amphisbaenia

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The Ear and Hearing in Amphisbaenia (Reptilia)

CARL GANS2

AND

ERNEST GLEN WEVER

D e p a r t m e n t of B i o l o g y , S t a t e U n i v e r s i t y

of

N e w Yorh a t Buf fa lo , a n d

A u d i t o r y R e s e a r c h Laboratories P r i n c e t o n U n i u e r s i t y ,

P r i n c et o n , N e w J e r s ey

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

jus t

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 a n 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:

A m -

phisbaena alba 3 specimens), A m p h i s -

bae na darwin i t rac hura (1

specimen),

A m p h i s b a e n a

manni

(7 specimens), Chir-

india langi 2 specimens), Cynisca leu-

cura

3

specimens), Zygaspis v io lacea

3 specimens),

Monope l t i s c . capens is

2 specimens), T r o g o n o p h i s w i e g m a n n i

(2 specimens), and

Bipes b iporus (4

spe-

cimens).

METHOD

The an imals 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 a n

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

The exper iments were carr ied out

in

the Auditory

Research Laboratories of Princeton University with

facilities provided by grants from the National Insti-

tu te of Neurological Diseases and Stroke. The speci-

men s were obta ined with funds f rom NSF GB-6521X .

2 Present address: Department of

Zoology,

The Uni-

versity of Michigan, A nn Arbor, Mich igan 48104.

17



18

CARL GANS AND ERNEST GLEN WEVER

TABLE

The specim ens used are deposited i n the Carl Gans (CG) collection. T he species used, the

catalogue numbers, the localities and the collectors are as follows: Amphisbnenn a l b a :

(no No.), Brazil, (dealer); same species (CG

371

71, Venezuela, Edo. Carabobo, Valencia

(S. M. McCown); same species (CG

3718),

Brazil,

S.

P. Jundiai, Sitio Bandeirante (W. C. A.

Bokermann).

Ampkisbaenn darwini trachurn:

(CG

3752),

Brazil, RGS, Tramandai, Emboaba

(C. P. Jaeger and

S.

Correa). Amphisbnena

manni:

(CG 3822, 3823, 3844, 3845, 3846, 3852,

3853, 3859, 3860, 3861, 3862, 3863) Hispaniola, Ile de la Tortue, Palmistes (C. R. Warren).

Bipes

b i p o ~ z t s : CG 3804, 3805, 3806, 3808) Mexico, Baja California, Sul de la 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). C y n i s c a leucura: (CG 4126), Ghana, Legon

(B. Hughes); same species: (CG 4151, 4152), Ghana, Legon, hill behind 2001. Dept. (B.

Hughes). Monopeltis c n p e n s i s : (CG 4456, 4457), South Africa, O.F.S. othaville (J. Visser).

Twgonopkis wiegmanni:

(2

specimens, no No.), Maroc (Dealer).

Zygnspis

violacea: CG

4546,

4558,4559),

Zulu land, N dum u Gam e 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 a n 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.

In 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

2 3 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

C h i r i n d i a l a n g i )

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 IN AMPHISBAENIA (REPTILIA)

19

In 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. In 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 in 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 is shaded.

The line equals 1 m m to scale.



20


Extracolurnel a'

Fig. 2

Lateral

view of the skull

of

Anzpk i sb t re7zn t ~ e n(Carnegie Museum no.

37636)

showing the stapes an d extracolumella.

A s

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 tha t, 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 ar ticulation 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 s b~ i e? ru

nnni

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

bne nn mnnni. The footplate is broad,

surgically; the system on the r ight is intact.

equalling the diameter of the otic capsule,

Figure

Scale

X 12.



EAR AND

H E A R I N G IN AMPHISBAENIA REPTILIA)

21

Fig. 4 Photomicrograph at a higher power of the right inner ear region

of

the same spe-

c imen 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.

In 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 ea r 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




Tectorial membrane

Fig,

5

Drawing

of

the auditory papilla

of A m p k i s b a e n a a l b a ,

from a section transverse

to the basilar membran e.

