Download Osseous inner ear structures and hearing in early

ZoologicalJournal of the Linnean Society (1995), 115: 47-71. With 6 figures
Osseous inner ear structures and hearing in
early marsupials and placentals
JIN MENG* AND RICHARD C. FOX
Laboratory for Vertebrate Paleontology, Departments of Geolog and Zoology, University
of Alberta, Edmonton, Alberta, Canada T6G 2E9
ReceiuedJuly 1994, acceptedfor publication December 7994
Based on the internal anatomy of petrosal bones as shown in radiographs and scanning
electron microscopy, the inner ear structures of Late Cretaceous marsupials and placentals
(about 65 Myr ago) from the Bug Creek Anthills locality of Montana, USA, are described.
The inner ears of Late Cretaceous marsupials and placentals are similar to each other in
having the following tribosphenic therian synapomorphies: a fully coiled cochlea, primary
and secondary osseous spiral laminae, the perilymphatic recess merging with the scala tympani
of the cochlea, an aqueductus cochleae, a true fenestra cochleae, a radial pattern of the
cochlear nerve and an elongate basilar membrane extending to the region between the
fenestra vestibuli and fenestra cochleae. The inner ear structures of living therians differ from
those of their Late Cretaceous relatives mainly in having a greater number of spiral turns of
the cochlea and a longer basilar membrane. Functionally, a coiled cochlea not only permits
the development of an elongate basilar membrane within a restricted space in the skull but
also allows a centralized nerve system to innervate the elongate basilar membrane. Qualitative
and quantitative analyses show that, with a typical therian inner ear, Late Cretaceous
marsupials and placentals were probably capable of high-frequency hearing.
0 1995 The Linnean Society of London
ADDITIONAL KEY WORDS:-Late
Cretaceous - America
-
Theria - anatomy.
CONTENTS
Introduction . . . . . . .
Material and methods . . . . .
Abbreviations . . . . . . .
Description . . . . . . .
Placental ears . . . . . .
Marsupial ears
. . . . .
Discussion
. . . . . . .
Identification of specimens
. .
Anatomical features . . . .
Hearing in early therian mammals .
Conclusions . . . . . . .
Acknowledgements . . . . .
References
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* Correspondence toJin Meng, present address: Department of Vertebrate Paleontology,American Museum
of Natural History, New York, NY 10024, U.S.A.
0024-4082/95/090047+25 $12.00/0
4.1
0 1995 The Linnean Society of London
JIN MENG AND K.C. FOX
INTRODUCTION
Living marsupials and placentals are anatomically similar in the cytological
architecture of the cochlea, making independent acquisition of the coiled cochlea
in these two groups unlikely (Fernandez & Schmidt, 1963).When rephrased in a
phylogenetic context, Ferniindez and Schmidt’s hypothesis implies that living
marsupials and placentals share a common ancestor that already had a fully coiled
cochlea. Other research implies that high-frequency hearing is primitive for therian
mammals, because primitive living therians, such as the opossum, tree shrew, and
hedgehog, can readily hear high-frequency sounds (Heffner, Ravizza & Masterton,
1969; Masterton, Heffner & Ravizza, 1969; Ravizza, Heffner & Masterton, 1969a,
1Y69b). Obviously, these conclusions are based exclusively on the anatomy of the
ear and the demonstrated capacity of hearing in living forms. However, until now,
little supporting evidence from the fossil record of early therian mammals has
been available. From these considerations, two questions arise about the otic
structures and hearing ability in early therian mammals: (1) Are the inner ear
structures of early marsupials and placentals as similar as they are in their living
relatives, so that Fernandez and Schmidt’s neontologically based hypothesis still
holds? (2) Is it valid to infer characteristics of hearing in early therian mammals
from morpholog~calevidence in fossils? With regard to the evolution of the therian
ear, a third question can also be asked: are there significant anatomical differences
in the inner ear between early marsupials and placentals on the one hand and
their Recent relatives on the other?
In this paper, we describe structures of the inner ear of Late Cretaceous
placentals and marsupials (from about 65 Myr ago). Although therian petrosals of
the same age have been previously documented (MacIntyre, 1972; Archibald,
1979; Wible, 1990),the internal anatomy of these bones was only briefly described
in MacIntyre’s paper. Our descriptions are based on nearly complete and partially
broken petrosals that allow direct observation of their external and internal
architecture; we also have employed scanning electron microscopy and
radiography to enhance our observations. These specimens represent the earliest
known inner ear structures in placentals and the second earliest in marsupials,
next only to specimens from the Oldman Formation of Alberta studied by Matthew
(1916)and recently by us (Meng & Fox, 1995); they are, however, among the best
preserved petrosals of both groups from the Late Cretaceous known to date. By
describing the specimens in detail, we attempt to provide a primitive morphotype
of the inner ear for marsupials and placentals. This in turn will serve as the grounds
for establishing character polarities of the inner ear within therians and for testing
previous hypotheses on therian phylogeny and the evolution of hearing.
MATERIAL AND METHODS
Specimens studied are housed in the Laboratory for Vertebrate Paleontology,
University of Alberta, and are listed in Table 1. These specimens were collected
from the Late Cretaceous Hell Creek Formation at the Bug Creek Anthills locality
(Sloan & Van Valen, 1965), Montana, by field parties from the University of
Alberta during the 1970s. Radiography and scanning electron microscopy (SEM)
were employed for observation of those features that are not available by ordinary
light microscopy. The radiographs were obtained using the Radiographic-
HEARING OF EARLY THERIANS
49
TABLE1. Measurements (mm) of specimens studied. A, number of spirals; B, length of
cochlea; C, long axis of round window; D, short axis of round window; E, long axis of
oval window; F, short axis of oval window; G, diameter of crus commune; H, diameter of
semicircular canal; I, radius of the loop of the lateral semicircular canal; J, radius of the
basal coil; K, widths of vestibular fissure (basal-apical).Asterisk indicates measurement from
radiograph. No dimension is measurable in UALVP 26033, 26038 and 34153
A
B
C
D
E
F
G
H
I
Placentals
UALVP 26033
UALVP 26038
UALVP 26041
UALVP 26042
UALVP 26043
UALVP 26044
UALVP 26045
UALVP 26046
UALVP 34149
UALVP 34150
UALVP 34151
UALVP 34152
UALVP 34153
Marsupials
UALVP 26040
UALVP 34154
J
K
-....
~~~
1.5
0.8
0.49
0.81
0.33
0.32
0.08-0.37
0.09- ?
0.21
1.5
1.5
1.5
1.5
7.1
6.7* 1.03 0.62
7.4
0.83 0.38
0.76
0.84
0.79
1.5
0.85
0.59
0.81
0.36
0.35
0.33
0.33
0.36
0.84
0.4
0.38
0.44
0.21
0.21
0.62
0.47
0.35
0.22 1.5*
1.5
7.3
1.5
5.8* 0.66
1.5
5.8
0.47
0.37
0.38
0.41
0.38
~
2.3
0.21 1.75*
0.2
0.2
0.2 1
1.52
2.3 0.08 - 0.34
0.08 - ?
0.09 - ?
2.0*
2.0
Fluoroscopic Inspection System and Ready Pack I1 Kodak Industrex M Film. The
tympanic side of each specimen was placed against the film to achieve the best
image of the cochlea. The SEM photographs were taken from uncoated specimens,
except in one instance (Fig. 1C).
Measurements, where possible, were made of the following dimensions: spiral
turns (one full turn = 360" coil), length of the cochlear canal, widths of the
vestibular fissure (Fig. 1) at the basal and apical regions, diameters of the fenestra
vestibuli and the fenestra cochleae, diameter of the semicircular canals, radius of
the loop of the lateral semicircular canal, and the maximal radius of the spiral.
