Download anatomy of the middle ear region of the avian skull: sphenisciformes

ANATOMY
OF
AVIAN
THE
MIDDLE
SKULL:
EAR
REGION
OF
THE
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 Sphenisciformes
lacksany detailson the middleear.
Walker (1888) studiedquadratemorphology
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,basitemporalplatform, eustachiantube, and the
trigeminalforamen. Shufeldt (1901) also failed to go into detailsof the
middleear regionin his osteological
studyof the penguins.More recently,
in a study of the evolutionof penguins,Simpson(1946) describedthe
skullof Paraptenodytes
antarcticus,a fossilpenguin.This studytheorized
a close relationship between the penguins and the Procellariiformes.
Crompton(1953) made a further study on penguinsand did an extensive
developmental
studyof the chondrocranium.
An analysisof middleear
anatomy of Procellariiformes,
includinga glossaryof avian middle ear
characters,appearsin Saiff (1974). Recently Frost et al. (1975) describedthe circulatorysystemin the head o/ Spheniscus
demersusin an
effort to describeheat-exchangesystemsin penguins.
Obviouslacunaeexistin the studyof the middleear of birds,including
Sphenisciformes.
This study describesthe anatomyof the middle ear
and basicraniaof the Sphenisciformes
and where possiblemakes comparisonswith Procellariiformes.
MATERIALS AND METItODS
This study is based on an analysisof charactersof specimensborrowed from the
Bird Department of the American Museum of Natural History. Peters (1931) was
usedas the basisfor the genericclassificationand 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.
MegadyptesantipodesAMNH 5613, 5615. PygoscelisadeliaeAMNH 5041. P. papua
A.MNIt 3196, 4361, 5373, 5766, 5973. Spheniscus
deraersus
AMNH 1625, 1310, 3875,
4042, 4069, 4942. S. huraboldtiAMNH 2768, 4920, 4921. S. raendiculusAMNH 3648,
3772. Dissected:
S. deraersus AMNH
4548.
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The Auk 93: 749-759. October 1976
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EDWARDSA•
ANATOMICAL
[Auk, Vol. 93
DESCRIPTIONS
EXTERNAL.--Theexternalauditory meatusis on the samehorizontal
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 rangesbetween 2.4 to 3.5 mm tall and 1.9 to 2.1 mm wide
(2 ears). The rim of the meatusdoesnot appearto be sopliableas to close
completely.
The external auditory canal is directedposteroventrally.No ridges
appear on the inner membranouslining of the canal. Ridges do appear
with somedegreeof consistency
in Procellariiformes
(Saiff 1974) although
the presenceor absenceof suchridgesmay 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 tympanicmembranecomesinto view. The tympanic
membraneis roughly circular in shape, mildly protubcrant, and faces
posterolaterad.It is composed
of a tough, thick outer layer that is quite
elasticand a thinner but equally tough inner layer. The outer layer of
the tympanic membrane is a continuationof 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 bonethat extendslaterally to touchthe rear of the dorsalend of the
quadrate; the ventral edgeof this plate is bent backwardhorizontallyto
form, alongwith a lateral extensionof the basitemporal
plate, the ventral
wall of the tympaniccavity.
The tympanicmembrane(seendriedin placein someskullsas well asin
situ in AMNH 4548) is stretchedacrossthe rear apertureof the tympanic
cavityfrom themetoticprocess
to the quadrate.On the medialwall of the
tympanic cavity is the fenestraovalis, posteriorto which is a pneumatic
foramen. Ventral to thesetwo structuresis the recessus
scalaetympani.
The seventh nerve foramen varies among the specimensexamined. A
facial foramenopeningwithin the tympaniccavity is lackingin Eudyptes,
October1976]
PenguinMiddleEar Region
VlI FR
751
AQF U/TR
C
I //
/
•X
!.....
PA
ET
BP MP CF
H
M
Fig. 1. Spi•eniscus
demersus
(AMNH 4042) obliqueventralview of the left middle
ear regionwith quadrateremoved:AQF, anteriorquadratefacet;BP, basitemporal
platform;C, columella;
CF, carotidforamen;
ET, entrance
to eustachian
canal;FP,
foramenprooticum;H, hypoglossal
foramen;IX, glossopharyngeal
foramen;•I,
metoticprocess;
MP, mammillaryprocess
of basitemporal
platform;OF, foramenfor
occipital
vein;P, pneumatic
foramen;
PA, foramen
for palatineartery;SF, stapedial
arterialforamen;TC, tympaniccavity;UTR, uppertympanicrecess;
VCL, exitpoint
from skullof venacapirislateralis;VIIp, foramenfor palatinebranchof facialnerve;
X, vagal foramen.
