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<oological Journal .f the Linnean Sociely (1991), 101: 131-168. With 1 1 figures
What did Morganucodon hear?
J . J . ROSOWSKI'.'
AND
A. GRAYBEAL',3
I
Eaton-Peabody Laboratory of Auditory Physiology, Massachusetts Eye and Ear
Injirmary, 243 Charles Street, Boston, M A 02114, U.S.A., 2Research Laboratory of
Electronics, Massachusetts Institute o f Technology, 77 Massachusetts Avenue, Cambridge,
M A 02139, U S .A , , and 31)epartment o f Integrative Biology, University o f Calfornia,
Berkeley, CA 94720, U.S.A.
Received Februay 1989, accepted f o r publication
3 4 1990
The structure of the middle and inner ear of Morganucodon, one of the oldest known mammals, is
reviewed and compared to the structure of the ears of extant mammals, reptiles and birds with
known auditory capabilities. Specifically, allometric relationships between ear dimensions (basilarmembrane length, tympanic-membrane area and stapes-footplate area) and specific features of the
audiogram are defined in extant ears. These relationships are then used to make several predictions
of auditory function in Morganucodon. The results point out that the ear structures of
Morganucodon- -are similar in dimensions to ear structures in both extant small mammals-with
predominantly high-frequency ( > 10 kHz) auditory capabilities, and reptiles and birds-~-with
better low and middle-frequency hearing ( < 5 kHz). Although the allometric analysis cannot by
itself determine whether Morganucodon heard more like present-day small mammals, or birds and
reptiles, the apparent stiffness of the Morganucodon middle ear is both more consistent with the highfrequency mammalian middle ear and would act to decrease the sensitivity of a bird-reptile middle
ear to low-frequency sound. Several likely hearing scenarios for Morganucodon are defined, including
a scenario in which these animals had ears like those of modern small mammals that are selectively
sensitive to high-frequency sounds, and a second scenario in which the Morganucodon ear was
moderately sensitive to sounds of a narrow middle-frequency range (5-7 kHz) and relatively
insensitive to sounds of higher or lower frequency. The evidence needed to substantiate either
scenario includes some objective measure of the stiffness of the Morganucodon ossicular system, while a
key datum needed to distinguish between the two hypotheses includes confirmation of the presence
or absence of a cochlear lamina in the Morganucodon inner ear.
KEY WORDS:--Mammals
-
evolution
-
middle ear
-
inner ear
CONTENTS
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,
. . .
Introduction .
A historical prrspertivr
. . . . , . . .
A review of the structure of the Morganucodon ear .
.
Predictions of auditory function from fossil ear structures
Methods .
.
.
. . . . . . . . . .
Predictions of auditory function from allometry
. .
T h e audiogram and auditory area as measures of auditory
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c 1991 1 hr Linnean 5ociet\ of London
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J. J. ROSOWSKI AND A. GRAYBEAL
. . . . . . . . .
The study population: choice of species
Definition of allometric relationships by linear regression techniques
. .
Results . . . . . . . . . . . . . . . . . .
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Relationships between body size and ear dimensions in extant amniotes
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Comparisons of ear dimensions in Morganucodon and extant amniotes
Predictions of Morganucodon auditory function from middle-ear dimensions .
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Predictions of Morganucodon auditory function from inner-ear dimensions
Likely auditory areas of Morganucodon-like ears . . . . . . . .
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Discussion . . . . . . . . . . . . . . . . .
Significance of the allometric analyses in extant ears . . . . . .
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Predictions of ear structure from allometry
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The auditory area of Morganucodon
General conclusions . . . . . . . . . . . . . . .
Acknowledgements
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References
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Appendices . . . . . . . . . . . . . . . . ,
1. Selected anatomic and audiometric data
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2. Power functions relating anatomy and audiometry . . . . . .
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INTRODUCTION
An historical perspective
One of the defining features of early mammals is the existence of a
‘mammalian’ squamosal-dentary jaw joint that freed the ‘reptilian’ quadratoarticular jaw joint for transformation into the ossicular system of the mammalian
middle ear (Crompton &Jenkins, 1973). These changes in jaw and ear structure
occurred gradually during the early and middle Mesozoic Era, and were
completed a t least 50 million years before the end of the Cretaceous and the
beginning of the age of mammals-see
Lillegraven, Kielan-Jaworowska &
Clemens (1979) for a series of discussions on this issue. Morganucodon, a shrewsized Mesozoic insectivore (body weight approximately 0.02 kg) that existed
200 million years ago, is of particular interest in studies of this transition since it
is thought to have been one of the earliest mammals and its skeleton exhibits
both reptilian and mammalian jaw joints (Kermack & Musset, 1958; Crompton
&Jenkins, 1973; Kermack, Musset & Rigney, 1973, 1981; Crompton & Parker,
1978).
The consequences of the evolutionary changes in mammalian jaw structure on
mastication have been well described (Crompton, 1963; Crompton & Jenkins,
1973; Crompton & Parker, 1978), while the consequences of the parallel changes
in auditory structure are less well understood. Historically there have been
several theories concerning the auditory capabilities of mammal-like reptiles and
early mammals, and these have been reviewed by Henson (1974) and Allin
(1975). Within the last 40 years, two competing theories have held sway. The
earlier was proposed by Westoll (1943-1945) and is based on the view that the
reptilian middle ear evolved very early on in tetrapod evolution in an ancestor
common to both modern reptilian and mammalian lineages. This supposition
led Westoll to suggest that the middle ears of mammal-like reptiles and early
mammals were similar in structure and function to those of modern reptiles with
a single auditory ossicle (the stapes) connected directly to the tympanic
membrane. Parrington (1949, 1979) also espoused this view. A different point of
view was proposed by Tumarkin (1955, 1968), who suggested that the
mammalian middle ear developed both relatively late in vertebrate evolution
WHAT DID MORGANUCODON HEAR?
133
and independently from the middle ears of modern reptiles. Allin (1975)
accepted Turnarkin’s arguments and produced an evolutionary sequence for the
development of the mammalian middle ear that assumes that the middle ear of
the earliest mammal-like reptiles had no role in the reception of airborne sound,
while the middle ears of the most advanced mammal-like reptiles are assumed to
have functioned much like those of present-day mammals with a three-bone
ossicular chain connecting the tympanic membrane and inner ear. Allin’s
sequence depends on the argument that in later mammal-like reptiles and early
mammals the bones of the reptilian jaw joint acted both as auditory ossicles as
well as jaw joint. Kermack and his coauthors (Kermack et al., 1981; Kermack &
Musset, 1983) accepted Allin’s views when they reconstructed the middle ear of
Morganucodon.
While the structure and function of the middle ear of early mammals has been
a point of controversy, most authors (Kermack et al., 1981; Kermack & Musset,
1983; Graybeal et al., 1989) agree that the short, straight auditory inner ear of
early mammals appears reptile-like-the mammalian cochlea is relatively long
and coiled, see Manley (1971, 1973). The combination of a ‘reptilian’ inner ear
in Morganucodon with an apparently mammalian middle ear led Kermack &
Musset (1983) to propose that these animals were not very sensitive to airborne
sound.
Others have speculated about hearing in early mammals. Masterton and his
co-workers (Masterton, Heffner & Ravizza, 1969) measured the behavioural
auditory sensitivity of many extant mammals and suggested that sensitivity to
high-frequency airborne sound is a primitive mammalian trait. Moreover, it is a
commonly held notion that primitive mammals escaped predation from diurnal
thecodonts and dinosaurs by adapting to a nocturnal existence, an existence that
places great demands on high-frequency hearing Uerison, 1973; Crompton &
Parker, 1978; Lillegraven, 1979; Kermack & Kermack, 1984). The purpose of
this report is to describe allometric analyses that tests the various hypotheses
concerning hearing in Morganucodon by comparing the size of its auditory
structures with the size of similar structures in extant amniotes with known
auditory functions.
A reuiew o f the structure o f the Morganucodon ear
Middle ear
The middle and external ears of terrestrial mammals, reptiles and birds act to
gather and conduct sound power from a sound source to the inner ear in some
frequency-selective manner (Waetzmann & Keibs, 1936; Khanna & Tonndorf,
1969; Tonndorf & Khanna, 1976; Shaw & Stinson, 1983; Rosowski et al., 1986;
Rosowski, Carney & Peake, 1988). The middle-ear structures of most extant
terrestrial amniotes include some relatively mobile sound-receiver surface,
usually the tympanic membrane, coupled to a bony footplate by an ossicular
system consisting of bones and ligaments. Motions of the tympanic membrane
move the ossicles and the footplate. Motions of the footplate generate sound
waves in the inner ear that stimulate the auditory mechano-receptors and
activate the auditory nerve and central nervous system (Wever & Lawrence,
1954; Dallos, 1973, 1981; Zwislocki, 1975; Merller, 1983).
J. J. ROSOWSKI AND A. GRAYBEAL
134
A
U
I mm
etroarticular
Prear t icular
lamina of
angular
window
Figure 1. The lower jaw and posteroventral aspect of the skull of Morganucodon. A, A schematic of the
medial surface of the right lower jaw of Morganucodon (after Kermack & Kermack, 1984). The
angular bone (the homologue of the mammalian tympanic bone) is thought to have been coupled to
the fused articular (homologue of the malleus), prearticular and surangular bones along their
common seam. These post-dentary elements insert in a groove in the medial surface of the dentary.
The reconstruction of the thin reflected lamina of the angular and the retroarticular process of the
articular is based on evidence from earlier mammal-like reptiles. The surface of the articulation
The surface of the articulation between the
between the articular and quadrate bones is labelled ‘0’.
dentary and squamosal bones is labelled ‘X’. B, A reconstruction of the posteroventral surface of the
left side of the Morgunucodon skull (after Kermack et al., 1981). The jaw articulations, ossicles and
bony surfaces are schematized. The ‘mammalian’ jaw articulation of the dentary and the squamosal
is marked ‘X’. The ‘reptilian’ jaw articulation of the articular (malleus) and quadrate (incus) is
marked ‘0’.
There is only indirect evidence for the existence of the quadrato-jugal and the
articulation of the stapes and quadrate (Kermack el al., 1981). The largest bone in the schematic is
the petrosal, which includes the promontory (the bony housing of the inner ear). Shading has been
used to add depth.
WHAT DID MORGANUCODON HEAR?
135
While the existence of an external ear in Morganucodon has been a point of
controversy (Allin, 1975; Parrington, 1979), and little is known about any softtissue middle-ear structures (e.g. the tympanic membrane), the bony structures
of the Morganucodon middle ear have been fairly well described (Kermack et al.,
1973, 1981, 1983: Crompton & Parker, 1978). Schematized views of the medial
surface of the lower jaw and posteroventral aspect of the skull of Morganucodon
are depicted in Fig. 1. The dentary bone is the primary component of the lower
jaw and the post-dentary elements-including
the angular, and the fused
articular, prearticular and surangular bones (Fig. 1A)-are reduced in size
relative to those of early mammal-like reptiles (Allin, 1975; Crompton & Parker,
1978). The post-dentary elements are believed to have been coupled together by
connective tissue along their long common seam (Allin, 1975; Kermack &
Musset, 1983), and the anterior portion of these elements are housed in a groove
in the medial surface of the dentary bone (Allin, 1975; Kermack el al., 1973,
1981). The posteroventral view of the skull (Fig. 1B) shows the ‘reptilian’ jaw
articulation of the articular and quadrate bones (0)as well as the attachment of
the quadrate bone and stapes. Although there is no direct evidence for the
pictured bony or ligamentous connection between the stapes and quadrate in
Morganucodon, such an articulation is not uncommon in mammal-like reptiles
(Broom, 1912; Hopson, 1966; Allin, 1975; Kermack et al., 1981). The
‘mammalian’ squamosal-dentary jaw articulation (X) is also visible.
Kermack et al. (1981) have described in detail the shape and dimensions of the
Morganucodon quadrate bone and stapes. These bones have linear dimensions of
less than 1 mm, and the mean area of 11 stapes footplates is 0.28 mm’. The
precise structure and dimensions of the angular and articular bones are less well
known, since all of the reported specimens of these bones appear incomplete. The
shortened or missing structures are the reflected lamina of the angular bone and
the retroarticular process of the articular. Kermack et al. (1981) reconstruction of
these bony elements (Fig. 1 ) is dependent on the structure of advanced
mammal-like reptiles (e.g. Bienotherium, described in Hopson, 1966). The size and
location of the tympanic membrane is even less well defined, see Allin (1975) and
Parrington (1979) for arguments for and against the location of the tympanic
membrane schematized in Figure 1. Kermack & Musset (1983) have argued for
the placement of the tympanic membrane observed in Fig. 1A and suggest that
such a tympanic membrane would have an area of 4.5 mm’. Parrington’s
arguments (1949, 1979) would lead to a much smaller, 1.0 mm’, tympanic
membrane placed posterior to the quadrate bone and partially bounded by the
squamosal bone-as is discussed by Kermack & Musset ( 1983).