The spiral turns of the cochlea were counted following the method of West (1985),
in which the starting point of the cochlear canal is at the inflection anterior to the
fenestra cochleae, where the cochlear duct begins its spiral course. The length of
the cochlea is measured along its longitudinal course close to the outer wall, which
approximates the length of the basilar membrane as the latter is positioned closer
to the outer than to the inner wall of the cochlea. The widths of the vestibular
fissure are used to approximate those of the basilar membrane. Because of erosion
of bone during preservation, the vestibular fissure is likely wider than it was in life,
and this is especially so in its apical section, for the osseous spiral laminae are
thinner and weaker there. The diameter of the semicircular canals is the average
of measurements of available canals in each specimen. All measurements (Table
1) were made with the Reflex Microscope (Reflex Measurements LTD), directly
from the specimens three-dimensionally and from the radiographs twodimensionally; therefore, those from the radiographs may be slightly smaller than
actual size. The 2 x magnification setting and the 5 pm mark were used in
measuring specimens. In describing petrosals, we follow the terminology of Gray
(1959), MacIntyre (1972), and Wible (1990). For orientation, the apex of the
50
JIN MENG AND R. C. FOX
Figure 1. Tympanic sides of incomplete pIacental petrosds (A, UALVP 2604-5; B, UALVP
2fiO1.3, left side) from the Late Cretaceous Hell Creek Formation at Bug Creek Anthills,
Montana. Scale bar = 1 rnm. See abbreviations for key.
promontorium is referred to as the anterior side of an isolated petrosal, the cranial
side as the dorsal, and the tympanic side as the ventral.
ABBREVIATIONS
aa
ac
acs
anterior ampulla
apex of the cochlea
area cribrosa superior
HEARING OF EARLY THERIANS
aqc
asc
bcc
cc
cac
COC
cs
cv
er
fac
fc
fi
fsm
fv
hF
iam
la
lhv
lsc
m
osl
Pa
PSC
rs
scm
sf
sPr
ssl
st
sv
tsf
vav
vf
VP
51
aqueductus cochleae
anterior semicircular canal
basal cochlear canal
crus commune
cochlear orifice of the aqueductus cochleae
cochlear canal
cavum supracochleae
crista vestibuli
epitympanic recess
facial canal
fenestra cochleae
fossa incudis
fossa for the stapedius muscle
fenestra vestibuli
hiatus Fallopii
internal acoustic meatus
lateral ampulla
canal for lateral head vein
lateral semicircular canal
modiolus
primary osseous spiral lamina
posterior ampulla
posterior semicircular canal
recessus sphericus
spiral canal of the modiolus
subarcuate fossa
cone-shaped swelling for the perilymphatic recess
secondary osseous spiral lamina
scala tympani
scala vestibuli
tractus spiralis foraminosus
vestibular orifice of the aqueductus vestibuli
vestibular fissure
vestibule proper
DESCRIPTION
Placental ears
Vestibule
The osseous labyrinth consists of a series of cavities within the petrosal, including
the vestibule, semicircular canals and cochlear canal (Figs 1 & 2). In several
specimens (UALVP 26033, 26042, 34149, 34151), the promontorium of the
petrosal is broken through the middle of the fenestravestibuli,the fenestra cochleae
and the internal acoustic meatus, exposing most of the vestibule. In other
specimens (26045 [Fig. IA], UALVP 26043 [Fig. lB], 34152), the ventral shell of
the promontorium has been worn away to a variable extent, exposing the vestibule
and the cochlear canal in ventral view. In life, the vestibule contains two sacs of
52
JIN MENG AND R. C. FOX
Figure 2. Cross-section of a placental cochlea (A, UALVP 34150, right side) and a part of
the osseous spiral lamina showing the orifices for the auditory nerve dendrites (B, part of
CALVP 2(i043'1. Scale bar = 1 mm in A and 1200 pm in B.
the membranous labyrinth, the utriculus and sacculus. By virtue of its position, the
vestibule in the Bug Creek placental petrosals occupies the central part of the
osseous labyrinth, and it communicates with the cochlear canal anteriorly and the
semicircular canals posteriorly (Figs lB, 3A & C). Although irregular in shape, the
vestibule roughly consists of an ovoid central space together with the ampullae,
which are distal to the central space. The central space narrows at its two ends,
which are confluent with the inflated ampullae. For convenience, we refer to the
central space between the two narrowed regions as the vestibule proper. The
fenestra vestibuli opens at its lateroventral side. On the medial side of the vestibule
HEARING OF EARLY THERIANS
c
53
D
Figure 3. Radiographs of placental (A, UALVP 26044) and marsupial (B, UALVP 26040)
petrosals (both left side, images photographically reversed) from the Late Cretaceous Hell
Creek Formation at Bug Creek Anthills, Montana, and reconstructions of the osseous labyrinth
of A (C) and B (D). In A and B, the anterior and posterior semicircular canals are partially
broken. Scale bar = 1 mm.
proper are the posterior ampulla and the crus commune (Figs lB, 3). The posterior
ampulla is the most medial space in the vestibule; it narrows posteriorly to give
rise to the posterior semicircular canal. A single, small foramen that transmitted a
branch of the vestibular nerve to the posterior ampulla opens near the anterior
wall of the posterior ampulla. This foramen can be traced through a short canal to
the internal acoustic meatus on the cerebellar side, where it is called the foramen
singulare. However, the two openings of the canal are invisible in the views
illustrated. Dorsomedial to the posterior ampulla, a large, circular crus commune
opens in the dorsal roof of the vestibule. There is no sharp boundary between the
posterior ampulla and the crus commune. Still medial to the crus commune, a low
ridge running nearly vertically on the anterior wall of the vestibule marks the
narrowed region between the vestibule proper and the space for the posterior
51
JIN MENG AND R.C. FOX
ampulla and crus commune (Fig. 1B).At the dorsal end of the ridge and lateral to
it opens the vestibular orifice of the aqueductus vestibuli, which transmitted the
ductus endolymphaticus in life. MacIntyre (1972) did not identify this structure in
his specimens. In addition, we found in several specimens a small foramen
posterior to the orifice of the aqueductus vestibuli; we believe it to be a separate
opening for the artery or vein or both that travelled with the ductus
endolymphaticus. In UALVP 26042, part of the bone on the cerebellar side of
the petrosal is transparent, and the aqueductus vestibuli can be seen extending
posteriorly and crossing over the crus commune. The cranial orifice of the
aqueductus vestibuli opens at the medial side of the crus commune at the position
where the latter bifurcates into the anterior and posterior semicircular canals. The
opening is dorsally sheltered by a lip-like bony projection, which is complete in
UALVP 34 150 but damaged in all other specimens.
In the vestibule proper, the space occupied by the saccule is termed the recessus
sphericus; it is a shallow, oval fossa in the anterior wall of the vestibule proper
(Fig. IB). Dorsomedially, the fossa terminates at the vestibular orifice of the
aqueductus vestibuli, while anteromedially, it connects with the base of the
cochlear canal. The dorsolateral side of the fossa is separated from the space for
the utricle by a faint, oblique ridge, presumably the crista vestibuli (Fig. 1B). We
were not able to locate a foramen or a cribriform area in the recessus sphericus
for passage of the vestibular nerve to the saccule. The utricle, located on the
posterodorsal side of the crista vestibuli, must have had an elongate shape and
was larger than the saccule. At the anterolateral end of the space for the utricle
and on the lateral side of the anterior crista vestibuli is a cribriform area that
permitted passage of the vestibular nerve to the utricle and to the anterior and
lateral ampullae. This cribriform area leads into a canal that also conveyed the
facial nerve within the internal acoustic meatus on the cerebellar side of the
petrosal (Fig. 2A). Lateral to the cribriform area, a blunt ridge on the roof of the
vestibule separates the vestibule proper from the anterior and lateral ampullae.
