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The Ear and Hearing in Amphisbaenia (Reptilia)

CARL GANS2 AND ERNEST GLEN WEVER


Department of Biology, State University of New Yorh at Buffalo, a n d
Auditory Research Laboratories, Princeton Uniuersity,
Princeton, New Jersey
ABSTRACT The burrowing squamates of the order Amphisbaenia lack
external ears. The middle ear involves an extremely large stapes with the head
of its shaft (columellar portion) projecting just posterior to and as far laterally
as the quadrate. In most species a cartilaginous extracolumella articulates with
the distal tip of the shaft and then stretches along the lower jaw and is attached
to the skin in the region of the second infralabial. Records of the electrical
potentials of the cochlea in some nine species show sensitivity curves whose
maxima are approximately -20dB for a standard output of 0.1 pv. The zone
of greatest sensitivity lies in the low frequencies, usually between 300 and
700 Hz. The sensitivity of amphisbaenians differs from that of snakes in being
fairly good above levels of 700 Hz, where the latter drops off sharply. Inter-
ruption of the extracolumella causes a 20 to 30 dB loss in sensitivity. Sound
waves applied asymmetrically produce different electrical responses in the two
ears, suggesting an explanation for behavioral observations on the utilization
of the system.
The form and function of the ear in
amphisbaenians are hardly known. Since
an external opening is lacking, the group
has been characterized as ear-less, and
only the structure of the middle ear has
had brief mention in treatments of the
anatomy of the skull. Some speculations
have been offered about auditory function
in general discussions of the life and hab-
its of these reptiles (Gans, '60, '68). That
hearing may play an important role in
such activities as the finding of food and
mates and predator avoidance seems a
reasonable assumption for these curious
animals whose life is mainly, sometimes
exclusively, subterranean and whose vi-
sion is apparently reduced to simple light
perception (Gans and Bonin, '63).
The present report presents evidence
on the functional characteristics of the
peripheral auditory mechanism in nine
species of amphisbaenians. It includes ob-
servations on the anatomy of the ear in
two species as well as preliminary data
on three others. For the functional studies
we recorded the electrical potentials of
the cochlea (Wever, '39, '66). These po-
tentials represent the activity of the audi-
tory hair cells and reflect the properties
of the receptive and conductive systems
J . EXP. ZOOL., 179 17-34
and of the mechanoelectric processes in
the cochlea.
The species studied (table 1) were: Am-
phisbaena alba ( 3 specimens), Amphis-
baena darwini trachura (1 specimen),
Amphisbaena manni (7 specimens), Chir-
india langi ( 2 specimens), Cynisca leu-
cura ( 3 specimens), Zygaspis violacea
( 3 specimens), Monopeltis c. capensis
( 2 specimens), Trogonophis wi egmanni
(2 specimens), and Bipes biporus (4 spe-
cimens).
METHOD
The animals were anesthetized with
20% solution of ethyl carbamate in phys-
iological saline, in dosages near 0.01 ml
per gram of body weight. The sensitivity
of the ear in terms of its cochlear poten-
tials was determined by recording from an
electrode in contact with the perilymph
of the saccule, which is readily accessible
through the dorsolateral surface of the
posterior region of the head. The skull
1 The experi ments were carri ed out in the Auditory
Research Laboratories of Princeton University wi th
facilities provided by grants from the Nati onal I nsti-
tute of Neurological Diseases and Stroke. The speci-
mens were obtai ned wi th funds from NSF GB-6521X.
2 Present address: Department of Zoology, The Uni-
versity of Michigan, Ann Arbor, Mi chi gan 48104.
17
18 CARL GANS AND ERNEST GLEN WEVER
TABLE 1
The specimens used are deposited i n the Carl Gans (CG) collection. The species used, the
catalogue numbers, the localities and the collectors are as follows: Amphisbnenn alba:
(no No.), Brazil, (dealer); same species (CG 371 71, Venezuela, Edo. Carabobo, Valencia
(S. M. McCown); same species (CG 3718), Brazil, S. P. J undiai, Sitio Bandeirante (W. C. A.
Bokermann). Ampkisbaenn darwini trachurn: (CG 3752), Brazil, RGS, Tramandai, Emboaba
(C. P. J aeger and S. Correa). Amphisbnena manni: (CG 3822, 3823, 3844, 3845, 3846, 3852,
3853, 3859, 3860, 3861, 3862, 3863) Hispaniola, Ile de l a Tortue, Palmistes (C. R. Warren).