TABLE 2

N u m b e r of h a i r c e l l s

Species

Number of

cells

Animal

number Left ear Right ear

A m p i sb a e n a a l b n

1500

1667

1668

A m p h i s b a e n a d t rr w in i t i n c h ti r a

1525

A m p h i s b n e n t r m u n n i

1520

1524

1547

1548

T r o g o n op h i s w i e g m a n n i

1736

B ip e s b iporz r s

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.

Am phi sbae na a lba has the largest num-

ber, averaging

154 N = 3) .

For A . dar-

wini

t rachura (N

= 1),

A . m a n n i N

=

5 ) , and T r o g o n o p h i s w i e g m a n n i N =

1)

the numbers are hardly distinguishable,

approximately 100. For Bipes b iporus the

number is smaller, mean

54

N = 4).

Cochlear potent ia l s tudies

1.

A m p h i s b a e n a a l b a .

The solid-lined

curve in figure

6

gives measurements of

auditory sensitivity in terms of cochlear

potentials for

a

specimen of


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 a n 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 HEARING

I N

AMPHISBAENIA (REPTILIA)

3 4 5

6 7 8 9 1 2

3 4

5

6 7 8 9 1

2 3

Frequency

Fig. 6 Auditory sensitivity to aerial sounds in 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, in decibels relative to

1 dyne

per sq cm, required to produce a cochlear potential of 0.1

pv. In 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 norm al 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

H z and fell

changes.

off fairly regularly for higher tones. When



24

C A R L GANS A N D 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. A m p h i s b a e n a d a r w i n i t rachura . The

sensitivity

of

a specimen of


d a r w i n i t r a c h u r a 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 in a specimen of

Anzphisbflena dwwin i

tmchzim

(left ear).

60

-

0

Frequency

Fig.

9

Sensitivity functions for the right ear of the same specimen as in th e preceding

figure, under normal conditions (solid line) and after cutting the extracolumella (broken line).



E A R A N D H E A R I N G I N A M P H I S B A E N I A R E P T I L I A )

5

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 H z averaged 40 dB

and for higher tones up to

7000 Hz

aver-

aged

23.5

dB.

3.

A mph i s baena ma nn i . The best sen-

sitivity of A m p h is b ae n a m a n n i is between

600 and

1500

Hz (fig. 10); i t declines

fairly rapidly for lower and higher tones.

In a second specimen (fig. l l ) , 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

r e q u e n c y

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

r e q u e n c y

Fig.

1 1

Sensitivity functions for another specimen of

Amphisbnena manni ,

under normal

conditions (solid line) an d after interrupt ing the extracolumella (broken line).



26

C A R L

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

In response to a vibrating needle ap- aeria l stimulation. The extracolumella

plied to the side of the face (solid line, was the n severed jus t 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

hea d, for norma l conditions (solid line) an d after severing the extracolum ella (broken line).

40

- 0

Fig.

13

Normal sensitivity curves for aerial sounds in a specimen of C h i r i n d i a langi at

two body tem perat ures as indicated.




7

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 in 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 a t

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 .

Z y gasp i s u io lac e a . The greatest

sensitivity of a specimen of

Z y gasp i s

vi-

olacea occurred at 300 and at 500

H z

with a sharp loss in the intermediate zone

as in C y ni sc a (fig. 15). The sensitivity

decline at higher frequencies is typical

of Phese animals.

7.

Monope l t i s c c ape ns i s . Best sen-

sitivity for a specimen of Monope l t i s c.

c ape ns i s

occurred at two points in the

low-frequency region, 200 and

500

H z,

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

H z

(fig. 17).

Severing of the extracolumella again led

to a more than 20 dB loss of sensitivity

(broken curve i n 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 M o n o p e l t i s c. c a p e n s i s , under nor-

ma l conditions.

100

1000

Frequency

10,000

Fig. 17

Sensitivity curves for

a

second specimen of

M o n o p e l t i s

c. c a p e n s i s

under normal

conditions (solid line) a nd after inter rupt ing the extracolumella (broken line).




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

1000

10,000

Frequency

Fig.

18

Aerial sensitivity curves obtained in a specimen of Monopeltis c. capensis with

an electrode applied

to

the left saccule (solid line) a nd a n 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 t he left side.

40

3

+20

2-

2 0

P

u

T2

m

a

0

-u

S

; 20

-

40

100 1000

Frequency

Fig. 19

A

sensitivity cu rve for a spe cim en of Trogonophis wiegmnnni.