Both anterior and lateral ampullae are bell-shaped and narrow distally to give rise
to the semicircular canals (Fig. 3 ) .
Semicircular canals
The three semicircular canals are generally posterior to the vestibule (Fig. 3).
The canals have a much smaller diameter than the ampullae and each forms part
of an oval loop. The anterior canal has the largest loop among the three. A
peculiarity of the canal system is that the ventral end of the posterior canal and
the medial end of the lateral canal merge before joining the posterior ampulla,
meaning that a second common canal is developed (Fig. 3C). Usually the crus
commune, formed by the medial end of the anterior canal and the dorsal end of
the posterior canals, is the only common canal in the inner ear. Because of the
second common canal, the soft semicircular canals possibly open into the utricle
by only four orifices (see Discussion)
The orientation of the semicircular canals in relation to the vestibule as seen in
broken petrosals is sometimes confusing. It is helpful to remember the basic
relationships of these structures. The crus commune is always at the dorsomedial
side of the vestibule and is accompanied by the vestibular orifice of the aqueductus
HEARING OF EARLY THERIANS
55
vestibuli. The twin ampullae (anterior and lateral) are at the lateral side of the
vestibule, with the anterior ampulla the more dorsal. The anterior canal forms
part, usually the posterior part, of the rim of the subarcuate fossa, whereas the
lateral canal surrounds the fossa for the stapedius muscle.
Cochlea
The cochlea lies anterior to the vestibule, and its structures are more complicated
than the structures described above. The cochlea is contained in the promontorium
and coils through about one and a half turns (Figs 1,2,3). The second turn of the
cochlea is separated from the first by a thin bony lamina. The cochlear canal
begins from the medial border of the recessus sphericus, where the vestibule is
confluent with the ventral part of the cochlea, the scala vestibuli. It should be
pointed out that in his description MacIntyre (1972: Fig. 6B) incorrectly reversed
the positions of the scala tympani and scala vestibuli. In the cross-section of the
therian cochlea, the scala tympani is always toward the cerebellar side of the
promontorium, while the scala vestibuli is toward the tympanic side. In primitive
therians, the tympanic side of the promontorium is generally ventral, and the
scala vestibuli is therefore ventral to the scala tympani (Fig. 2A). However, the
orientation of the cochlea may be changed when the number of the cochlear
spirals increases or the braincase inflates. The relative positions of the scalae will
change along with the reorientation of the cochlea.
Two bony laminae that divide the cochlear canal begin at the medial border of
the recessus sphericus: the primary (inner) osseous spiral lamina projects outward
from the medial wall of the cochlea; the secondary (outer) osseous spiral lamina
projects inward initially from the wall that forms the bony bridge between the
fenestra cochleae and fenestra vestibuli and then continues along the outer wall of
the cochlea (Figs 1, 2A). In life, these two laminae partially separate the vestibule
and the scala vestibuli from the scala tympani (Fig. 2A). From their starting
point, the laminae extend ventrally for a short distance and then rapidly curve
ventromedially to a nearly horizontal position anterior to the fenestra cochleae.
Therefore, an inflection of the laminae is formed at their basal part. The two
laminae differ in their height. At the basal part of the cochlea, the primary osseous
spiral lamina is about three times as high as the secondary osseous lamina. The
two laminae are separated by a narrow gap, the vestibular fissure (Fig. 1A). The
vestibular fissure is bridged in life by the basilar membrane, which in turn supports
the organ of Corti containing the auditory receptor cells. The laminae, and the
vestibular fissure as well, wind ventrally along the course of the cochlea from base
to apex, counterclockwise if in the left petrosal, clockwise in the right. The primary
osseous spiral lamina continues to the apex of the cochlea, whereas the secondary
osseous spiral lamina vanishes after a half turn. As they spiral, the laminae decrease
in height. Consequently, the vestibular fissure is very narrow at the base but
gradually widens towards the apex of the cochlea (Table l),a taper in a direction
opposite to that of the cochlear canal.
The osseous spiral laminae nearly divide the cochlear canal into two parts: the
scala vestibuli on the tympanic side and the scala tympani on the cerebellar side
(Fig. 2A). Because the vestibular fissure is filled by the basilar membrane in life,
the scala vestibuli and the scala tympani were separated from each other
throughout, except at the apex, where a small opening, the helicotrema, permits
50
.JIN MENG AND R. C. FOX
communication between the two scalae. The scala tympani communicates with
the middle ear cavity by the fenestra cochleae, which is covered by the secondary
tympanic membrane in life, whereas the scala vestibuli is confluent with the
vestibule and therefore communicates with the fenestra vestibuli, which in life was
closed by the footplate of the stapes. Inside the fenestra cochleae, the roof of the
scala tympani bears a cone-shaped swelling, which is surrounded by a distinct
trench except at its posteromedial side that is continuous with the dorsal edge of
the fenestra cochleae. At the medial end of the trench lies the cochlear orifice of
the aqueductus cochleae. The swollen area is believed to be correspond to the
position for the perilymphatic recess in reptiles and monotremes (Gray, 1908a;
see Discussion).
The osseous spiral laminae differ considerably in their structure. The secondary
osseous spiral lamina is single-layered, with a sharp free edge, and projects slightly
ventrally. The primary osseous spiral lamina, however, can be viewed as consisting
of two layers of bone, of which the lower layer is thicker than the upper. Both
layers merge distally to form the free edge of the lamina. In cross-section, the
primary osseous spiral lamina is Y-shaped, with its two branches joining to the
medial wall of the cochlea to confine a canal that runs along within the primary
osseous spiral lamina from the base to the apex of the cochlea. This canal is the
spiral canal of the modiolus, which in life contained the spiral ganglion of the
auditory nerve cells. The stem of the “Y” is not solid bone; instead, it is penetrated
by numerous radially arranged tubules that transmit the fibres of the auditory
nerve cells to the organ of Corti. In a well-preserved specimen (Fig. lA), a distinct
line near the outer edge of the primary osseous spiral lamina is interpreted as the
original position of the exit for the terminal nerve fibres to the organ of Corti, but
SEM photographs fail to reveal any openings along this line. However, in a
somewhat worn specimen (Fig. 2B), terminal orifices of these tubules are observed
along the outer edge of the primary osseous spiral lamina. These orifices provide
potential evidence for estimating the density of the nerve fibres and number of
hair cells.
The primary osseous spiral lamina coils around the central cone-shaped
structure, the modiolus. In specimens in which the lamina has been broken, the
modiolus can be seen to be penetrated by numerous orifices, the tractus spiralis
foraminosus (Fig. 2A), through which the fibres of the spiral ganglion pass into the
internal acoustic meatus. In conjunction with the tractus spiralis foraminosus, a
cribriform belt is present in the internal acoustic meatus on the cerebellar side of
the petrosal. In other words, the cochlear division of the auditory nerve must
branch into small bundles in order to pass through the petrosal wall.
On the cerebellar side of the petrosal, the deep internal acoustic meatus is
divided into an upper and a lower opening. The upper opening contains the canal
for the facial nerve anteriorly and a circular cribriform area posteriorly (Fig. 2A).