The precise middle-ear mechanism in Morganucodon is not clear, however
Kermack et al.’s reconstruction of the Morganucodon middle ear (Kermack &
Musset, 1983) suggests that sound energy incident on the tympanic membrane
could have caused the coupled angular (tympanic) and articular (malleus) bones
to rotate as a unit within the groove they shared on the medial surface of the
dentary (Fig. 2). This rotation would have been coupled to the quadrate (incus)
bone, through the quadrato-articular joint, and would have caused the stapes,
oriented perpendicular to the axis, to rock in the oval window (Fig. 2B). For this
scheme to be correct, the attachment of the quadrate and squamosal bone must
have been loose enough to have allowed rotation of the quadrate during middleear motions (but firm enough to have kept the quadrate fixed when it functioned
J. J. ROSOWSKI AND A. GRAYBEAL
136
A
Surangular
/
Dentary
Hypothetical
axis of
rotation
Articular
---" II
I
Prea r ticular
Groove
Reflected
lamina of
angular
Axis of
rotat ion
I
membrane
Angular
(tympanic)
Figure 2. A hypothetical mechanism for ossicular motion in Morganucodon. A, The medial surface of
the right jaw, showing the long symphysis between the angular, and the fused articular, prearticular
and surangular as well as their housing within the dentary groove. The dashed line is a hypothetical
complex. B, An expanded view of
axis for rotations of the tympanic membrane-angular-articular
the posterior portion (box) of the lower jaw including the quadrate and stapes. Rotation of the
tympanic-membrane and its supporting bones around the hypothetical axis causes rotation of the
quadrate and a rocking of the coupled stapes.
as a jaw joint). The loss of soft tissues during fossilization makes it difficult to test
assumptions concerning either the flexibility to rotation of the quadrate or the
rigidity of the angulo-articular, articulo-quadrate and quadrato-stapes joints.
Inner ear
The auditory inner ears of amniotes are highly specialized organs made up of
several fluid-filled compartments, a membrane that moves in response to sound
WHAT DID MORGANUCODON HEAR?
137
Morgonucodon petrosol promontory
Ventroloterol view
A
TL7
B
Oval window
Anterior
D
.-Vestibular
Dorsal
4
Anterior
Medial
Promontorium
/
Figure 3. The petrosal promontory and cochlear cavity of a right ear from two different views (as
reconstructed by Graybeal et a / . , 1989). A, C, T h e external surface of the promontory showing the
oval window, round window, remnants of the anterior lamina, the medial foramina of the auditory
nerves and a foramen for the facial nerve. B, D, T h e cochlear space. T h e auditory inner ear fits in a
2.5-3.1 mm long slightly curved tube. No bony lamina is readily apparent. Remnants of the
vestibular space are visible posterior and dorsal to the cochlear space.
and a large number of mechano-receptors and neural elements that sense
acoustic disturbances and transmit information about these disturbances to the
auditory central-nervous system. As in all mammals, the inner ear is housed in
the petrosal bone, a prominent member of the ventrolateral wall of the
Morganucodon skull (Fig. 1B). The external surface of the complete petrosal has
been described in detail by Kermack et al. (1981) while the external and internal
surfaces of the promontory (that part of the bone containing the auditory inner
ear) have been described by Graybeal et al. (1989). Figure 3 is a reconstruction
of the external surface (Fig. 3A,C) and internal spaces (Fig. 3B,D) of a right
promontory in two different views. The cochlear windows mark the posterior
surface of the promontory. The cochlear space inside the promontory appears as
a smooth, slightly curved and tapered tube suggestive of the cochlear capsule of a
bird or crocodilian (Manley, 1971, 1973; Wever, 1978; Smith, 1985; Graybeal et
al., 1989). The ‘bird or reptile-like’ appearance comes from three features.
138
J. J. ROSOWSKI AND A. GRAYBEAL
(1) The length of the cochlear space is shorter than that in most mammals, only
2.5-3.1 mm from the most posterior edge of the windows to the anterior tip of
the space (Graybeal et al., 1989). ( 2 ) One of the distinctive features of a
mammalian cochlea is the presence of a bony cochlear lamina, yet Graybeal et al.
(1989) found no clear evidence of such a lamina in the available Morganucodon
material, while Kermack et al. (1981) suggests that a small ridge visible through
the broken cochlear windows in one of their specimens is a remnant of the
cochlear lamina. It is also possible that a fragile bony shelf would not have
survived either fossilization or specimen preparation (Graybeal et a/., 1989).
(3) The barely noticeable curvature of the Morganucodon auditory inner ear is not
consistent with the inner ears of extant mammals. All therian cochleae are
coiled, and the cochleae of the monotremes curve through at least 180" (Manley,
1971, 1973).
The structure that plays the largest role in determining the amniote inner-ear
response to acoustic stimuli is the basilar membrane (Bkkby, 1960; Zwislocki,
1965, 1975). The mechano-receptive hair cells sit on this membrane, and
membrane motion is a necessary condition for acoustic stimulation of the
receptors (Davis, 1965; Dallos, 1981; Weiss & Leong, 1985). Basilar-membrane
motions are limited by the impedance of the membrane that in turn depends on
membrane dimensions including thickness, width and length (BCkksy, 1960;
Greenwood, 1961; Zwislocki, 1965, 1975). The loss of soft tissue and any
cochlear lamina during fossilization and preparation of available Morganucodon
specimens makes it impossible to estimate the width and thickness of the basilar
membrane in these animals, but the basilar-membrane length may be
approximated from the length of the bony capsule (Graybeal et al., 1989).
Ear dimensions
The dimensions of the Morganucodon ear that are relevant to the later
allometric analyses are summarized in Table 1. The true area of the stapes
footplate probably falls between Kermack et al. (1981) estimate of 0.28 mm' and
the 0.5 mm' estimated for oval-window area by Graybeal et al. (1989).
A footplate area of 0.4 mm' is assumed. It is also assumed that the 4.5 mm2
tympanic-membrane area estimated by Kermack & Musset (1983) is correct and
their contention, that the alternative membrane area ( 1.O mm') defined by
Parrington's arguments is too small, is accepted. Cochlear cavity length, as
reported by Graybeal et al. (1989), may either underestimate or overestimate the
length of the basilar membrane; a membrane length of 3.1 mm, that is the
longest of their three measured cavity lengths, is assumed. It should be noted
that since the analyses presented in this report concern comparisons of ear
TABLE
1. Relevant dimensions of Morganucodon
Body weight
Stapes-footplate area
Tympanic-membrane area
Basilar-membrane length
0.02 kg
0.28 mmz
1 0 . 5 mm2
0.4 mm2
c. 4.5 mm*
4.5 mm2
2.53.1 mm
3.1 mm
Crompton &Jenkins, 1973
Kermack et af., 1981
Graybeal et al., 1989
Assumed in this study
Kermack & Musset, 1983
Assumed in this study
Graybeal ef al., 1989
Assumed in this study
WHAT DID MORGANUCODON HEAR?
139
dimensions in the amniote population, where ear dimensions vary over several
orders of magnitude, small (factors of two) errors in these estimates of
Morganucodon ear dimensions will have little effect on the results of the analyses.
Predictions of auditory function from fossil ear structures
The inadequacy o f models of the ear
Although Fig. 2 suggests that the Morganucodon middle ear functioned
qualitatively like the middle ears of extant animals, how does one quantify
auditory function in this as well as other extinct animals? One approach is to use
the simple ‘ideal transformer’ model of middle-ear action, where the
transformation ratio depends solely on the linear dimensions of the auditory
ossicles and the areas of the tympanic membrane and stapes footplate (e.g. Allin,
1975; Kermack & Musset, 1983). This model assumes that the structures of the
middle ear do not contribute to the mechanics of the auditory periphery.
Contrary to this assumption, actual measurements of middle-ear function in
extant ears indicate that the mass, stiffness and damping within the tympanic
membrane, ossicles and ossicular connections play a large role in determining
middle-ear function and overall auditory performance (Mdler, 1961; Zwislocki,
1962, 1963, 1975; Dallos, 1973; Tonndorf & Khanna, 1976; Lynch, Nedzelnitsky
& Peake, 1982; Shaw & Stinson, 1983, Rosowski et al., 1985). Therefore, though
the ideal transformer is often used as a starting point for more complete models
of middle-ear action (Wever & Lawrence, 1954; Dallos, 1973; Zwislocki, 1975),
this simple model by itself can lead to spurious descriptions of middle-ear
function.
An alternative model would be a complete mechano-acoustic analysis of the
auditory structures in Morganucodon, but such an analysis would be highly
dependent on the unknown mechanical properties of the auditory soft tissues
including the tympanic membrane and the ossicular joints (Zwislocki, 1962;
Lynch et al., 1982; Rosowski et al., 1985). Lack of knowledge about these soft
tissue structures makes it impossible to predict accurately auditory function in
Morganucodon based solely on acoustical and mechanical considerations.
Structure-function relationships in extant animals
As an alternative, comparisons of known auditory function with bony ear
structure in extant terrestrial amniotes might point out general relationships
between auditory function and the bony structure of ears. Such a comparative
approach may help define or at least restrict the possible auditory function of
fossil ears, and might also separate the significant features of a ‘bird or reptilelike’ ear from those of a ‘mammal-like’ ear. Significant trends defined by these
procedures can then be used to predict auditory function in Morganucodon.
METHODS
Predictions o f auditory function f r o m allometry
Allometry, in its broadest sense, is the study of size and its consequences
(Gould, 1966). This report will investigate whether or not allometric
relationships exist between the size of the bony auditory structures and hearing
J. J. ROSOWSKI AND A. GRAYBEAL
140
capabilities in extant animals. Such relationships will then be used to predict a
range of audiometric features for an extant amniote (either mammal or birdreptile) with ear structures of the size of Morganucodon. The predicted features
will then be combined to predict the most likely auditory function of
Morganucodon.
The audiogram and auditory area as memures of auditory function
Though several means exist for quantifying auditory function in extant
animals, the most general measure is the pure-tone audiogram, or threshold level
us. tone-frequency contour (Fig. 4).The audiogram is a behavioural measure of
auditory sensitivity and represents an integration of the acoustic, mechanic and
neural responses of the external, middle and inner ear as well as the auditory
central nervous system. Several lines of evidence suggest that the audiogram is
primarily determined by the peripheral auditory system, including the external,
middle and inner ear (Khanna & Tonndorf, 1969; Dallos, 1973; Zwislocki, 1975;
Shaw & Stinson, 1983; Rosowski et aZ.,1986).
Audiograms have been measured in a large number of mammalian and avian
species (Saunders & Rosowski, 1979; Heffner & Masterton, 1980; Dooling, 1980;
Heffner, 1983; Fay, 1988), unfortunately, the only reptilian audiogram available
is that of the red-eared turtle, Chrysemys scripta elegans (Patterson, 1966). There
80
I
2
20
a
0
P
r
v)
t
.c
o
I-
l(r Budgerigar
-20
0.0I
---
I
I
I
1
0.I
I
10
100
Frequency ( kHz 1
Figure 4. Pure-tone audiograms (threshold sound-level-frequency contours) for the cat (Felir catus;
Heffner & Heffner, 1985), mouse ( M u musculus; Heffner & Masterton, 1980), budgerigar
(Melapsztacus undulatus; Dooling & Saunders, 1975) and Tokay gecko (Gekko gecko; after Manley,
1981). The abscissa is tone frequency scaled in kHz ( 1 kHz = 1000 cps). The left ordinate is the
minimum sound pressure level in dB SPL (dB re 20 micropascals) required to produce a behavioural
response to a tone, while the right ordinate is the threshold sound pressure scaled in pascals.
WHAT DID MORGAXUCODOX HEAR?
141
are, however, extensive measurements of sound-evoked neural activity from the
auditory nerves of several reptiles (in alligator lizard, Gerrhonotus multicarinatus, by
Weiss et al., 1976; in a varanid, Varanus bengalensis, by Manley, 1977; in caiman,
Caiman crocodilus, by Klinke & Pause, 1980; in Tokay gecko, Gekko gecko, by
Eatock, Manley & Pawson, 1981), and these data have been used to construct
'neural audiograms' for these species (Manley, 1981) . Sample audiograms from a
bird, a reptile and a few mammals are illustrated in Fig. 4. The budgerigar and
Tokay gecko are most sensitive to sounds of a narrow frequency range centred
about 2 kHz and do not respond to even very loud sounds of frequencies above
10 kHz, while the cat is most sensitive to sound frequencies of a wider and higher
1-30 kHz range, and the mouse is most sensitive to a narrow high-frequency
range centered about 18 kHz. These audiograms typify the commonly perceived
inter-class differences in amniote auditory function, i.e. birds and reptiles are
most sensitive to sounds of low and moderate frequencies-less than 5 kHz, and
only mammals are sensitive to sounds of frequencies much greater than 10 kHz
(Manley, 1973; Ilooling, 1980).
