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Anatomy of the Middle Ear Region of the Avian Skull: Sphenisciformes

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Anatomy of the Middle Ear Region of the Avian Skull: Sphenisciformes ANATOMY OF THE MIDDLE EAR REGION OF THE AVIAN SKULL: SPHENISCIFORMES EDWARD SAIFF WHEN I reviewedthe literature on the middle ear regionof birds (Saiff 1974), it became obvious that few anatomical studies have been made on this regionin birds, penguinsin particular. Watson's (1883) report on the anatomyof the Sphenisciformeslacks any detailson the middleear. Walker (1888) studiedquadrate morphology in a large variety of birds includingSphenisciformes. Pycraft (1898) describedthe skullof penguins but passedover the middle ear region save for a few brief statementsre- gardingthe quadrate,basitemporal platform, eustachiantube, and the trigeminalforamen. Shufeldt (1901) also failed to go into detailsof the middleear regionin his osteologicalstudy of the penguins.More recently, in a study of the evolution of penguins,Simpson (1946) describedthe skull of Paraptenodytesantarcticus, a fossilpenguin. This studytheorized a close relationship between the penguins and the Procellariiformes. Crompton (1953) made a further study on penguinsand did an extensive developmentalstudy of the chondrocranium.An analysisof middle ear anatomy of Procellariiformes,including a glossaryof avian middle ear characters,appears in Saiff (1974). Recently Frost et al. (1975) de- scribedthe circulatory systemin the head o/ Spheniscusdemersus in an effort to describeheat-exchange systems in penguins. Obviouslacunae exist in the studyof the middleear of birds,including Sphenisciformes.This study describesthe anatomyof the middle ear and basicraniaof the Sphenisciformesand where possiblemakes com- parisonswith Procellariiformes. MATERIALS AND METItODS This study is based on an analysis of charactersof specimensborrowed from the Bird Department of the American Museum of Natural History. Peters (1931) was used as the basis for the genericclassification and Wetmore (1930) for the higher taxa. I studied the following specimens: dried skull: Aptenodytes/orsteri AMNH 3745. A. patagonicaAMNH 1623, 2611, 3139, 4630, 4383, 4382. Eudyptes chrysolophus AMNH 5974. E. crestatusAMNH 3854, 5398, 5972. E. pachyrhynchusAMNH no number. E. schlegeliAMNH 5399. Eudyptula rainor AMNH 5314, 5620, 6257. Megadyptesantipodes AMNH 5613, 5615. Pygoscelisadeliae AMNH 5041. P. papua A.MNIt 3196, 4361, 5373, 5766, 5973. Spheniscusderaersus AMNH 1625, 1310, 3875, 4042, 4069, 4942. S. huraboldtiAMNH 2768, 4920, 4921. S. raendiculusAMNH 3648, 3772. Dissected: S. deraersus AMNH 4548. 749 The Auk 93: 749-759. October 1976 750 EDWARDSA• [Auk, Vol. 93 ANATOMICAL DESCRIPTIONS EXTERNAL.--Theexternal auditory meatusis on the same horizontal plane as the gape. The meatus lies on the border of a white band of feathersthat runs first over and then behind the eye and a dark feather patch that extendsposterior to the gape onto the throa region. The feathers that cover the external meatus grow only from its anterior rim. The meatus ranges between 2.4 to 3.5 mm tall and 1.9 to 2.1 mm wide (2 ears). The rim of the meatusdoes not appearto be sopliable as to close completely. The external auditory canal is directed posteroventrally.No ridges appear on the inner membranouslining of the canal. Ridges do appear with somedegree of consistencyin Procellariiformes(Saiff 1974) although the presenceor absenceof suchridges may be an effect of preservation. Upon removal of the m. depressormandibulac, the oater membrane coveringof the external auditory canal becomesvisible and when this is dissectedopen the tympanicmembrane comes into view. The tympanic membrane is roughly circular in shape, mildly protubcrant, and faces posterolaterad.It is composedof a tough, thick outer layer that is quite elastic and a thinner but equally tough inner layer. The outer layer of the tympanic membrane is a continuation of the lining of the external auditory canal while the inner layer is continuouswith the epithelium lining the middle ear cavity. The inferior processof the extra-columella, coveredby its ligament,lies embeddedwithin the inner tympaniclayer. Here the tympanic membrane is thickened. The tympanic membrane separatesthe externalauditory canal from the middle ear cavity. ANATOMY O1' THE MIDDLE EAR REGION. The middle ear of all six generaof penguinsis characterizedby a conicaltympanic cavity as seen in Fig. 1 that opensto the rear of the skull medial to the quadrate. Watson (1883) clearly figured this region but did not label it. The dorsal,ventral, and anteriorwall of the tympaniccavity is a curvedplate of bone that extendslaterally to touch the rear of the dorsalend of the quadrate; the ventral edgeof this plate is bent backwardhorizontally to form, alongwith a lateral extensionof the basitemporalplate, the ventral wall of the