Bipes bi po~zt s: (CG 3804, 3805, 3806, 3808) Mexico, Baja California, Sul de l a Paz (L. W.
Robbins). Chirindin langi: (CG 4033, 4035), Mozambique, 15 miles southeast of Vila de
Manica (D. G. Broadley, C. Gans and J . Visser). Cyni sca leucura: (CG 4126), Ghana, Legon
(B. Hughes); same species: (CG 4151, 4152), Ghana, Legon, hill behind 2001. Dept. (B.
Hughes). Monopeltis cnpensi s: (CG 4456, 4457), South Africa, O.F.S., Bothaville (J . Visser).
Twgonopki s wi egmanni : (2 specimens, no No.), Maroc (Dealer). Zygnspi s violacea: CG 4546,
4558,4559), Zululand, Ndumu Game Reserve (A. C. Pooley).
was exposed and a small hole was drilled
of a size that was tightly filled by the ta-
pered end of a fine steel needle that was
insulated except at the tip. Two other
electrodes, one of which was grounded,
were located on inactive tissues of the
region. The electrodes led to a differen-
tial preamplifier that provided an 80-db
rejection of stray potentials picked up
between two of the electrodes and the
grounded lead.
The animal was stimulated with a
series of tones that ordinarily covered the
range from 100 to 10,000 Hz, but in some
instances included lower frequencies. For
aerial stimulation the tones were produced
by a loudspeaker outside the shielded
chamber in which the animal was kept
and were conducted through the wall by
a tube. This tube terminated in a sound
cannula whose tip was located over the
facial region close to the skin surface. To
avoid any possibility of mechanical con-
duction to the animal, this tube was held
out of direct contact and the narrow gap
between its rim and the skin was filled
with petroleum jelly to make a tight
acoustic seal. A probe tube leading to a
condenser microphone ran concentrically
within the sound tube and ended near its
tip, and the system was calibrated to pro-
vide readings of sound pressure. The
physiological state of the animal was gen-
erally monitored by display of an elec-
trocardiogram.
Vibratory stimulation for other experi-
ments was produced by a crystal vibrator
that actuated a steel needle, the blunted
end of which could be applied to the body
surface. The vibrator was fitted with an
accelerometer and was calibrated by
means of a "Fotonic sensor," a device
utilizing fiber optics for the precise mea-
surement of vibratory amplitudes.
The stimuli were presented at the in-
tensities necessary to produce some small
but reliably observable level of potential,
which, because of the physiological noise
present, was set between 0.05 and 0.2 pv.
I n the curves the results are reported for
a standard output of 0.1 pv; when the
measured values differed from this level
the sound required was calculated, since
our tests had shown that the response at
low levels is a linear function of sound
pressure. The earliest measurements were
always repeated to check that the animal
had not deteriorated during the test
sequence.
Most of the measurements were made
at room temperature, which was about
23"C, since at higher temperatures the
animals seemed to desiccate rapidly, mu-
cous production increased, and we en-
countered very significant mortality. Only
in one instance ( Chi r i ndi a l angi ) were we
able to obtain readings at higher temper-
atures. These readings support the results
of Werner ('68) that the general curve
shape remains similar but shifts to a
higher frequency range, while the sensi-
tivity increases slightly. Unfortunately
there are no published data for the pre-
ferred body temperatures of any amphis-
baenean. For this reason and because of
the relatively minor changes in absolute
values we deferred collection of temper-
ature data until after behavioral observa-
tions have been completed, when addi-
tional specimens may be available.
EAR AND HEARING I N AMPHISBAENIA (REPTILIA) 19
I n many of the experiments, special
procedures were carried out to study the
processes of sound perception and the
transmission of vibrations to the cochlea.
The effect of severing the extracolumella,
singly or multiply, was studied in several
animals. I n such operations the extra-
columella was first exposed by dissecting
away the overlying skin and muscle. The
effect of this procedure on sensitivity was
then checked prior to cutting the extra-
columella itself. Systematic exploration
of the lateral surface of the head with
the mechanical vibrator was intended to
locate the sensitive zones. The direction-
ality of sound reception was tested by re-
cording from both ears while stimulating
with asymmetrically placed aerial sounds.
