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~oologkal3ournaloffhe Linnem So&& (1997), 121: 249-291. With 12 figures
An X-radiographic and SEM study of the
osseous inner ear of multituberculates and
monotremes (Mammalia):implications for
mammalian phylogeny and evolution of hearing
RICHARD C. FOX'
Laboratory for Vertebrate Paleontology, Department o f Biological Sciences, Universib o f Alberta,
Edmonton, Alberta, 76G 2E9, Canada
JIN MENG2
Department o f Ertebrate Paleontology, American Museum of Natural History, Central Park
10024, U S A . and Institute o f Vertebrate Paleontology
West at 79th Street, New Erk,
and Paleoanthropology, 20. Box 643, Be$%, China
Received FebwaT 1996; accepted for publication S;b 1996
Multituberculate petrosals with well-preserved, three-dimensional internal anatomy from the
Late Cretaceous/early Paleocene Bug Creek Anthills, Montana, U.S.A., are described from
X-radiographic and SEM images, as well as from conventional visual observations, and are
compared with the anatomy of the osseous inner ear in monotremes and in primitive nontherian and therian mammals. Results of this study indicate that: (1) the cochlea of at least
some multituberculates retained a lagena, previously known only in monotremes among
mammals; (2) an enlarged vestibule evolved in several lineages of multituberculates independently, and hence is not a synapomorphy of the order; (3) the cochlear canal lacks
osseous laminae in support of the short, wide basilar membrane, which was probably
inefficient in responding to high-frequency airborne vibrations; and (4) consequently, boneconducted hearing in some multituberculate species may have been important in interpretation
of their surroundings. Comparisons with the inner ear of monotremes and primitive therians
indicate that curvature of the cochlea and cribriform plates for passage of vestibulocochlear
nerve branches through the petrosal are unlikely homologues between monotremes and
therians. From non-therian to therian mammals, there is a distinct morphological gap in the
inner ear transition, characterized by acquisition of a number of neomorphs in the therian
inner ear; an intermediate stage has yet to be discovered.
0 1997 The Linnean Societv of London
ADDITIONAL KEY WORDS:-anatomy
America.
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Late Cretaceous
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Multituberculata
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North
' Corresponding author.
* Present address: Department of Biology, University of Massachusetts, Amherst, MA 01003, U.S.A.
0024-4082/97/110249+43 $25.00/0/zj960089
249
0 1997 The Linnean Society of London
Introduction . . . . .
llaterial and methods
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5Iatrrial
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~lcthods . . . .
'l'rrnmiiioloLT . . .
;ibbrr~~iations . . . .
lkscription . . . . .
llultituberculates
.
llonotremes . . .
Discussion . . . . .
l'hylogrnetic implicatioiis
1;uiictional implicatioIis .
.\cknou Irdgeinents
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Krfcrciico . . . . .
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\Yhile tlie origin of the mammalian ear has long been of interest to comparative
anatomists (e.g. Gaupp, 1913; Goodrich, 1958), significant new perspectives concerning it have recently been provided by vertebrate palaeontologists. Important
information from the fossil record has been especially relevant to studies focusing
on: ( I ) transformation of the reptilian jaw suspensorium into the triossicular hearing
systcm of mammals (e.g. Allin, 1975, 1986); (2) reconstruction of vessels and nerves
on tlie external surfaces of the petrosal bone as dictated by grooves, foramina, or
other external structures preserved there (e.g. MacIntyre, 1972; Wible, 1990; Rougier,
JYible & Hopson, 1992); (3) reconstruction of the soft tissue anatomy of the inner
ear as inferrcd from the internal bony architecture of the petrosal (e.g. Allin, 1986;
Luo & Ketten, 1991). In assessing the significance of such studies, one weds to
rcmember that the fossil specimens contain the only direct evidence that is available
concerning the course of evolution of the ear. At the same time, these fossils arc
the source of novel characters in a temporal context, and can contribute to both
phylogenetic reconstruction and functional interpretation on that account.
:Ilthough recent gains in knowledge of the early mammalian ear have been
important, they have not been uniform, across all parts of the hearing apparatus.
AIost is known about the middle ear (see Kermack, 1963; Hopson, 1966, 1969;
hlacIntyre, 1972; Allin, 1975, 1986; Archibald, 1979; Kermack et al., 1981; Prothero,
1983: Miao & Lillegravcn, 1986; Novacek & Wyss, 1986; Graybeal et al., 1989;
Rougier et a/., 1992; M'ible & Hopson, 1993; Meng, 1992; Meng & n'yss, 1995),
ivhile knowledge of inner ear morphology has been more difficult'to obtain, if on1)because of the small number of specimens in collections in which crucial delicate
structures arc well preserved. The few investigations of the early mammalian inner
car that lia\re been published reveal only general features, such as the shape of the
cochlea as obtained by serial sections and computerized tomography (CT) (KielanJaivorowska et al., 1986; Allin, 1986; Graybeal et al., 1989; Luo gL Kctten, 1991;
Luo ~t al., 1995). Indeed, for all fossil mammals, detailed inner ear morpholoE has
been established in but a few, highly specialized, Cenozoic species (e.g. some Tertiary
cetaceans [Fleischer, 1976; Ketten, 19921); comparable details are little kn0u.n in
mammals from any time in the Mesozoic. This lack of knowledge is particularly
urifortunatc because the inner ear is clearly more important than the middle ear in
INNER EAR OF MULTITUBERCULATES
25 I
mammalian hearing-and
the inner ear contains important phylogenetic information, as well, especially at higher taxonomic levels. It is in this context that
we have recently described the osteology of the inner ear and explored its phylogenetic
and functional implications among representative early placentals and marsupials
(Meng & Fox, 1993, 1995a, b). However, during the course of that research, we
also examined the inner ear of Late Cretaceous multituberculates, relying especially
on X-radiographic and SEM images but utilizing direct visual inspection, in addition.
The results of the multituberculate study are presented here, and are contrasted
with aspects of the inner ear in monotremes, as well as in primitive marsupials and
placentals as revealed by our earlier work.
MATERIAL AND METHODS
Material
The multituberculate petrosals of this study were collected from the Hell Creek
Formation at the Bug Creek Anthills locality, McCone County, Montana (Sloan &
Van Valen, 1965)by the first author using dry- and underwater-screening techniques,
and are listed in Table 1. It is important to note that these specimens have required
no preparation of external or internal features other than removal of loose sand
and silt with a camel’s hair brush or, occasionally, with a finely ground needle;
hence, no dissolution of delicate structures, always a danger in acid-preparation,
nor damage as a consequence of mechanical preparation, has altered the morphology
of the specimens after they were collected (see, e.g. Graybeal et al., [1989: 1141;
Rosowski & Graybeal [1991: 1381).The specimens are catalogued in the Laboratory
for Vertebrate Paleontology, Department of Biological Sciences,University ofAlberta
(UALVP). The current uncertainty as to the age of fossils at the Bug Creek locality,
whether latest Cretaceous or earliest Palaeocene or both (e.g. Archibald & Lofgren,
1990; Lofgren, 1995), is irrelevant to the purposes of this paper, which are morphologic, phylogenetic and functional, not biostratigraphic.
In our Bug Creek collection, multituberculate petrosals of three different morphologies have been recognized, as represented by UALVP 34 144, 26039, and
26037, respectively, and our descriptions are based on these three specimens. Other
specimens in this collection are fragmentary; therefore, they are not described here,
but all are listed in Table 1. UALVP 34 144 may belong to the same group of
multituberculates as the petrosals (MCZ 19177, ZPAL MK-1) studied by KielanJaworowska et al. (1986), while the other two specimens appear different from any
Hell Creek petrosals that have been previously described (see, e.g. Kielan-Jaworowska
et al., 1986; Luo, 1989; Wible & Hopson, 1995). Taxonomic identification of all
such isolated specimens, even to family level, is uncertain (see Kielan-Jaworowska
et al., 1986 for similar conclusions), and must await the collection of articulated
cranial material in which diagnostic evidence, especially dentitions, is preserved.
Luo (1989) recognized three petrosals having different morphologies among the
Bug Creek multituberculates, and UALVP 34144 may well correspond to his
‘Ptilodontoidea’ (cf. Luo, 1989: fig. 4, MCZ 21345; fig. 5, MCZ 19177), but we
have been unable to assign others of our specimens to his categories. For example,
in UALVP 26039, the mastoid region appears to have been fenestrated, a ptilodontoid
252
R. C . FOX AND J. MENG
condition according to Luo (1989), but this specimen also has a large vestibule,
which Luo (1989) believed to be a taeniolabidoid character. In light of these
uncertainties, we have not attempted to assign our specimens to any subgroup of
multituberculates (although recognizing that it is virtually certain that they are not
plagiaulacoid in their affinities: plagiaulacoids are thought to have become extinct
in the Early Cretaceous). The monotreme petrosals included in this study are from
specimens in the collections of the departments of Vertebrate Paleontology and
Mammalogy, American Museum of Natural History, New York.
Methods
For X-radiographic examination of internal structures of the petrosal, we used the
Radiographic-Fluoroscopic Inspection System and Ready Pack I1 Kodak Industrex M
Film. Usually, when the tympanic side of a specimen is placed against the film, a
clear image of the cochlea can be obtained.
A latex endocast taken from one of our specimens, UALVP 26039, has been
useful in revealing fine details of vestibular structure and was constructed according
to the following protocol. The petrosal was carefully enclosed in plasticene, blocking
all openings except for a broken area in the wall near the fenestra vestibuli (fig. 3);
this area allowed access into the interior spaces of the bone. Thin layers of moulding
latex were successively painted on to the inner surface of the vestibule with a camel’s
hair brush in order to build a self-supporting latex wall. After the latex had dried,
talcum powder was sprayed into the vestibule with syringe and needle to coat the
exposed surfaces of the latex wall and prevent opposing parts of it from adhering
to each other during removal of the endocast. The endocast was then carefully freed
from the vestibular walls, extracted from the petrosal, and coated for scanning
electron microscopy (Fig. 4). Other SEM photographs were taken directly from
uncoated specimens.
Measurements of the specimens included in this study are presented in Table 1.
All measurements were made using the Reflex Microscope (Reflex Measurement
LTD), either directly from the specimens themselves or from radiographs. The 2 x
magnification setting and the 5 micron mark on the microscope were used when
taking measurements. In our study, the starting point of the cochlear canal is
considered to be at the notch produced by the perilymphatic duct in the interior
ridge that defines the perilymphatic recess, well anterior to the depression marking
the recess (see e.g. UALVP 26037 Fig. 51, a broken right petrosal in which these
parts are particularly well preserved). The length of the cochlea was measured along
its longitudinal mid-axis; the width of the cochlea was taken at its base.
In our descriptions, we refer to the tympanic side of the petrosal as ventral, the
cranial side as dorsal, and the apical end of the promontorium as anterior, although
the petrosal was probably oriented in the skull such that the tympanic side actually
faced ventrolaterally and the cranial side dorsomedially. For anatomical features,
we follow the terminology of Gray (1959), Kielan-Jaworowska et a/. (1986) and
Rougier et al. (1992), unless otherwise specified. We use the term ‘cochlear canal’
INNER EAR OF MULTITUBERCULATES
253
for the osseous structure that in living monotremes and multituberculates contained
the soft cochlear duct (basilar papilla) and lagena; in therians, in which no lagena
is developed, the cochlear canal contained the soft cochlear duct alone (see also Luo
& Ketten, 1991). In our usage, the term ‘cochlea’ refers, then, to the cochlear canal
and cochlear duct together.
We use the terms ‘Mammalia’, ‘Theria’, ‘Pelycosauria’,‘Cynodontia’, and ‘Reptilia’ in their traditional, widely understood senses, as in Lillegraven et al. (1979) and
Carroll (1988).