Eudyptula,
Megadyptes,
andSpheniscus.
Crompton
(1953) studiedthedevelopmental
process
involvedin this arrangement
in Spheniscus.
The
palatinenerveentersthe carotidcanalthrougha foramenon its dorsomedialsurface
in orderto runforwardalongwiththecarotidartery.The
sectionof the carotidcanalwherethe palatinenerveand carotidartery
traveltogetherrepresents
the parabasal
canal.At the anterolateral
edge
of the parabasalcanal is a foramen for the forward continuationof the
palatinenerve. Justanteriorto thispalatinenerveforamenis a larger
foramenfor the palatine artery. The hyomandibularbranch of the
facial nerveexits from a foramenlocatedposterodorsal
and lateral to
752
Et)w^a• S^•v
[Auk, Vol. 93
the fenestraovalisand then leavesthe middleear 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 tympaniccavity. 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 opensposteriorlyinto the middle ear cavity. The posterior
openingis directed toward the foramenhousingthe stapedialartery. It
seemsreasonableto assumethat the hyomandibularnerve travels within
this bony canalup to the stapedialcanal and leavesthe middleear region
via the stapedialcanal and the stapedialarterial foramen. Anteroventral
to the facial foramena foramenentersthe carotidcanalfrom the tympanic
cavity. Presumably the palatine nerve travels along the wall of the
tympanic cavity to enter the carotid canal throughthis 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 fossaeseparatedby a vertical
ridge of bone. On this ridge is a foramenthat is patent only on the left
side in one of the specimensexaminedhere (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
palatinebranchwould 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 speciesexaminedhad a bony canal for the stapedialartery dorsal
to the columella,deep to the tympaniccavity. Posteriorto entry into
the middle ear, the stapedialcanal runs medial to a vertical bar of bone
(the lateral edge of the metotic process) connectingthe rear of the
paroccipitalprocessto the rear of the basitemporalplatform.
Running anteriorly in the ventrolateralportion of the tympaniccavity
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 referredto by Pycraft (1898) as a downgrowthfrom the
alisphenoidwing of the parasphenoid.Anteriorly, the tympaniccavity
is blind. The blind area presumablyrepresentsthe presphenoidsinus
of several Procellariiformes,
Pelecaniformes,
and Ciconiiformes(Salff
1973).
In all penguinsexaminedthe carotid artery enters the carotid canal
throughthecarotidforamen,whichis locatedventromedial
to the tympanic
October 1976]
Penguin Middle Ear Region
753
cavity. The carotidartery is neverexposed
within the tympaniccavity.
Just beforeenteringthe middleear, the carotidartery givesoff a dorsal
branch,the stapedialartery, which lies dorsalto the columella.Deep to
the stapedialartery, and alsodorsalto the columellais the venacapitis
lateralis. Togetherthe stapedialartery complexof vesselsand that of the
vena capitis lateralis form arete mirabile locatedlateral to the foramen
prooticum. The vena capitis lateralis leaves the middle ear through a
notch in the anterodorsaledgeof the tympaniccavity just deep to the
quadrate.
In Megadyptesand Aptenodytesa large dorsallydirectedpneumatic
foramen enters into the braincaseposterior to the dorsal rim of the
tympaniccavity and deepto the point of entry of the stapedialartery
into the middle ear. None of the other generahas such an opening.
All formshave a foramenjust anterior to the articulatorysurfacefor
the headof the quadratein the paroccipitalprocess.This foramentakes
the form of an elongateslit and appearsto be the true upper tympanic
recess.Anterior to the upper tympanicrecessis an openingin much the
positionof theuppertympanicrecess
of the Diomedeidae
andProcellariidae
(Saiff 1974); this openingin penguinsentersthe brain cavityand appears
to bepneumatic.In theProcellariiformes,
Pelecaniformes,
Sphenisciformes,
and Ciconiiformes,
the true uppertympanicrecessis separatedfrom the
brain cavity by an imperforatewall of bone (Saiff 1973).