After the electrical tests had been com-
pleted, each anesthetized animal was per-
fused through the circulatory system by
means of a cannula inserted through the
ventricle into the ascending aortic ves-
sels. Perfusion with physiological saline
to flush out the blood was followed by a
fixative containing mercuric chloride,
potassium dichromate, sodium sulfate,
and formaldehyde. The fixation was con-
tinued for 40 to 60 minutes. The head
was then removed and the tissues trimmed
to a block containing both ears. This block
was replaced in fixative, decalcified in
0.5% nitric acid, dehydrated in an as-
cending series of alcohol from 10 to 100%
by 10% steps, and embedded in celloidin.
The hardened celloidin block was sec-
tioned (horizontally, at an angle of about
15" toward the transverse) at 20 p inter-
vals perpendicular to the long axis of the
basilar membrane. Every section i n the
region of the ear was mounted separately
and stained with hematoxylin, azocarmine,
and orange G, a combination giving good
differentiation of the auditory hair cells.
While the procedure yields excellent pres-
ervation, it requires 10-12 months.
At the time of this report the histolog-
ical treatment is complete on 14 animals
belonging to five species: three specimens
of Amphisbaena alba, one of A. darwini
trachura, five of A. manni , one of Trogo-
nophis wiegmanni, and four of Bipes bi-
porus. Several other specimens are still
in preparation, and detailed morpholog-
ical description is deferred until the his-
tological study is completed.
RESULTS
Anatomical observations
Earlier studies, especially those of Ver-
sluys (1898) on the ear region and of
Gans ('60) on the Trogonophidae, have
included observations on the ear's struc-
ture and some descriptions of the auditory
mechanism. While none of the 140 species
of the order (Gans, '67) has an external
ear (fig. l), all have middle and inner ear
structures, concealed below the uninter-
rupted dermal segments covering the
head.
Fig. 1 Dorsal, lateral and ventral views of the
head of Amphisbaenn mnnni (American Museum
no. 49726), to show the pattern of dermal seg-
mentation. The second left infralabial i s shaded.
The line equals 1 mm to scale.
20 CARL GANS AND ERNEST GLEN WEVER
Extracolurnel la'
Fig. 2 Lateral view of the skull of Anzpkisbtre7zn c t ~ec n (Carnegie Museum no. 37636)
showing the stapes and extracolumella.
As in all other reptiles, the middle ear
mechanism consists of columellar and ex-
tracolumellar elements, but their form is
quite distinct (Baird, '70).
There is always an osseous coluniella,
also called a stapes. This element has a
broad footplate resting in the oval window
and a relatively short shaft (columellar
portion) the distal head of which connects
with a generally cartilaginous extracol-
umella that, except in Bipes, ultiniately
attaches to the skin anterior to the an-
gulus oris.
In the genus Anzphisbaenn the extra-
columella is a long, slender rod that ex-
tends from the stapes anterolaterally and
then anteriorly as shown in the drawing
(fig. 2) and the photomicrograph (fig. 3) .
Near its columellar articulation the extra-
columella runs through dense connective
and muscular tissues along the lateral
side of the quadrate bone on the medial
side of a muscle layer. More anteriorly
beyond the articulation of the lower jaw
it emerges as a structure lying freely in
the subcutaneous space. Its anterior por-
tion enters the dermal layer of the skin
within which it shows broad connective
tissue attachment; after a forward course
as far as the two posterior teeth, it tapers Fig. 3 Photomicrograph of a section through
to a slender thread and ends.
the head of a specimen of A?np/ ?i sb~i e?ru mnnni,
depicts further details of the
showing the cochlear capsules and middle ear
structures. The posterior portion of the extra-
stapes and its connections in Amphis- columella on the left side had been interrupted
bnenn mnnni. The footplate is broad, surgically; the system on the right is intact.
equalling the diameter of the otic capsule,
Figure
Scale X 12.
EAR AND HEARI NG I N AMPHISBAENIA (REPTI LI A)
21
Fig. 4 Photomicrograph at a higher power of the right i nner ear region of the same spe-
cimen as in the previous figure. e, extracolumella; f, footplate of stapes; s, shaft of stapes.
Scale X 60
of which it forms the anterolateral wall.
The anterior portion of this ossicle makes
a wide articulation with the prootic bone,
while the smaller posterior portion is held
to the lateral wall of the capsule by a
wider ligament. The neck and headpiece
extend farthest laterally. The articular
surface is clearly indicated, while the con-
nection to the expanded end of the extra-
columella lacks an articular cleft and
seems relatively rigid.
I n Trogonophis the stapes has much the
same form as in Amphisbaena, but the
extracolumella is a short, plate-shaped
cartilage expanding ventrally. Its forward
extension passes only a short distance an-
terior to the mandibular joint, and then
connects to a broad band of dense connec-
tive tissue that continues anterolaterally
to fuse with the deep layer of the skin.