ABBREVIATIONS
aa
acs
aF
a1
aqc
asc
bm
cac
cc
cn
COC
er
fcn
fib
fPr
fsb
fv
gcn
glsc
P d
gsu
anterior ampulla
area cribrosa superior
aquaeductus Fallopii
anterior lamina of petrosal
aquaeductus cochleae
anterior semicircular canal
basilar membrane
cochlear orifice of aquaeductus
cochleae
crus commune
cochlear nerve (branch of eighth
cranial nerve)
cochlear canal
epitympanic recess
foramen for cochlear nerve
foramen for inferior branch of
vestibular nerve
fossa for perilymphatic recess
foramen for superior branch of
vestibular nerve
fenestra vestibuli
grooves for cochlear nerve
gyrus of lateral semicircular canal
groove containing the secondary
perilymphatic duct
groove between sacculus and
utriculus
la
lar
lateral ampulla
lateral aperture of perilymphatic
recess ( = recessus scalae tympani)
If
lateral flange of petrosal
lsc
lateral semicircular canal
mss
mastoid surface that contacts
squamosal
notch
for posterior branch of
nPb
vestibular nerve
promontorium
P
posterior ampulla
Pa
perilymphatic recess
Per
perilymphatic foramen
Pf
processus recessus
P‘
posterior semicircular canal
PSC
recessus sphericus
rs
Sf
subarcuate fossa
groove
for stapedial artery
sg
cone-shaped
swelling (‘bulging’) for
sPr
perilymphatic recess
st
scala tympani
tractus spiralis foraminosus
tsf
tensor tympani fossa
ttf
V
vestibule
vnib inferior branch of vestibular nerve
vnpb posterior branch of vestibular nerve
vnsb superior branch of vestibular nerve
DESCRIPTION
Multituberculates
(left petrosal)
Although several studies have demonstrated that the vestibule in many multituberculates is inflated (Miao, 1988; Luo, 1989; Luo & Ketten, 1991)’ in UALVP
UALVP 341 44
2.54
R. C. FOX AND J. MENC
34144 it clearly is not (see below), as evidenced by the retention of a deep, welldefined paroccipital fossa externally and by the configuration of the cavity itself as
shown in the X-radiograph (Figs 1, 2). In keeping with the external morpholog of
the specimen (Fig. l), the X-radiograph also shows that the lateral semicircular
canal and depression for the paroccipital process are located posteroventral to the
vestibule, and that the semicircular canals open into bell-shaped ampullae at the
two ends of the vestibule. As in the ear of early tribosphenic therians (Meng & Fox,
1995a, b), the ampullae in this specimen are significantly larger in diameter than
the canals; in contrast to the therian ear, however, the region between the ampullae
and the vestibule proper remains relatively wide, not narrowed to form a neck.
In the X-radiograph of UALVP 34144, the spaces for the sacculus and utriculus
are not clearly differentiated from one another, but the approximate dimensions of
thc two cavities in the specimen can be inferred from two lines of evidence: first, as
in most mammals, the semicircular canals join the utriculus through five openings
one for the crus coInmune, the others for the medial entrance to the lateral
semicircular canal and the three ampullae, respectively-such that the distancc
between the junctions of the semicircular canals with the vestibule furnishes at least
minimum dimensions for the utriculus. Second, while the sacculus in mammals is
usually located at the anteroventral side of the utriculus, in UALVP 34144 the
requisite space is very limited and the sac that it contained must have been
correspondingly small. In keeping with these proportions, the foramen for the
sacculus branch of the vestibular nerve in UALVP 34144 is very much smaller than
that for the utriculus branch (see below).
In UALVP 34144, the cochlear canal arises anterior to the medial part of the
vestibule, closer to the posterior ampulla than to the anterior and lateral ampullae.
Thr canal extends anteriorly and horizontally, and bends laterally. Its curved course
is suggested by the external topography of the promontorium but is explicitly
documented in the X-radiograph. The canal maintains a constant diameter along
its length, except at its terminus, which is rounded; unfortunately, its cross-sectional
shape cannot be determined, either from the X-radiograph or visually, under
magnification. No internal structures within the canal are evident from the Xradiograph. However, the X-radiograph does show four pale, branching lines that
cross the cochlear canal nearly normal to its long axis; these have not been seen in
other specimens, and their significance is unknown. They may represent small
grooves or canals for arterial pathways as occur in living mammals (Axelsson, 1974).
Several features of the inner ear can be directly observed through openings in
UALVP 34144. As seen through the lateral aperture of the perilymphatic recess (Fig.
1A; sre below and Discussion for terminology), a prominent ridge curves into the
cochlear cavity from the aperture and defines an ovate fossa, adjacent to the groove
for the secondary perilymphatic duct anteromedially (see Discussion for terminology)
and separate from the vestibule more internally. The ridge curves down on to the
dorsal side of the bony bar between the lateral aperture and fenestra vestibuli (crista
interfenestralis [Wible etal., 1995]),and then swings back more medially, ending slightly
internal to the ventral rim of the lateral aperture. Neither ridge nor fossa have been
recognized and described in multituberculates previously. From its position and shape,
it seems likely that the fossa is the ‘perilymph recess’ of Gray (1 908a: 523) which housed
the perilymphatic sac (Romer &Parsons, 1986),and that the ridge formed the boundary
between the recess and the cochlear canal; hence, in life the perilymphatic sac was
only narrowly confluent with the cochlear duct. More proximally, the perilymphatic
~
INNER EAR OF MULTITUBERCULATES
255
Figure 1. Unidentified multituberculate, incomplete left petrosal (UALVP 34144), Bug Creek Anthills
locality, Hell Creek Formation, Montana, USA A, tympanic (ventral) view; B, cranial (dorsal) view.
Scale bar = 1 mm. See Abbreviations for key.
R. C . FOX AND J. MENG
2.56
A
B
C
D
la
cc
Figure 2. X-radiographs of unidentified multituberculate, incomplete left petrosals (A, UALVP 34144;
B, UALVP 26039), Bug Creek Anthills locality, Hell Creek Formation, Montana, USA. C and D
outline restorations of the inner ear based on X-radiographs; note that the semicircular canals in A
are partly broken. See Abbreviations for key.
system communicates with the subarachnoid space via the secondary perilymphatic
duct in mammals, and correspondingly in UALVP 34144, as in other multituberculates
(see e.g. Luo, 1989),a well-defined sulcus for the secondary perilymphatic duct crosses
the dorsal rim of the lateral aperture; there is no separate bony canal (aquaeductus
cochleae) developed for the duct as in therians. Hence, the lateral aperture of the
perilymphatic recess in multituberculates is equivalent to the fenestra cochleae plus
aquaeductus of therians, representing a more primitive pattern in a transformation
series (de Beer, 1937; Zeller, 1993).
O n the cranial (cerebellar) side of UALVP 34144, four foramina open into the
internal acoustic meatus, which is shallow but clearly defined, matching in that
respect the internal acoustic meatus in the petrosals of various other Late Cretaceous
multituberculates that have been described (see Luo, 1989: 13-14, table 2). Ho\ve\,er,
in these other species, the morphological pattern may be different: for example, in
IYNER EAR OF MULTITUBERCC'IATES
257
some, only three foramina have been observed (e.g. see Kielan-Jaworowska et al.,
1986: 586). In UALVP 34144, the foramina are divided into two groups by a crest
or crista falciformis. On the lateral (dorsal) side of the crista are three foramina,
arranged in a triangle. The anteriormost is the aquaeductus Fallopii, which transmitted the facial nerve to the tympanic side of the petrosal. Posterior to the
aquaeductus, the smallest foramen of the three penetrates the anterior wall of the
vestibule; it conveyed the inferior branch of the vestibular nerve to the sacculus and
is the functional equivalent of the area cribrosa media in therians. The internal
(vestibular) opening of this foramen can not be seen in UALVP 34144 because the
vestibular wall here is complete, but its position is confirmed by other specimens
(e.g. UALVP 26037, 26039) in which the wall is broken, exposing the internal
structure of the vestibule (see below). The most lateral (or dorsal) foramen, not
visible in the illustrations, is the largest of the three. It is the entrance to a short
channel that runs posterolaterally to the lateral side of the vestibule, and probably
carried the superior branch of the vestibular nerve to the utriculus and to the lateral
and anterior ampullae; accordingly, this foramen must be functionally equivalent
to the area cribosa superior in therians. In Figure lB, only the aquaeductus Fallopii
is visible.
O n the medial (ventral) side of the crista falciformis only a single, large foramen
is present. It opens into the cochlear canal and must have carried at least the
cochlear nerve, which was probably housed in a broad groove between the foramen
and the canal. However, several lines of evidence indicate that this foramen may
also have conveyed the posterior branch of the vestibular nerve, which ran to the
posterior ampulla: first, in the most proximal part of the cochlear canal, a welldefined trough, visible through the fenestra vestibuli, leads from the foramen
posteromedially to the posterior ampulla. This trough is bounded medially by the
ridge bordering the fossa for the perilymphatic recess; while it is best preserved in
UALVP 26039, it can be clearly seen in UALVP 34144, as well. Second, other
foramina in the internal acoustic meatus are too distant from the posterior ampulla
to have contained the posterior branch of the vestibular nerve. This is especially
clear in UALVP 26039, in which the vestibule is inflated. Third, the foramen that
we believe transmitted the nerve to the sacculus seems too small to have conveyed
a second branch of the vestibular nerve as well, nor is it in any way subdivided, as
if it carried two nerve rami. Therefore, the large foramen on the medial side of the
crista falciformis is equivalent to the foramen singulare for the posterior branch of
the vestibular nerve plus the cribriform area for the cochlear nerve in therians (by
contrast, Luo [1989: 13-14] and Lillegraven & Hahn [1993: 541 believed that only
the cochlear nerve occupied this foramen, but they did not have access to the
internal anatomy of the petrosals that they studied). Hence, the arrangement of the
foramina for the eighth cranial nerve in multituberculates is different from that of
therians, leading to the suspicion that the crista falciformis in multituberculates may
not be homologous to the therian crista. It is now known that multituberculates
primitively had a common fossa housing facial and vestibulocochlear foramina (in
Late Jurassic paulchoffatiids: see Lillegraven & Hahn, 1993: 54-55), contrary to
conclusions from other work (Hahn, 1988; Wible & Hopson, 1993).
(left petrosal)
Although this specimen is larger overall (Fig. 3), the inflated vestibule is the most
prominent feature distinguishing it from UALVP 34144. Both the X-radiograph
UALVP 26039
Figure 3. Unidcntified multituberculate, incomplete left petrosal (UALVP 26039), Bug Creek ;2iithills
localit)-. Hrll Crcek Formation. hlontana, USA: -4, t?mpanic (ventral) vicw; R, cranial (dorsal) view,
\\ith thr approximate anterior side upward. Stale bar = 1 mm. See Ilbbreviations for key.
INNER EAR OF MULTITUBERCULATES
259
Figure 4. SEM photographs of latex endocast of vestibule, UALVP 26039: A, approximately anterior
view; B, dorsal view, with the approximate anterior side downward. Scale bar = 1 mm. See Abbreviations
for key.
(Fig. 2B) and the endocast (Fig. 4) of UALVP 26039 show a nearly spherical
vestibule, which has a maximum diameter of 4mm. Inflation of the vestibule has
displaced the petrosal wall ventrally and posteriorly, and has considerably modified
the topography of the mastoid part of the bone. In addition to reduction of the
fossa for the paroccipital process, the lateral semicircular canal is embedded in the
posterior wall of the vestibule, as revealed by the X-radiograph. Nonetheless, the
semicircular canals open into the vestibule according to the same pattern as in
UALVP 34 144, although the ampullae are significantly smaller relative to the size
of the inflated vestibule. As shown by the endocast (Fig. 4), the crus commune is at
the dorsal side, the anterior and lateral ampullae at the lateral side, and the posterior
ampulla and medial end of the lateral semicircular canal at the medial side of the
vestibule.
The posterior half of the vestibule is smooth and spherical, while the anterior
side is associated with several structures. There is little doubt that both the sacculus
and utriculus were enlarged to fill the vestibule in this specimen, but the utriculus
was probably the larger of the two, partly for the reasons discussed above in relation
to UALVP 34144. However, the endocast of UALVP 26039 provides additional
and even more direct evidence in support of this interpretation: it indicates that the
superior branch of the vestibular nerve was large, and ran laterally to the anterior
and lateral ampullae and to the utriculus; the inferior branch entered at the center
of the oval recessus sphericus for the sacculus, which is outlined by a shallow groove;
the posterior branch, entering the inner ear together with the cochlear nerve, ran
posteromedially to the posterior ampulla.
Because of the larger size of UALVP 26039, the cochlear canal is broader in that
specimen than in UALVP 34144; in cross section, it is obviously oval, wider than
high, but not round, contrary to what has been reported for multituberculates
generally (Luo & Ketten, 1991; Wible & Hopson, 1993: 54). The canal in UALVP
26039 is straighter than in 34144; whether or not this difference is size-dependent
260
R. C. FOX AND J. MENG
is not clear. The X-radiograph reveals a particularly interesting feature of the canal
in UALVP 26039-the inflation of its apical region (Fig. 2B), which strongly suggests
the presence of a lagena (see below).