In order to simplify the comparison of audiograms from many species, several
features were extracted from audiograms of interest (Fig. 5) including: (1) the
lowest or best threshold, (2) the best frequency and a (3) bandwidth, (4) centre
frequency, ( 5 ) low- and (6) high-frequency bound. The last four features are
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to-'
60
10-
40
IO-~
20
lo+
0
10-5
-20
0.01
0.I
10
I
Frequency ( k H z
100
1
Figure 5. 'l'hr audiogram of' the cat is used to describe the definition of best frequency, best
threshold, auditory bandwidth, high- and low-frequency limits, centre frequency and auditory area.
T h e frequency limits are defined by the intersection of the audiogram with a sound level 30 dB
greater than the best threshold. T h e bandwidth is the ratio of the high- to low-frequency limit (in
decades). The centre frequency is the geometric mean of the high and ION frequency limits. The
auditory area includes all of the sound frequency-pressure space above the threshold curve and
below the limits of pain (not shown here).
J. J. ROSOWSKI AND A. GRAYBEAL
142
defined by the intersection of the audiogram with a horizontal line placed 30 dB
above the best threshold. Similar techniques have been used by others
(Masterton et al., 1969; Dooling, 1980; Heffner & Masterton, 1980).
The shaded area of the frequency and sound-level domain above the
audiogram is commonly referred to as the auditory area, and contains all of the
combinations of sound frequency and level that can be heard by the animal in
question. The auditory area does have an upper bound, that is not included in
Fig. 5. In humans, intense sound pressures ( > 100 dB SPL) evoke either a
tickling sensation or pain in the ear that supersedes the auditory sensation. This
upper limit of the area is of little consequence to the subsequent discussion, since,
the final outcome of this report will be predictions of the lower limits of the
auditory area in Morganucodon.
The study population: choice of species
Measurements of basilar-membrane length and projected planar areas of the
tympanic membrane and stapes footplate were gathered from the literature
(Table 2, Appendix 1) for animals with known audiograms. Since only
terrestrial animals have middle ears specialized for the reception of airborne
sound, aquatic species have been ignored, with the exception of the semi-aquatic
red-eared turtle. Middle-ear area measurements and audiograms were found for
23 amniote species. Basilar-membrane lengths were found for 19 species with
reported audiograms. The total analysis population included 26 species-1 6
mammals, five birds and five reptiles. Two different breeds of dog (Canis canis) of
greatly different body size are included in the analysis population (Heffner,
1983), and for two mammalian genera, Equus and Rhinolophus, the audiogram
and structural measurements were made on different species. The audiograms
and basilar-membrane lengths come from the domestic horse ( E . caballus) and
horseshoe bat (R. ferrumequinum) while the middle ear measurements were made
on the zebra (E. zebra) and R. simulator. In most cases, the structural and
audiometric measurements represent mean measurements taken from small
separate experimental populations, and the body weights represent some general
population mean (Walker, 1968).
The use of audiometric and anatomic data gathered with varied methods from
different laboratories adds to the variability within the analysis population. In
TABLE
2. Group of extant species for structure-function
comparison
Vertebrate
class
Mammals
Birds
Reptiles
Total
Species with
known audiogram
and middle-ear
measurements
Species with
known audiogram
and inner-ear
Species with
measurements
All three
15/16t
4
11
3
3
5
19
22/23?
10
2
3
15
?Number of species with known stapes footplate arealnumber of
species with known tympanic membrane area.
WHAT DID MORGANUCODON HEAR?
143
order to minimize this variability, data were chosen from as few laboratories as
possible; in cases where multiple audiometric or anatomic measurements have
been made, the data chosen were collected by laboratories that had contributed
data from other species. Accordingly, much of the selected audiometric data
were collected by Drs Masterton, Heffners and their colleagues while much of
the selected anatomic data were collected by Dr Fleischer (Appendix 1 ) .
Dejinition of allometric relationships by linear regression techniques
Model I, least-squares linear-regression techniques were used to fit power
functions, y = ax', to the data describing body weights, middle-ear dimensions
and audiometric features of the analysis population. The body weight and
anatomic estimates were used as independent variables. The probability that the
exponent (log-log slope) of the power function equalled zero was used to
quantify the significance of each relationship. The predictive power of each
relationship was quantified by the 95 yo confidence limits of prediction (Sokal &
Rohlf, 1969).
RESULTS
RelationJhips between body size and ear dimensions in extant amniotes
Before one can argue that allometric relationships in extant animals can be
used to predict auditory function in extinct animals, it should first be shown that
there are features in common between the extant and extinct animals. One
source of resemblance might be similar relationships between the size of the
animal and the sizes of auditory structures. I n order to test for such similarities,
the dimensions of the Morganucodon ear were compared with allometric functions
relating body weight to the middle-ear areas and basilar-membrane lengths in
the analysis population (Fig. 6; Appendix 2). These allometric functions are of
interest by themselves and will be discussed before the actual comparisons
between Morganucodon and extant animals are performed.
The middle-ear areas of the analysis population are plotted against body
weight in Fig. 6A,B. Much of the variability in these plots can be explained by
single power functions calculated to fit all of the extant data, regardless of class.
Not all extant ears are well fit by the power functions; the red-eared turtle has
middle-ear areas that are larger than expected from the power-function fit, while
some of the smallest mammals-mouse and bat (Rhinolophus simulator)-have
middle-ear areas that are smaller than predicted. Similar relationships between
middle-ear area and body weight have been previously reported for mammals
(Pye & Hinchcliffe, 1976; Khanna & Tonndorf, 1978; Hunt & Korth, 1980;
Heffner, 1983), and other vertebrate groups (Kirikae, 1960).
The relationship observed between basilar-membrane length and body weight
in extant ears (Fig. 6C) is more complicated. A significant power function
explains some of the variability in the body weight and basilar-membrane length
data from all amniotes, but it is obvious that the different vertebrate classes
would be better fit by separate regression lines.
A complicating factor in the relationships between body weight and ear
dimensions in extant animals is that ear dimensions also correlate with some
J. J. ROSOWSKI AND A. GRAYBEAL
144
A
' .
100
.
.
.*..."I .*.....I ....."I
1 FP Area = 0.97
Body weight
P<O.I%
.
.
....
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0
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10000
WHAT D I D MORGANUCODOH HEAR?
145
audiometric parameters, as will be discussed later. This dependence on
audiometric features contributes to some of the outlying points in Fig. 6A,B, e.g.
the red-eared turtle is a small to moderate-sized animal whose best-hearing
frequency is much lower than other animals of its body weight. Similarly the
mouse and kangaroo rat (Dipodomys merriami) are of similar body weight but
have greatly different audiograms. If the different anatomical features show
similar dependences on audiometric features and body weight, then the
anatomical data can be normalized for these factors by plotting one anatomical
feature against another (Fig. 7).
Plotting tympanic-membrane area against footplate area clearly produces a
tightly grouped data set (Fig. 7A). The turtle, kangaroo rat and mouse middleear areas--that diverged from the population trend when middle-ear areas were
plotted against body weight (Fig. 6A,B))cluster about a single power function
with the rest of the analysis population in Fig. 7A. Additionally, the power
function fit to the extant middle-ear areas is more significant than the function fit
to the variation in either area with body weight. A similar normalization
produced by plotting the extant middle-ear areas against basilar-membrane
length, does not result in such a simple outcome (Fig. 7B,C). Except for a
moderately significant allometric relationship between the footplate area and
basilar-membrane length in mammals (the thin line in Fig. 7B) no significant
relationships between the middle-ear areas and basilar-membrane length can be
found in the analysis population.
Comparisons of ear dimensions in Morganucodon and extant amniotes
Qualitatively, Fig. 6 illustrates that the dimensions of Morganucodon's basilarmembrane, stapes footplate and tympanic membrane (the Xs) are similar to
Figure 6. Comparisons of the body weight and car dimensions of Morganucodon and extant terrestrial
amniotes. T h e data points are separated by class. Data from mammals are plotted as open circles,
from birds as filled squares and from reptiles as grey diamonds. T h e Morganucodon data are plotted
with 'X'. Power-functions and lines are least-squares linear regression fits of all of the logtransformed extant data. The significance of the exponent is coded by line type; thick solid lines
denote exponents that are highly significant (the probability that the exponent = 0 is less than
0.1%), thick dashed lines and thin solid lines denote exponents which are less significant ( P < lo!,
and P < 5yn respectively). A, A log-log comparison of the area of the stapes footplate with body
weight in 2 2 extant amniotes (15 mammals, four birds and three reptiles) and Morganucodon. The
extant data set has been restricted to only those species with audiometric measurements
(Appendix I ) . T h e power function fit to all of the extant data is highly significant, the probability
that the exponent of the power function equals 0 is less than O.lq$. The standard error of estimate
about the power function was used to calculate the 95qb confidence interval for a footplate area
predicted from a body weight of 0.02 kg. T h e predicted range, 0.21-0.68 mm2, compares well with
the 0.4 mm2 stapes footplate area of Morganucodon. B, Comparison of the area of the tympanic
membrane with body weight in 24 extant amniotes (17 mammals including two dogs, four birds and
three reptiles) and Morganucodon. T h e probability that the exponent of the power function fit to the
extant data is 0 is less than I:$. T h e 95% confidence interval of prediction for the tympanic
membrane area of a 0.02 kg extant amniote is 6.4-18 mm2. T h e estimated tympanic-membrane area
in Morganucodon is slightly lower, 4.5 mm2. C, Comparison of the length of the basilar membrane and
body weight in 19 extant amniotes ( 1 I mammals, three birds and five reptiles). Although the data
from the three classes appear to cluster about separate allometric relationships, a single power
function significant at the 506 level can be fit to the grouped extant data. A power function relating
the mammalian data (membrane length = 16 body weight' 15, not shown) is significant at the 0.1".6
level. Other power functions fit to the reptilian, bird and the grouped non-mammalian data
(Appendix 2B) are not significant ( P> 5"/,).
146
PC5%
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-
WHAT D I D M O R G A X U C O D O X HEAR?
147
those dimensions in some extant amniotes. The footplate of Morganucodon is
comparable in area to those of birds-budgerigar, canary (Serinus canarius) and
alligator lizard and gecko and small
cowbird (Molothrus ater), reptiles-the
mammals-gerbil (Meriones unguiculatus), tree shrew ( Tupaia glis) and laboratory
rat (Rattus norvgicus), while the tympanic membrane area of Morganucodon is most
similar to that of the canary, alligator lizard and mouse. The Morganucodon
basilar membrane is less than half the length of the smallest mammalian
membrane in the analysis population-the mouse at 6.8 mm-and most similar
in length to membranes of the larger budgerigar, pigeon (Columba liuia), gecko
and caiman (Caiman crocodilus) . Quantitatively, the observed relationship
between amniote footplate area and body weight is consistent with the estimated
body weight and the 0.4 mm' footplate area of Morganucodon-the
95%
confidence limits of prediction for footplate area based on a body weight of
0.02 kg range from 0.21-0.68 mm', while the 4.5 mm2 Morganucodon tympanic
membrane area falls slightly below the range of areas predicted for a 0.02 kg
body weight by the power function fit of Fig. 6B-the 95% confidence limits of
prediction range from 6.4- 18.0 mm'. The body weight and basilar-membrane
length of Morganucodon are consistent with the allometric function fit to the data
from all amniotes (Fig. 6C), fall below the relatively narrow 9501, confidence
interval (6.7-13.0 mm) predicted by the mammalian data alone and are within
the wide ranges predicted by relationships calculated from the bird and reptile
data.
The relationships between the dimensions of the Morganucodon ear can also be
compared with the relationships observed between the ear dimensions in extant
ears (Fig. 7). The Morganucodon middle-ear areas are not as well fit by the power
function that relates these areas in extant ears (Fig. 7A), the area ofits tympanic
membrane (4.5 mm') falls somewhat below the 95% confidence limits of
prediction (8.8-14.0 mm') for a footplate of 0.4 mm'. This result, together with
the result of Fig. 6B suggest that the estimate of Morganucodon tympanicmembrane area is about one-half the area expected for an extant animal of
similar body size or footplate area.
