than in the carinates examined. The quadrate, too, shows its uniqueness in Slrulhio particularly in the articulatory surfaces for the zygomatic process and the mandible. 21 I ACKNOWLEDGEMENTS Drs Warren Porter and Sheila Mahoney kindly supplied me with a frozen head of Stmthio cumelw for dissection. Dr Wesley Lanyon and Mr Alan O'Connell of the American Museum of Natural History, New York () and Drs Storrs Olson and Richard Zusi of the United States National Museum (Smithsonian Institution), Washington, D.C. (USNM) allowed me to study material under their care. Dr Zusi also was kind enough to provide me with some data over the telephone. Drs Richard Graham, Samuel McDowell, Alick Walker and Ken Whetstone read and commented on the manuscript. The Ramapo College Graphics Centre (Frank Cavallo and Erik Unhjem) helped to prepare the figures. Research time to coniplete this study was provided by a Research Release Grant from Ramapo College. A portion of this paper was read at the XVII International Ornithological Congress held in Berlin, West Germany during June, REFERENCES BAUMEL, J. J., KING, A. S., LUCAS, A. M., BREAZILE, J. E. & EVANS, H. E. (Eds), Nomina Analmica Avium. London: Academic Press. de BEER, G. R The developmmc ofthe Vertebrate Shull. Oxford University Press. de BEER, G. R. & BARRINGTON. E. J. W., The segmentation and chondrification of the skull of the duck. Philosophical Traluactiom ofthe Royal So&& (B), 223: BELLAIRS, A. D. 'A., Skeleton. In A. L. Thompson (Ed.), A New Dutimty OjBirds: New York: McGraw Hill. I~III.I,AIKS, A. U.'A. (Ic JENKIN, C. R., The skeleton of birds. In J. A. Marshall (Ed.), RioloD and (.'W/t/JW~l/iiV' I'hydofl o/ Sirdr. I: London & New York: Academic Press. BOCK, W. J., The cranial evidence for ratite affinities. Proceedings 13th I n t d Ornithological Congress: BROCK, G. T., The morphology of the ostrich chondromnium. PrcueedingJ Ojthe Zoological Society Oj London, 1078: COlTAM, P The pelecanifonn characters of the skeleton of the shoebilled stork. B W e p s rex. Bullelin o/ the British Museum (Natural History), (Zoology), 5: COUES, E., Key to North Amnicdn Birds, 5th ed. Boston, Mass.: D. Estes. CROMFTON, A. W., The development of the chondrocranium of Sphmirw demersus with special reference to the columella auris of birds. Acta Zdopca, 34: FRANK. G., The development of the chondrocranium of the ostrich. A n d 4th University OjStelldosch, 30A(4): I AKJ I<I<. I' Sl~rdirri ulier die Tri~eminwvcrsorgle Kaumwhulnlur &r Snuropisden. Kopenhagen: C. Reitzel.

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