Owing to breakage near the fenestra vestibuli in UALVP 26039, a low rounded
ridge with surfaces of finished bone can be seen in place ventrolateral to the internal
opening for the cochlear nerve. This ridge extends longitudinally along the inner
surface of the lateral wall of the cochlear canal and terminates at a level about onethird of the total length of the canal from the cochlear base. UALVP 26037 (below)
clearly shows that this ridge marks the entry of the cochlear nerve into the cochlear
canal, and because its surfaces are entirely of finished bone, we conclude that it did
not support a therian-like bony lamina projecting yet further into the lumen of the
canal, nor did it serve as the passageway for the cochlear nerve, as in therians. The
more distal parts of the inner surface of the cochlear canal are exposed by breakage
anteriorly on the ventral surface of the promontorium (Fig. 3), and can be seen to
be entirely smooth. Finally, the fossa for the perilymphatic recess (and its associated
ridge), the groove for the secondary perilyrnphatic duct, the trough that may have
carried the posterior branch of the vestibular nerve, and the foramina within the
internal acoustic meatus are all present in the same positions and have the same
relations to one another in UALVP 26039 as in 34144. In UALVP 26039, however,
the foramen for the inferior branch of the vestibular nerve is somewhat larger
(relatively, as well as absolutely) than in 34144, and a small foramen opens in the
bridge of bone that separates the inferior and lateral vestibular foramina. The
vestibular opening connecting with this foramen has not been identified, and it may
only be a nutritive foramen supplying the bone. However, UALVP 26034, an
incomplete specimen from Bug Creek, shows a small foramen in this same position
that opens internally, into the vestibule.
UALVP 26037 (right petrosal)
This specimen is from a multituberculate substantially smaller than those represented by 34144 and 26039. It is incomplete, but owing to fortuitous breakage in
the mastoid (Fig. 5), anterior and ventral parts of the vestibule are amply exposed.
O n the anteroventral wall of the vestibule, the oval depression marking the recessus
sphericus for the sacculus is well defined. The foramen that transmitted the inferior
branch of the vestibular nerve to the sacculus penetrates the vestibular wall at the
anterodorsal edge of the recessus. Medial to the recessus is the large opening that
communicates between the vestibule and the cochlear canal. The dorsal edge of
this opening is interrupted by a relatively large, nearly semicircular notch for the
trough that presumably carried the posterior branch of the vestibular nerve to the
posterior ampulla. Also medial to the opening is a narrow, relatively high ridge that
rises from the floor of the vestibule and separates the vestibule proper from the
space that contained the posterior ampulla and the orifice of the lateral semicircular
canal. The crus commune is exposed at a broken surface laterally on the dorsal side
of the vestibulc.
The anteromedial wall ofthe promontorium is broken in UALVP 26037, revealing
most of the cochlear canal. The canal is slightly bent laterally, and its curvature is
mirrored externally by the medial rim of the tensor tympani fossa (M. major fossa
of Luo, 1989). As before, the cochlear canal is not round in cross section, but oval,
higher medially than laterally, and with its long axis transversely oriented. As in
INNER EAR OF MULTITUBERCULATES
261
Figure 5. Unidentified multituberculate, incomplete right petrosal (UALVP 26037), Bug Creek Anthills
locality, Hell Creek Formation, Montana, USA A, lateral (slightly dorsal); B, tympanic (ventral) view.
Scale bar = 1 mm. See Abbreviations for key.
UALVP 26039, a low longitudinal ridge is developed proximally on the inner surface
of the lateral wall of the canal marking the most proximal course of the cochlear
nerve within the canal. No other structures arise from the walls of the canal, which
as far as can be determined from the parts preserved, are entirely smooth, composed
of finished bone. No evidence of a shelf or other structure that might indicate the
development of a bony lamina that contained the cochlear nerve or supported a
basilar membrane is present. The distalmost parts of the canal are partly preserved
in this specimen and as a consequence of breakage, are Sully exposed to view. These
indicate a slight expansion of the walls of the canal towards its terminus, consistent
with a lagena having been developed there. The fossa for the perilymphatic recess
and its associated ridge, the groove marking the course of the secondary perilymphatic
duct (particularly well developed on this specimen), the trough for the posterior
branch of the vestibular nerve, and the foramina within the internal acoustic meatus
do not differ significantly from those in UALVP 34144 and UALVP 26039.
Monotrmes
As shown in Figure 6, the petrosal of Tachyglossus is much larger and more massive
than that in Ornithorhynchus. The vestibule in Tachyglossus is roughly oval, with its two
ends narrowing to give rise to the ampullae of the semicircular canals. From base
to terminus, the cochlear canal curves in the same direction that typifies mammals
generally, that is, clockwise in the right ear and counterclockwise in the left; the
complete curvature is about 180". In its diameter, the canal remains nearly constant
262
R. C;. FOX AND J. MENG
B
COC
Fig-urc 6. Radiographs of cranial and ear r r p n s of Tuc~~Io.rsus
(A and C, AhlNH 42257. teachirig
collection of the Departmrnt of Vertebrate PaleontoloLgy)and OmithoihynchuJ (B and D, XP\INH 1 3 15
C:. ,A,, tcachirig collection of DVP). A and R are at the same scale; C and D are not to the samc scale.
C is photographically reversed from A.
INNER EAR OF MULTITUBERCUL4TES
263
through most of its length, although its apical region appears to be somewhat
inflated, housing a lagena (Pritchard, 1881). No osseous structures within the canal
are evident from the X-radiographs, nor have such structures been observed through
breaks in the walls of the promontorium in the available specimens. Our observations
in these respects are in agreement with those previously made on the petrosal of
Tuchyglossus by other workers (see e.g. Luo & Ketten, 1991).
The cochlear canal in Ornithorhynchus differs somewhat from that in Tuchyglossus:
it is relatively straight proximally but abruptly bent distally, or ‘sickle shaped’ (Zeller,
1993: 10I), at its terminus (Fig. 6B, D). As shown in the X-radiographs, the curvature
of the canal is certainly less than 270°, contrary to some previous observations (see
below), and is even less than the nearly semicircular canal of Tadyglossus. In
Ornithorhynchus, as in Tuchyglossus (Gray, 1908a), the apical region of the canal is
slightly expanded and in life held the lagena at the tip of the cochlear duct
(Pritchard, 1881), and from the X-radiographs, the diameter of the cochlear canal
in Ornithorhynchus shows little difference from base to the apical lagena, as already
noted by Gates et ul. (1974).
A left petrosal of Ornithorhynchus (AMNH 179983 [Mammalogy]) that is broken
through the fenestra vestibuli, perilymphatic foramen, internal acoustic meatus
and cochlear canal reveals aspects of otic morphology that have not been clearly
described before (Fig. 7). On the cerebellar side of the petrosal within the
internal acoustic meatus, the passageway for the facial nerve is a single oval
foramen, as in therians. Also as in therians, the foramen for the vestibular nerve
and the foramen for the cochlear nerve (the tractus spiralis foraminosus in
therians) are closed by cribriform plates. In contrast to the pattern in therians,
the cribriform area for the cochlear nerve does not form a spiral belt. No
secondary lamina is developed on the inner surface of the bony bridge between
the fenestra vestibuli and the lateral aperture of the perilymphatic recess, nor is
this lamina present on the inner surface of the cochlear canal, resembling
multituberculates but not therians in this respect. However, on the dorsal surface
of the canal in this specimen (Fig. 7), many (approximately a dozen) small
grooves fan out from the internal acoustic meatus toward the canal at an angle
nearly perpendicular to its course. This indicates that the cochlear nerve branches
into small rami as it approaches the basilar membrane in Ornithohynchus. It also
demonstrates that the pathway for the cochlear nerve can leave bony traces on
the inner surface of the cochlear canal, a phenomenon that has not been
observed in any fossil forms other than therians (Meng & Fox, 1995a, h). This
pattern differs from Pritchard’s (1881) report that the cochlear nerve runs parallel
to the ‘lamina’ (see Discussion). It also differs from the therian condition in that
the cochlear nerve is not supported by an osseous lamina projecting into the
lumen of the cochlear canal and dividing the canal into a scala tympani and
scala vestibuli, in agreement with previous observations by Zeller (1989) and
Luo & Ketten (1991). Although possessing a cribriform area for the entrance of
the cochlear nerve, a modiolus is not developed within the petrosal, which differs
from the therian pattern. Finally, the perilymphatic foramen opens directly into
the cochlear canal with no fossa and ridge intervening within the petrosal
internal to the opening. This pattern contrasts with that in therians (Meng &
Fox, 1995a, b), as well as multituberculates, as described above. The space
housing the lagena in AMNH 179983 is smoothly rounded, as in the
multituberculate petrosals already discussed.
R. C. FOX AND J. MENG
F i p r c 7. SEM photographs of broken left petrosal of Omithor/ynchus, (AMNH 179983 FIammalogy]):
A. cranial view, showing internal acoustic meatus and related structures; B, lateral view (of counterpart
of A), showing inside of cochlea. Scale bar = 1 mm. See Abbreviations for key.
DISCUSSIOK
Peribmphatic foramen and fenestra cochleae
As we pointed out in previous work (Meng & Fox, 1995b), Gray (1 908a) undertook
the first thorough discussion of the relationships of the perilymphatic recess, fenestra
cochleae and aquaeductus cochleae among reptiles, birds and mammals, although
de Beer (1937: 401-402) has also contributed importantly to understanding of the
relationships of these structures in living vertebrates. From their results, those from
later (especially palaeontological) studies, and our own data on the inner ear in
primitive mammals, we have summarized several features of this region that we
INNER EAR OF MULTITUBERCULA’IES
265
believe to be synapomorphies of therians. These include: (1) merger of the perilymphatic recess with the basal part of the scala tympani within the petrosal bone;
(2) formation of the fenestra cochleae and aquaeductus cochleae by development of
the processus recessus, a caudal outgrowth of the pars cochlearis of the auditory
capsule (de Beer, 1937; Kermack et al., 1981; Zeller, 1985a, b; Wible, 1990); and
(3) separation of the fenestra cochleae and fenestra vestibuli by a wide bony bridge
that supports the basal part of the secondary lamina on its inner surface; hence, the
basilar membrane in therians was elongated not only apically but also proximally,
extending to the area between the fenestra cochleae and fenestra vestibuli. In nontherian mammals, the bony bridge between the fenestra vestibuli and the lateral
aperture of the perilymphatic recess is usually narrow, and a bony lamina along the
outer wall within the cochlear canal on the inner surface of the bridge is not
devefoped. Therians are characterized additionally by a spiral cochlea, a primary
osseous spiral lamina, a radial pattern of the cochlear nerve and a modiolus that
forms the central axis or pillar of the cochlear spiral (Gray, 1959; Meng & Fox,
1995b). Kncelestes@ougier etal., 1992; Hopson & Rougier, 1993),ofLower Cretaceous
age and the only pre-tribosphenic therian in which the basicranial region of the
skull is known, may display intermediate conditions in this region, but its inner ear
morphology has yet to be described.
Here we discuss the homologies and distribution of several of these features,
starting with the perilymphatic foramen, the aquaeductus cochleae, and the fenestra
cochleae in therian and non-therian mammals (Fig.8). To understand these structures
in fossils, reference must be made to the perilymphatic system in living taxa (see
e.g. Gray, 1908a; de Burlet, 1934; de Beer, 1937; Kuhn, 1971; Wever, 1978, 1985;
Zeller, 1985a, b, 1989, 1993), but the discussion below attempts to extend these
works to the history of early mammals, and within a broader comparative context
than in the literature at present. In return, the fossil record can contribute to
understanding of the evolution of the mammalian ear, for which data from living
forms alone are not sufficient.
In our consideration of the perilymphatic system, we first explore two issues: (1)
the perilymphatic duct in relation to the perilymphatic foramen and the aquaeductus
cochleae, and (2) the secondary tympanic membrane in relation to the lateral
aperture of the perilymphatic recess ( = recessus scalae tympani of authors; see Gray,
1908a) and the fenestra cochleae. The anatomy of these structures is well displayed
in lizards and crocodilians (e.g. Wever, 1978),and their sequence in the perilymphatic
system-scala leading to foramen leading to sac-appears
to be primitive for
tetrapods (de Beer, 1937; see Wever, [1985] for Recent amphibians as further
confirmation of the primitive attributes of this pattern).