The clear ordering of basilar-membrane length among the different amniote
classes observed in Figs 6C, 7B and 7C-where the basilar-membrane lengths of
mammals are long, reptiles short and birds intermediate-has led to suggestions
that this length is one of the distinguishing features between the ears of different
classes (Wever, 1974; Manley, 1971, 1973). However, the intermediate length of
the Morganucodon basilar membrane, the wide variation in basilar-membrane
lengths in animals of small body size and the limited number of small mammals
included in the study population preclude a strict classification of the
Figure 7 . Comparisons of the relationships between middle-ear areas and basilar membrane length
in Morganucodon and extant terrestrial amniotes. The extant data are coded by class as in Fig. 6. The
Morganucodon data are coded with an 'X'. The significance of the fitted lines is coded by line weight
and quality. A, A comparison of the area of the stapes footplate and tympanic membrane in
Morganucodon and 22 extant animals (15 mammals, four birds and three reptiles). The power
function fit to all of the extant data has a highly significant exponent. B, Comparison of footplate
area and basilar-membrane length in Morganucodon and 15 extant amniotes (10 mammals, two birds
and three reptiles). No significant relationship between area and length exist for all amniotes, but a
power-function fit only to the mammalian data has an exponent that is moderately significant. C,
Compares tympanic-membrane area and basilar-membrane length for the same population used in
B. No significant relationships between area and length were identified.
148
J. J. ROSOWSKI AND A. GRAYBEAL
Morganucodon ear as either bird- or reptile-like based solely on membrane length.
Certainly, the data of Fig. 7B are consistent with a mammalian classification for
Morganucodon, since the area of the Morganucodon footplate falls within the 95%
confidence limits predicted for a mammalian basilar membrane 3.1 mm in
length.
Predictions of Morganucodon auditory function f r o m middle-ear dimension5
The earlier comparisons of ear dimensions show some similarities between
these dimensions in Morganucodon and extant amniotes of similar size. Next,
significant relationships between auditory function and ear dimensions will be
demonstrated in extant ears and then used to predict the auditory function of
Morganucodon-like ears. The demonstration of significant structure-function
relationships in extant amniotes is complicated by both the presence of obvious
interclass differences, and the small number of birds and reptiles in the analysis
population. I n order to minimize these complications, separate relationships are
defined for the mammalian and the grouped bird and reptile data. (Because of
the general similarity of auditory structures in birds and reptiles and the small
number of species from these classes in the study population they are grouped
together as bird-reptiles in this and later analyses.) Figure 8 illustrates that there
are significant power-function relationships (Appendix 2) between the footplate
areas and certain audiometric features in extant amniotes. Similar relationships
can be observed between the tympanic-membrane area and audiometry
(Appendix 2).
The data of Figure 8 fit into several categories. (a) A class independent
relationship explains much of the variation seen across all amniotes in the
relationship between low-frequency limit and footplate area. (b) I n some cases,
the mammalian and bird-reptile data are fit by strong separate relationships, e.g.
the relationships between centre frequency, high-frequency limit and the middleear areas. These separations by class are consistent with the idea that while
mammals and bird-reptiles of similar size have similar middle-ear areas, their
auditory abilities are very different-i.e. mammals have better high-frequency
hearing than reptiles or birds with similar sized middle ears. (c) There are also
cases where significant relationships are observed between footplate area and
audiometry in either mammals or bird-reptiles but not both, e.g. best frequency
us. footplate area in mammals and best threshold us. footplate area in birds and
reptiles.
The allometric relationships of Figure 8 and Appendix 2 can be used to
predict audiometric features for mammals and non-mammals with middle-ear
equal to that of Morganucodon, but since the significances of the relationships
vary, their predictive values vary. Moreover, the significance of the exponent is
not by itself an accurate estimate of the predictive value of each relationship;
accurate predictions of function from structure can be made when the variation
of the audiometric feature in the population is small, even if the feature does not
vary with middle-ear area (exponent of 0). I n order to quantify the individual
predictive value of each relationship the standard error of estimate has been used
to calculate the 95% confidence limits of predictions (Sokal and Rohlf, 1969).
Good predictive relationships generate narrow confidence limits, while poor
predictors generate wide limits.
W H A T D I D MORGAXUCODON HEAR?
149
----
P < 0 .I%
O.I%<P<I%
l%<P<5%
5%<P
-
--I
V
x
a,
'-46,
KangaroaP'
-2
255
c
ac
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0.1
0.01
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4
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0 .I
I
10
100
0.01
0. I
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10
100
0.1
0.01
0.1
0.01
0.1
I
10
100
0.01
0.1
I
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10
10
100
100
Footplate area (mm2 1
Figure 8. Data relating the footplate area and the frequency and threshold features extracted from
audiograms of extant animals. The data points are coded by class. T h e lines represent power
functions fit to either the mammal or bird-reptile data by least-squares methods. T h e level of
significance is coded by line type. Highly significant relationships (the probability that the exponent
equals zero is les than O.lo/o)-the thick solid lines-were found between footplate area and centre
and low-frequency of the audiogram in mammals. Slightly less significant relationships (0.I"< <
P < 1 %)-the thick dashed lines-were observed between footplate area and best-frequency,
low-frequency and bandwidth in mammals as well as between area and centre frequency and highfrequency limit in bird-reptiles.
In general, the ranges of auditory features predicted for amniotes with
Morganucodon-like middle-ear areas are relatively narrow (within a factor of
three), and there is a clear separation between some of the predictions for
mammals and bird-reptiles (Table 3 ) . The narrow ranges of predicted features
result from either a significant relationship between ear dimension and
audiometry (as is the case for the predicted centre frequencies), a narrow range
of features within the study population (the case for predictions of best threshold
in mammals), or some combination of these two. A mammal with a stapes
J. J. ROSOWSKI AND A. GRAYBEAL
150
TABLE
3. Audiometric featurest
~
Feature
Predicted for a
mammalian ear
Predicted for a
bird-reptile ear
Predicted for a stapes-footplate area of 0.4 mm2
6.1 < 11 < 20 kHz
Best frequency
5.6 < 7.6 < 10 kHz
Centre frequency
0.63 < 1.1 < 2.0 kHz
Low-frequency limit
42 < 51 < 62 kHz
High-frequency limit
1.4 < 1.7 < 1.9 decades
Bandwidth
-8 < -3 < 2 dB SPL
Best threshold
0.54 < 1.6 < 4.8 kHz
0.79 < 1.3 < 2.1 kHz
0.1 1 < 0.25 < 0.56 kHz
4.2 < 6.4 < 9.6 kHz
1.0 < 1.4 < 1.8 decades
2 < 10 < 18 dB SPL
Predicted for a tympanic mnnbrane area of 4.5 mn?
Best frequency
9.7 < 21 < 46 kHz
Centre frequency
11 < 15 < 21 kHz
Low-frequency limit
1.7 < 3.2 < 6.3 kHz
High-frequency limit
50 < 68 < 92 kHz
Bandwidth
0.99 < 1.3 < 1.7 decades
Best threshold
-11<-4<3dBSPL
0.32 < 1.8 < 10 kHz
0.91 < 2.2 < 5.2 kHz
0.14 < 0.47 < 1.6 kHz
4.1 < 10 < 24 kHz
0.77 < 1.3 < 1.9 decades
- 1 2 < 2 < 16dBSPL
Predicted for a basilar-membrane length of 3.1 mm
Best frequency
0.83 < 12 < 160 kHz
Centre frequency
3.4 < 21 < 130 kHz
Low-frequency limit
0.16 < 3.1 < 59 kHz
High-frequency limit
54 < 150 < 400 kHz
Bandwidth
0.63 < 1.7 < 2.7 decades
Best threshold
-16 < - 1 < 13 dB SPL
0.92 < 1.7 < 3.1 kHz
0.50 < 0.88 < 1.6 kHz
0.08 < 0.16 < 0.33 kHz
2.9 < 4.9 < 8.3 kHz
1.2 < 1.5 < 1.7 decades
-4 < 4 < 13 dB SPL
?Each cell contains the parameter predicted by the specific ear dimension for either
a mammalian or bird-reptile ear, as well as the lower and upper limits of the 95%
confidence interval of prediction.
footplate of 0.4 mm2 is predicted to have an audiogram with a best frequency
between 6.1 and 20 kHz and with a high frequency limit between 42 and
62 kHz, while a bird or reptile with an identically sized footplate will have a best
frequency of 0.54-4.8 kHz, and a high-frequency limit of less than 10 kHz. The
best thresholds predicted for mammalian ears are quite low, -8-2 dB SPL,
while the thresholds predicted for non-mammal ears are somewhat higher,
2-18 dB SPL. Both the mammalian and non-mammalian relationships predict a
relatively narrow sensitive bandwidth of 1-2 decades for an ear with 0.4 mm2
stapes footplate. Predicted audiometric features based on a tympanic membrane
area of 4.5 mm2 give rise to broader limits of somewhat higher frequencies
(Table 3).
Predictions of Morganucodon auditory function from inner-ear dimensions
The inner-ear data and audiometric features from the analysis population
were also used to generate power functions that related basilar-membrane length
and audiometry in extant amniotes (Fig. 9; Appendix 2), though few strong
allometric relationships were apparent. The most significant relationship
observed in the mammalian data is an inverse relationship between the highfrequency hearing limit and basilar-membrane length-see West ( 1985) for a
similar observation. This inverse relationship points out a subtle distinction
between mammals and bird-reptiles; in the later group short basilar-membranes
WHAT D I D MORGANUCODON HEAR?
Pt0.196
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151
-------
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o o
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Basilar-membrane length (mm)
Figure 9. Data relating the basilar-membrane length and the frequency and threshold features
extracted from audiograms of extant animals. T h e data points are coded by class. T h e lines
represent power functions fit to either the mammal or bird-reptile data by least-squares methods.
T h e level of significance is coded by line type. Very significant relationships (0.1yo < P < 1%) -the
thick dashed lines---were observed between membrane length and high-frequency limit in mammals
as well as length and best threshold in non-mammals. Moderately significant relationships (1% <
P < 5yo)-the thin solid lines-were observed between length and centre frequency in mammals
and length and best frequency in bird-reptiles.
are usually associated with low-frequency hearing (Manley, 1971, 1973), while
in the former short membrane length is associated with better high-frequency
hearing. The most significant relationship observed in birds and reptiles is
between best threshold and basilar-membrane length. Weaker relationships can
be found between best frequency and membrane length in bird-reptiles and
centre frequency and membrane length in mammals.
The 95% confidence limits of predictions based on the relationships of Fig. 9
are noted in Table 3. The predicted ranges of audiometric features for a bird-
152
J. J. ROSOWSKI AND A. GRAYBEAL
reptile inner ear with a 3.1 mm long basilar membrane are comparable to the
ranges predicted from the analysis of stapes-footplate area and audiometric
features in bird-reptiles. (The narrow width of some of the ranges result
primarily from the narrow range of features within the non-mammalian study
population, e.g. low-frequency limit and bandwidth). The ranges of the
audiometric features predicted for a 3.1 mm long mammalian basilar membrane
are for the most part very broad and non-specific (larger than a factor of 30).
These broad ranges are consistent with the suggestion that the mammalian inner
ear acts as a non-selective power detector at auditory threshold (Khanna &
Sherrick, 1981; Rosowski et al., 1986).
Likely auditory areas of Morganucodon-like ears
The auditory area represents the combination of sound frequencies and levels
that are heard by an animal. Likely auditory areas for mammals or bird-reptiles
with Morganucodon-likemiddle- and inner-ear dimensions can be defined from the
ranges of predicted audiometric features listed in Table 3. These likely auditory
areas are plausible limits for discussions of the auditory function of Morganucodon.
The combination of predicted ranges of audiometric features in Table 3 can
be used in many schemes to reconstruct audiograms and auditory areas. Two
simple schemes follow; the first makes use of the absolute predictions of
audiometric features that result from the allometric analyses summarized in
Table 3, the second includes the probable ranges of the predicted audiometric
features (Fig. 10). These schemes both use the estimates of best frequency and
low- and high-frequency limits along with estimates of the best threshold to
predict the lower-limits of the auditory area and are defined in detail in the
caption of Fig. 10. The darker regions in Fig. 10 envelope the auditory areas
constructed from the absolute predictions and represent one set of estimates of
the combinations of sound frequencies and levels that would be audible to
mammals or bird-reptiles with Morganucodon-like ear dimensions. A separate
estimate has been made for each of the three ear dimensions used in the analyses.
The darker areas are fairly narrow, and are generally of higher frequency and
extend to lower levels in the mammalian case. In addition, the areas estimated
for each amniote grouping are more alike than across-group estimates predicted
from the same ear dimension.