The facial canal can be traced into the ventral side of the tympanic cavity, whereas
the cribriform area shows in the vestibule as mentioned above. This cribriform
area is the area cribrosa superior for the passage of the vestibular nerve to the
utricle and to the anterior and lateral ampullae. In the lower opening, the small
foramen singulare for the passage of the vestibular nerve to the posterior ampulla
is found at the posterior end of the cribriform belt that bears the tractus spiralis
foraminosus. The area cribrosa media, for the nerve to the saccule, is not certainly
identified, but is possibly in the lateral wall of the lower opening.
HEARING OF EARLY THERIANS
57
Figure 4. Tympanic side of a marsupial petrosal (UALVP 34154, right side) from the Late
Cretaceous Hell Creek Formation at Bug Creek Anthills, Montana. Scale bar = 1 mm.
Marsupial ears
In UALVP 26040, no groove for the stapedial artery on the surface of the
promontorium is evident. The fenestra vestibuli is slightly oval and much less
elongate than that in the placental petrosals. In addition, although broken and
considerably worn, a shallow groove posterolateral to the secondary facial foramen
indicates the presence of a short prootic canal. In UALVP 34154 (Fig. 4), the
promontorium is broken at the medial side of the fenestra vestibuli, but a slightly
oval fenestra vestibuli is still recognizable. In this specimen, a narrow and short
prootic canal is present posterolateral to the secondary facial foramen; it opens
posteriorly into a concave area on the squamosal side of the petrosal. This concave
area is likely a part of the sulcus for the prootic sinus. These two petrosals share
features that are different from those of placentals but are similar to those of other
marsupial petrosals from the same locality (Wible, 1990):the hiatus Fallopii opens
at the lateral border of the petrosal, the secondary facial foramen is large, the
stapedius fossa is narrow, and the rim of the fenestra vestibuli is not deeply
socketed.
The structure of the inner ear is directly available from UALVP 34154 in which
the ventral surface of the promontorium has been eroded away so that the vestibule
and the cochlear canal are exposed (Fig. 4). The radiograph helps to outline the
general shape of the inner ear in UALVP 26040. By and large, it appears that the
inner ear structures are similar to those of the ug Creek placentals. They both
have one and a half turns of the cochlear canal and fully developed osseous spiral
laminae. The only significant difference is that a second common canal of the
semicircular canals is absent in the marsupial petrosals. The marsupial petrosals
B
58
JIN MENG AND R. C. FOX
are slightly smaller than the placental petrosals and, therefore, the semicircular
canals and the vestibule are more tightly packed (Fig. 3) and the cochlear canal
shorter (Table 1).
DISCUSSION
IdentiJication of specimens
MacIntyre (1972) described two types of placental petrosals from Bug Creek
that he termed ‘ferungulate’ and ‘unguiculate’, respectively. However, we found it
difficult, following MacIntyre’s criteria, to assign our placental petrosals to either
of the two types; we therefore simply regard them as placental petrosals
collectively. These specimens are believed to be placental because they display
the following external features: (1) the ventral surface of the promontorium is
crossed by distinct grooves for the promontory and the stapedial arteries, although
these are Iikely primitive features in eutherians; (2) the fenestra vestibuli is elliptical
and socketed; (3) the canal for the lateral head vein (Wible & Hopson, 1995) is
absent; (4) the sulcus for the prootic sinus is absent. These features correspond to
those reported in other primitive placental petrosals (MacIntyre, 1972; Archibald,
1979; Wible, 1990). Owing to the thorough description of Late Cretaceous
marsupial petrosals by Wible (1990),the identification of our specimens becomes
easier. The two specimens are from marsupials because of absence of the stapedial
groove, slightly oval fenestra vestibuli and presence of a short, narrow canal for
the lateral head vein. These two petrosals likely belong to Petrosal Type C of
Wible because of a short canal for the greater petrosal nerve, a fairly large hiatus
Fallopii and an epitympanic recess that, while incomplete, appears to have been
narrow.
Anatomical features
Semicircular canals
It is almost a universal pattern in vertebrates that the semicircular canals
communicate with the vestibule by five orifices: the crus commune, the medial
opening of the lateral semicircular canal and the three ampullae (Gray, 1908a, b;
Gray, 1955; Kluge, 1977; Romer & Parsons, 1986; Wever, 1978, 1985; Lewis,
Leverenz & Black, 1985). In this pattern, the lateral semicircular duct joins the
utricle at some point along the posterior limb, or occasionally opens into the crus
commune (Gray, 1955:171). The crus commune is the passage normally shared
by two canals, usually the posterior and anterior canals, before entering the
vestibule. However, variations occur occasionally in the formation of the crus
commune in vertebrates. For instance, in elasmobranchs the posterior canal is
separate and a common duct is formed by the anterior and lateral canals (Baird,
1974; Lewis et a l , 1985). In the Bug Creek placental petrosals, a second common
canal is formed by the lateral and posterior canals, and therefore the bony
semicircular canals open into the vestibule by only four orifices. This condition is
contrary to the reconstruction of the labyrinth by MacIntyre (1972) and is similar
to no other mammals known to us except dogs (Evans & Christensen, 1979). It is
possible that this bony structure indicates a second common canal for the soft
HEARING OF EARLY THEFUANS
59
semicircular canals, but this cannot be surely demonstrated in fossils. Further
survey in living forms may provide useful information.
Perilymphatic recess and fenestra cochleae
Gray (1908a)undertook the first thorough discussion of the relationships of the
aqueductus cochleae, perilymphatic recess and fenestra cochleae among birds,
reptiles and mammals. In reptiles, birds, and monotremes, a distinct perilymphatic
recess (Gray, 1908a),or perilymphatic sac (Romer & Parsons, 1986),is connected
with the scala tympani of the cochleae by virtue of an oval opening, the
perilymphatic foramen. The perilymphatic foramen in the petrosal of
Ornithorhynchus is superficially similar in position to the fenestra cochleae of
therians and is usually called so (but see Zeller, 1989; Wible & Hopson, 1993).
The perilymphatic recess in Ornithorhynchw is contained in an egg-shaped fossa
medial to the perilymphatic foramen. The fossa is medially bounded by a bony
ridge in its full breadth and a groove containing the perilymphatic duct lies at its
anterior side. Similar condition is seen in Tachyglossus except that the perilymphatic
duct lies at the posterior side of the recess (Gray, 1908a). In therians the
perilymphatic recess is entirely enclosed within the fenestra cochleae, and the
perilymphatic foramen between the cochleae and the perilymphatic recess is so
widened that the perilymphatic recess merges with the scala tympani of the
cochlear canal. The position of the perilymphatic recess in therians is represented
by a cone-shapedstructurein the scala tympani of the cochlear canal (Gray, 1908a).