Ventral to the perforationinto the brain cavity and anterior to the
tympaniccavity is the foramenprooticum.Pycraft (1898) describedthe
morphologyof the foramenprooticumas well as that of the pneumatic
foramen dorsal to it.
At the base of the skull posterior to the tympanic cavity are the
glossopharyngeal,
vagal,andhypoglossal
foramina,whichCrompton(1953)
described.The glossopharyngeal
and vagal foraminaare locatedin the
metotic process.Pycraft (1898) describedthe posterioraspectof the
skulland the basitemporal
platform,the formerbeingvariableamongthe
generawhilethe latter is constant.The basitemporal
platformas seenfrom
belowis triangularand concave.The eustachiantubes make the lateral
edgescurl ventrally,hencethe concavity.At the rear of the basitemporal
platform on each side is a weak mamillary process."In all generabut
Spheniscus
there is a well-markedprecondylarfossa"(Pycraft 1898). In
all respects,
savethe mamillaryprocess,
the basitemporal
platform(Table
1) of Sphenisciformes
is verysimilarto that of Procellariiformes,
especially
Diomedea (Saiff 1974).
In all the generaof penguinsthe eustachiantubesare at least partly
coveredby bone. In Eudyptes,Spheniscus,
and Megadyptesthe bony
coveringextendsto near the anteriorend of the basitemporal
platform
754
EDWARD
SAIFF
[Auk, Vol. 93
October 1976]
PenguinMiddle Ear Region
755
while in Eudyptula, Aptenodytes,and Pygoscelis
it coversonly the posterior half of the eustachian tube.
QUADRATE
ANDITS RELATIONTO THE MIDDLEEAR.--Pycraft (1898)
describedthe quadrateof the penguins. The quadrate articulatesnear
the anteriorendof theparoccipital
process
by two heads.The articulation
is strengthened
by a broadligamentconnectingthe paroccipitalprocess
and the Jarera]edgeof the curvedarticu]atorysurfaceof the outermost
headof the quadrate.A portionof this ligamentextendsto the dorsalmost
lip of the tympanic cavity. The vena capiris]ateralis runs just deep to
this portionof the ligament. The angieof articulationis approximately
at right angleswith the long axis of the head. Posteriorto the point
of articulationa ventral curveof the paroccipitalprocessextendsabout
halfway down the ]eve] of the tympanic cavity.
The quadrateitself exhibitsa deep capitu]argrooveseparatingthe
prootic and squamosa]-opisthotic
articu]ar headswith the paroccipital
process.The facetsfor thesearticu]ar headsin the paroccipitalprocess
are quite distinct from each other. A line drawn throughthese facets
intersectsthe long axis of the skull at app,roximate]ya 45-degreeangie.
The uppertympanicrecessis locatedanteriorto thesetwo facets. The
penguinsshowsomeslight variability with regard to the orbital process.
That of Eudyptula,Eudyptes,and Spheniscus
is curvedslightly upward
with the superiorborder sharper than the inferior. In Pygoscelisthe
orbital processis similar in shape but longer. In Aptenodytesand
Megadyptesthe orbital processis taller than thosedescribedabovealthoughof the sameapproximatelength as the Eudyptula grouping.
The pterygoidarticulatorysurfacelies ventral and medialto the orbital
process.The quadrato-jugalarticulatory surfaceis at the base of the
quadrateshaft on its lateral aspectjust dorsalto the mandibulararticulatory surface.Little variability amongthe severalgeneraof Spheniscidae
exists in the mandibular articulatory surface. Pycraft (1898) failed
to describethis portion of the quadrate. The penguinhas a shallow
trochleargrooveseparatingthe inner and outer condylarpairs and no
grooveto distinguishthe two condylesof the outer condylarpair from
each other save for a shallowdepressionin Eudyptula and Megadyptes.
The two condylesof the inner condylarpair are distinctfrom eachother
but the groove separatingthem is much shallowerthan in Diomedea
(Saiff 1974).
The quadrateof penguinslacksa pneumaticforamen.
DISCUSSION
PRESPI-IENOID SINus.•The
anatomical literature
makes little mention
of this structure. Watson (1883) figured it in his description of the
756
Et)w^,al>
S^•w
[Auk, Vol. 93
osteology
of the penguinsand Pycraft (1898) madesomementionof it.