Although the regions of darker shading in Fig. 10 tell us something about the
tendencies of the audiometric features predicted for Morganucodon-like ears, they
ignore the variable confidence intervals of the prediction procedures (Table 3)
and thereby underestimate the limits imposed on the possible auditory area by
the allometric analyses. The influence of the confidence intervals is included in
the regions of lighter shading in Fig. 10, where the prominence of the lighter
regions is directly related to the width of the 95% confidence interval for each of
the predicted features. Narrow bands of lighter shading result from narrow
confidence intervals, e.g. those predicted by the mammalian middle-ear areas
(the left panels of Fig. 9A,B). Wide bands of lighter shading are produced by
broad confidence intervals, e.g. those predicted for mammals with
Morganucodon-like basilar-membrane lengths (the left panel of Fig. 9C). The
combination of the dark and light shadings define the limits imposed on auditory
area by each ear dimension. There is a low probability that sound frequency-
WHAT DID MORGANUCODON HEAR?
153
Auditory areas of
Moraanucodon- like ears
Predicted for mammals
Predicted for bird-reDtiles
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D
c
o
m0
-20
0.01
Frequency ( k H z 1
Figure 10. Auditory areas computed from the predicted ranges of audiometric features produced by
the allometric analysis. Predictions are made for mammals and bird-reptiles with Mol-ganucodon-like
ear dimensions. Separate predictions are made for each of the three ear dimensions used in the
analyses. T h e dark areas are estimates of auditory area drawn with three points: a centre point [ 1)
defined by the predicted best frequency and best threshold, a low-frequency point ( 2 ) defined by the
low-frequency limit and a level 30 dB greater than best threshold, and a high-frequency point ( 3 )
defined by the high-frequency limit and a level 30 dB above the best threshold. The lighter areas
represent the addition of uncertainties to these simple estimates of auditory area. T h e lower limits of
the lighter areas are defined by four points: two centre points (4 and 5) defined by the upper and
lower 95"/, confidence limits of the best-frequency estimate with levels equal to the lower confidence
limit around the best-threshold estimate, the lowest frequency point ( 6 ) is at the lower bound of the
95% confidence interval about the predicted low-frequency limit and a level equal to 30 dB above
the lower bound of the confidence limit around best threshold, the highest frequency point (7) is at
the same level and a frequency equal to the upper bound of the 95% confidence interval around the
high-frequency limit. Panels A, B and C illustrate the audible areas predicted for animals with a
Morganucodon-like footplate area, tympanic-membrane area, and basilar-membrane length
respectively.
40
-
20
-
0-
-20
Mammalian ears
........
........ ........
I
0.01
I
I
0.1
I
. Bird-reptile
-
I
..-...-I
10
100
....
1000
ears
Mammalian
ears
-20
........ ................................... i
I
0.01
0.1
I
10
100
1000
100
1000
Bird-reptile inner ear
and mammalian middle aer
-
2
0.01
0.1
0
I
10
2
Frequency ( k H L )
Figure 1 1. The most-likely auditory areas predicted for amniotes with Morganucodon-like ear
dimensions. A, The most-likely auditory area of a mammal with Morganucodon-like ear dimensions.
The auditory area is defined by the area of overlap of the shaded regions on the left-hand side of
Fig. 10. B, The most-likely auditory area of a bird-reptile with Morganucodon-like ear dimensions.
The auditory area is defined by the area of overlap of the shaded regions on the right-hand side of
Fig. 10. The dashed lines outline the most-likely auditory area for a mammal defined in Fig. 11A. C ,
The likely auditory area of an amniote with a bird-reptile like inner ear and mammal-like middle
ear of Morganucodon-like dimensions is defined by the area of overlap between the shaded regions on
the left-hand side of Fig.lOA, B and the right-hand side of Fig. IOC.
WHAT DID MORGANUCODON HEAR?
155
level pairs outside of the shaded regions will be heard by animals with
Morganucodon-like ear dimensions, while sound frequency-level pairs within the
shaded regions are more likely to be heard.
Since each of the three ear dimensions imposes their own limits on the
auditory area of Morganucodon-like ears, the region of overlap of the three limits
defines a ‘most-likely auditory area’ for Morganucodon-like ears (Fig. 1 lA,B).
Separate areas can be constructed for mammalian or bird-reptile ears with
Morganucodon-like ear dimensions, and not surprisingly, the most-likely auditory
area for a mammalian ear is of higher frequency and includes lower sound levels
than the most-likely auditory area predicted for a bird-reptile ear (Fig. 11B).
These differences in most-likely auditory area are similar to the differences in the
auditory capabilities of extant small mammals and bird-reptiles. (Compare the
predicted areas with the audiograms of mouse, budgerigar and gecko in Fig. 4).
The definitions of the limits on auditory area imposed by different ear structures
in different classes of ears permits the construction of hypothetical auditory areas
for ears of mixed classes, e.g. Fig. 11C shows the auditory area defined by the
overlap of the limits on auditory area imposed by a mammalian middle ear of
Morganucodon-like dimensions and a bird-reptile inner ear with Morganucodon-like
basilar-membrane length.
The allometric analyses, by themselves, cannot determine which of the mostlikely auditory areas for extant amniotes of Morganucodon-like ear dimensions
(Fig. 11) best describes the auditory area of Morganucodon. This limitation arises
because the overlap of the middle-ear dimensions of the different amniote classes
and the intermediate length of the Morganucodon basilar membrane precludes
classifying the Morganucodon ear as either mammalian or non-mammalian.
Additional structural information that helps further classify the Morganucodon ear
will be discussed.
DISCUSSION
Signijicance of the allometric analyses in extant ears
In retrospect, the final results of the allometric analyses are not surprising.
Several comparative studies (Saunders & Johnstone, 1972; Manley, 1973;
Wever, 1978; Dooling, 1980) have already implied that mammals and birdreptiles with similar ear dimensions have different auditory areas. The analyses
performed here, nonetheless, are unique in that they have quantified the limits of
prediction about such structure-function comparisons in terrestrial amniote ears.
The analyses also produced a number of results that are of interest in themselves.
First, significant relationships have been revealed between body size and ear
size in extant amniotes. Much of the variation in the middle-ear areas of all
amniotes can be explained by significant allometric relationships between each
area and body weight (Fig. 6A,B). Similar relationships have been alluded to by
earlier investigators (Kirikae, 1960; Pye & Hinchcliffe, 1976), but have only
been quantified for the grouped ears of mammals (Khanna & Tonndorf, 1978;
Hunt & Korth, 1980) and dogs (Heffner, 1983). A significant allometric
relationship has also been demonstrated between the length of the basilar
membrane and body weight in mammals but not reptiles and birds (Fig. 6C).
Secondly, the areas of the tympanic membrane and footplate in all amniotes
are shown to be significantly related by a single function. This relationship has
156
J. J. ROSOWSKI AND A. GRAYBEAL
been quantified by a power function with an exponent that is significantly
different from 1 (Fig. 7A); but the data are also well fit by a simple linear
relationship where tympanic-membrane arealstapes-footplate area = 22. Kirikae
( 1960) suggested a similar relationship between tympanic-membrane and ovalwindow areas in mammals but not birds or reptiles.
Thirdly, there are highly significant relationships between middle-ear
dimensions (stapes-footplate and tympanic-membrane area) and audiometric
features. These relationships are generally class dependent (Fig. 8). The areas of
the mammalian middle ear were observed to be inversely related to the lowfrequency limit, centre frequency, high-frequency limit and directly related to
the bandwidth of the species audiogram. Separate highly-significant inverse
relationships were demonstrated between the areas of the bird-reptile middle ear
and the centre frequency and high-frequency limit of the audiogram. The
relationships quantified for both mammalian and non-mammalian middle ears
are consistent with the notion that smaller membrane and footplate areas
respond best to sounds of smaller wave lengths and higher frequencies (Khanna
& Tonndorf, 1978). Other authors have noted similar inverse relationships
between middle-ear size and best frequency in select groups of mammals
(Henson, 1961; Fleischer, 1978).
Fourthly, there are a few audiometric features that are significantly related to
basilar-membrane length in a class-dependent manner (Fig. 9). These include
inverse relationships between best threshold and basilar-membrane length in
birds and reptiles as well as high-frequency limit and basilar-membrane length
in mammals. The later relationship has been previously described by West
(1985) although the significance of the inverse relationship has not been
generally appreciated. While several authors have related the poor highfrequency hearing in reptiles and birds to their short basilar membranes
(Manley, 1971, 1973; Wever, 1974), in mammals, short basilar membranes are
associated with poor low-frequency hearing and better high-frequency hearing.
The inverse relationship observed between basilar-membrane length and best
threshold in the non-mammals of the analysis population is heavily influenced by
the extremely low best threshold of the long-membraned barn owl and the
extremely high best threshold of the short-membraned red-eared turtle.
Predictions of ear structure from allometry
The simple allometric relationships described between body size and the
middle-ear areas of all terrestrial amniotes (Figs 6, 7) shed some light on
arguments concerning the ear structure of extinct animals. As has been noted,
there is some controversy concerning the size and location of the tympanic
membrane in Morganucodon. One group (Westoll, 1943, 1945; Hopson, 1966;
Parrington, 1979) has argued that the tympanic membrane of Morganucodon and
similar animals was located behind the quadrate bone, partially bounded by the
squamosal bone, and that there was a direct connection between the tympanic
membrane and the stapes. Another group (Allin, 1975; Kermack & Musset,
1983) contends that the tympanic membrane was located in the lower jaw, and
was connected to the angular and articular bones, as pictured in Figs 1, 2 of this
report. One of the arguments of the latter group is that a post-quadrate
tympanic membrane in Morganucodon would have been too small, about 1 mm',
WHAT DID hf0RGANUCODO.N HEAR?
157
to act as an effective sound receiver (Kermack & Musset, 1983). The
relationships between body size and the middle-ear areas described in this report
also argue against the smaller post-quadrate tympanic membrane. Indeed,
comparisons with extant animals of similar body weight (Fig. 6B) and footplate
area (Fig. 7A) suggest that the larger area of a angulo-articular tympanic
membrane (4.5 mm‘) is already only one-half of the area expected for an
amniote of Morganucodon’s size, while the smaller 1 mm2 maximum area of a
post-quadrate tympanic membrane area is one-tenth of the expected area as well
as one-half the area of the smallest membrane in the analysis population.
Clearly, the comparative analyses favour the larger membrane area associated
with the lower-jaw location.
T h e auditory area o f Morganucodon
Predictions of auditory function f r o m allometry: how f a r can one extrapolate function from
structure?
The allometric analyses presented in this report have enabled predictions of
auditory function in mammalian or bird-reptile ears with Morganucodon-like
dimensions. How can one extrapolate those functions to Morganucodon? Some
basic questions about such extrapolations include whether an auditory area
predicted from extant animals is applicable to Morganucodon, and if so, should the
prediction be based on mammalian, bird or reptile ears?
Arguments for extrapolating Morganucodon auditory function from extant
animals include: ( 1 ) all amniote ears contain a sound-receptive membrane
coupled to a footplate by an ossicular system and a fluid-filled inner ear,
therefore, the suggestion that similar structures in extinct animals functioned in a
similar manner is probably valid; (2) the dimensions of Morganucodon’s ear
structures appear roughly consistent with those of extant animals of similar body
size (Figs 6, 7 ) .
Questions concerning the applicability of extrapolations from either mammals
or non-mammalian amniotes are more difficult to answer. Although, the
allometric analyses reported here point out that the ears of these two amniote
groups function in different manners (e.g. a mammalian ear is more sensitive to
higher frequency sounds than a non-mammalian ear of similar dimensions),
there is much overlap in the sizes of the auditory structures within each class.
Based solely on the dimensions of the ear, there is no reason to prefer the
auditory area predicted by one type of ear over the other.
There is another level of question regarding the extrapolation of auditory
function from the data presented in this report, i.e. can the function of unique
anatomic features be extrapolated from the relationships described by the
analysis population? The dimensions of Morganucodon’s auditory structures are
bracketed by those of extant animals with similar body weight, with one
exception; at one-half the length of the smallest mammalian basilar membrane
in the study population, the length of the Morganucodon basilar membrane is
distinctive. This unique basilar-membrane length is partly responsible for the
wide limits around the functional predictions based on extant mammalian
membrane lengths. More accurate predictions of auditory function might be
possible if other extant mammals of small body size and short membrane lengths,
e.g. shrews, could be added to the analysis population. Although we’ve found no
158
J. J. ROSOWSKI AND A. GRAYBEAL
measurements of basilar-membrane length or audiograms in shrews, descriptions
of their cochlea (Platzer & Firbas, 1966) suggest basilar membrane lengths of
4-5 mm, and the principal frequencies of shrew vocalizations used in
echolocation range between 25 and 60 kHz (Gould, Negus & Novick, 1964).
These lengths and frequency limits are roughly consistent with the significant
relationship observed between membrane length and high-frequency limit
(Fig. 9), and would bridge part of the gap between Morganucodon and the
mammals in the present analysis population.