In Bipes biporus the extracolumella
takes still a different form. From the col-
umellar articulation it extends laterally
and somewhat posteriorly for a compara-
tively short distance after which it ter-
minates in a flat headpiece that lies just
posterior to the quadrate bone. Its precise
relations to the enveloping soft tissues
need further study.
The inner ear exhibits considerable uni-
formity in the species examined so far.
The basilar membrane has a distorted
oval form, is nearly as wide as it is long,
and bears an auditory papilla as shown
in cross section of Amphisbaena alba in
figure 5. In this section, which is from
the midregion of the basilar membrane,
there are 12 rows of hair cells whose cili-
ary tufts are embedded in a thick tec-
torial plate. These tufts extend into pits
in the lower surface of the plate. The tec-
torial membrane is attached to the plate
near its middle as shown. This arrange-
ment closely resembles that found in tur-
tles (Wever, unpublished).
Counts of the cochlear hair cells were
made in the specimens for which serial
sections were available and the preserva-
tion and staining were suitable. The re-
sults are given in table 2. The size of the
22 CARL GANS AND ERNEST GLEN WEVER
Tectorial membrane
Fig, 5 Drawing of the auditory papilla of Ampk i s bae na al ba, from a section transverse
to the basilar membrane.
TABLE 2
Nu mb e r of hai r cells
Species
Number of cells
Animal
number Left ear Right ear
A m p hi s ba e na a l bn 1500
1667
1668
Amphi s bae na dtrrwini t i ncht i ra 1525
Amphi sbnent r mu n n i 1520
1524
1547
1548
Tr ogonophi s wi e g mann i 1736
Bi pes biporzrs 1522
1553
1554
1555
148 150
159 168
143
99 105
- 109
-
107 138
99 78
81 82
94 106
56 -
45 53
47 67
56 55
hair cell population varies with species.
Amphisbaena alba has the largest num-
ber, averaging 154 (N = 3) . For A. dar-
wini trachura (N = 1), A. manni (N =
5) , and Trogonophis wi egmanni (N = 1)
the numbers are hardly distinguishable,
approximately 100. For Bipes biporus the
number is smaller, mean 54 (N = 4).
Cochlear potential studies
1. Amphisbaena alba. The solid-lined
curve in figure 6 gives measurements of
auditory sensitivity in terms of cochlear
potentials for a specimen of Amphisbaena
alba, under the usual conditions. This
curve reaches its lowest level, represent-
ing the greatest sensitivity, in the region
of 200 to 600 Hz, and then, as the fre-
quency increases, it rises, at first slowly
and then more rapidly, up to 5000 Hz.
Here an inversion appears, after which
the upward rise continues.
After these tests had been concluded,
the extracolumella was cut anteriorly,
leaving only its posterior two-thirds con-
nected to the stapes. The results are
shown by the broken curve of this figure.
The sensitivity suffered a considerable
loss, extending over the frequencies up
EAR AND HEARI NG I N AMPHI SBAENI A (REPTI LI A)
1 2 3 4 5 6 7 8 9 1 2 3 4 5 6 7 8 9 1
23
Frequency
Fig. 6 Auditory sensitivity to aerial sounds i n a specimen of Amphisbaena alba under
normal conditions (solid line) and after interrupting the extracolumella (broken line). The
curves represent for various frequencies the sound pressure, i n decibels relative to 1 dyne
per sq cm, required to produce a cochlear potential of 0.1 pv. I n this and the following
figures, frequency is in cycles per second (Hz).
100 1000
Frequency
10,000
Fig. 7
Sensitivity curves in a second specimen of Amphisbaena alba under normal condi-
tions (solid line) and after two successive interruptions of the extracolumella, one in the
anterior portion of this rod (long-dashed curve) and the other more posteriorly (short-dashed
curve).
to 2000 Hz and averaging 33 dB. For tones In a second specimen (solid-lined curve
above this point at which observations of figure 7), the sensitivity was greatest
could be made, there were no significant in the range from 100 to 290 Hz and fell
changes.
off fairly regularly for higher tones. When
24 CARL GANS AND ERNEST GLEN WEVER
the extracolumella was first cut at an an-
terior position (long-dashed curve), and
then at a more posterior site (short-
dashed curve) the sensitivity fell progres-
sively. Apart from one inversion, the sec-
ond of these impairment curves lies above
the first, showing that sensitivity is re-
lated to the intact length of the extra-
columella.