According to a broad spectrum of vertebrate morphologists (Gray, 1980a; de
Beer, 1937; Goodrich, 1958; Wever, 1978; Bellairs & Kamal, 1981; Rieppel, 1985;
Zeller, 1985a, b, 1993; Manley, 1990), the perilymphatic foramen in living nonmammalian amniotes carries the perilymphatic duct between the perilymphatic sac
and the scala tympani of the cochlea, with the sac held within the bony perilymphatic
recess. For example, although Gray (1908a) did not use the term ‘perilymphatic
foramen’, his equivalent, ‘oval opening’, refers to this passage between the perilymphatic recess and the cochlea in birds and mammals. According to de Beer
(1937: 40 1 4 0 2 ) , “the term foramen perilymphaticum [refers to] the posterior
opening in the wall of the auditory capsule of Tetrapoda, through which the ductus
perilymphaticus leaves the cavity of the capsule and enters the recessus scalae
Figure 8. SEA1 photographs showing perilymphatic foramen and related structures in Rug Creek
manimals and extant Omitlzorh3,nc-hus. A, unidcntified placental, incomplete left pctrosal (left is approxiniatcly anterior) (UA1,VP 26043 [see LZeng & Fox, 199SbI); B, unidentified multituberculate:
iriconiplcte right petrosal (UA4L\’P 26037); C, Onzit/zor/ync/iu.c,left ear region (AIlNH 13 15 C. A . ~
teaching collection, Department of Vertebrate Paleontology); D, unidentified multituherculatr. leli
p r t r o d (L;AL\‘P 26039). B and 1) are approximately posteromedial views of the promontorium. The
\.c.ntralpart of thc promontorium in the placental petrosal (A) is broken. exposing thc internal structure5
of thc petrosal. In A, the solid sqiiarc indicates the approximate position of the perilymphatic fbrarnrn
\vithin the cochlea. bet\vccn the hasc of the scala tympani (st) and the perilymphatic recess (qx.‘conch a p e d bulging’ for the perilymphatic recess of Gray); the dashed circle indicates thc position of thr
feriestra rochlcac (hoken) and the arrotv marks the lateral rdge of the fcnestra \-rstibuli. In B arid 1).
the lateral aperture of the perilymphatic recess is in a plane that bounds the per, pf. and most of gpd
mcdially; therefore per, pf, and gpd are within the petrosal bone in B and 1); b u t more cxtcrriall\located in C:. Not to scale. See Xbbreviations for kc).
tympani”, while for Wever (1978: 72), “from the scala tympani a short tube, often
not xvell defined. runs as the perilymphatic duct through the perilymphatic foramen
into the rccesus [scalae tympani], where it expands to form the perilymphatic sac”.
In mammals, however, the term ‘perilymphatic duct’ is conventionally applicd to
the tube that communicates between the perilymphatic space of the cochlea arid
the subarachnoid space of the braincase (Gray, 1959; Schuknecht, 1970; Zeller,
1985a, b). As it leaves the petrosal, this duct is contained in a groove or sulcus in
non-therian mammals and in the bony canal termed aquaeductus cochleae in
t herians (Fig. 8).Because the sulcus or aquaeductus cochlea contains a ‘perilymphatic
duct’ extending between the perilymphatic recess and the subarachnoid space iii
mammals, but the prrilymphatic foramen in non-mammalian amniotes hold5 a
INNER EAR OF hfULTITUBERCULATES
267
‘perilymphatic duct’ extending between the scala tympani and the perilymphatic
recess, it is necessary to distinguish terminologically between the two structures.
Therefore, we term the duct between the scala tympani and perilymphatic sac the
‘primary perilymphatic duct’ and the more elongate tube between the perilymphatic
sac and the subarachnoid space in mammals the ‘secondary perilymphatic duct’.
According to Gray (1908a: 525, fig. I), the structure equivalent to the mammalian
perilymphatic duct in non-mammalian amniotes is a “dehiscence on roof of perilymphatic recess through which the perilymph is in direct communication with the
cerebro-spinal fluid. This dehiscence becomes drawn out into the form of a short
tube in the bird and a long tube in the mammal, and in these two divisions is
termed the aqueduct of the perilymph”. Apparently, the secondary duct is a
neomorph that grows from the perilymphatic sac; it is not simply an elongation of
the primary duct.
An example of these differences in living mammals is provided by Tachyglossus,in
which a definite perilymphatic recess holding a perilymphatic sac is developed (Gray,
1908a): the sac communicates with the scala tympani by the primary perilymphatic
duct passing through the perilymphatic foramen (the ‘oval opening’ of Gray), and
the secondary perilymphatic duct is a long tube that extends from the posterior end
of the perilymphatic sac (ibid.: pl. 20, fig. 10). In Omithorhynchus, Zeller (1985a, 1993)
observed a similar pattern: the perilymphatic duct passes into the perilymphatic
recess, where it widens, and on leaving the recess, it runs medially in a groove to
the cranial cavity. It should be pointed out that although Zeller (1985a, 1993)
considered the elongation of the perilymphatic duct in mammals to be secondary,
he concluded that the elongation took place independently in Zchyglossus and therian
mammals, because in Tachyglossus the glossopharyngeal nerve runs together with the
perilymphatic duct within the aquaeductus cochleae (Kuhn, 197 1). Zeller’s (1985a,
1993) description includes the primary and the secondary perilymphatic ducts
differentiated by us.
The second issue of interest concerns the fenestra cochleae, the lateral aperture
of the perilymphatic recess and the secondary tympanic membrane. In lizards and
crocodilians, the fluid-filled perilymphatic sac faces onto the air-filled tympanic
cavity via an opening conventionally termed ‘round window’ or ‘fenestra rotunda’
(Wever, 1978). For purposes of discussion here, however, a better term for the
‘round window’ in lizards and crocodilians is ‘lateral aperture of the perilymphatic
recess’ or ‘lateral aperture of the recessus scala tympani’ (de Beer, 1937; Bellairs &
Kamal, 1981; Zeller, 1993): it is doubtful that this opening is homologous to the
‘round window’ (termed, henceforth, fenestra cochleae) of living therians, even
though the latter has a comparable position and function to the opening in lizards
and crocodilians (see below), and in fact, de Beer (1937) coined the term ‘fenestra
pseudorotunda’ for the crocodilian ‘round window’. The part of the sac wall that
closes the lateral aperture off from the tympanic cavity in lizards and crocodilians
is generally termed the ‘secondary tympanic membrane’, a pressure-releasing device
of the perilymphatic system (Weber, 1978). Unlike de Beer (1937), Zeller (1985a, b,
1993) believed that the secondary tympanic membrane is homologous throughout
the Amniota, including mammals, and that the fenestra cochleae (rotunda)of therians
is homologous with the lateral aperture of the recessus scalae tympani of reptiles,
although Bellairs & Kamal (1981) and Rieppel (1985) were less certain. By incorporating evidence from early mammals and other amniotes into the data from
268
R C FOX AND J MENG
living forms, as discussed below, the homology of these structures may be considered
fi-om a palaeontological perspective, in which multituberculates play a key role.
As described above, we have identified the perilymphatic recess in all of the
multituberculate petrosals in our Bug Creek collection that have this region preserved
and accessible to inspection. The recess is marked by a clearly defined depression
in the roof of the petrosal between the cochlear canal and the enlarged external
opening posteromedial to the fenestra vestibuli (Fig. 8B, D). The recess communicates
with the scala tympani via an inner opening, the perilymphatic foramen, that is
defined by a distinct crest. In multituberculates, the inner and external openings
have not been clearly distinguished and described before (e.g. Kielan-Jaworowska
et al., 1986; Luo, 1989; Lillegraven & Hahn, 1993; Wible & Hopson, 1993). If our
identification of the perilymphatic foramen in multituberculates as a structure that
is located wzthin the interior of the petrosal is correct, that is, internal to the perilymphatic
recess, this external opening obviously cannot itself be the perilymphatic foramen.
We believe the external opening is simply a lateral aperture of the perilymphatic
recess over which the secondary tympanic membrane was stretched in life. As noted
above, the rim of the aperture is cut by a narrow but well-defined groove for
the secondary perilymphatic duct in its passage to the subarachnoid space. The
configuration of this groove agrees with studies of the multituberculate petrosal by
previous workers (Kielan-Jaworowska et al., 1986; Luo, 1989; Lillegraven & Hahn,
1993; \/t’ible & Hopson, 1993, 1995).
We have sought to extend our observations on the proximal parts of the
perilymphatic system in multituberculates to other mammals, and have found that
the basic multituberculate pattern may have been already established in the early
stages of mammalian history, as is presently best exemplified by the Early Jurassic
non-therian mammal, Morganucodon. Kermack et al. (1981) have shown that in
.Vlorgunucodon, the perilymphatic foramen (which they termed ‘fenestra cochleae’) is
kvell developed, equal in size to or even larger than the fenestra vestibuli. The rim
of the opening in Morganucodon is cut by a narrow groove for the secondary
perilymphatic duct. Although some aspects of the internal anatomy of the petrosal
in Morganucodon are known from serial sections and C T scans (Grayheal et al., 1989;
Luo et al., 1995), fine details comparable to those of the Bug Creek multituberculate
pctrosals described here have yet to be determined: for example, whether or not a
perilymphatic recess is present in Morganucodon is not clear. Of published material,
however, some specimens (Kermack et al., 1981: figs 75B, 83A; Luo, 1994: fig. 6.3A)
display a recess of some kind medial to the perilymphatic foramen, whereas in other
specimens (e.g. Kermack et ul., 1981: fig. 82A), this recess is less distinct. The
location of the recess suggests that it is the perilymphatic recess, resembling that in
multituberculates and monotremes, although it seems less internally placed than in
multituberculates. The variable conditions of the recess in actual specimens in
,tlorgunucodon suggest that the perilymphatic sac may have been at least partly held
in some individuals by a distinct osseous depression medial to the perilymphatic
foramen. Detailed description and illustration of this region in Morganucodon, comparable to that which we have provided for multituberculates and monotremes (fig.
8), are needed to clarify the features in question, but whenever further evidence
becomes available, we hold that Morganucodon will be in accord with the primiti1.e
amniote pattern in which the cochlear canal is partly separated from the more
proximal perilymphatic recess (which held a perilymphatic sac), and the perilymphatic
foramen opens between the two spaces. From these considerations, we believe that
INNER EAR OF MULTITUBERCUWTES
269
the lateral aperture of the perilymphatic recess ofMorganucodonshould be distinguished
from the perilymphatic foramen, in keeping with conclusions that de Beer (1 937)
and Zeller (1987, 1993) had already determined from living mammals, and in
agreement with our own conclusions regarding multituberculates. Where, then, was
the secondary tympanic membrane attached in Morganucodon and multituberculates?
Kermack et al. (1 98 1) noted that preservation of some petrosals of Molganucodon
was complete enough to show that at least part of the rim of what they called the
‘fenestra cochleae’ was developed as a thin flange of bone; they interpreted this
flange to be a support for a secondary tympanic membrane. Instead, we believe
that this flange is the counterpart of that in the multituberculate petrosals described
above that defines the perilymphatic foramen and separates the scala tympani from
the perilymphatic recess. If so, the secondary tympanic membrane in Morganucodon
would have been medial to the perilymphatic recess and sac, just as in other
amniotes, and would have attached to the poorly defined external edges of the
recess found there, not to the flange. In Ornithorhynchus, it is the lateral aperture of
the perilymphatic recess, not the perilymphatic foramen, that is closed by the
secondary tympanic membrane (Gray, 1908a; Kuhn, 197 1; Zeller, 1991; see below),
and the osseous rim that supports the membrane is poorly developed (Zeller, 1993:
10 1)-just as we hypothesize for Morganucodon.
In multituberculates, the lateral aperture (traditionally called the ‘perilymphatic
foramen’, ‘fenestra cochleae’ or ‘round window’ by authors, but incorrectly) is better
defined, encircled by a complete rim of bone (Fig. 8B, D). According to. our
determination of homologies, this opening must have been closed by the secondary
tympanic membrane, with the perilymphatic foramen and perilymphatic recess
located more internally in the petrosal than in Mo?ganucodon and Ornithorhynchus. In
contrast to the assumption that Kermack et al. (1 98 1) made in respect to Morganucodon,
attachment of the secondary tympanic membrane may or may not leave distinctive
marks on the bone. Two of the Bug Creek petrosals described above, UALVP
26037 and 26039, show the development of a narrow groove along the ventral part
of the rim of the lateral aperture that splits the rim into two parallel flanges, perhaps
evidence of a secondary tympanic membrane attaching there. However, other parts
of the rim in these specimens are smoothly rounded, and the ventral rim itself is
smoothly rounded in UALVP 34 144, also a well-preserved specimen: no flanges are
developed. In Didebhis (UALVP unnumbered specimens), the rim of the fenestra
cochleae is smoothly rounded in its entirety, and the bone lacks a distinctive
configuration that might be taken as the site of attachment of the secondary tympanic
membrane, even though a membrane is present in Didebhir, as in other living
therians. As noted above, the same is true for the lateral aperture of the perilymphatic
recess in Ornithorhynchus: no distinct osseous crest or rim for attachment of the
membrane has been observed (Fig. 8C). Consequently, the lack of a flange along
parts of the rim of what we identify as the lateral aperture can not qualify as
evidence that a secondary tympanic membrane did not attach to this rim in
Morganucodon nor in multituberculates. Conversely, the three-dimensional curvature
of the internal ridge that we believe defines the perilymphatic foramen and recess
internally in the petrosal of multituberculates precludes it from supporting the
secondary tympanic membrane, which need have been held in only a single plane,
as by the rim of the lateral aperture.
If our interpretation of the attachment of the secondary tympanic membrane in
Morganucodon and multituberculates is correct, the primary perilymphatic duct was
“70
R. C. FOX KYD J. MENG
short in these forms, as it is in monotremes. The path for the secondary perilymphatic
duct as it leaves the petrosal is clear in Morganucodon and multituberculates, following
the groove that arises at the antermedial extremity of the perilymphatic recess; its
location as it leaves the recess is comparable to that of the cochlear (internal) orifice
of the aquaeductus cochleae in Late Cretaceous therians (Meng & Fox, 1995b, fig.