There seemslittle doubt that the presphenoidsinus is pneumatic. In
the Sphenisciformes
it is shallow,poorlydeveloped,
and directedanteromedially. Its lateral wall fusesventrallywith the free edgeof the
basitemporal
platformandis in closecontactposteriorly
with thequadrate
shaft. The downward extensionoffers lateral protection to the carotid
artery and eustachian
tube (Table 1). Suchprotectionis absentin the
Diomedeidaealthoughit is presentto varying degreesin other Procellariiformes(Saiff 1974). Only in Daption capensis
amongthe Procellariiformesdoesthe hind portion of the lateral wall of the presphenoid
sinus come into contact with the quadrate, a condition also seen in
penguins.
Uvw• T¾•rVA•iCR•c•ss.--The positionof the entranceto the upper
tympanicrecesswith respectto the facetsfor the headof the quadrate
has beenusedas a taxonomiccharacterin birds (Lowe 1926, Saiff 1974).
All the Sphenisciformes
have a small, slit-shapedentranceto the upper
tympanic recessthat lies anterior to the paired quadrate facets. In
the Diomedeidae,
Pelecanoididae,
and Procellariidae
of the Procellariiformesthe entranceis muchlarger than in the penguinsbut the position
with respectto the quadratefacetsis the same.The entranceto theupper
tympanic
recess
in the Hydrobatidae
of the Procellariiformes
is smalland
locatedbetweenthe quadratefacetsandnot anteriorto them(Saiff 1974).
FACIALFo•AMEN.--Aptenodytes
is the only Sphenisciform
that has a
facial foramenopeningwithin the middle ear. The palatine ramuscontinues forward to the parabasalcanal; the hyomandibularramuspasses
througha foramenin the ventral wall of a canal that continuesposterodorsallyto join thestapedialarterialcanal.Presumably
thehyomandibular
nervepasses
into the stapedialarterialcanaland thenleavesthe middle
ear throughthe stapedialarterial foramen. Crompton(1953) gave an
accountof the early development
of the chondrocranium
of Spheniscus
demersus
includinga description
with figuresof the ontogeny
of the facial
foramen,
its subsequent
closing
over,andthepathultimatelytakenby the
facial nerve.
ME:ro:rxcP•ocEss.--Crompton(1953) discussed
muchof the literature
concernedwith this structure,as well as its developmentin Spheniscus
demersus.All the Sphenisciformes
have a strong metotic processperforatedby vascularforaminaaswellasforaminafor the glossopharyngeal,
vagus,and hypoglossal
nerves. In many respectsthe metoticprocessof
thepenguins
is markedlydifferentfromthat of theProcellariiformes
(Saiff
1974). The metoticprocess
of the Diomedeidae
is weakand lacksevena
separateglossopharyngeal
foramen.Also lackingare vascularforamina
as in all the Procellariiformes
I previouslyexamined(Saiff 1974).
October 1976]
Penguin Middle Ear Region
757
ENTRYor CIRCULATION
INTO THE HEAD.--In the singlespecimenthat
wasdissected,the relativepositionof the foramenmagnumwith respectto
the basitempora]
platform showsthat the carotid artery and vena capiris
]atera]is do not have to bend to enter the head from the neck. Frost eta].
(1975) figure this in their recentpaper. This is a different arrangement
from that in the Proce]]ariiformes
(Saiff 1974). Even so, the vena capiris
]atera]is,stapedia]artery, and carotid artery of penguinspassthrough
foraminain the metoticprocess,as in the Pe]acaniformes
(Saiff 1973),
rather than enteringthe middle ear in front of the metoticprocessas
in the Proce]]ariiformes.
MIDDLEEAUARTERIES.--Thecarotid artery of the Sphenisciformes
is
completelyencasedin a bony tunnel as it traversesthe middleear. The
stapedia]artery is alsoprotectedon its lateral, roedial,and ventral sides.
This protectionresultsfrom the closeproximity of the quadrateand the
lateral wail of the presphenoid
sinus,whichform a canalfor the stapedial
artery.
RETEMII•mILE.--In this study I dissectedonly a singlespecimen,and
it had arete mirabile. Frost et al. (1975) also found arete mirabile
in his dissections
of S. demersus.Saiff (1973) describedthe presenceor
absence of the structure in several other birds. As far as can be determined
no physiologicalor behavioralfeature distinguishesthe forms possessing
arete mirabilefrom thosethat lack one. Frost et al. (1975) discussed
the
literature concerningretia mirabile as heat-exchange
systems.Certainly
further studies involving dissectionsof more speciesare in order.