tympanic cavity. The tympanicmembrane (seen dried in placein someskulls as well as in situ in AMNH 4548) is stretchedacross the rear apertureof the tympanic cavityfrom the metoticprocess to the quadrate.On the medialwall of the tympanic cavity is the fenestraovalis, posteriorto which is a pneumatic foramen. Ventral to thesetwo structuresis the recessusscalae tympani. The seventh nerve foramen varies among the specimensexamined. A facial foramenopening within the tympaniccavity is lackingin Eudyptes, October1976] PenguinMiddle Ear Region 751 VlI FR AQF U/TRC I / / / •X !..... H PA ET BP MP CF M Fig. 1. Spi•eniscusdemersus (AMNH 4042) obliqueventral view of the left middle ear regionwith quadrateremoved: AQF, anteriorquadrate facet; BP, basitemporal platform;C, columella;CF, carotidforamen; ET, entranceto eustachiancanal; FP, foramenprooticum; H, hypoglossalforamen; IX, glossopharyngealforamen; •I, metoticprocess; MP, mammillaryprocess of basitemporalplatform; OF, foramenfor occipitalvein; P, pneumaticforamen; PA, foramenfor palatineartery; SF, stapedial arterialforamen; TC, tympaniccavity; UTR, uppertympanic recess; VCL, exit point from skullof venacapiris lateralis; VIIp, foramenfor palatinebranch of facialnerve; X, vagal foramen. Eudyptula,Megadyptes, and Spheniscus. Crompton (1953) studiedthe de- velopmentalprocess involved in this arrangementin Spheniscus.The palatinenerve enters the carotidcanal through a foramenon its dorso- medialsurface in orderto runforward along with the carotid artery. The sectionof the carotidcanal where the palatinenerve and carotidartery traveltogether represents the parabasalcanal. At the anterolateraledge of the parabasalcanal is a foramen for the forward continuationof the palatinenerve. Just anteriorto this palatinenerve foramen is a larger foramenfor the palatine artery. The hyomandibularbranch of the facial nerveexits from a foramenlocated posterodorsal and lateral to 752 Et)w^a• S^•v [Auk, Vol. 93 the fenestraovalis and then leavesthe middle ear regionwith the stapedial artery throughthe stapedialarterial foramen. One specimenof Eudyptula (AMNH 5314) I examinedhad a foramenonly on the right side of the inner wall of the tympanic cavity. This foramenis coveredover by a membraneand is probably pneumatic. Aptenodytes has a facial foramen. Dorsal and lateral to the facial foramen is an overhang of bone that is a forward continuation of the lateral wall of a canal that curvesposterodorsally above the fenestra ovalis and opensposteriorly into the middle ear cavity. The posterior openingis directed toward the foramen housingthe stapedialartery. It seemsreasonable to assumethat the hyomandibularnerve travels within this bony canal up to the stapedialcanal and leavesthe middle ear region via the stapedialcanal and the stapedial arterial foramen. Anteroventral to the facial foramena foramenenters the carotidcanal from the tympanic cavity. Presumably the palatine nerve travels along the wall of the tympanic cavity to enter the carotid canal through this foramen. The presenceof a facial foramen opening into the middle ear of Pygosceliscannot be determined without a dissection. Anterolateral to the fenestraovalis in Pygoscelisare two fossaeseparated by a vertical ridge of bone. On this ridge is a foramenthat is patent only on the left side in one of the specimensexamined here (AMNH 5766) and in none of the others. It is not possibleto tell whether this foramen is for the facial nerve, and if so, for which branch. It is doubtful, though,that the palatinebranch would exit from this foramen. If it did, it wouldhave to travel posteriorlyfor almost the entire length of the tympanic cavity in order to enter the carotid canal as there is no foramen that leads into the carotid canal from the tympaniccavity as is presentin Aptenodytes. All speciesexamined had a bony canal for the stapedial artery dorsal to the columella,deep to the tympanic cavity. Posteriorto entry into the middle ear, the stapedial canal runs medial to a vertical bar of bone (the lateral edge of the metotic process) connectingthe rear of the paroccipitalprocess to the rear of the basitemporalplatform. Running anteriorly in the ventrolateralportion of the tympanic cavity are two bony canals: a lateral canal for the eustachiantube, and a more dorsomedialcarotid canal. These two canals are separatedby a thin plate of bone referred to by Pycraft (1898) as a downgrowthfrom the alisphenoidwing of the parasphenoid.Anteriorly, the tympaniccavity is blind. The blind area presumablyrepresents the presphenoidsinus of several Procellariiformes,Pelecaniformes, and Ciconiiformes(Salff 1973). In all penguinsexamined the carotid artery enters the carotid canal throughthe carotidforamen, which is locatedventromedial to the tympanic October 1976] Penguin Middle Ear Region 753 cavity. The carotidartery is neverexposed within the tympaniccavity.
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