1; Fig. 8A), a point of significance in reconstructing the evolution of the therian
pattern. The therian oriface is at the medial end of a ridge that reflects the position
of the perilymphatic foramen within the cochlea (marked by a black square in fig.
812) hetween the scala tympani and the perilymphatic recess. According to Gra).
( I 908a: 523), there is little development of a clear-cut boundary between cochlea
(scala tympani) and perilymphatic recess in living therians, and the recess is indistinct,
represented only by what he called a ‘cone-shaped bulging’ (Gray, 1908a); we havc
extended Gray’s observations to Late Cretaceous therians, in which we have
identified a cone-shaped swelling, as well (Meng & Fox, 1995b: figs 1, 4). Because
of their comparable positions in relation to the perilymphatic foramen, the therian
fenestra cochleae and the aqueductus cochleae are readily derivable evolutionarily
from division of the lateral aperture of the perilymphatic recess (as the recess is
seen, for example, in multituberculates) by formation of a processus recessus, the
latter documented in the ontogeny of the therian petrosal (e.g. de Beer, 1929, 1937;
Zeller, 1993). This transformation series from the fossil evidence gains support from
at least two forms that may show morphologically intermediate stages: Encelestes and
an unnamed taxon represented by a newly described, isolated petrosal from the
Khoobur locality, Lower Cretaceous, Mongolia (Rougier et al., 1992; Wible et al.,
1995; Rougier et al., 1996); in both, a fenestra cgchleae and aquaeductus cochleae
arc developed (we note, however, that the fenestra cochleae in the Khoobur petrosal
was described as the perilymphatic foramen [Wible et al., 19951)but an aquaeductus
cochleae has since been identified in this specimen [Rougier et al., 19961). In the
Khoobur petrosal, the perilymphatic recess is completely contained within the
petrosal, but a spiral lamina accommodating the cochlear nerve had not yet
developed (personal observation, JM) and the cochlea is straight (Wible et al., 1995:
3 ) . Presence of the secondary spiral lamina has been cited in Hincelestes (Wible et al.,
1995: appendices 1 and 2), but evidence for it and the morphology of the inner ear
more generally are undescribed. Hence, the fossil evidence of early mammals is
consistent with de Beer’s (1937) conclusion from ontogenetic studies that part of the
latcral aperture of the perilymphatic recess (not the perilymphatic foramen) in nonthcrian mammals becomes the fenestra cochleae of therians, and that the secondar)tympanic membrane covering the aperture or its derivative fenestra cochleae is
homologous in these forms.
Our choice of lizards and crocodilians as an out-group to establish the primitive
amniote and primitive mammalian sequence of perilymphatic recess-perilymphatic
foramen-cochlear canal leads to an additional question, however. Is the lateral
apcrture of the perilymphatic recess in primitive mammals homologous to the ‘round
window’ of non-synapsid amniotes and, hence, is the secondary tympanic membrane
homologous among all amniotes, as Zeller (1985a, b, 1993) has maintained? M’e
helie1.e not, with the substance of our conclusion based on evidence from the fossil
record of early amniotes. That record indicates, it is now generally agreed, that the
most primitive synapsids, the Palaeozoic pelycosaurs, probably lacked a tympanic
mcmbrane, and if capable of hearing airborne sounds at all, these animals could
have transmitted only low frequencies to the otic capsule, via the intervention of
INNER EAR OF MULTITUBEKCUIA’rES
25 1
unspecialized surface tissues activating the massive stapes (Allin, 1975, 1986; Allin
& Hopson, 1992). Indeed, the bones intervening between any superficial soft tissues
in the future tympanic area and the stapes seem themselves incapable of independent
movement, thereby further limiting the potential for stapedial activation in sound
transmission (Allin & Hopson, 1992). Pelycosaurs lacked a lateral aperture that
would have supported a secondary tympanic membrane and lacked the perilymphatic
foramen (Romer & Price, 1940; Olson, 1944; Allin & Hopson, 1992), possessing
only a jugular foramen for the exit of cranial nerves IX, X, and XI and the internal
jugular vein (Romer & Price, 1940; Romer, 1956).
In primitive cynodonts (e.g. 7hrinaxodon and Probainognathus; see Allin & Hopson,
1992: fig. 28.8; Luo et al., 1995: fig. lA), the pelycosaur pattern in the proximal
perilymphatic system appears to have been maintained: a separate perilymphatic
foramen is not developed. In a young specimen of lhrinaxodon liorhinus, Estes (1961:
fig. 3) restored the major parts of the inner ear as if they were in place, with the
‘fenestra rotunda’ at the end of a ‘distinct channel’ opening within the walls of the
jugular foramen (p. 172). While cynodonts at the Thinaxadon stage of evolution
probably were capable of hearing air-borne sounds via a specialized tympanum and
moveable connecting bones (AUin, 1975, 1986; Allin & Hopson, 1992), Estes’ (1961)
restoration suggests that the secondary tympanic membrane was probably not
developed as no part of the perilymphatic system seems to have abutted against the
air-filled tympanic cavity.
Among pre-mammalian synapsids, tritheledonts and tritylodonts are the first to
resemble mammals explicitly in the history of the proximal perilymphatic system.
They display an opening adjacent to but not confluent with the jugular foramen,
although the two openings are closer to one another than in early mammals (Allin
& Hopson, 1992; Crompton & Luo, 1993; Lucas & Luo, 1993). Olkobphus well
represents this stage: both the new opening and the jugular foramen are completely
encircled by bone, but they are housed in a common recess with only a slender
osseous bar between them (Crompton, 1964: fig. 8; Luo, 1994: fig. 6.3D). Th‘is new
opening is the perilymphatic foramen, opening in the wall of the auditory capsule
(de Beer, 1937), although it has been mistakenly termed ‘round window’ by some
workers (Luo, 1994; Luo et al., 1995). Relying on the pattern in lizards as a model
(e.g. Wever, 1978: 72-74; fig. 3-13), one can envisage in Oligokyphus a perilymphatic
sac held in the common recess that communicates with the scala tympani through
the perilymphatic foramen laterally, expands into the cranial cavity through the
jugular foramen medially, and closes the opening for the common recess ventrally.
Because the perilymphatic and jugular foramina are so near to each other in
Oligokyphus, development of a secondary perilymphatic duct seems not necessary (see
e.g. Luo, 1994: fig. 6.3D). Continued expansion of the otic capsule and basicranium
with refinement of hearing and increasing size of the brain would have resulted in
further spatial separation of the perilymphatic foramen from the jugular foramen,
as seen, for instance, in Morganucodon and other early mammals (Kermack et al.,
1981; Crompton & Luo, 1993; Lucas & Luo, 1993; Luo et al., 1995). In those groups
having the two foramina more distantly separated than does Oligokyihus (perhaps
accompanied by reduction of the perilymphatic sac), the secondary perilymphatic
duct was developed and a groove holding it was formed. These definitely include
morganucodontids (Kermack et al., 198l), Haldanodon (Lillegraven & Krusat, 1991:
fig. 8), triconodontids (Wible & Hopson, 1993: fig. 5.3B), multituberculates (KielanJaworowska et al., 1986; Luo, 1989; this paper), and monotremes (Wible & Hopson,
272
K C:. FOX AND J RfENG
1993);whether or not a groove for the duct is present in tritheledontids, tritylodontids.
Adelobasileus, or Sznoconodon has been disputed (sec Rougier et al. [1996]), but does
not altcr the sequence of morphological events established here in our attempt to
determine the homologies of the secondary tympanic membrane among amniotes.
In summary, the major features of the evolution of the proximal perilymphatic
qystcm from pelycosaurs to early mammals when interpreted in a context of
comparative information from living amniotes seem straightforward and explain the
nature of thc perilymphatic foramen, the lateral aperture of the perilymphatic recess,
the fenestra cochleae, and (implied) secondary tympanic membrane: we conclude
that the ‘mammal-like’ aspects of the perilymphatic system in non-synapsid amniotes
are homoplasious, but how satisfactorily does this account apply to living mammals?
The only problematic living mammals in this respect are monotremes. In TactyglossuJ, a superficially therian-like, partial ‘aquaeductus cochleae’ is developed that
contains the secondary perilymphatic duct, but it also contains the glossopharyngeal
newe. This pattern has clearly evolved independently of that in therians, in which
the true aquaeductus cochleae contains only the secondary perilymphatic duct, not
the nerve (Kuhn, 1971; Gauthier et al., 1988; Zeller, 1993). Quite different is thc
arrangement in Ornithorhynchus, in which the secondary perilymphatic duct is not yet
enclosed in a bony aquaeductus (resembling in that respect multituberculates and
other non-therian mammals), and the perilymphatic recess is little ossified (in contrast
to that in multituberculates and presumably more primitive). We agree with Zeller
(1 993)) however, that the secondary tympanic membrane is homologous in living
monotremes, irrespective of ontogenetic differences in the development of the lateral
aperture of the perilymphatic recess and position of the secondary perilymphatic
duct in Tuchyglossus and Ornithorhynchus. At present, the fossil record can make no
contribution to understanding of these patterns.
Szzt) ofthe vestibule
It is nobv well known that in several multituberculate genera the vestibule of the
labyrinth is enlarged (Miao, 1988; Luo, 1989). It is significantly larger relative to
petrosal size and inferred skull size than that in monotremes, therians and lMorganucodon
(Luo & Ketten, 1991: fig. 4)) and enlargement of the vestibule has been interpreted
dS a possible multituberculate synapomorphy (Luo, 1989; Luo & Krtten, 1991;
Simmons, 1993). An extreme expression of this specialization is seen in the earl)
Tertiary multituberculate Lambdopsalzs (Miao, 1988; Meng & Wyss, 1995). Indeed,
the vestibule in Lambdopsalis is so inflated that it was originally identified as the
tvmpanic bulla, from which the specific name, L. bulla, is derived (Chow & Qi,
1978). Lillegraven & Hahn (1 993) have shown, however, that the vestibule is not
inflated in the Late Jurassic Paulchoffatiidae, the most primitive multituberculates
known. As noted above, the vestibule is not inflated in UALVP 34144, either, and
in this respect the specimen resembles the petrosal of paulchoffatiids and the
Paleocene ptilodontoid Ptzlodus montanus (Simpson, 1937). In sum, the distribution of
an inflated vestibule among multituberculates suggests that inflation is a derived
condition within the order, and that it probably originated more than once,
independently, given the phylogeny of multituberculates (Simmons, 1993). As a
consequence of inflation, the lateral semicircular canal can be embedded in the
poyterior wall of the vestibule, as in UALVP 26039, or can even become confluent
with the vestibule, as in LambdopsaliJ (Miao, 1988; Meng & Wyss, 1995).
INNER EAR OF MULTITUBERCULATES
273
Inflation of the vestibule mostly reflects inflation of the sacculus and utriculus.
These are the two primary sacs that occupied the vestibule in life, and the available
evidence indicates that they filled the entire vestibule in multituberculates, leaving
no significant parts of it free. Luo & Ketten (1991: 225) were not certain of the
relative sizes of the two sacs in multituberculates, stating: “It remains unclear from
our CT scans of the petrosal and previous studies (Kielan-Jaworowska et al., 1986;
Miao, 1988; Luo, 1989) whether the vestibular inflation of multituberculates relates
to the enlargement of the saccule, the utricle, or both”. It is indeed difficult to make
this assessment from only osseous remains, but it is not impossible given the
opportunity for direct visual inspection of the interior of the petrosal, as we have
already shown. Based on our own observations, it is certain that the utriculus was
the major occupant of the inflated vestibule in multituberculates, as it appears to
be in at least Tachyglossus among monotremes (Griffiths, 1968; Jmgensen & Locket,
1995; although see Gray [1908a: 5 191 for an opposing view). However, because the
condition in potential outgroups within the Mammalia, including Adelobasileus,
Sinoconodon and Morganucodon, is unknown (Luo & Ketten, 1991; Luo et al., 1995),
the polarity of this character cannot be established at present.
Curvature of cochlear canal
In most reptiles, the cochlear canal (also termed cochleolagenar canal, cochleolagenar recess, or cochlear recess) is short and is ventral to the vestibule (Miller,
1966, 1968; Baird, 1970, 1974; Wever, 1978; Lewis et al., 1985). The canal in
crocodilians is somewhat elongate and bends anteroventrally (Wever, 1967, 1978;
Baird, 1970; Manley, 1970). In birds, it is also variably elongate but bends medially,
in a direction opposite to that in monotremes and therians (Pritchard, 1881). In
cynodonts, the cochlear canal is usually short and is located anteroventral to the
vestibule (Estes, 1961; Quiroga, 1979; Allin, 1986; Allin & Hopson, 1992; Luo et
al., 1995), although Simpson (1933: 288-9) reconstructed the cynodont ear with a
more elongate cochlea that extends “downward and forward from the floor of the
vestibule, very much as in Ornithorhynchus”.