The therian condition has been recorded in the Oldman marsupial petrosals (Meng
& Fox, 1995) and is documented in more detail in the specimens described
herein. The same condition may also exist in Kncelestes, an Early Cretaceous nontribosphenic therian, which already had an independent aqueductus cochleae
(Rougier, Wible & Hopson, 1992). As in Ornithorhynchus, the so-called fenestra
cochleae in primitive mammals, such as Morganucodon(Kermack,Musset & Rigney,
1981), triconodonts (Kermack, 1963), multituberculates (Hahn, 1988; KielanJaworowska, Presley & Poplin, 1986; Luo, 1989) or in the petrosal from the
Morrison Formation (Prothero, 1983), is not equivalent to the therian fenestra
cochleae, but represents the perilymphatic foramen between the cochlear canal
and the perilymphatic recess. In those primitive mammals, except for
multituberculates, the position of the perilymphatic recess is probably represented
by a concave area medial to the so-called fenestra cochleae. We found that in
some Late Cretaceous multituberculates (specimens in UALVP collection) a
distinct fossa presumably for the perilymphatic recess is located internally toward
the cochlear cavity, relative to the plane of the so-called fenestra cochleae. A
narrow groove presumably containing the perilymphatic duct (personal
observation)lies at the anteromedial side of the fossa and notches the anterodorsal
rim of the ‘fenestra cochleae’. With results from other studies and our unpublished
data on the ear of primitive mammals, we can summarize a few features in this
region of ear, which are believed to be synapomorphies for therians. First, the
perilymphatic recess merges with the basal part of the scala tympani. Second, the
processus recessus, a caudal outgrowth of the pars cochlearis of the auditory
capsule (de Beer, 1937; Kermack et al., 1981; Zeller, 1985; Wible, 1990),separates
two openings: a therian fenestra cochleae and an aqueductus cochleae or cochlear
canaliculus, which lodges the perilymphatic duct that communicates between the
perilymphatic space of the cochlea and the subarachnoid space (Gray, 1959;
Iio
JIN MENG AND R.C . FOX
Schuknecht, 1970; Evans & Christensen, 1979).Third, the fenestra cochleae and
the fenestra vestibuli are separated by a bony bridge that is broad and bears on its
inner surface the basal part of the secondary lamina. This implies that the basilar
membrane has been elongated not only apically but also basally and extends to
the area between the fenestra cochleae and fenestra vestibuli. In non-therian
mammals, the bony bridge between the fenestra vestibuli and the perilymphatic
foramen is narrow and bears no bony lamina on its inner surface.
Osseous spiral laminae
The osseous spiral laminae, both the primary and the secondary osseous spiral
laminae, are absent in early mammals, such as Morganucodon (Kermack et al., 1981;
Graybeal et al., 1989), Triconodon (Kermack, 1963), multituberculates (KielanJaworowska et al., 1986; Luo & Ketten, 1991; personal observation) and
inonotremes (Luo & Ketten, 1991).It is unlikely that absence of the osseous spiral
laminae, particularly the primary osseous spiral lamina, in these forms is a result
of damage during preservation or preparation, because the laminae and related
structures for the cochlear nerve probably cannot be completely erased if the
cochlear canal remains intact. The osseous laminae are unknown in the Early
Cretaceous non-tribosphenic therian Vincelestes (Rougier et al., 1992) and in a
tribosphenic petrosal from the Late Cretaceous Milk River Formation (83 Myr) of
Alberta (Meng & Fox, 1993, 1995), because internal structures are not
determinable in these specimens. The earliest known osseous spiral laminae are
documented in marsupial petrosals from the Late Cretaceous Oldman Formation
(Meng & Fox, 1993, 1995), a unit that is significantly older than the Hell Creek
Formation (Lillegraven & McKenna, 1986). Development of the osseous spiral
laminae is likely related to the coiling of the cochlear canal and is probably critical
in the auditory function of therian ears. These laminae provide a stable, rigid
supporting frame for attachment of a narrow basilar membrane. They also provide
a means to maintain the shape of the basilar membrane. The cochlear canal in
therians is a tube that tapers from its base to the apex, whereas the taper of the
basilar membrane is in the opposite direction, with the most distal part the widest
(Gray, 1955; von Bekesy, 1960). This configuration of the basilar membrane is
obtained by reduction of the height of the osseous spiral laminae from the basal
to the apical end of the cochlea. In addition, the primary osseous spiral lamina
houses the passages for the radially arranged cochlear nerve fibres that innervate
an elongate and coiled organ of Corti. Although the height and length of the
osseous spiral laminae vary among mammals, the configurations of these laminae
in Late Cretaceous therians show no substantial difference from those in living
ones. Because they are known only in tribosphenic therians and because in birds
and reptiles the lamina is cartilaginous (Mulroy, 1974; Wever, 1978; Smith, 198,5),
the osseous spiral laminae are probably synapomorphies for tribosphenic therians.
Presence of the secondary spiral lamina should be a primitive condition within
subgroups of therians, for instance, in mysticete cetaceans (Ketten, 1992).
Coiling of the cochlea
In non-tribosphenic therians, elongation of the cochlear duct is permitted by
coiling. Although it has been predicted that a coiled cochlea (with more than one
complete turn) probably evolved sometime before the Early Cretaceous and that
the LateJurassic is probably the latest time for the first appearance of a coiled
HEARING OF EARLY THERIANS
61
cochlea (Fernhdez & Schmidt, 1963),the earliest record of a fully coiled cochlea
is documented by the petrosal of a possible tribosphenic therian from the Late
Cretaceous Milk River Formation of Alberta (Meng & Fox, 1993, 1995). The
cochlear canal in that specimen has one and a quarter turns with a similar diameter
throughout and coils loosely. In separate research, we found, using radiography,
that the osseous cochlear canal in the platypus is less curved than that of the
echidna, contrary to the widespread current belief that the cochlea of the platypus
curves at 270" while the echidna curves at 180" (Kermack et a l , 1981; Luo &
Ketten, 1991; Allin & Hopson, 1992). In the non-tribosphenic therian Encelestes
from the Early Cretaceous, the cochlear canal has only a 270" turn (Rougier et aZ.,
1992). Therefore, we assume that the basic pattern of inner ears for marsupials
and placentals, with a fully coiled cochlea and osseous spiral laminae, was
established during the Early Cretaceous and that a cochlea with a complete spiral
turn is apparently a tribosphenic therian synapomorphy. It is evident that cochlea
with relatively few spiral turns, such as those in Late Cretaceous therians, are more
primitive than those with more spiral turns, as seen in most geologically younger
therian mammals. In living therians, only the marsupial mole, the hedgehog, and
the sea-cow possess a cochlea with as few as one and a half turns (Gray, 1908b;
Lewis et a l , 1985).
Coiling provides an economical means of housing an elongate basilar membrane
in the skull (Meyer, 1907) but does not seem to provide any functional advantage
in hearing, as indicated from the fact that travelling waves propagated on the
basilar membrane in straight and circular models of the cochlea are similar (von
Bkkksy, 1960, 1970).Although a coiled cochlea provides the potential for housing
a longer basilar membrane in limited space of the skull than does an uncoiled
cochlea, a positive relationship between basilar membrane length and the number
of coils is not present (West, 1985). Mammals with fewer spiral turns may have a
longer basilar membrane, such as the elephant, whereas those with more spiral
turns may have a shorter basilar membrane, as in the guinea big. Apparently, the
length of the basilar membrane is related to body size and weight (Graybeal et aL,
1989; Rosowski & Graybeal, 1991). A cochlea with fewer turns may contain a
longer basilar membrane than one with more turns if the spirals have a larger
diameter. A larger diameter of the spirals generally corresponds to a larger
promontorium of the petrosal and thus to a larger body size as well. The basilar
membrane lengths in the Bug Creek marsupials and placentals (approximated by
the cochlear canal lengths) are shorter than those in most extant mammals (Keen,
1939, 1940; Wollack, 1963; Manley, 1971, 1972; West, 1985) and are close to that
of the laboratory mouse and rat. However, we found that the petrosals of the Late
Cretaceous therians are much larger than that of the mouse and rat in absolute
dimensions. This suggests that the cochlea with fewer coils and shorter length in
Late Cretaceous marsupials and placentals are not only a consequence of small
body size but also represent a primitive condition in the inner ear of therians.
Innervation of the cochlea
In primitive mammals, such as Morganucodon (Kermack et a l , 1981) and
multituberculates (Kielan-Jaworowska et a l , 1986; Luo, 1989; personal
observation), the cochlear division of the auditory nerve passes into the cochlear
cavity through a single foramen, contrasting sharply to the condition in therians.