EUSTACI-IIANTu•E.--This
structure runs from the anteroventral region
of the middle ear cavity to a medianopeningin the rear of the palate,
which it shares with its fellow from the other side of the head.
The
eustachiantube of the Sphenisciformes
runs along the edge of the basitemporal platform in a long canal that is at least partly protected by
boneon all sidesin all genera.
Qu•ml•TE.--Pycraft (1898) and Shufeldt (1901) describedquadrate
structurein penguins.The sphenisciform
quadrateis at right angleswith
respectto the long axis of the skull (in lateral view), and an extensive
capitular groove separatesthe paired condylesof the quadrate head.
Dorsal to the capitular groovein the paroccipitalprocessa wide ridge
of bone separatesthe facets for the quadrate head. These facets are
perpendicularto the long axis of the skull. The upper tympanicrecessis
just anteriorto a line drawn betweenthe two facets.
The orbital processof the severalspeciesof penguinsvaries a bit but
noneis significantlydifferentfrom that of the albatross(Saiff 1973). The
arrangementof condylesof the mandibulararticulatory surfaceis also
as in Diomedea (Saiff 1973), but the condylesof the penguinsare
758
Eow^•o S^rvv
[Auk, Vol. 93
separatedby groovesthat are quite a bit shallowerand lesselongatedthan
in the albatross.
CONCLUSIONS
Althougha numberof authors,notably Murphy (1936), Murphy and
Harper (1921), and Simpson(1946), have held the Sphenisciformes
to be
closelyrelatedto the Procellariiformes,
the middleear givesno confirmation of it. Indeed, a cursoryexaminationof five of the characterscovered
in this work indicatesthat the middle ear of the gull, Larus argentatus,
comes closer to the penguins than do those of the Diomedeidae or
Procellariidae(Table 1). At the same time severalother characteristics
are sharedby severalProcellariiformes
and Sphenisciformes,
suchas ridges
on the wallsof the externalauditorycanal,the presenceof arete mirabile,
basitemporal
platformsavethe mammillaryprocess,
and positionof upper
tympanic recesswith respectto the quadratefacets.
Wetmore (1930), Peters (1931), Murphy (1936), Simpson(1946), and
Storer (1960, 1971) agree that the Spheniscidae
are composedof six
genera, which my data confirm. The Sphenisciformes
are easily distinguishedfrom the Procellariiformes(Saiff 1973, 1974) and the Pelecaniformesand Ciconiiformes(Saiff 1973) by the penguins'wide presphenoid
sinus,which has a lateral wall that fusesto the basitemporalplatform and
is in closecontactwith the medial edgeof the quadrateshaft, thoughthe
presphenoidsinus extendsonly a short distancerostrad.
All the penguinssaveAptenodyteslack a facial foramen. Perhapsthis
is another characterindicatingthe primitivenessof that genusamongthe
Sphenisciformes.Many workers have studied the ancestry of extant
penguinsand do not agreeon which genusis the mostprimitive and nearest
to the ancestral form. Pycraft (1898) favored Eudyptula based on his
osteologicalanalysis of temporal fossae,upper jaw, quadratojugalbar,
sternum and pectoral limb, while Wilson (1907), basedon color char-
actersof the head plumage,believedAptenodytesclosestto the primitive
form.
ACKNOWLEDGMENTS
Much of the data presentedhere was part of a thesis at Rutgers University done
under the supervisionof Samuel B. McDowell. Iohn Maroney, Charles O'Brien,
Alan O'Conne]], Dean Amadon, Waiter Bock, and Wesley Lanyon kindly allowed
me to study specimens under their care. The Ramapo College Graphics Center
prepared Fig. 1.
SUMMARY
The osteologyand soft anatomy of the middle ear regionof the skull are
describedfor the Sphenisciformes
with particularemphasis
on the foramina
for nervesand blood vessels.Also discussed
is the morphologyof the
October 1976]
PenguinMiddle l•ar Region
759
basicranium
and the quadrate. Comparativeanalysisof the characters
are usedto assess
taxonomicconclusions.
Little supportis addedto the
theorythat the penguinsare closelyrelatedto the Procellariiformes.
The paper is part of a seriesthat attemptsto allow an assessment
of
evolutionaryrelationships
within the Avesbasedon the anatomyof the
middle ear region.
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