2. Amphi sbaena darwi ni trachura. The
sensitivity of a specimen of Amphi sbaena
darwi ni trachura with the sound source
placed forward on the lower jaw is rea-
sonably uniform up to 600 Hz, after which
the curve rises sharply showing a loss of
sensitivity, and then falls rapidly to the
point of best response at 1000 Hz (fig. 8).
The sensitivity decreases for the upper
frequencies. Even in the low-tone region
the sensitivity is slight. A second sound
probe position near the center of the sec-
ond infralabial gave somewhat greater
sensitivity (fig. 9). The form of the curve
is similar except that the sharp rise at
100 1000
Frequency
10, 000
Fig. 8 A normal sensitivity function i n a specimen of Anzphisbflena dwwi ni t mchzi m
(left ear).
+ 60
- 20
Frequency
Fig. 9 Sensitivity functions for the right ear of the same specimen as i n the preceding
figure, under normal conditions (solid line) and after cutting the extracolumella (broken line).
EAR AND HEARI NG I N AMPHI SBAENI A (REPTI LI A) 25
700 Hz is absent. The extracolumella was
then severed just anterior to its connec-
tion with the stapes, so that nearly all of
this element was disconnected. The result
was a large loss of sensitivity, which for
the tones up to 1000 Hz averaged 40 dB
and for higher tones up to 7000 Hz aver-
aged 23.5 dB.
3. Amphisbaena manni. The best sen-
sitivity of Amphisbaena manni is between
600 and 1500 Hz (fig. 10); i t declines
fairly rapidly for lower and higher tones.
I n a second specimen (fig. ll), the form
of the curve is similar, but the most sen-
sitive region extends from 500 to 1000 Hz,
and the degree of sensitivity is a little
Frequency
Fig. 10 Sensitivity function for a specimen of Amphisbtrena manni , under normal
conditions.
1 2 3 4 5 6 7 8 9 1 2 3 4 5 6 7 8 9 1
Frequency
Fig. 11 Sensitivity functions for another specimen of Amphisbnena manni , under normal
conditions (solid line) and after interrupting the extracolumella (broken line).
26 CARL GANS AND ERNEST GLEN WEVER
less. When the extracolumella was severed fig. 12), maximum sensitivity occurred at
just anterior to its connection to the 500 Hz, which was lower than for aerial
stapes, the loss of sensitivity (broken stimulation. The most sensitive zone was
curve) averaged 41 dB for tones up to also more restricted, but the level of sen-
2500 Hz and 20.3 dB for higher tones. sitivity was otherwise similar to that with
I n response to a vibrating needle ap- aerial stimulation. The extracolumella
plied to the side of the face (solid line, was then severed just anterior to its con-
1 2 3 4 5 6 7 8 9 1 2 3 4 5 6 7 8 9 1
Frequency
Fig. 12 Sensitivity functions for a specimen of Amphisbaena manni under stimulation
with mechanical vibrations applied through a needle to the skin surface at the side of the
head, for normal conditions (solid line) and after severing the extracolumella (broken line).
+ 40
- 40
Fig. 13 Normal sensitivity curves for aerial sounds i n a specimen of Chirindia langi at
two body temperatures as indicated.
EAR AND HEARING IN AMPHISBAENIA (REPTILIA) 27
nection to the stapes, and the measure-
ments repeated (dashed line) with only
slight effect on sensitivity.
4. Chirindia langi. Two curves for a
specimen of Chirindia langi, taken respec-
tively at 24.4"C and 29.4"C, are shown in
figure 13. At the lower temperature the
curve reaches its lowest point (greatest
sensitivity) at 500 Hz, whereas at the
higher temperature this point is in the
higher frequencies, around 3000 Hz.
There is also a shift i n the two ends of
the curve; at the higher temperature the
low end is raised and the high end is
lowered. This type of modification of audi-
tory sensitivity was shown to be a regular
occurrence in extensive experiments on
lizards by Werner ('68).
5. Cynisca leucura. The curve from
Cynisca leucura indicates that the great-
est responsiveness is at 300 and at 500 Hz,
with a rapid decline to 800 Hz, then a
leveling and a further decline for the
upper frequencies (fig. 14).
Fig. 14
conditions.
An aerial sensitivity curve for a specimen of Cynisca leucura under normal
Frequency
Fig. 15
conditions.