Injuence of other features of the Morganucodon ear on auditory function
Although the allometric analyses do not allow us to specify whether the
Morganucodon ear was either mammal- or non-mammal-like, other structural
features of the ear may be used to distinguish one ear type from the other.
The presence of a pinna and long external auditory canal is a mammalian trait, but
the existence of either in Morganucodon is a matter of conjecture. The evidence for
a post-quadrate ear canal in mammal-like reptiles and early mammals
(Parrington, 1949, 1979; Hopson, 1966) has been reinterpreted by Allin (1975)
and is inconsistent with the placement of the tympanic membrane favoured by
Allin (1975) and Kermack & Musset (1983). The lack of firm evidence for or
against a pinna does not permit further classification of the Morganucodon ear.
There are qualitative differences in the stzfness of the middle-ear of different
mammals and non-mammals. Most birds, reptiles and many larger mammals
have flaccid middle-ears in which the ossicular system is freely mobile with little
or no attachment to the surrounding bone (Wever & Lawrence, 1954; Bkkksy,
1960; Saunders & Johnstone, 1972; Fleischer, 1978; Wever, 1978). However, in
small mammals with small middle-ear dimensions-e.g. house mouse, rats, bats
and shrews-as well as monotremes and marsupials there is a large and firm
attachment between the tympanic bone and malleus (Aitkin &Johnstone, 1972;
Fleischer, 1973, 1978; Gates et al., 1974) that is not unlike the suggested
symphyseal attachment between their homologues, the angular and articular
bones, in Morganucodon. Several authors have associated such strong malleartympanic linkage with middle ears that are selectively receptive to highfrequency sound (Reysenbach de Haan, 1958; Fleischer, 1973, 1978). There is
also evidence that these extensive mallear-tympanic attachments result in ‘stiff
middle ears with a reduced sensitivity to low-frequency sounds. The strong
symphyseal connections between the tympanic bone and malleus in the echidna
and house mouse result in low-frequency tympanic-membrane motions that are
10-30 times smaller than those observed in mammals, reptiles and birds with
freely mobile middle ears (Aitkin & Johnstone, 1972; Saunders & Johnstone,
1972; Saunders & Summers, 1982). I n the Morganucodon ear, as reconstructed by
Kermack et al. (1981, 1983), the middle ear motions would be constrained by the
stiffness to rotation of both the angulo-articular complex and the quadrate
(Fig. 2B). The likely stiffness of the ligamentous connections between the
Morganucodon angulo-articular complex and dentary, and between the quadrate
and the squamosal, which might be substantiated by some objective comparison
of the dimensions of these ligaments in Morganucodon and extant animals, is
inconsistent with the freely mobile middle ears of birds, reptiles and large
mammals, and more like the stiff middle ears of small mammals with better
high-frequency hearing and poor sensitivity to low-frequency sounds.
WHAT DID MORGANUCODON HEAR?
159
A bony cochlear lamina is another structural difference between bird-reptile and
mammalian ears. The cochlear lamina supports one side of the basilar
membrane in all amniotes and helps determine the membrane’s width. In birds
and reptiles the lamina is cartilaginous (Mulroy, 1974; Wever, 1978; Smith,
1985) while a bony lamina is present in all extant mammalian ears. A welldeveloped bony lamina has been associated with sensitivity to high-frequency
sound, and in those mammals sensitive to ultra-high sound frequencies a second
lamina is often apparent (Reysenbach de Haan, 1958; Fleischer, 1973; Pye &
Hinchcliffe, 1976). The seeming lack of a bony lamina makes the inner ears from
the available Morganucodon material appear bird or reptile-like, but it is not clear
that such a lamina would have survived the processes of fossilization or
preparation (Graybeal et al., 1989). Future investigations of unprepared
Morganucodon inner ears may well demonstrate the presence of a bony lamina in
these early mammals.
The lack of cochlear coiling contributes to the non-mammalian appearance of
the Morganucodon inner ear, but the utility of the coiled cochlea in mammals is
unclear. The cochlear curvature appears to have minimal effect on the auditory
sensitivity of most mammals (BkkCsy, 1960; Zwislocki, 1965; Allen, 1977; Steele
& Taber, 1981), but some authors have suggested that coiling affects the
sensitivity to ultra-high frequency sound (Ketten, 1984; West, 1985). It has also
been suggested that coiling simply permits compact storage of the long
mammalian basilar membrane, see West (1985) for a discussion of this point. At
any rate, the lack of cochlear coiling places no limits on the auditory sensitivity
to most sounds and probably does not contribute to the differences in inner-ear
function observed between mammals and other amniotes.
The most-likely auditory areas
The allometric analyses reported here result in several ‘most-likely’ auditory
areas for amniotes with Morganucodon-like ear dimensions (Fig. 1 1 ) . These
auditory areas are produced by the combination of the limits imposed by
Morganucodon-like middle- and inner-ear dimensions in either mammals or bird
reptiles (Fig. 10). For example, the auditory area illustrated in Fig. 11C has
been defined as the region of overlap of the limits imposed on auditory area by a
Morganucodon-sized mammalian tympanic membrane and footplate and a birdreptile basilar membrane of Morganucodon-like length. Another alternative
auditory area can be constructed by the overlap of the broad limits imposed by a
mammalian basilar membrane of Morganucodon-like length and a bird-reptile
middle ear, however, this area is virtually identical to the area defined for birdreptile middle and inner ears (Fig. 11B).
As has already been discussed, the allometric analyses by themselves are not
capable of distinguishing between any of the most-likely auditory areas defined
in Fig. 1 1, however some of the other structural features of the Morganucodon ear
suggest the following ranking of the likelihood of the predicted areas.
The freely mobile middle ear in extant birds and reptiles is inconsistent with
the likely stiffness of the middle ear described by Kermack & Musset’s (1983)
reconstruction of the Morganucodon, and therefore the auditory area predicted for
an extant bird or reptile with Morganucodon-like ear dimensions (Fig. 11B) is
considered the least probable of the three auditory areas predicted by the
allometric analyses. Alternative middle-ear reconstructions that result in a
160
J. J. ROSOWSKI AND A. GRAYBEAL
similar tympanic-membrane area while bypassing the apparent stiffness of the
angulo-dentary and quadrato-squamosal joints (e.g. a direct connection between
the stapes and lower-jaw tympanic membrane) would be more consistent with
the bird-reptile like auditory area predicted for Morganucodon-sized ears, but are
less likely from other considerations (Westoll, 1943, 1945; Parrington, 1979;
Allin, 1975; Kermack et al., 1981, 1983).
The auditory area that results from the combination of a mammalian middle
ear and bird-reptile inner ear of Morganucodon-like dimensions suggests an ear
that is sensitive to a very narrow range of moderate frequencies with poor
sensitivity to both high and low-frequency sound (Fig. 11C). Such an auditory
area is qualitatively similar to the function hypothesized for the Morganucodon ear
by Kermack & Musset (1983). However, the presence of a reptile-like inner ear
in an advanced member of the mammal-like reptile line seems improbable, and
the combination of a such an inner ear with a mammal-like middle ear is
non-parsimonious.
The most-likely auditory area for Morganucodon is the area predicted for a
mammal with Morganucodon-like dimensions (Fig. 1 1A). The auditory function
predicted by this area is similar to the function predicted for a primitive
mammal from both the audiometric data of Masterton and co-workers
(Masterton et al., 1969) and the ethological arguments of Jerison (1973). The
selection of this area as most-likely is consistent with the stiff small mammal-like
middle ear of Morganucodon, presumes a mammal-like inner ear function for the
short uncoiled cochlea of Morganucodon, and assumes that the lack of a bony
lamina in the available Morganucodon material is an artefact of either fossilization
or preparation. A clear demonstration of a bony cochlear lamina in the
Morganucodon inner ear would greatly increase the likelihood that the mammallike auditory area is a correct description of auditory function in this animal.
GENERAL CONCLUSIONS
Significant allometric relationships can be found between body size, ear
dimensions and auditory function in extant amniotes, and these relationships can
be used to make predictions of auditory function in extinct mammals. Extant
mammals with Morganucodon-like stapes-footplate and tympanic-membrane areas
are small in size, are most sensitive to relatively high-frequency sounds ( 2
6 kHz) and hear sounds of frequencies greater than 50 kHz, while extant reptiles
and birds with similar middle-ear areas are of varied body size, are most sensitive
to sounds near 1 kHz and are insensitive to sound frequencies greater than
10 kHz. The apparent high stiffness of the Morganucodon middle ear is most like
the ears of small extant mammals, while the middle ears of birds and reptiles are
flaccid and freely-mobile. Moreover, although the inner ear of Morganucodon (as
reconstructed by Graybeal et al., 1989) appears reptile-like, the evidence for this
classification is not conclusive, and mammals with a short Morganucodon-like
basilar membrane would be expected to be sensitive to high-frequency sounds.
Therefore, the evidence suggests that the middle and inner ear of Morganucodon
functioned much like those of modern small mammals with high-frequency
hearing. An alternative suggestion is that the combination of a small stiff
mammalian middle ear and bird-reptile-like inner ear in Morganucodon resulted
in an ear that was sensitive to a narrow range of moderate frequencies. Evidence
WHAT DID M O R G A N U C O D O N HEAR?
161
for or against the presence of a bony cochlear lamina in Morganucodon would help
distinguish between the alternative auditory areas, while either of the two mostprobable alternatives would be supported by some objective measure of the
stiffness of the Morganucodon middle ear.
ACKNOWLEDGEMENTS
The authors would like to thank Drs A. W. Crompton, D. R. Ketten, N. Y.-S.
Kiang, W. T. Peake and W. F. Sewell for their help and advice. We are also
grateful for the assistance of the staff of the Eaton-Peabody Laboratory. This
work was funded by National Institute of Health grants DC-POI-00119 and
DC-RO 1-00194.
REFERENCES
AITKIN, L. hl. & JOHNSTONE, B. M., 1972. Middle-ear function in a monotreme: the echidna
( Tachyglossus aculeatus) . Journal of Experimental ,Soology, I@: 245-250.
ALLEN, J. B., 1977. Two-dimensional cochlear fluid model. Journal of the Acoustical Sociefv o/. .4merica, 61:
110-1 19.
ALLIN, E. F., 1975., Lvolution of the mammalian middle ear. Journal oj'.Morphology. 147: 403--437.
BEKESEY, G. V., 1960. Experiments in Hearing. New York: McGraw Hill.
BROOM, R., 1912. O n the structure of the internal ear and the relations of the basicranial nerves in Diyzodon,
and on the homology of the mammalian auditory ossicles. Proceedings of' the ~oologicalSociety of I.ondon, ??:
4 1942.5.
CROMPTON, A. W., 1963. O n the lower jaw of Diarthognathus and thc origin of thr mammalian lowrr jaw.
ProceedintJ of the ,Soological Society of London, 140: 697-753.
CROMPTON, .4.W. & JENKINS, F. A., Jr., 1973. Mammals from reptiles: A review of mammalian origins.
Annual Revieuis of Earth and Planetary Sciences, I : 131-135.
CROMPTON, A . W. & PARKER, P., 1978. Evolution of the mammalian masticator); apparatus. American
Scientist, 66: 192 -201.
DALLOS, P., 1973. The Auditory Periphery. New York: Academic Press.
DALLOS, P., 1981. Cochlear physiology. Annual Review of Psychology, 32: 153-190.
DAVIS, H., 1965. A model for transducer action in the chochlea. Cold Spring Harbor S,mposza in &antitatioe
Biology, 30: 181-190.
DOOLING, R . J., 1980. Behavior and psychophysics ofhearing in birds. In A. N. Popper & R . R. Fay (Eds),
Comparative Studies oJ- Hearing zn Vertebrates: 261-288. New York: Springer-Verlag.
DOOLING, R . J. & SAUNDERS, J. C., 1975. Hearing in the parakeet (Melapsitacus undulatus): Absolute
thresholds, critical ratios, frequency-difference limens and vocalizations. Journal of Comparative and
Physiological Pg~hology,88: 1-20.
DOOLING, R. J., MULLIGAN, J. A. & MILLER, J. D., 1971. Auditory sensitivity and song spectrum of the
common canary (Serinus canarius). Journal of the Acoustical Society of America, 50: 700-709.
EATOCK, R. A,, MANLEY, G. A. & PAWSON, L., 1981. Auditory nerve fiber activity in the Tokay Gecko:
I. Implications for cochlear processing. Journal of Comparative P h y s i o l o ~A , 142: 203-2 18.
FAY, R. R., 1988. Hearing in Vertebrates. Winnetka, Illinois: Hill-Fay Associates.