62
JIN MENG AND R.C. FOX
In early therians, such as those from the Oldman Formation (Meng & Fox, 1993,
1995) and the Bug Creek Anthills, the cochlear nerve branches into many small
fibres, which pass through numerous tubules (the tractus spiralis foraminosis) in
the modiolus in a radial fashion that has been well documented in extant mammals
(Lorente de NO, 1937; Bast & Anson, 1949; Gray, 1959; Bredberg, 1968;
Spoendlin, 1972, 1974). The cochlear nerve dendrites approach the basilar
membrane through the tubules within the primaxy osseous spiral lamina in a
direction perpendicular to the course of the basilar membrane.
In monotremes, the passage for the cochlear nerve is similar to that of therians
in having a cribriform plate in the internal acoustic meatus (Simpson, 1938;
Kermack et al., 1981),although the monotreme cochlea is not spiral. According to
Pritchard (1881: 275) : “The course taken by the cochlear nerve and its branches
differ[s] in no essential points from those of the typical Mammals. There is in the
former a ganglion very similar in relative position and component cells to the
ganglion spirale. The only differences are that, whereas in the spiral cochlea the
nerve trunk necessarily runs at right angles to the lamina spiralis, in this cochlea
it runs parallel to the corresponding lamina.” In addition, recent study indicates
that an osseous spiral lamina is absent in the cochlea on monotremes (Luo &
Ketten, 1991))indicating that a radial pattern of the cochlear nerve is not present.
A cribriform area may be present in the non-tribosphenic therian fincelestes
because no specific foramina within the deep internal acoustic meatus, with the
exception of the opening for the facial nerve, have been identified (Rougier et a l ,
1992).Whether a radial pattern of the cochlear nerve is present therein is unknown.
A radial pattern of the cochlear nerve may be another synapomorphy for
tribosphenic therians.
It is possible that the cochlear functions to minimize differences in length among
acoustic nerve fibres (West, 1985). When the basilar membrane progressively
increased its length in therian mammals, the nerve fibres that innervated the hair
cells at the apex of the basilar membrane must have become increasingly longer
than those at the base, if the cochlear nerve had passed the cochlea via a single
foramen as probably in the ears of Murganucudun and multituberculates and
extended along the basilar membrane as in the ears of monotremes (Pritchard,
1881). This pattern might result in a considerable difference in nerve impulse
conduction time from the two ends of the basilar membrane to the auditory cortex
of the brain. A radial pattern of the cochlear nerve, in a coiled cochlea, is perhaps
the only way to avoid this problem and therefore would be the most efficient
means to innervate an elongate, coiled organ of Corti. It is also possible that a
radial pattern of the cochlear nerve may provide a spacious pathway for a large
number of the nerve fibres. Manley (1972) pointed out that animals with short
basilar membranes are less sensitive to sound, a phenomenon that may be partly
due to their possessing only a small number of hair cells. Wever (1974 :450)
also stated that along with increase in the length of the auditory papilla (basilar
membrane) from amphibians to mammals, there is an increase in the number of
hair cells. Therefore, assuming the same number of nerve cells supply the same
number of hair cells, the number of the nerve fibres running through the petrosal
will increase. If in therians the cochlear nerve with an increased number of fibres
had run through the cochlea as in those of Murganucudun and multituberculates, it
would require a single enlarged foramen for the pathway of the cochlear nerves
and extra space to contain the nerves within the cochlea.
HEARING OF EARLY THERIANS
63
Hearing in ear4 therian mammals
It has been postulated on the basis of hearing in primitive living mammals, such
as the opossum, tree shrew, and hedgehog, that early mammals probably had
high-frequency hearing (Heffner et a l , 1969; Masterton et ah, 1969; Heffner &
Heffner, 1992). Until now, supporting evidence for this hypothesis has been little
known from fossils. Quantitative data for inner ear structures in fossil therian
mammals have been recorded only from a few specialized groups, such as
cetaceans, which have massive petrosal bones (Fleischer, 1976; Ketten, 1992). In
primitive mammals, such as Morganucodon, the length of the cochlear canal, taken
to approximate the length of the basilar membrane, has been used to predict
auditory function (Rosowski & Graybeal, 1991). However, there are at least two
problems concerning cochlear length in Morganucodon. First, the measurements of
the cochlear length are inconsistent in different studies: in some (Graybeal et aZ.,
1989; Rosowski & Graybeal, 1991),the length of the cochlear canal in Morganucodon
was measured from the most posterior edge of ‘the windows’ to the anterior tip of
the canal (we understand that ‘the windows’ implies the round and oval windows).
In others (Luo & Ketten, 1991: Fig. 3D), the same length was taken from the
anterior edge of the windows to the anterior tip of the canal. Second, the cochlear
length in Morganucodon may not be a good approximation of that of the basilar
membrane, because a lagena was likely present at the apical end of the cochlea, if
one looks at this within a phylogenetic context. Among extant mammals, only
monotremes primitively possess the lagena, comparable to that of reptiles and
birds (Pritchard, 1881; Denker, 1901; Alexander, 1904; Gray, 1908a; Fernandez
& Schmidt, 1963; Griffiths, 1968, 1978). Manley (1971 : 611) speculated that the
cochlear canals of Triconodon probably also contained a lagena macula, although
they were very short, e.g. 3-4 mm (Kermack, 1963). This feature was probably
present in multituberculates as well, where it is represented by an apical expansion
of the cochlea (Meng & Fox, 1993). Assuming absence of the lagena in
Morganucodon creates either convergence or reversal of this feature in mammalian
evolution, given the sister-group position of Morganucodon to other mammals
(Wible & Hopson, 1993).
Moreover, it is obvious that length of the basilar membrane is certainly not the
only factor responsible for ability of hearing, for instance, for determining highand low-frequency limits. Some birds, such as the barn owl, q t o alba, have a
longer basilar membrane (Manley, 1971, 1972) than do some small mammals,
such as the laboratory mouse and rat (West, 1985),while most birds have a shorter
basilar membrane than most mammals; nonetheless, the hearing frequencies of
birds generally are considerably lower than those of mammals, except for a few
specialized forms such as the elephant. Clearly, other structures of the ear must be
taken into account in assessing auditory function of animals. It follows that any
structure-function relationship concerning hearing that is derived from living forms
cannot be applied to fossils unless the ear structures of fossil forms can be
demonstrated to be comparable with those of living species. Therefore, the
relationships between the basilar membrane length and frequency of hearing
within living therian mammals (West, 1985; Rosowski & Graybeal, 1991)cannot be
readily applied to primitive mammals such as Morganucodon (Rosowski & Graybeal,
1991) and multituberculates, because the inner ear structures of these forms are
either poorly known or are different from that on any therian. In contrast, the ears
04
JIN MENG AND R.C. FOX
of Late Cretaceous therians appear to be similar, if not identical, in basic plan to
those of their living relatives as we presented above; thus, we can validly estimate
the auditory capabilities in these fossil forms by comparing their ears with those
of their living descendants. However, it should be pointed out that our
reconstruction of the hearing capabilities in fossils is at the gross-anatomical level
of osseous structures. The decisive factors in functional anatomy are soft-tissues,
of which only some can be inferred from osseous structures.