An aerial sensitivity curve for a specimen of Zygaspis violacea under normal
28 CARL GANS AND ERNEST GLEN WEVER
6. Zygaspis uiolacea. The greatest
sensitivity of a specimen of Zygaspis vi-
olacea occurred at 300 and at 500 Hz
with a sharp loss in the intermediate zone
as in Cynisca (fig. 15). The sensitivity
decline at higher frequencies is typical
of Phese animals.
7. Monopeltis c . capensis. Best sen-
sitivity for a specimen of Monopeltis c.
capensis occurred at two points in the
low-frequency region, 200 and 500 Hz,
with lesser responses between, and with
+40
the usual decline in the high frequencies
(fig. 16).
In another specimen, the normal curve
(solid line) also shows two points of great
sensitivity, at 200 and 600 Hz (fig. 17).
Severing of the extracolumella again led
to a more than 20 dB loss of sensitivity
(broken curve in fig. 17).
Another experiment documented the
directional characteristics of the amphis-
baenid ear. The animal was stimulated
via sound tube and response recorded from
- 40
100 1000
Frequency
10,000
Fig. 16 An aerial sensitivity curve for a specimen of Monopel t i s c. capensi s, under nor-
mal conditions.
100 1000
Frequency
10,000
Fig. 17 Sensitivity curves for a second specimen of Monopel t i s c. capensi s under normal
conditions (solid line) and after interrupting the extracolumella (broken line).
EAR AND HEARING IN AMPHISBAENIA (REPTILIA) 29
both saccules. The results obtained from
the right ear are shown by the solid line
of figure 18 and those from the left ear
by the broken line. In general (all except
2 points), there is a clear difference in
favor of the ipsilateral ear. A greater dif-
ferential response occurred when stimula-
tion was carried out by placing the sound
tube at a distance of 5 cm from the right
side of the face.
100
8. Trogonophis wiegmanni. A speci-
men of Trogonophis wiegmanni showed
excellent sensitivity with the maximum
falling between 300 and 500 Hz (fig. 19),
in an experiment extended down to 40 Hz.
Figure 20 compares results for aerial and
vibratory stimulation in a second speci-
men. The aerial curve is much like the
previous one, though the region of good
sensitivity is broader. The curve for vibra-
2 3 4 5 6 7 8 9 1 9 1
1000 10,000
Frequency
Fig. 18 Aerial sensitivity curves obtained i n a specimen of Monopeltis c. capensis with
an electrode applied to the left saccule (solid line) and an electrode applied to the right sac-
Cole (broken line). For both sets of observations the sound tube was close to the surface of
the face on the left side.
+ 40
3 +20
2-
2 0
P
u m
T2
m
a
0.
-u
S
3
&
5; - 20
- 40
100 1000
Frequency
Fig. 19 A sensitivity curve for a specimen of Trogonophis wiegmnnni.
100
30 CARL GANS AND ERNEST GLEN WEVER
2 3 4 5 6 7 8 9 1 2 3 4 5 6 7 8 9 1 4 5 6 7 8 9 1
Frequency
1000 10,000
Fig. 20
Sensitivity curves obtained i n another specimen of Trogonophis wiegmnnni with
aerial stimulation (solid line) and with vibratory stimulation (broken line). The ordinate
scale represents decibels relative to a sound pressure of 1 dyne per sq cm for the aerial
stimuli and decibels relative to an amplitude of 1 mp for the mechanical stimuli.
Fig. 21 A sketch of the left side of the head of a specimen of Trogonophis wiegmcinni
showing the scalation and the locations used for stimulating with a vibrating needle. As
figure 2 has shown, the extracolumella runs from a deep connection with the stapes (around
positions 18-19) forward along the infralabials (to about position 15). Its fibrous extension
continues to about position 14.
tory stimulation is irregular, and shows
two regions of good sensitivity, one at
500 Hz and another at 1500-2500 Hz.
Further tests explored the reception of
vibratory stimuli by the lateral surface of
the head. The blunted end of the vibrat-
ing needle was brought into firm contact
with the supra- and infralabilas and with
those segments posteriorly in line well be-
yond the position of the stapes (see num-
bered circles in fig. 21). At each place the
contact pressure of the needle was ad-
justed to give a maximum response at a
frequency of 400 Hz, and the stimulus
amplitude varied to produce a constant
Figure 22 shows the amplitudes, in de-
cibels relative to an arbitrary zero level
output of 0.2 pv.