FERNANDEZ, C., 1952. Dimensions of the cochlea (guinea pig). Journal ofthe Acoustiral Society of America, 24:
5 19-523.
FLEISCHER, G., 1973. Studien am Skelett des Gehororgans der Saugetiere, einschlirsslich des Menschen.
Saugetierkundl. Mztteilungen (Munchen), 21: 13 1-239.
FLEISCHER, G., 1978. Evolutionary principles of the mammalian middle car. Advance5 in Anatomy. Embryology
and Cell Biology, 55: 3-69.
GATES, G. R., SAUNDERS, J . C., BOCK, G. R., AITKIN, L. M. & ELLIC)T, ,M. A,, 1974. Peripheral
auditory function in the platypus, Ornithorhyncuc anatinus. Journal of the Acoustical Society qf America, 56:
152-156.
GOULD, S. J., 1966. Allometry and size in ontogeny and phylogeny. Biological Keuzess, 41: 587-640.
GOULD, E., NEGUS, N. C. & NOVICK, A,, 1964. Evidence for echolocation in shrews. Journal oJ
Experimeutal ,Soology, 156: 19-38.
GRAYBEAL, A,, ROSOWSKI, J. J . , KETTEN, D. R . & C R O M P T O N , A. W., 1989. Inner-ear structure in
Morganucodon, an early Jurassic mammal. ~oologicalJou~nal o f t h e Linnean Society, 96: 107-1 17.
GREENWOOD, D. G., 1961. Critical bandwidth and the frequency coordinates of the basilar membrane.
Journal of the Aroustical Society of America, 33: 1344-1356.
162
J. J. ROSOWSKI AND A. GRAYBEAL
HEFFNER, H. E., 1983. Hearing in large and small dogs: absolute thresholds and size of the tympanic
membrane. Behavioral Neuroscimce, 97: 3 1 G 3 18.
HEFFNER, R. S. & HEFFNER, H. E., 1982. Hearing in the elephant (Elephas maximus): absolute sensitivity,
frequency discrimination, and sound localization. Journal of Comparative and Physiological Psychology, 96:
926-944.
HEFFNER, R. S. & HEFFNER, H. E., 1983. Hearing in large mammals: horses (Equus caballus) and cattle
(Bos taurus). Behavioral Neuroscience, 97: 299-309.
HEFFNER, R. S. & HEFFNER, H. E., 1985. Hearing range of the domestic cat. Hearing Research, 19: 85-88.
HEFFNER, H. E. & MASTERTON, R. B., 1980. Hearing in Glires: domestic rabbit, cotton rat, feral house
mouse and kangaroo rat. Journal ofthe Acoustical Society of America, 68: 1584-1599.
HEFFNER, R. S., HEFFNER, H. E. & MASTERTON, R. B., 1971. Behavioral measurement ofabsolute and
frequency-difference thresholds in guinea pig. Journal of the Acoustical Society of America, 49: 1888-1895.
HENSON, 0. W., 1961. Some morphological and functional aspects of certain structures of the middle ear in
bats and insectivores. Kansas University Science Bulletin, 42: 15 1-255.
HENSON, 0. W., 1974. Comparative anatomy of the middle ear. In W. D. Keidel & W. D. Neff (Eds),
Handbook of Sensory Physiology, Vol. VII The Auditory System: Anatomy-Physiology: 4 2 3 4 5 4 . New York:
Springer-Verlag.
HOPSON, J. A,, 1966. The origin of the mammalian middle ear. American zoologist, 6: 437450.
HUNT, R. M. & KORTH, W. W., 1980. The auditory region of Dermoptera: morphology and function
relative to other living mammals. JOUTW~ of Morphology, 164: 167-2 1 1.
JERISON, H. J., 1973. Evolution of Brain and Intelligence. New York: Academic Press.
KELLY, J. B. & MASTERTON, R. B., 1977. Auditory sensitivity of the albino rat. Journal of Comparative and
Physiological Psychology, 91: 93Ck936.
KERMACK, D. M. & KERMACK, K. A., 1984. The Evolution of Mammalian Characters. London: Croom
Helm.
KERMACK, K. A. & MUSSET, F., 1958. The jaw articulation of the Docodonta and the classification of
Mesozoic mammals. Proceedings of the Royal Society ( B ) , 149: 204-215.
KERMACK, K. A. & MUSSET, F., 1983. The ear in mammal-like reptiles and early mammals. Acta
Palaeontologica Polonica, 28: 148-158.
KERMACK, K. A., MUSSET, F. & RIGNEY, H. W., 1973. The lower jaw of Morganucodon. zoological Journal
of the Linnean Society, 53: 87-175.
KERMACK, K. A,, MUSSET, F. & RIGNEY, H. W., 1981. The skull of Morganucodon. zoological Journal of
the Linnean Society, 71: 1-158.
KETTEN, D. R., 1984. Correlations of morphology with frequency for Odontocete cochlea: systematics and topdog.
Unpublished Ph. D. thesis, The Johns Hopkins University.
KIRIKAE, I., 1960. The Structure and Function of the Middle Ear. Tokyo: University of Tokyo Press.
KHANNA, S. M. & SHERRICK, C., 1981. The comparative sensitivity of selected receptor systems. In
T. Gualtierotti (Ed.), The Vestibular System: Function and Morphology: 337-348. New York: Springer-Verlag.
KHANNA, S. M. & TONNDORF, J., 1969. Middle ear power transfer. Archives Klin. Exp. Ohren-Nasen
Kehlkop3erkd. Heilk., 193: 78-88.
KHANNA, S. M. & TONNDORF, J., 1978. Physical and physiologic principles controlling auditory
sensitivity in primates. In C. R. Noback (Ed.), Neurobiology of Primates: 2.352. New York: Plenum Press.
KLINKE, R. & PAUSE, M., 1980. Discharge properties of primary auditory fibres in the caiman, Caiman
crocodilus: comparisons and contrast to the mammalian auditory nerve. Experimental Brain Research, 38:
137-150.
KONISHI, M., 1973. How the owl tracks its prey. American Scientist, 61: 414-424.
LAY, D. M., 1972. The anatomy, physiology, functional significance and evolution of specialized hearing
organs of gerbelline rodents. Journal of Morphology, 138: 41-120.
LILLEGRAVEN, J. A., 1979. Introduction. In J. A. Litlegraven, Z. Kielan-Jaworowska & W. A. Clemens
(Eds), Mesozoic Mammals: the First Two-thirds of Mammalian History. 1 4 . Berkeley: University of California
Press.
LILLEGRAVEN, J. A., KIELAN-JAWOROWSKA, Z. & CLEMENS, W. A,, 1979. Mesozoic Mammals: the
First Two-thirdc of Mammalian History. Berkeley: University of California Press.
LONG, G. R. & SCHNITZLER, H.-U., 1975. Behavioral audiograms from the bat Rhinolophusferrumequinum.
Journal of Comparative Physiology ( A ) , 100: 21 1-219.
LYNCH, T. J., 111, NEDZELNITSKY, V. & PEAKE, W. T., 1982. Input impedance of the cochlea in cat.
Journal of the Acoustical Society of America, 72: 108-130.
MANLEY, G. A,, 1971. Some aspects of the evolution of hearing in vertebrates. Nature, 230: 506-509.
MANLEY, G. A,, 1973. A review of some current concepts of the functional evolution of the ear. Evolution, 26:
6 0 8 4 2 1.
MANLEY, G. A,, 1977. Response patterns and peripheral origin of auditory nerve fibers in the monitor lizard,
Varanus bengalensis. Journal of Comparative Physiology ( A ) , 118: 249-260.
MANLEY, G. A,, 1981. A review of the auditory physiology of reptiles. In, D. Ottoson (Ed.), Progress in Sensory
Physiology, Vol. 2: 49-1 34. New York: Springer-Verlag.
WHAT D I D M O R G A N U C O D O N HEAR?
I63
MASTERTON, B., HEFFNER, H. & RAVIZZA, R., 1969. T h e evolution of human hearing. Journal of the
Acoustical Society of America, 45: 966-985.
MILLER, J. D., 1970. Audibility curve of the chinchilla. Journal ofthe Acoustical Socieb of America, 48: 513-523.
MOLLER, A. R., 1961. Network model of the middle ear. Journal of the Acouslical SoczeQ of America, 33:
168-1 76.
M 0 L L E R , A. R., 1983. Auditory Physiology. New York: Academic Press.
MULROY, M. J., 1974. T h e cochlear anatomy of the alligator lizard. Brain, Behavior and Euolution, 10: 69-87.
PARRINGTON, F. R., 1949. Remarks on a theory of evolution of the tetrapod middle ear. j'ournal of
Laryngology and Otology, 63: 58&595.
PARRINGTON, F. R., 1979. l h e evolution of the mammalian middle and outer ears: A personal view.
Biological Reviews, 54: 369-387.
PATTERSON, W. C., 1966. Hearing in the turtle. Jotcrnal of Auditory Research, 6: 4 5 3 4 6 4 .
PLATZER, W. & FIRBAS, W., 1966. Die Cochlea der Soricidae (Ihre Windungszahl und absolute Grosse).
Anat. An<. B d . , 117: 101-1 13.
, R., 1976. The comparative anatomy of the ear. In R . Hinchcliffe & D. Harrison
PYE, A. & HINCHCLI
(Eds), Scientific Foundations of Otolaryngology: 184-202. Chicago: Yearbook Medical Publishers.
REYSENBACH DE HAAN, F. W., 1958. Hearing in whales. Acta Otolaryngologira, Supplementum, 134: 1-1 14.
ROSOWSKI, J. J., CARNEY, L. H. & PEAKE, W. T., 1988. T h e radiation impedance of the external ear of
cat: Measurements and applications. Journal of the Acoustical Society of America, 84: 1695-1 708.
ROSOWSKI, J. J., CARNEY, L. H., LYNCH, T. J., 111 & PEAKE, W. T., 1986. The effectiveness of the
external and middle ears in coupling acoustic power into the cochlea. In J. B. Allen, J. L. Hall, A.
Hubbard, S.T. Neely & A. Tubis (Eds), Peripheral Auditory Mechanisms: 3-12. New York: Springcr-Verlag.
ROSOWSKI, J. J., PEAKE, W. T . , LYNCH, T. J., 111, LEONG, R. & WEISS, T. F., 1985. A model for
signal transmission in an car having hair cells with free-standing stereocilia, 11. Macromechanical stage.
Hearing Research, 20: 139- 155.
RYAN, A., 1976. Hearing sensitivity in the Mongolian gerbil. Journal of the Acoustzcal Society of America, 59;
1222-1226.
SACHS, M. B., SINNCYI', J. .XI.,& HEINZ, R. D., 1978. Behavioral and physiological studies of hearing in
birds. Federation Proceedings, 37: 2329-2335.
SAUNDERS, J. C., 1985. Auditory structure and function in the bird middle ear: An evaluation by SEM and
capacitive probe. Hearing Research, 18: 253-268.
SAUNDERS, J . C. & JOHNSTONE, B. M . , 1972. A comparative analysis of middle-ear function in nonmammalian vertebrates. Acta Otolaryngologica, 73: 353-361.
SAUNDERS, J. C. & ROSOWSKI, J. J , , 1979. Assessment ofhearing in animals. In \\'. E'. Rintelmann (Ed.),
The Assessment of Hearing. Baltimore: University Park Press.
SAUNDERS, J. C. & SUMMERS, R. M., 1982. Auditory structure and function in the mouse middle ear: An
evaluation by SEM and capacitive probe. Journal of Comparative Physiology ( A j , 146: 517-525.
SHAW, E. A. G. & STINSON, M . R., 1983. The human external and middle ear: models and concepts. In
E. deBoer & M.A. Viergrver (Eds), Mechanics of Hearing: 3-10. Delft University Press.
SIVIAN, L. J . & WHITE, S. D., 1933. O n minimum audible fields. Journal ofthe Acoustical Sociely qfAmerica, 4 :
288-32 1.
S M I T H , C. A,, 1981. Recent advances in the structural correlates of auditory receptors I n D. Ottoson (Ed.),
Progress in Sensory P/ysio/ogy, Chl. 2: 1-182. New York: Springer-Verlag.
S M I T H , C. A,, 1985. Inner ear. In A. S. King & J . MacLelland (Eds),Form and Funcliou in Birds, 3: 273-310.
London: Academic Press.
SOKAL, R. R. & ROHLF, E'. J., 1969. Biometry. San Francisco: \.I.'. H . Freeman and Company.
STEELE, C. R . & TABER, L. A,, 1981. Three-dimensional model calculations for the guinea-pig cochlea.
Journal of the Acoustical Soriety of America, 69: I 107-1 1 I 1.
TONNDORF, J. & KHANNA, S. M., 1976. Mechanics of the auditory system. I n R. Hinchcliffr & D.