The cochlear canal of primitive mammals has been most extensively studied in
Morganucodon. In Morganucodon it resembles that of multituberculates in several respects:
Graybeal et al. (1989) found the canal to be “a slightly curved tube” (p. 112),
‘%-tually straight tube” (p. 113), “straight” (p. 114), or “had a very slight curve”
(p. 115), while Kermack et al. (1981) described it as “almost straight”. Rosowski &
Graybeal (1991) portrayed the Morganucodon canal as similar to that in birds and
crocodilians, and Graybeal et al. (1989: 1 14) characterized it in much the same way.
The special resemblances that these authors noted are in its shortness and relative
straightness, and in its lack of bony lamina (Rosowski & Graybeal, 1991: 138)features, however, that are also seen in multituberculates. Although none of the
above authors have explicitly stated the direction in which the cochlear canal curves
in Molganucodon, it seems to be laterad (see especially Rosowski & Graybeal, 1991:
fig. 3B, D), as in other primitive mammals but not reptiles or birds.
Knowledge of inner ear morphology in the most primitive mammals has been
amplified significantly by recent description of the petrosal in Sznoco~odon(Luo et al.,
1995). In this genus, the cochlear canal is still more primitive in certain respects
than in Morganucodon. The Sinoconodon canal is about half the length of that in
Morganucodon, and is straight proximally but is slightly curved laterally towards the
R. C . FOX AND J. MENG
2i-I
TARI,E
I . Comparative measurements of multituberculate petrosals, Bug Creek Anthills locality. :1,
length of cochlea; B, long axis of fenestra cochleae; C, short axis of fenestra cochleae; D; long axis of
fenrstra vestihuli; E, short axis of fcnestra vestibuli; F, diameter of crus commune; G. diametrr of
semicircular canal; H, radius of lateral semicircular canal; I, diameter of cochlear canal. Aatrrisks
indicate measurements from X-radiographs
A
UALYP 26032
LALVP 2603-1
L.ILVP 26035
UALYP 26036
UALVP 2603 7
L-AI,vP 26039
L-~AI,\’P31111
H
c:
u
c
F
0.62
3.3*
+.9*
0.78
4.5*
0.99
1.311
0.54
1.2
0.88
0.53
0.87
H
1
4.0*
2.j*
1.-17*
0.22
0.53
0.86
G
0.66
0.55
0.22
0.33
0.3
1.1:3*
terminus, more so than in Murganucodon (Luo et al., 1995: 118, table 1). Thc
configuration of the cochlear canal is unknown in Adelobasileus, purportedly the
earlicst known mammal (Lucas & Hunt, 1990; Lucas & Luo, 1993; Luo et al., 1995).
O u r demonstration that in multituberculate petrosals having otherwise different
morphologies (see e.g. Fig. 2), the cochlear canal extends anteriorly in a nearly
horizontal plane and curves slightly laterally clearly differs from obsemations reported
by Sloan (1979), Mia0 (1988) and Luo & Ketten (1991). According to Sloan (1979),
the cochlear canal is ‘hooked’ in the early Tertiary neoplagiaulacid Ecppudus (but
see Miao [1988] for reservations), whereas a ‘rod-like and straight’ cochlea has been
cited for Catopsalis, ?Meniscoessus and Lumbdopsalis (Miao, 1988; Luo & Ketten, 1991 ;
and see Luo et al., 1995). Our observations are more in keeping with those of
Simpson (1937: 751) on Ptiludus, in which a slightly curved cochlear canal appears
to have been developed. In all known multituberculates in which the cochlea is
definitely curved, the direction of curvature matches that in other mammals, i.e.
clockwise in the right ear and counterclockwise in the left, but the degree of curvature
in multituberculates appears to differ among different taxa. From what is known so
far, we suspect that lateral cun7ature of the cochlea may be a synapomorphy of thc
Mammalia (see e.g. Lillegraven & Krusat [1991] for ~ u ~ d u n o ~but
u ~ )any
, final
conclusion along these lines must await clarification of cochlear morpholo9 in
Ade&basileus and in a broader array of primitive mammals, including primiti\.e
multituberculates, than is presently available.
The degree of curvature of the cochlea in monotremes has been uncertain, with
conflicting accounts recorded in the literature, as we have discussed elsewhere (Meng
& Fox, 1995b). Kermack et al. (198 I), citing Denker (1 90 l), reported that the cochlea
curves 180” in Tacachygossus and 270” in Ornithorhynchus, and this conclusion has been
widely accepted since (e.g. Kerinack & Mussett, 1983; Wible, 1990; Luo & Ketten,
1991; Allin & Hopson, 1992). However, in describing the cochlea in Ornithor/ynchuJ,
Pritchard (1881: 267) had long before observed: “This tube is directed almost
horizontally forwards and is slightly curved outward, its apex forming a little
projection on the outer border of the petrous bone close to its pointed end”, and,
as illustrated (Pritchard, 1881: pl. 45I), the cochlea is only slightly cuwed, about
180”. Gray (1908a: 5 18)made much the same observation: “In reality, the labyrinth
of the echidna presents in this, as in other aspects, a very considerable advance
upon that of the platypus, in which there is only the slightest degrec of curnature
INNER EAR OF MULTITUBERCULATES
275
in the cochlea, with a bulbous knob on the tip of the organ”. But according to
Griffiths (1978: 189), in Ornithorhynchus “the cochlea exhibits a three-quarter spiral
turn and terminates in a lagena with lagenar macula” (and see J~rgensen& Locket,
1995: fig. l), while Zeller (1993: 101) reported that “the monotreme cochlear duct
is only slightly curved; its rostra1 end, containing the papilla lagenae, is sickle
shaped”.
The disagreement about curvature in the monotreme cochlea may well have its
source at least partly in what have been different meanings for the term ‘cochlea’
by different authors. The term sometimes seems to refer to the membranous structure
that consists of the endolymphatic and perilymphatic ducts (the soft tissue cochlear
duct and scala vestibuli and tympani), at other times to the cochlear canal (the bony
housing for the ducts) or even to both, in different publications. Here we attempt
to clarify these differences so that the nature and significance of our own observations
are clear. In mammals, the cochlear duct is in indivisible association with the scalae
as parts of the membranous labyrinth, and is contained within the osseous cochlear
canal, a part of the bony labyrinth. In monotremes, two lines of evidence indicate
that the soft membranous ducts may have a greater curvature than does the osseous
canal in which they are housed. First, Luo & Ketten (1991: 226) have shown that
in the monotreme inner ear “the bony cochlear cavity does not coil in correspondence
to the coiled membranous labyrinth”, an observation which obviously contradicts
that of Pritchard (188 1). Second, with decalcification of the petrosal in preparing a
specimen for examination of the soft tissues within, it is possible that the membranous
ducts come to display a variable degree of curvature, even greater than that of the
cochlear canal itself, but only as a consequence of tissue distortion during the
decalcification technique; in specimens that have undergone this treatment to
enhance the visibility of the membranous ducts, it is impossible to tell with certainty
what the original curvature of the ducts within the canal might have been. In any
case, no evidence exists to indicate what the degree of curvature of the membranous
ducts within the osseous canal actually was in multituberculates or any other early
mammals (cf. Wible & Hopson, 1993: 54): curvature of the ducts may have matched
that of the canal or it may have exceeded it, given the observations of Luo & Ketten
(199 1) for monotremes. This leads us to conclude that any meaningful comparison
in such studies must be between the same structures, and that can only be a
comparison of the osseous canal between extant and fossil forms.
During the evolution of therians, the cochlear canal probably achieved its first
full turn and then subsequent turns only gradually, with early steps in this transformation being documented by the Early Cretaceous pre-tribosphenic therian
Encelestes (270” curvature: Rougier, 1990; Rougier et al., 1992) and therian petrosals
from Late Cretaceous species (slightly more than 360” curvature: Meng & Fox,
1993, 1995a, b). In all extant therians, the membranous ducts spiral through at least
one and a half turns (Fernandez, 1952; Fernandez & Schmidt, 1963; von BCkksy,
1960; Pye, 1966a, b; Wever, 1974; Wever et al., 197 1, 1972; Fleischer, 1976; Bruns,
1976; Aitkin et al., 1979; Lewis et al., 1985), and the only living therians that are
known to have as few as one and a half turns are the marsupial mole, hedgehog
and sea-cow (Gray, 1980b; Lewis et al., 1985). In Mesozoic therians for which the
internal cochlear structure is known, there is probably a closer correspondence
between curvature of the membranous ducts and curvature of the osseous canal
than in non-therians owing to the support of the ducts in therians by the osseous
laminae that arise from the walls of the canal. The origin of these laminae within
276
R. C. FOX AVD J. MENG
the Theria has, however, yet to be determined, with observations and descriptions
of them from no species older than Late Cretaceous (Meng & Fox, 1995a, b).
hngth of cochlea
Obviously, the length of the cochlear canal is an important aspect of cochlear
size in a functional context, but it is of significance phylogenetically, as well. Because
the cochlear cavity is proportionally short and straight in extant diapsid reptiles
(Oelrich, 1956; Wever, 1978; Bellairs & Kamal, 1981) and in therapsids (Olson,
1944; Estes, 1961; Allin, 1986; Allin & Hopson, 1992), Luo & Ketten (1991) and
Luo et al. (1995: table 1) concluded that the cochlear canal in multituberculates and
Morganucodon is longer (relative to skull length) and thus more derived than the canal
in therapsid outgroups. However, we have found that comparisons of the length of
the cochlear canal in previous work (e.g. Graybeal et al., 1989; Luo & Ketten, 1991;
Rosowski & Graybeal, 1991) are sometimes oflimited usefulness because of differences
in identifying the point at which the canal begins (and see Luo et al. [1995: table
11). In our studies of the inner ear in Late Cretaceous therians, this point was taken
to be at the inflection of the osseous spiral lamina anterior to the fenestra cochleae,
where the cochlear duct begins its spiral course (Meng & Fox, 1995a, b). Because
the cochlear canal in multituberculates has no osseous lamina, we have objectively
defined the starting point of the cochlear duct as at the point where the secondary
perilymphatic duct notches the rim of the perilymphatic foramen: this point most
closely corresponds to the position of the aquaeductus cochleae at the base of the
scala tympani in therians. For Sinoconodon, Luo et al. (1995: 1 18) measured the length
of the canal from the anterior rim of the fenestra vestibuli to the terminus, a
somewhat different dimension from ours in that it includes part of the vestibule. A
potentially more important statistic than the raw measurement of the length of the
cochlear canal is its length relative to skull length (Luo et al., 1995: table 1)-although
in the present context this is of limited use owing to the lack of association of
petrosals with complete skulls in our sample and, indeed, for most early mammals.
The length of the cochlear canal in modern therians corresponds directly to the
length of the basilar membrane because the lagena is no longer present as a distal
extension of the cochlear duct in these mammals. This relationship between canal
and membrane is assumed to hold as well in the Late Cretaceous therians that we
investigated previously (Meng & Fox, 1995a, b). In other early mammals, such as
Morganucodon (Graybeal et al., 1989) and multituberculates, the length of the cochlea
must also have approximated the length of the basilar membrane, but this approximation was probably less precise than that in therians because of the presence
of a lagena (see below).
Pattern of innervation of the cochlea
Previous work has indicated that in primitive mammals, such as Morganucodon
(Kermack et al., 198 l), Haldanodon (Lillegraven & Krusat, 199 1) and multituberculates
(Kielan-Jaworowska et al., 1986; Luo, 1989; Lillegraven & Hahn, 1993; Figs 1, 3,
9B), the cochlear division of the auditory nerve passes through the petrosal wall via
a single foramen, thereby contrasting sharply with the condition in extant therians
(Lorente de NO, 1937; Bast & Anson, 1949; Gray, 1959; Bredberg, 1968; Spoendlin,
1972, 1974; Sando, 1965). In even the earliest tribosphenic therians for which
evidence is available (Meng & Fox, 1995a, b, c), the cochlear nerve branches into
INNER EAR OF MULTITUBERCULATES
277
Figure 9. SEM photographs showing the cribriform plate of a therian (A) and the single foramen of
a multituberculate (B) for the cochlear nerve in the internal acoustic meatus. Not to scale. See
Abbreviations for key.
COC
bm
C
A
B
c
Figure 10. Diagrams showing cochlear innervation patterns. A, a hypothetical parallel innervation
pattern for a coiled cochlea; B, a parallel innervation pattern presumably present in early mammals,
including multituberculates; C, a radial pattern in therians. See text for discussion. See Abbreviations
for key.
many small rami that pass through the numerous tubules (the tractus spiralis
foraminosis) of the modiolus (Fig. 9A), forming a radial pattern matching that in
extant therians.