EAR AND HEARING I N AMPHISBAENIA (REPTILIA)
31
- 10
5
P
2
11
0
-L
>
0.
required for the standard response, as a
function of distance from the tip of the
jaw for both the lower jaw (solid line) and
the upper jaw (broken line). In this
graph, unlike the others, the lower the
curve the less the sensitivity. It is seen
that along both upper and lower jaws
there is no significant variation of sensi-
tivity with position until the vibrator
reaches the zone where the extracolum-
ella lies deep to the jaw muscles; sensi-
tivity then sinks sharply to a new and
much lower level.
9. Bipes biporus. Our results for Bipes
bi porus are to be regarded as preliminary,
- -
I I I I
because at the time of these tests we were
unaware that the extracolumella termi-
nated posterior to the quadrate. Presum-
ably, the sound tube for aerial stimula-
tion should not have been located adjacent
to the anterior portion of the head. Four
animals tested with aerial sounds showed
a range of sensitivity represented by the
two curves of figure 23. The solid-lined
curve indicates a level of best sensitivity
that is about the same as observed in
other amphisbaenians, but differs in that
this falls in the high tones, around 3000
Hz. The dashed curve shows rather little
sensitivity, with irregularities, and does
+ 40
+20
P
V al
D
2
$ 0 m
al
a
U
S
3
L
64 -20
- 40
100 1000 10,000
Frequency
Fig. 23 Aerial sensitivity curves i n two specimens of Bipes biporus, chosen to show the
range obtained.
32 CARL GANS AND ERNEST GLEN WEVER
v)
-
3+20
V a,
6
1 ' 0
3
Q
E,
: -20
7,
0
L
+-
.-
> 1+40E
- 40
100
2 3 4 5 6 7 8 9 1 2 3 4 5 6 7
1000
Frequency
10,000
Fig. 24 Sensitivity curves obtained for vibratory stimulation in a specimen of Bipes
biporiis with the needle applied to the side of the face near the stapes ((solid line) and to the
front region of the lower j aw (broken line).
not agree in form with the other curve.
Whether these differences are due to the
manner of presentation of the sounds or
to other conditions of the tests, or repre-
sent actual individual variations, is dif-
ficult to say.
Figure 24 shows two curves obtained by
vibratory stimulation, one (solid line) by
placing the vibrating needle on the side
of the face in the region of the stapes and
the other (broken line) by placing it on
the front edge of the lower jaw. The two
functions have much the same form, but,
in general, stimulation near the stapes
shows the greater sensitivity. The level of
sensitivity is similar to that found by this
method in other species.
DI SCUSSI ON
The observations clearly show that am-
phisbaenians are sensitive to aerial
sounds, and that these sounds are con-
ducted to the inner ear by way of the skin
along the lower jaw, the extracolumella,
and the stapes. In amphisbaenians gener-
ally the extracolumella projects anteriorly
to provide a dermal connection lateral to
the mandible. Bi pes bi por us represents an
exception since its extracolumella is short
and attaches to the skin in the immediate
vicinity of the quadrate.
In the members of the family Amphis-
baenidae (genera Amphi s bae na, Chi r i ndi a,
Cyni s ca, Monopel t i s, and Zygas pi s ) , the
extracolumellar rod extends far forward
into the skin layer, lateral to the lower
jaw. I n Tr ogonophi s , the extracolumella
does not itself run as far forward as a
cartilaginous structure but is extended
by a strong band of connective tissue that
evidently serves the same purpose. Gans
('60) showed that this connective tissue
apparently serves as the starting point for
the ossification of the extracolumella seen
in the trogonophid genera Di pl omet opon
and Agamodon. Here the tissue has be-
come ossified, and many of the connec-
tions run to the upper rather than the
lower lip.
Most amphisbaenian ears have a region
of greatest sensitivity in the low frequen-
cies, usually between 300 and 700 Hz.
This zone often contains two points of
high sensitivity separated by a less sensi-
tive zone. I n Amphi s bae na manni the best
region seems to be slightly higher (be-
tween 700 and 1000 Hz), and it may be
still higher in Bi pes bi por us . Most of the
amphisbaenian species yielded sensitivity
curves whose maximum was approximate-
ly -20 dB though there was considerable
variation and Tr ogonophi s repeatedly
reached - 40 dB.
The levels of cochlear potentials may
be compared with similar results on other
squamates, which also showed large vari-
EAR AND HEARING IN AMPHISBAENIA (REPTILIA) 33
ation; a rough mean for lizards is around
-40 dB (for a response of 0.1 ~v ) , but
many species are far more sensitive, up
to -60 dB or better. Various species of
the Sceloporus group give lower maxima
around -20dB although their regions of
good response are broader than those
found in amphisbaenians (Wever and
Peterson, '63, and Wever unpublished).