We believe that valid qualitative predictions of the auditory capabilities in
some fossil forms can be made from structure-function relationships based on ear
structures of extant therians. Such relationships having particular importance
are: (1) osseous spiral laminae that support the basilar membrane imply a highfrequency ear (Brown & Pye, 1975; Fleischer, 1973; Pye & Hinchcliffe, 1976;
Zwisloki, 1981; Graybeal et al., 1989; @) small mammals with close-set ears are
better able to hear high-frequency sounds (Masterton et a l , 1969; Heffner &
Heffner, 1992); (3) therians with a short basilar membrane are most sensitive to
high-frequency sounds while those with long basilar membrane are most sensitive
to low-frequency sounds (West, 1985; Rosowski & Graybeal, 1991); and (4) a
narrow basilar membrane is most suitable for high-frequency hearing (Manley,
197 1, 1972). While it is true that no structure-function relationship is universally
applicable in mammals-because hearing is dependent on many parameters of the
outer, middle and inner ear (Pye, 1979), many of which are little known (Zwislocki,
198 1)-the above mentioned structure-function relationships are probably most
reliable if applied to certain groups, such as nonspecialized terrestrial therians
(Ketten, 1992). Because Late Cretaceous therians were small and were most likely
nonspecialized terrestrial mammals and because their ear structures appear to be
like those of extant therians, the above relationships should be applicable to them
and the conclusion can be reached that the ears of early tribosphenic therians
were probably capable of high-frequency hearing.
A valid quantitative estimation of the auditory capacities of fossil forms may
also be possible, because some of the bony dimensions of the ear can be measured
as is in living mammals. Several functions have been proposed to calculate auditory
capabilities by using ear dimensions in extant mammals, such as: (1) definition of
frequency limits, estimated by using area of the stapedial footplate or of the oval
window (Rosowski & Graybeal, 1991), basilar membrane length and number
of spiral turns of the cochlea (West, 1985; Rosowski & Graybeal, 1991); (2)
determination of the highest characteristic frequencies of single neurons, estimated
from the basilar membrane length and widths (Manley, 1971, 1972); and (3)
construction of position-frequency maps, plotted by using the cochlear length and
the upper frequency limit of hearing (Greenwood, 1961, 1990; Fay, 1992). These
functions, although far from perfect even for living mammals because only one or
two variables are considered, are probably the simplest and best ways to estimate
the hearing capabilities of fossil mammals (Rosowski & Graybeal, 1991; Fay,
1992).
Figure 5 shows the frequency ranges in hearing among various living tetrapods
and the Bug Creek therians. The low- and high-frequency limits of hearing in the
Bug Creek therians and in selected living terrestrial placentals are estimated from
formulae that express relationships between the frequency limits on the one hand
and basilar membrane length and spiral turns of the cochlea on the other at the
60 dB sound pressure level (SPL).These formulae were developed by West ( 1 x 6 )
HEARING OF EARLY THERIANS
65
100
U a O O
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living mammals fossils
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5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
TAXA
Figure 5. Diagram showing frequency ranges of hearing in some living vertebrates and Late
Cretaceous therians. Original frequency limits of terrestrial placentals (West, 1985), birds and
reptiles (Rosowski & Graybeal, 1991) are plotted in squares (m =lower limit; 0 =upper
limit). Circles represent the lower ( 0 )and upper (0)frequency limits of hearing in Late
Cretaceous therians and in living terrestrial placentals that are calculated from the formulae
p e n by West (1985): 1. log (low-frequency limit at 60 dB SPL) = 1.76-1.66 log (L.N);
r = -0.98 (P <0.001); 2. log (high-frequency limit at 60 dB SPL) = 2.42-0.994 log (LjN);
r = -0.88 (P <0.01) where SPL stands for the sound pressure level, L for length of the
basilar membrane, and N for number of spiral turns. Selected taxa and their lower and
upper frequency limits of hearing (original/calculated in kHz) are: (1) man (0.029-19/0.0321.44); (2) cat (0.053-77jO.053-35.61); (3) elephant (0.017-10.5jO.017-10.06); (4) cow (0.02335/0.017-24.58); (5) common rabbit (0.096-49jO.14-43.59); (6) guinea pig (0,045-49/0.03760.96); (7) chinchilla (0.05-33jO.073-43.12); (8) laboratory rat (0.39-72jO.345-61.55); (9)
laboratory mouse (0.9-79/0.72-75.72); (10) Bug Creek placental (/l.127-55.89); (11) Bug Creek
marsupial (/1.586-68.57); (12) pigeon (0.05-4.9/); (13) budgie (0.31-6.2/); (14) cowbird (0.418.9/); (15) canary (0.63-7.7/): (16) barn owl (0.34-ll/); (17) caiman (0.15-3.0/); (18) turtle
(0.05-0.9/); (19) tokay gecko (0.11-54); (20) alligator lizard (0.2-4.0/; (21) monitor lizard
(0.22-3.6/). The basilar membrane length in the Late Cretaceous placentals is the average of
the cochlea lengths in four specimens (7.125 mm; Table 1). Those in living mammals used
in the calculation are from West (198Fi). For taxa 2 and 3, the original and estimated lower
limits are overlapped respectively.
from living terrestrial mammals in which the length of the basilar membrane is
found to be inversely related to the frequency limits of hearing, i.e. the longer the
basilar membrane, the lower the frequency limits. The calculated frequency limits
of mammals are plotted against original data collected from various auditory
experiments in living therians (West, 1985), birds and reptiles (Rosowski &
Graybeal, 1991). The low-frequency limits in the fossil forms (above 1 kHz) are
higher than those in living terrestrial mammals and in living birds and reptiles.
The high-frequency limits are 55.89 and 68.57 kHz for the Late Cretaceous
placentals and marsupials, respectively. The frequency of hearing in these fossil
forms appears to be within a normal mammalian range, for the average of lowfrequency limits in living mammals is 255 Hz (Heffner & Masterton, 1980), while
JIN MENG AND R. C. FOX
66
T\im22. Frequency limits in fossil therians, calculated by using the power
functions provided by Rosowski & Graybeal (1991) and Rosowski (lW!).
FP = footplate area in mm' (0.223 in placental/0.229 in marsupial);
BM = basilar membrane length in mm (7.125 in placental/5.8 in marsupial).
FP and BM of the Late Cretaceous placentals are the averages of the
studied specimens (Table 1)
~~~
~
Power function
~~~
~
Low frequency Limit (kHz)= 0 40FP I I
High frequency Limit (kHz)= 34FP '"
Low-frequency Limit (kHz)= 13BM ''
High frequency Limit (kHz)= 391BM-""'
Marsupial
Placental
21
22
61
123
87 7
~
02
1577
73 8
the average of high-frequency limits in mammals is 53 kHz (Masterton et al, 1969)
or 55.4 kHz (Heffner & Masterton, 1980). The upper limits of hearing in the Late
Cretaceous therians are substantially higher than those of birds and reptiles, and
the hearing ranges of frequency in the fossil therians are also broader than those
of non-mammalian tetrapods.
There are alternative equations (Rosowski & Graybeal, 1991; Rosowski, 1992)
concerning footplate area-frequency and basilar membrane length-frequency
relationships (Table 2). The results derived from the equation using footplate area,
approximated by the area of the oval window, are fairly close to those calculated
from West's formulae, although the high-frequency limits from that based on
basilar membrane length are higher.
Manley (1971, 1972) showed that a correlation exists between the basilar
membrane value and the highest characteristic frequencies of single neurons in
various vertebrates. The characteristic frequency is the one to which an auditory
neuron is most sensitive. The basilar membrane value is represented by the
formula: (L/Ww:Ww.Wn)/lOO, in which L stands for length, Ww for greatest
width, and Wn for least width of the basilar membrane. Therefore, not only the
length but also the widths of the basilar membrane are taken into account in
consideration of tetrapod hearing. The conclusion derived from this correlation is
that a long, narrow basilar membrane responds best to a higher frequency. The
basilar membrane value of the Late Cretaceous placentals is approximately seven,
which is between those of living mammals and non-mammalian tetrapods. This
value roughly correlates with the highest characteristic frequency of 10-1 1 kHz.