The cochlear nerve in adult monotremes resembles its homologue in therians in
that it passes through a cribriform plate (the area cribosa anterior of Alexander
[ 19041 and Gaupp [1908a, b]) in the floor of the internal acoustic meatus (Simpson,
1938; Kermack et al., 1981; Fig. 7). Once within the canal, the newe differs in its
orientation from that in therians. As Pritchard (1881: 275) noted, the nerve in the
therian spiral cochlea “necessarily runs at right angles to the lamina spiralis, [whereas]
in this cochlea [of platypus] it runs parallel to the corresponding lamina” (see our
description of the apparent nerve pattern in a specimen of Ornithorhynchus -above,
however). We term the latter configuration of the nerve the ‘parallel pattern’ or
‘fanned pattern’ (Fig. 10B), and given the short, relatively straight cochlear canal of
multituberculates, the fibres of the cochlear nerve must also have followed a similar
pattern in that group. This pattern may well be less efficient in certain respects than
278
R C FOX XYDJ MENG
the radial pattern of therians, especially in innervating an elongate organ of Corti.
It is likely that the radial pattern of the cochlear nerve in therians functions to
minimize differences in length required of individual fibres that pass to different
parts along the basilar membrane (West, 1985; Meng & Fox, 1995a, b, c). In therians
in which the basilar membrane is elongate, a parallel pattern of the cochlear nerve
fibres, as in monotremes (Pritchard, 1881)-and presumably, from the shape of the
cochlear canal, in Morganucodon, Haldanodon and multituberculates as well--would
require that fibres innervating hair cells distally would need to be significantly longer
than those passing to proximal cells, nearer to the base of the membrane (Fig. 1OA).
Therefore, for those mammals in which the cochlear canal is elongate and has
several spirals (over four spirals in the guinea-pig, for example [Manley, 1972; Lewis
et al., 1985]), this pattern would result in a significant difference in conduction time
of the nerve impulse from the two ends of the basilar membrane to the auditory
cortex of the brain. Such a pattern, however, is not present in reality. A radial
pattern of the cochlear nerve in all tribosphenic therians minimizes this difference,
d hypothesis to be further tested.
The blood Lressels that supply the cochlear ganglion and its cell bodies housed in
the spiral canal of the modiolus adopt a different pattern in therians. As shown by
Axelsson (1 974), the main trunk of the spiral modiolar artery spirals along with thc
cochlea, between the acoustic nerve centrally and the spiral ganglion peripherally.
The spiral modiolar vein follows a similar route. The size of the spiral modiolar
artery gradually diminishes as it gives off branches on its way from the base to the
apex of the cochlea.
Ikgmi
Monotremes are the only living mammals known that possess a lagena at the
distal end of the cochlear duct, a specialization comparable to that in reptiles and
birds (Pritchard, 1881; Denker, 1901; Alexander, 1904; Gray, 1908a, b; Fernandez
8L Schmidt, 1963; Griffiths, 1968, 1978;Jorgensen & Locket, 1995). Manley (1972:
61 1) thought that “the cochlear canals of early mammals, which probably also
contained a lagena macula, were very short e.g. 3-4mm in Triconodon mordux
(Kermack, 1963)”.Although this statement seems likely to be a valid characterization
of the cochlea in early mammals-at least for non-therians-no evidence of a lagena
in Triconodon is actually known, nor has any structure that suggests its presence been
previously found in Morganucodon (Graybeal et al., 1989), Sinoconodon (Luo et al., 1995),
or any other early mammals. Accordingly, it is of great interest that the X-radiograph
of at least one of our multituberculate specimens (UALVP 26039) unambiguously
displays an inflated terminus of the cochlear canal, comparable to that of monotremes.
\Ye believe that this structure provides the first evidence of the lagena in mammals
other than monotremes; no other realistic interpretation of the structure suggests
itself. The other specimens (UALVP 34144, 26037) do not show a terminus that is
expanded to the same degree, but while the distal end of the canal ends abruptly
in these specimens, at a rounded tip, it is nonetheless slightly expanded relative to
thc proximally adjacent parts of the canal. Previous studies (Luo & Ketten, 1991:
fig. 3) have indicated that distally the cochlear canal narrows, rather than expands,
in certain multituberculates as well as in monotremes; therefore, if a lagena was
actually present in these multituberculates, it is either not reflected osseously by an
inflated cochlear terminus or the method of reconstruction of the canal based on
serial sections has been too coarse to capture details of its actual shape.
INNER EAR OF MULTITUBERCULATES
279
PHYLOGENETIC IMPLICATIONS
At present, no consensus concerning the phylogenetic position of multituberculates
exists among specialists who have recently concerned themselves with the question
(Kemp, 1983; Miao, 1988, 1991; Rowe, 1988, 1993; Wible, 1991; Kielan-Jaworowska, 1992; Sereno & McKenna, 1995). Postcranial resemblances have been
cited in support of a multituberculate-therian sister-group relationship on the one
hand (but see Kielan-Jaworowska & Gambaryan [1994] for an alternative), whereas
dental features have been invoked in support of a monotreme-therian sister-group
relationship to the exclusion of multituberculates on the other (Archer et al., 1985).
As a further complicating factor, the monotreme-multituberculate affinities originally
suggested by Broom (1914), and then elaborated on by Kermack & KielanJaworowska (1971) from resemblances in structure of the braincase, have gained
renewed support from recent work (Hopson & Rougier, 1993; Wible & Hopson,
1993; Meng & Wyss, 1995). Given this current diversity of opinion, which stems
ultimately from different speculations about which morphological similarities are
homologous and which are homoplasious in the absence of a definitive fossil record
connecting multituberculates to other mammals, the relationships for multituberculates remain unresolved (Rougier et al., 1992; Wible et al., 1995). It is in
this context that we discuss the phylogenetic implications of two features of the
multituberculate ear examined in our study, the curvature of the cochlea and the
inflation of the vestibule, that previous authors have concluded were informative in
determining the relationships of multituberculates.
The configuration of the cochlea is a character sometimes thought to be important
in determining the interrelationships of the major mammalian lineages. A cochlea
having a curvature of greater than 180” has been cited as support for the hypothesis
that monotremes and therians are sister-groups (Luo & Ketten, 199l), or as a trait
that is at least consistent with a monotreme-multituberculate-therianclade (Rowe,
1988). However, either a reversal in multituberculates to a short, uncoiled cochlea
is required by Rowe’s analysis, or coiling of the cochlea in monotremes and higher
therians is not homologous, the latter evidently being Rowe’s preference p.Rowe,
pers. comm. in Luo & Ketten, 1991: 2251; and see below). Unexpectedly, and in
contrast to the conclusions of previous workers (e.g. Luo & Ketten, 1991), our study
shows that the osseous cochlear canal of Ornithorhynchus is in fact less curved than
that of Tachyglussus (Fig. G), while at the same time it is not significantly more curved
than that in at least some multituberculates (compare e.g. Figs 2 and 6). Given that
the inner ear of early monotremes (Archer et al., 1985, 1992; Pascual et al., 1992;
Flannery et al., 1995) and that of therians more primitive than Encelestes is unknown,
we caution that the curvature of the cochlear canal may be an unreliable character
for determination of phylogenetic relationships between these groups. Furthermore,
from the evidence of a lagena-like expansion of the cochlear canal in the multituberculate petrosals described above, the absence ofa lagena can not be interpreted
either as a derived feature uniting all multituberculates or linking multituberculates
with other mammals that lack a lagena. By contrast, the cribriform passage for the
cochlear nerve in monotremes is a condition anatomically more similar to the
therian pattern than to that in multituberculates, although it is preceded by a “more
united foramen” ontogenetically in monotremes (Simpson, 1938: 1 l), and hence,
may not be homologous to the pattern in therians.
The peculiar curvature of the cochlear duct in Ornithurhynchusas discussed by Luo
280
R. C. FOX Ah’D J. MENG
& Ketten (1991) raises the question as to whether the curvature is homologous to
the coiling in therians (Zeller, 1989), especially since the duct in Tuc’achyglossusis not
curved the same way as has been purported for that in Ornithorhynchus, while the
duct in therians always coils in correspondence with the osseous cochlear canal
(Gray, 1908a, b; Fernandez & Schmidt, 1963; Lewis et al., 1985). From these
differences, we conclude that curvature of the cochlear duct in Omithorhynchus is
unlikely a precursor of the coiled duct in therians, and that, instead, the monotreme
condition is apomorphous, and hence not validly invoked as support of monotremetherian relationships. In addition, our X-radiographs indicate that the diameter of
the cochlear canal in neither Ornithorhynchus nor Tachyglossus changes substantially
along its length proximal to the lagenar expansion, contrary to Luo & Ketten (1 99 1:
fig. 3). The 270” bend of the cochlear duct within the narrow osseous canal in
Ornithorhynchus, as observed by Luo & Ketten, is abrupt, an unexpected configuration
for a hearing function that is dependent on vibrations of the basilar membrane.
The question of the propagation of travelling waves along a basilar membrane
having these properties remains unanswered; no comparable pattern is known in
other vertebrates (Wever, 1978, 1985; Lewis et al., 1985; Manley, 1990).
The second feature of the petrosal sometimes thought to be significant in
determining the relationships of multituberculates-inflation of the vestibuleappears from our study to be a derived state, occurring only in some advanced
species, and hence not indicative of monophyly of the order. This conclusion is
strengthened by its agreement with the size distribution of the vestibule in more
primitive mammals and in their therapsid predecessors. Although Luo & Ketten
(1991: 226), citing earlier work (Olson, 1944; Quiroga, 1979; Bellairs & Kamal,
1981; Allin, 1986), observed that the vestibule in therapsids and diapsid reptiles is
relatively small, this comparison is valid only when it is made with those advanced
multituberculates in which the vestibule is clearly inflated. Furthermore, it need be
remembered that the size of the vestibule in therapsids relative to that in mammals
(including Morganucodon, early multituberculates, monotremes and therians) is unknown; no broad-spectrum comparisons of this kind have yet been undertaken. The
vestibule in primitive synapsids has been characterized as ‘very large’, but its apparent
size in these groups may be misleading, at least in part as the vestibule was probably
lined with ‘substantial amounts’ of cartilage in life, a tissue that is not normally
preserved by the processes of fossilization (Allin & Hopson, 1992: 606). Similarly,
the apparent confluence of the cavity of the horizontal semicircular canal with the
vestibule in these animals may be only an artifact of the failure of cartilage lining
the vestibular walls to fossilize (Allin & Hopson, 1992: 606).
A different view of the significance of vestibular size to the analysis of early
mammalian interrelationships was furnished by Gray (1 908a: 520), in comparing
monotremes and extant reptiles: “In one respect, however, the vestibule of the
echidna’s labyrinth is distinctly more like that of mammals than that of at least the
majority of reptiles. Its size, relative to the rest of the organ, is small, whereas in
reptiles the vestibule is frequently the bulkiest portion of the whole labyrinth and
occupies almost all the space contained by the planes of the three canals”. In this
perspective, the vestibule of Morgunucodon is mammal-like in its small size (Graybeal
ef d.,
1989; Luo & Ketten, 1991) and in its freedom from the semicircular canals
except at their terminal openings. A recent reconstruction of the endocast of the
inner ear from serial sections indicates that the vestibule in Sinoconodon is similar to
that in Morgunucodon in these regards (Luo et al., 1995). Consequently, if a small
INNER EAR OF MULTITUBERCULATES
28 1
vestibule and free semicircular canals are mammalian characters and Sinoconodon
plus Morganucodon comprise the outgroup of multituberculates, monotremes and
therians, two distributional patterns of vestibular morphology suggest themselves:
first, the vestibule in multituberculates evolved from a small, uninflated ancestral
state, as exemplified by Sinoconodon and Morganucodon, implying that the common
ancestry of multituberculates, monotremes and therians had a small, uninflated
vestibule, as well. Alternatively, the small, uninflated vestibule of monotremes and
therians is the consequence of a reversal from an inflated vestibule in the predecessors
of these two clades-either in their immediate common ancestry, if monotremes
and therians are sister-groups (a relationship that from present' evidence seems
unlikely; see e.g. Flannery et al., 1995), or at a more remote 'node' in the central
mammalian stem, or in the therapsid ancestors of mammals. We conclude that an
uninflated, Morganucodon-like vestibule marked the earliest mammals and was retained
in the earliest multituberculates-this is the more realistic hypothesis biologically
(functionally), and is in keeping with our earlier argument from different evidence
that an inflated vestibule is a uniquely derived feature only for one or more subgroups
within the Multituberculata.
Figure 11 summarizes the distributions of inner ear features, based on this and
our previous studies. We have found no derived characters of the inner ear that
indicate a preferred position of multituberculates among mammals nor that ally
monotremes with therians. In light of the evidence presented in this paper, several
derived conditions of monotremes, such as a curved cochlear canal of up to 180°,
a cribriform plate for the passage of the cochlear nerve and grooves for the nerve
fibres within the cochlea, are autopomorphies of monotremes. An array of neomorphs
of the inner ear diagnoses the clade of tribosphenic therians, and these document
a distinct morphological gap in the transition from the non-therian to therian ear.