The chameleons so far studied vary great-
ly according to the special mechanisms
that have been developed as substitutes
for the absent tympanic membrane and
round window; usually the sensitivity is
relatively poor but in some species may
approach -20 dB (Wever, '68, '69a,b).
The general shapes of the curves are
nevertheless remarkably similar in lizards
and amphisbaenians.
The sensitivity of some species of snakes
agrees with those determined for amphis-
baenians in giving maxima around -20
dB in the low frequencies from 200 to
700 Hz. The sensitivities of snakes do,
however, drop off most rapidly above 700
Hz (Wever and Vernon, '60).
Among non-squamate reptiles, turtles
always exhibit the greatest sensitivity in
the low range. Their curves are generally
quite sharply peaked here with a particu-
larly rapid decline in sensitivity for high
tones. The maximum sensitivity level of
turtles varies widely, with some species
having the same magnitude as amphis-
baenials while others reach sensitivities
up to -60 dB. Crocodilians are generally
more sensitive showing both a broader
range of good sensitivity and maxima
around -60 dB (Wever and Vernon, '57).
Experiments well document the differ-
ential function of the middle ear appara-
tus. The sensitivity, particularly in the
low range (below 1000 Hz) drops drastic-
ally (by 20 to 30 dB) whenever the extra-
columella is severed (figs. 6, 7, 9, 11, 17).
Supplementary and sequential transec-
tions of the extracolumella show (cf. figs.
3, 7) that the length remaining intact re-
lates to the level of absolute sensitivity,
which in some cases dropped by as much
as 40 dB.
The experiments with the mechanical
vibrator show that the response to signals
applied anywhere along the head (1) is
fairly constant regardless of the site of
application and (2) does not diminish
when the extracolumella is transected.
These experiments (on Amphisbaena alba
and A. manni ) suggest that the extracol-
umella functions in transmitting aerial
sounds or other low-displacement vibra-
tions from the anterior labial surface to
the inner ear. From these observations,
the signals under usual life conditions
could be aerial sounds or vibrations of the
substratum. Probably both are utilized
under suitable conditions. The structure
of the labial system should permit re-
sponse to subterranean vibration when
the face is held in contact with the tun-
nel wall.
The experiments on Monopeltis capen-
si s document that at least this species
has a small but significant differential
sensitivity to asymmetrical sounds, a sen-
sitivity which is probably enhanced by
central bilateral inhibition. This then
suggests an explanation for the earlier
observation (Gans, '60) that these animals
appear to discover their prey by sound.
It also opens the way to a variety of be-
havioral analyses.
LITERATURE CITED
Baird, I. L. 1970 The anatomy of the reptilian
ear. I n: The Biology of the Reptilia. Vol. 2b.
C. Gans and T. S. Parsons, eds. Academic Press,
London, pp. 192-275.
Gans, C. 1960 Studies on amphisbaenids (Am-
phisbaenia: Reptilia). 1. A taxonomic revision
of the Trogonophinae and a functional inter-
pretation of the amphisbaenid adaptive pattern.
Bull. Amer. Mus. Nat. Hist., 119: 129-204.
A checklist of the recent amphis-
baenians (Amphisbaenia: Reptilia). Bull. Amer.
Mus. Nat. Hist., 135: 61-106.
1968 Relative success of divergent
pathways i n amphisbaenian specialization.
Amer. Nat., 102: 345-362.
Gans, C., and J . J . Bonin 1963 Acoustic activ-
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Versluys, J . 1898 Die mittlere und aussere
Ohrsphare der Lacertilia und Rhynchocephalia.
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Werner, Y. L. ,1968 The function of the i nner
ear i n lizards: temperature effects i n Gekko-
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Wever, E. G. 1939 The electrical respogses of
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1966 Electrical potentials of the coch-
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1968 The ear of the chameleon: Chn-
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1969a The ear of the chameleon: the
round window problem. J . Exp. Zool., 171: 1-6.
1967
34 CARL GANS AND ERNEST GLEN WEVER
1969b The ear of the chameleon: Clzn- Wever, E. G., and J . A. Vernon 1957 Auditory
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Wever, E. G., and E. A. Peterson 1963 Audi- ___ 1960 'The problem of hearing i n snakes.
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