Because the actual width of the basilar membrane in Late Cretaceous placentals
was probably narrower than that of the preserved vestibular fissure, the basilar
membrane value and thus the highest characteristic frequency could have been
higher. In addition, it is known that the base to apex variation in basilar membrane
width is one of the factors corresponding to the frequency range of hearing in
tetrapods (Manley, 1971, 1972; West, 1985) and that small difference in basal and
apical dimensions of the basilar membrane corresponds to narrow frequency range
(Ketten, 1992; Ketten, Ode11 & Domning, 1992). The width gradients in the Late
Cretaceous placentals are relatively small, suggesting that the range of frequencies
encoded was probably narrow. Certain conflicts seem to exist between the
relationships developed by West and Manley. This is probably because West's
formulae are solely based on data from terrestrial mammals, whereas Manley's is
from mammals plus birds and reptiles. Nonetheless, all results in general support
HEARING OF EARLY THERIANS
67
Figure 6. Position-frequency maps for Late Cretaceous marsupials and placentals. The plotting
is from the equation (Fay, 1992): P = (l-(log,,(f/0.008F)+1)/2.1)L, in which P is for the
position on the basilar membrane corresponding to a given frequency f; f for any frequency
within the frequency range of each species; F for the highest audible frequency; L for the
basilar membrane length. The highest frequencies for the fossil marsupial and placental are
estimated by using the equation given in Figure 5 .
the assumption that high-frequency hearing is a distinctive character of therian
mammals and is present in early therian species (Heffner et al, 1969; Masterton
et al, 1969; Heffner & Heffner, 1992).The results also suggest that high-frequency
hearing in mammals is not only a consequence of acquisition of a triossicular
system in the middle ear (Masterton et a l , 1969),but also a result of modifications
of the inner ear itself (Manley, 1972).
Fay (1992 :247) suggested: “if the fossil record allows estimates of cochlear
length, and if the frequency range of hearing can be estimated from middle ear
morphology, then we can, in principle, estimate absolute position-frequency maps
for ancestral species.” Employing the above estimated upper frequency limits, we
further plot the absolute position-frequency maps for Late Cretaceous marsupials
and placentals (Fig. 6). The function used here was originally developed by
Greenwood (1961) and is supported by various experimental data (von Bkkksy,
1961; Liberman, 1982; Greenwood, 1990). It specified that a given frequency is
sensed at a particular position along the basilar membrane in such a distribution
that higher frequencies are basal while lower are apical. The function was
afterwards modified by Fay (1992) so that the position-frequency maps can be
calculated by using two species-specific variables: the basilar membrane length
and the upper frequency limit of hearing. The position-frequency maps for Late
Cretaceous therians are similar to those of extant small mammals such as the
laboratory mouse and rat (Fay, 1992).
Within mammalian evolution, transformation of the quadrate and articular
bones from part of the jaw suspension into the incus and malleus, part of the
auditory device, is a remarkable event. That the hearing ability of mammals
changed along with this morphological modification seems to be a logical
conclusion, but the degree of change remains nothing more than a bold
speculation. Webster (1992 : 789) postulated that such a morphological change
68
JIN MENG AND R. C. FOX
“suggests the interesting possibility that sensitive hearing of airborne sounds arose
‘suddenly’, when the posterior jaw elements were freed to form a stiff, microtype
middle ear. Because of its small size and its stiffness, such an ear would have given
the capacity to hear frequencies above 12,000 Hz, provided the inner ear could
cope with these higher frequencies. Among the vertebrates, this hearing range is
unique to mammals,” Our studies of the ears of Late Cretaceous therians show
that change in the middle ear is only one of the two major steps in this modification
of the mammalian hearing apparatus; the other is the change in structures of the
inner ear as described here and elsewhere (Meng & Fox, 1995). Based primarily
on middle ear anatomy, some specialists (Rosowski & Graybeal, 1991; Rosowski,
1992) have come to the conclusion that high-frequency hearing predated
Morganucodon, an early transitional mammal, in which the quadrate and articular
are not yet suspended. The inner ear structures of Morganucodon, however, hardly
constitute a high-frequency device comparable to that of therians; they are birdlike (Kermack et aZ., 1981; Graybeal et ak, 1989; Rosowski & Graybeal, 1991).
Although multituberculates have developed a triossicular system (Miao &
Lillegraven, 1986), their inner ear is similar to that of Morganucodon (Kielam
Jaworowska et al., 1986; Luo & Ketten, 1991; Meng & Fox, 1993, personal
observation). In both forms, the inner ear lacks several structures, such as the
osseous spiral laminae, that characterize the high-frequency ear of therians.
Therefore, the inner ears of these forms may not have been able to cope with high
frequencies, even though their middle ears appear capable of high-frequency
hearing. Consequently, this means that a high-frequency middle ear predates a
high-frequency inner ear in mammalian evolution.
The fossil record documents a sequence of critical morphologcal changes in
the inner ear of mammals. As mentioned above, in the non-tribosphenic therian
fincelestes from the Early Cretaceous, the cochlear canal has only a 270” turn. In
the earliest known tribosphenic therian (Meng & Fox, 1995),the cochlea has only
one and a quarter turns, which has a constant diameter from base to apex and
coils loosely. In the ears described here, the cochlea has one and a half turns and
coils more tightly. In later therians, the number of cochlear coils is usually more
than two, with greater tapering (Lewis et ak, 1985). This suggests that a coiled
cochlea in therians was gradually achieved and that sensitive hearing of airborne
sounds may well be gradually achieved too.
CONCLUSIONS
(1) Although minor differences between the groups exist, Late Cretaceous
marsupials and placentals are similar in their inner ear structures in possessing the
following tribosphenic therian synapomorphies: a fully coiled cochlea, primary
and secondary osseous spiral laminae, the perilymphatic recess merging with the
scala tympani of the cochlea, a bony aqueductus cochleae, a true fenestra cochleae,
a radial pattern of the cochlear nerve and an elongate basilar membrane that
extends to the regon between the fenestra cochleae and fenestra vestibuli. These
resemblances confirm a common ancestry for the two groups at the tribosphenic
level.
(2) The basic anatomical pattern of the inner ear in marsupials and placentals
was probably achieved during the Early Cretaceous. The inner ear structures of
HEARING OF EARLY THERIANS
69
living therians differ from those of their Late Cretaceous relatives mainly in having
more spiral turns of the cochlea and a longer basilar membrane.
(3) Functionally, a coiled cochlea not only permits the development of an
elongate basilar membrane within a restricted space in the skull but also allows
a centralized nerve system to innervate the elongate basilar membrane most
efficiently.
(4)Late Cretaceous marsupials and placentals were probably capable of highfrequency hearing, in which the above-mentioned inner ear structures must have
played important roles. With lengthening and widening or narrowing of the basilar
membrane, an enormous diversity in hearing capacities evolved among therian
mammals thereafter.
ACKNOWLEDGEMENTS
We thank Z.-X. Luo, G. A. Manley for suggestions and discussion; two
anonymous reviewers for instructive and helpful comments; G. D. Braybrook for
preparing SEM photographs. J. M. is supported by a Postdoctoral Fellowship from
the Natural Sciences and Engineering Research Council of Canada (NSERC) and
the University of Alberta. Approximately 60% of financial support for research by
RCF on Cretaceous and Early Tertiary mammals is provided by NSERC operating
grants to him.
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