Harrison (Eds), Scientijc Foundations of Otolaryngology: 237-252. Chicago: Yearbook Medical Publishers.
T U M A R K I N , A., 1955. O n the evolution of the auditory conducting apparatus: a new theory based on
functional considerations. Eoulution, 9: 22 1-242.
T U M A R K I N , A,, 1968. Evolution of the auditory conducting apparatus in terrestrial vertebrates. In A. V. S.
deReuck & J. Knight (Eds),Ciha Foundation Symposium on Heartng Mechanisms in C'erlehrates; 18-37. London:
Churchill.
WAETZMANN, E. \'. & KEIBS, L., 1936. Theoretischer und experimeriteller Vergleich van
Horschwellenmessungen. Akustische zeitschrift, I : 1-1 2.
WALKER, E. P., 1968. Mammals ofthe World, Vols. I G3 II. Baltimore. Maryland: 'I'hc Johns Hopkins Press.
WEBSTER, D. B. & WEBSTER, M., 1972. Kangaroo rat auditory thresholds before and after middle ear
reduction. Brain, Behavior and Evolution, 5 : 41-53.
WEISS, T. F. & LEONG, R., 1985. A model for signal transmission in an ear ha\ing hair cclls with freestanding stereocilia, 111. Micromechanical stage. Hearing Research, 20; 157- 174.
WEISS, T. F., MULROY, M. J., T U R N E R , R . G. & PIKE, L. L., 1976. 'l'uning of single fibers in the
cochlear nerve of the alligator lizard: relation to receptor morphology. Brain Research, 115; 7 1-90,
164
J. J. ROSOWSKI AND A. GRAYBEAL
WEST, C. D., 1985. The relationship of the spiral turns of the cochlea and the length of the hasilar membrane
to the range of audible frequencies in ground dwelling mammals. Journal of the Acoustical Society of America,
77: 1091-1101.
WESTOLL, T. S., 1943. The hyomandibular of Eusthopteron and the tetrapod middle ear. Proceedings of the
Royal Society, B, 131: 393414.
WESTOLL, T . S., 1944. New light on the mammalian ear ossicles. Nature, 154: 770-771.
WESTOLL, T . S. 1945. The mammalian middle ear. Nature, 155: 1 1 4 1 15.
WEVER, E. G., 1974. The evolution ofvertebrate hearing. In W. D. Keidal & W. D. Neff, (Eds), Handbook of
Senrory Physiology, Vol. V / I The Auditory System: Anatomy Physiology: 423454. New York: Springer-Verlag.
WEVER, E. G., 1978. The Reptile Ear. Princeton, New Jersey: Princeton University Press.
WEVER, E. G. & LAWRENCE, M., 1954. Physiological Acoustics. Princeton, New Jersey: Princeton University
Press.
WOLLACK, C. H., 1963. The auditory acuity of sheep. Jo~rnalofAuditory Research, 3: 121-132.
ZWISLOCKI, J. J., 1962. Analysis of middle ear function. Part I: Input impedance. Journal of the Acoustical
Society of America, 34: 1514-1523.
ZWISLOCKI, J. J., 1963. Analysis of middle ear function. Part 11: Guinea-pig ear. Journal of the Acoustical
Society of America, 35: 1034-1040.
ZWISLOCKI, J. J., 1965. Analysis of some auditory characteristics. In R. D. Luce & E. Galanter (Eds),
Handbook of Mathematical Psychology: 1-98. New York: Wiley.
ZWISLOCKI, J. J., 1975. The role of the external and middle ear in sound transmission. In D. B. Tower
(Ed.), The Neruous System, Volume 3, Human Communication and its Disorders: 45-55. New York: Raven.
36”
6.8”
15”
9.733
6300
400
2.5
0.18
75
0.045
0.05
1 .8
50
0.20
0.016
Elephant
Zebra
Horse
Cat
Bushbaby
Man
Gerbil
Mouse
Rabbit
Sheep
Rat
Bat
0.I3‘
1.4’
0.43’
0.093”
0.76“
3.2j4
0.76”
2.0”
375
9.6’
4.0”
2314
60T4
35”
36‘
205
I .3$
0.805
435
4.55
~
30”
8.0’”
0.05
Kangaroo rat
1.25”
71’
2.P
1933
0.80
Chinchilla
52“
35h
Tympanir
membrane
(mm‘)
55h
25i
~
2.4j4
Footplatr
area
(mm?
0.88’
Guinea-pig
Cauia
porcelluJ
Chinchilla
laniger
Dipodomys
merriami
Elephas maximus
Equus zebra
Equus caballus
Felis catus
Galago
senegalensis
Homo
Meriones
unguiculatus
Mus musculus
Oryclolagus
cuniculu,
Ouis ar ia
Rattus
noruegicus
Rhinolophus
simulator
Basilarmembrane
imm)
I g4
650
4.2h
456
0.40
cow
Dog
(ks)
Body
weight
Bas tauruJ
Canis cants
Species
Common
name
APPENDIX 1: SELECTED ANATOMIC AND AUDIOMETRIC DATA
10”’
812
16”
2.0”
4.0’’
4.OZ4
2.0*
8.09
8.0Z0
-
12
0
-9
5
-4
3
4
7
-3
8
I .0’
~
9
0
4
-9
-2
-11
Best
threshold
(dli SPLl
1 .0’!
2.8”
8.0’
8.0fi
8.0‘
8.01°
Best
frequency
(kHz)
I .3
I .8
I .2
2. I
2.0
2.3
2.2
2.5
2. I
~
2. I
2.5
2.5
2.3
I .8
1.8
2.0
Bandwidth
(decades)
T h e following tables list t h e d a t a used in t h e plots and regression calculations described in t h e text
0.90
1.6
3.9
0.33
0.15
0.21
0.16
0.20
0.36
-
0.06
0.10
0.09
0.29
0.40
0.20
0.55
ikHz)
Low
limit
34
55
62
38
14
46
27
59
47
6.9
34
29
19
38
36
35
2.035
0.5"
1.635
0.063
0.032
15
~
0.8035
0.2813
1235
-
0.70''
2.23
0.303*
0.4023
0.715
4.0t6
__
2.025
3.OZ5
2.8'
16"
82"
Best
frequency
(kHz)
2.01
Tympanic
membrane
(mm2)
0.4626
0.32"
1.0Z6
0.4Iz6
0.5E5
~
Footplate
area
(mm?
10
17
18
39
5
- 18
13
8
10
0
-9
-4
Best
threshold
(dB SPL)
1.2
1.7
1.3
1.3
1.3
3.0
0.9
5.0
4.0
3.6
0.05
0.11
0.20
0.22
11
7.7
8.9
4.9
6.2
44
90
0.15
0.34
0.41
0.63
I .3
1.1
1.5
0.05
0.31
1.76
10
2.0
1.3
1.4
0.95
Bandwidth
(decades)
'Dooling et al., 1971; 'Dooling & Saunders, 1975; 3Eatock et al., 1981; 'Firnandez, 1952; 5Fleischer, 1973; 6Heffner, 1983; 7Heffner & Heffner, 1982; 'Heffner & Heffner, 1983;
'Heffner & Heffner, 1985; "Heffner et al., 1971; "Heffner & Masterton, 1980; "Kelly & Masterton, 1977; I3Ketten, unpublished; "Kirikae, 1960; "Klinke & Pause, 1980; I6Konishi,
1973; I7Lay, 1972; "Long & Schnitzler, 1975; IgManley, 1977; 'Wasterton et al., 1969; "Miller, 1970; 22Mulroy, 1974; Z3Patterson,W. C., 1966; 24Ryan, 1976; '%achs et al., 1978;
'%sunders, 1985; 27Saunders& Summers, 1982; "Sivian & White, 1933; "Smith, 1981; 30Smith, 1985; 3iWebster & Webster, 1972; 3weiss et al., 1976; 33West, 1985; 34Wever ti
Lawrence, 1954; 35Wever, 1978; 36Wollack,1963.
0.635
1030
0.5
0.30
Barn owl
-
~
3.935
0.15
0.10
Cowbird
Canary
3.8"
2.329
~
16.133
Basilarmembrane
(mm)
50
0.31
0.10
0.23
Tree shrew
Pigeon
Budgie
0.016
Bat
Caiman
Caiman
crocodilus
Chrysemys
Turtle
scripta elegans
Gekko gecko
Tokay gecko
Genhonotus
Alligator
multicarinatus
liz.
Varanus
Monitor
bengalensis
lizard
REPTILES
AVES
Columba liuia
Melopsittacus
undulatus
Molothrus ater
Serinus
canarius
Tyto alba
Rhinolophus
fenumequinum
Tupaia glis
Species
Common
name
APPENDIX 1: continued
167
WHAT D I D MORGAXUCODON HEAR?
2:
POWER
FUNCTIONS
RELATING
ANATOMY AND AUDIOMETRY
Abbreviations: BW = Body weight in kg; FP = footplate area in
mm';
T M = tympanic-membrane area in mm';
BM =
Basilar-membrane length in mm; BF = best frequency in kHz;
LF = low-frequency limit in kHz; H F = high-frequency limit in
kHz; BT = best threshold in pascals; FR = bandwidth (hifrequency/low); CF = centre frequency in kHz.
APPENDIX
Power function
Y =
a
xb
Correlation
coefficient?
1. BODY WEIGHT AND EAR DIMENSIONS
Amnzotes
Fp =
0.97 BWo24
0.65
TM =
25 BWot9
0.61
BM =
7.1 BUT0 19
0.50
Mammals
FP =
0.85 BWo24
0.77
TM =
20 BWo
0.67
BM =
16 BWo l5
0.90
.'Van-mammals
FI' =
7.6 BW' I
0.78
TM =
63 BWo62
0.57
BM =
2.2 BWo l o
0.26
2 NITHIN-EAR DIMENSIONS
Amntotes
25 F p 8 '
TM =
20 BMom
TM =
FP =
0.81 BMoo3
Mammals
25 FPB8
TM =
0 7 2 BM"
TM =
0 02 BMI4
FP =
.Van-mammals
TM =
20 F P 7 '
TM =
25 BM0I8
1 2 BM-04'
F1' =
Significance
of exponent* ( O U )
< 0.1
< I
<5
< 0.1
< I
< 0.1
<5
>5
>5
0.92
0.09
0.03
< 0.1
>5
>5
0.93
0.58
0.68
< 0.1
0.90
-0.14
-0.24
>5
<5
< I
>5
>5
3. E.4R DIMENSIONS AND AUDIOMETRIC FEATURES
Mammals
5.9 FP-066
0.67
< I
B1: =
LF =
0.43 FP-I'
-0.82
< 0.1
40 FP-036
-0.83
< 0.1
HF =
BT =
0.01 FP3'
0.22
>5
FR =
79.4 F P 6 '
0.65
<1
4.0 FP-07'
-0.88
CF =
< 0.1
63 TM-O7'
20 T M - ' '
130 T M - 0 3 5
BI; =
LF =
HF =
BT=
FR
CF
=
=
BF
=
LF =
HF
=
FR
CF
=
Err =
=
2x
- 0.69
- 0.88
< I
< 0.1
-0.77
0.22
0.75
-0.92
< 0.1
TM3'
6.0 TMo8'
50 T M - 0 7 7
BM-043
BM-''
BM-OE5
BM-04*
BMo3'
BM-"
-0.22
-0.49
-0.77
-0.02
0.18
- 0.62
>5
>5
< I
>5
>5
20
13
400
0.1
3.2
63
>5
< 0.1
< 0.1
<5
J. J. ROSOWSKI AND A. GRAYBEAL
168
APPENDIX 2 continued
Power function
Y =
a
Correlation
coefficientt
Significance
of exponent* (yo)
-0.35
-0.75
-0.89
0.82
0.1 1
-0.88
>5
<5
< I
<5
>5
< l
TM-'''
TM-074
TM-OM
TM''
TM0I6
TM-O&
-0.23
-0.75
-0.78
-0.79
0.24
-0.82
>5
1 5
<5
<5
>5
<5
BMo8'
BMoZ3
BMo5
BM-32
BMo2'
BM036
0.81
0.3
0.69
-0.85
0.44
0.54
<5
1 5
>5
< 1
>5
>5
2
Non-mammals
BF =
LF =
HF =
BT =
FR =
CF =
1.3 FP-OZ5
0.15 FP-05'
4.0 FP-05'
I x 1017 F P I ~
25 F P w
0.76 FR-055
BF =
LF =
HF =
BT =
FR =
CF =
2.6
1.4
25
1 x 10-I'
16
5.9
BF =
LF =
HF =
BT =
FR =
CF =
0.66
0.12
2.8
1 x 10"
25
0.59
*The probability that the exponent equals zero.
?Correlation coefficient of the log-transformed variables.