From presently known forms, an intermediate stage is lacking, even if Encelestes
(Rougier et al., 1992) is included.
FUNCTIONAL IMPLICATIONS
Air-conducted hearing in multituberculates
We have already speculated on hearing abilities in Late Cretaceous therians
(Meng & Fox, 199513) using regression equations derived from acoustical data in
living mammals (Manley, 1971, 1972; West, 1985; Rosowski & Graybeal, 1991;
Rosowski, 1992). We applied these equations to data from fossils, following the
rationale that inner ear structures in the extinct therians that we studied are virtually
identical to those of their extant relatives and would have imposed similar constraints
on function in Late Cretaceous species. The inner ear structures that are of greatest
interest in these comparisons are discussed elsewhere (Meng & Fox, 1993, 1995a,
b) and listed in Figure 11.
Owing to differences in anatomy, there is no basis for applying the equations that
are applicable to the inner ear in therians to the numeric data from the petrosals
of multituberculates and other early non-therian mammals. It is certain that at least
some of the unique features of the therian ear play important roles in the high
frequency hearing that is universal in therians and that is already indicated in
Late Cretaceous species. For example, the basilar membrane in Late Cretaceous
R. C. FOX AND J. hlENG
Figure 1 1. Cladogram depicting distribution of inner ear features in selected mammalian p u p s . 1.
S o inner ear feature diagnoses this node given the position of multituberculates; threr ear ossicles
may he characteristic. 2, Independent osseous aqueductus cochleae (Rougier et al., 1992). 3, A lullp
coiled cochlrar canal, reduction of the lagena, development of primary and secondary osseous spiral
laminae, development of the modiolus, a perilymphatic recess that merges with the scala tympani of
the cochlea, a radial pattern of the cochlear nerve, and a narrow, elongate basilar nienihranc that is
supported by the osseous spiral laminae and that extends from the inner surface of the bony hridgc
between the fencstra cochleae and fenestra vestibuli (5leng & Fox, 1993, 1995a, h). 4, A nearly 180"
cull-rd cochlea, a cribriform plate for the passage of the cochlear nerve in the internal acoustic meatus.
and grooves for the branched cochlear nerve within the cochlea. 5, S o inner ear synapomorphp: an
inflatcd vestibule occurs in subgroups of this clade. Sce text for discussion.
marsupials and placentals was supported by rigid osseous spiral laminae and was
narrow (Meng & Fox, 1995a, b). The presence of the secondary osseous spiral
lamina in extant terrestrial therians implies a high frequency ear (Reysenbach de
Haan, 1956; Hinchclfie & Pye, 1969; Sales & Pye, 1974; Ketten, 1992), while a
narrow basilar membrane is also a likely correlate of high-frequency hearing (hlanlq .
1971, 1972; Ketten, 1992). Unfortunately, the width of the basilar membrane in
rnultituberculates and other early non-therians cannot be determined from direct
evidmce, because neither a rigid osseous frame nor evidence of cartilaginous
structures arising from the walls of the cochlear canal as support for the membrane arc
preserved in these species. However, the lack of such structures in multituberculates
suggests that the basilar membrane was wider than in therians having cochleae
otherwise of the same diameter and/or supported by a relatively flexible franc of
cartilage; hence the multituberculate ear was less well adapted to high-frequency
hearing.
Other than in its lack of a cribriform plate in the internal acoustic meatus and
grooves within the cochlea for the cochlear nerve, the inner ear of multitubcrculates
in its overall anatomy is most comparable of that of monotremes. Unfortunately,
little is known about the relationship between the configuration of the inner ear and
hearing ability in either the platypus or echidnas. What is known from previous
work on monotreme hearing function implies that the ear in these animals is
relatively inefficient in sensing airborne vibrations, and that consequently monotremes
occupy an intermediate level in hearing ability between extant reptiles and other
mammals (Aitkin &Johnstone, 1972; Gates et al., 1974). From present knowledge
of petrosal anatomy, it seems likely that the ability to hear airborne sounds in
INNER EAR OF MULTITUBERCUL4TES
283
multituberculates and other early mammals having a straight or nearly straight
cochlea was no better than that of living monotremes.
In addition to the lack of osseous cochlear laminae, two other features may have
influenced the hearing ability of multituberculates: the inflated vestibule and the
length of the cochlear canal. Based on comparison with certain extant amphibians
and turtles (Patterson, 1960; Bramble, 1982; Lewis & Narins, 1985; Wever, 1985)
that have an enlarged vestibule and are sensitive to low frequency sounds, Luo &
Ketten (1991: 226) concluded that the enlargement of the vestibular space in
multituberculates was probably indicative of adaptation to low frequency hearing.
We agree with this conclusion, but we approach the subject not from a comparison
with non-mammalian tetrapods but from the perspective of functional morphology.
In this context, the acoustical phenomena demonstrated by the experiments and
models of Bkktsy (1 960) are crucial: these show that since high frequency vibrations
dissipate rapidly with distance, they are sensed at the proximal part of the basilar
membrane, near the footplate of the stapes, whereas low frequency vibrations are
sensed more distally, towards the apex. This tonotopic organization is found not
only in mammals but is also generally applicable to birds and reptiles, excepting
only squamates (Manley, 1990). The distribution of frequencies along the basilar
membrane is also reflected in an orderly projection of the auditory nerve fibres on
the brain nuclei, as demonstrated in mammals (Sando, 1965). Apparently, the
distance from the stapes to the basilar membrane is one of the factors affecting
frequency limits sensed by mammals (Btktsy, 1960). In multituberculates, and
probably in other early mammals that lacked osseous laminae, the basilar membrane
failed to extend proximally to the inner surface of the bony bridge between the
fenestra vestibuli and fenestra cochleae, thereby failing to approach the footplate of
the stapes closely. This pattern contrasts with the condition in Late Cretaceous
marsupials and placentals in which the basilar membrane extended to the bridge,
as indicated by the presence of the secondary osseous spiral lamina there (Meng &
Fox, 1995a, b).
In those multituberculates in which the vestibule is inflated, the gap between the
fenestra vestibuli and the most proximal part of the basilar membrane may be
further increased as a consequence of vestibular inflation. An extreme example of
this pattern is seen in Lumbdopsalis (Meng, 1988; Meng & Wyss, 1995): the fenestra
vestibuli is positioned relatively far from the entrance to the cochlear canal simply
as a consequence of the greatly inflated vestibule. In fact, the distance from the
fenestra to the canal in Lambdopsalis is equal to the total length of the canal itself
(pers. observ.). In this case, it seems likely that high-frequency vibrations could easily
have been dissipated before they were able to activate the basilar membrane.
In living mammals, the cochlea is the major acoustic organ, whereas the vestibule
(containing the sacculus and the utriculus) is primarily concerned with balance
sensitivity (Wilson & Melvill Jones, 1979; Stebbins, 1983: 55; Lewis et al., 1985: 82).
In the evolution of tetrapods from amphibians to mammals, the auditory papilla
(precursor to the basilar membrane) increased substantially in length, with a
corresponding increase in the number of hair cells (Wever, 1974: 450). Manley
(1972: 616) recognized the adaptive significance of these changes, noting that
“animals with short membranes are less sensitive to sound, a phenomenon which
may be partly due to their possessing only a small number of hair cells”. If elongation
of the cochlea approximates elongation of the basilar membrane (and we assume it
does), a longer membrane would obviously support more hair cells within it, with
28.1
R. C. FOX ANDJ. MEN(;
the effect of both increasing the range in frequency of sounds that an organism can
receive (Manley, 197 1, 1972; Wever, 1974) and enhancing the ability to discriminate
between frequencies within that greater range (Manley, 1972; Allin & Hopson,
1992). It must be pointed out, however, that a short cochlea does not in all
cases imply low frequency hearing: some investigations have revealed an inverse
relationship between basilar-membrane length and high-frequency hearing, i.e.
certain eutherian mammals with the shortest basilar membrane are most sensitive
to high frequency sounds (West, 1985).
The cochlear canal in multituberculates is among the longest in early mammals
(Luo & Ketten, 1991; Luo et al., 1995), but it is still considerably shorter than that
in therians of the sarhe body size (Keen, 1940; Bkkksy, 1944, 1960; Schuknecht,
1953; Manley, 1971, 1972; West, 1985; Rosowski & Graybeal, 1991; Fay, 1992:
Ketten, 1992; Meng & Fox, 1995a, b). In retaining a relatively short, straight.
cochlear canal, the ear of multituberculates not only resembles that in other known
primitive mammals (Sznoconodon, Morganucodon, monotremes), but it also resembles
those of living reptiles and birds; consequently, it is a reasonable conclusion that
multituberculates were capable of hearing only lower frequency airborne sounds in
a narrower frequency range than therian mammals, resembling in that respect living
monotremes and non-mammalian amniotes. The ear in multituberculates could
have been as sensitive to airborne sounds as that of monotremes but less so than
that of therians.
Bone-conducted hearing in multituberculates
The inflated vestibule is such a conspicuous aspect of petrosal structure in those
multituberculates in which it occurs, it must have had some special function. We
are in agreement with other authors who have concluded that inflation of the
vestibule is likely an adaptation for low frequency and bone-conducted hearing
(Miao, 1988; Luo & Ketten, 1991). This hypothesis is consistent with the assumed
fossorial life of some multituberculates (Miao, 1988; Kielan-Jaworowska, 1 989:
Kielan-Jaworowska & Qi, 1990; Luo & Ketten, 1991), as well as with the relatively
massive ear bones of Lambdopsalis (Miao & Lillegraven, 1986; Meng, 1992; Meng &
Wyss, 1995). Most mammals, including man, are capable of bone-conducted hearing
(see e.g. Wever & Lawrence, 1954; Bkkesy, 1960). According to Bkkksy (1960),
vibrations picked by the bones of the ear can be roughly resolved into parallel,
compressional and rotational components affecting the cochlea and middle ear. If
an asymmetry is present between the volume of the scala tympani and scala vestibuli.
i.e. the space of the scala vestibuli is larger than that of the scala tympani, parallel
and compressional vibrations can produce a significant displacement of fluid near
the stapes, which causes disturbance of the basilar membrane (Fig. 12). If inflation
of the vestibule, as in some multituberculates, greatly increases the space between
the footplate of the stapes and the scala vestibuli, then bone-conducted hearing may
become necessary. It may well have been the case that some multituberculates,
namely those in which the vestibule was greatly enlarged, were more highly adapted
to bone-conducted hearing than for the reception of airborne sounds.
It is well known that bone can transmit high frequency vibrations effecti\Tely
(Bkkesy, 1960). For example, the human ear responds to airborne sounds only up
to 20kc./s. in frequency, but the inner ear can sense sounds up to lOOkc./s.,
although different frequencies higher than 15 kc./s. cannot be readily distinguished
INNER EAR OF MULTITUBERCULATES
285
c
.Stap
h
Round
.-
A
B
Figure 12. Diagrams showing two patterns of bone-conducted hearing. A, the cochlea under parallel
vibrations; and B, the cochlea under compressional vibrations (after Wever & Lawrence, 1954; Btkksy,
1960). See text for discussion.
(Pumphrey, 1950). Whether high frequency bone-conducted vibrations are audible
as sound depends in part on the structure and physiology of sound-receiving and
transmitting soft tissues of the inner ear, as well as those of the brain, none of which
are preserved as fossils. Hence, it is uncertain whether high frequency vibrations
transmitted by bone-conduction could have been sensed as sound in multituberculates
if only because the inner ear of multituberculates is significantly different in structure
from that of therians, and of course nothing is known of multituberculate auditory
physiology.
ACKNOWLEDGEMENTS
We thank the field parties from the University of Alberta who assisted in collecting
the samples that contained the multituberculate specimens described here. Mrs A.
Voss, UALVP, sorted the screened concentrates from Bug Creek; L.A. Lindoe
constructed the latex endocast of the vestibule of UALVP 26039; G.D. Braybrook
prepared the SEM photographs. We thank R.D.E. MacPhee, Department of
Mammalogy, and R.H. Tedford, M.C. McKenna, MJ. Novacek and G.W. Rougier,
Department of Vertebrate Paleontology, the American Museum of Natural History,
for permission to study monotreme specimens and for access to the Khoobur petrosal
specimens under their care. The manuscript was improved with comments from
two anonymous reviewers, to whom we extend our thanks. Approximately 60% of
financial support for research by RCF on Cretaceous and early Tertiary mammals
is provided by Natural Science and Engineering Research Council (NSERC) of
Canada operating grants to him. During the course of this study, Meng has been
supported by a felldwship from NSERC, the Frick Postdoctoral Fellowship from
the AMNH and an NSF grant (DEB-9508685).
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