100



30

C A R L G A N S A N D E R N E S T G L E N W E V E R

2 3 4 5 6 7 8 9 1 2 3 4 5 6 7 8 9 1

5 6

7 8 9

Frequency

1000 10,000

Fig.

20

Sensitivity curves obtained in 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 a nd decibels relative to a n amplitu de of

1

m p for the me chanic al stimuli.

Fig.

21

A sketch of the left side of the head of a specimen of Trogonophis wiegmcinni

showing the scalation a nd the locations used for stimulat ing 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). A t 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

ampli tude 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

P

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 b iporus .

Our resul ts for

B i p es

b i p o r u s

are to be regarded as preliminary,

-

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

+ 2 0

P

l

D

0

al

U

S

6 -20

- 0

100 1000 10,000

Frequency

Fig. 23

Aerial sensitivity curves in two specimens of Bipes biporus chosen to show the

range obtained.



3


v

-

3 + 2 0

1 0

Q

E

20

7

+-

.

>

1 40E

0

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 B i p e s

biporiis with the needle applied to the side of the face nea r t he stapes ((solid line) an d to th e

front region of th e lower j a w (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 stimulat ion , 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.

DISCUSSION

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.

B i p e s b i p o r u s

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 A m p h i s b a e n a , C h i r in d i a ,

C y n i s c a , M o n o p e l t i s , and Z y g a s p i s ) , the

extracolumellar rod extends far forward

into the skin layer, lateral to the lower

jaw. In T r o g o n o p h i 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 D i p l o m e t o p o n

and A g a m o d o n . 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. In A m p h i s b a e n a manni the best

region seems to be slightly higher (be-

tween 700 and 1000 Hz) , and it may be

still higher in B i p e s b i p o r u s . Most of the

amphisbaenian species yielded sensitivity

curves whose maximum was approximate-

ly

-20

dB though there was considerable

variation and T r o g o n o p h i 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

- 4 0

dB (for a response of

0 .1

~ v ) , ut

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 simi lar 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 -6 0 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 A m p h i s b a e n a a lb a

and A . m a n n i ) 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 subte rranean vibration when

the face is held in contact with the tun-

nel wall.

The experiments on Monope l t i s capen-

s i 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. In: The Biology of the Reptilia. Vol.

2b.

C . Gans and T. S. Parsons, eds. Academic Press,

London, p p. 192-275.

Gans,

C .

1960 Studies on amph isbaen ids (Am-

phisbaenia: Reptilia). 1. A taxonomic revision

of the Trogonophinae and

a

functional inter-

pretation of the amphis baenid ad aptive patt ern.

Bull. Amer. Mus. Nat. Hist., 119: 129-204.

A

checklist of the recent amphis-

bae nian s (A mphis baenia: Reptilia). Bull. Amer.

Mus. Nat. Hist., 135: 61-106.

1968 Relative success of divergent

pathways in amphisbaenian specialization.

Amer.

Nat. ,

10 2: 345-362.

Gans, C., and J. J. Bonin 196 3 Acoustic activ-

ity recorder for burrowing animals. Science,

140: 398.

Versluys,

J.

1898 Die mittlere und aussere

Ohrsphare der Lacertilia und Rhynchocephalia.

Zool. Jb', Abt. Anat. , 12: 16 1 4 0 6 .

Werner, Y. L. ,1968 The function

of

the inner

ear in lizards: temperature effects in Gekko-

noidea and Iguanidae. Proc. 11th Ann. Meet-

ing, SOC.Study of Amphib. Rept., J. Herpetol.,

. 2: 178.

Wever,

E .

G. 193 9 The electrical respogses of

the ear. Psychol. Bull., 36: 143-187.

1966 Electrical pot enti als of the coch-

lea. Physiol. Revs., 46: 102-127.

1968 The ear

of

the chameleon:

C h n -

miicleo s e n e g a l e m i s and Chiimcleleo

qziilensis.

J. Exp. Zool., 168: 42 34 3 6.

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

mneleo koknelii

a n d

C k a m c t e l e o jnchsoni.

J. responses in the spectacled caiman. J. Cell. and

Exp. Zool., 171: 3 0 5 3 1 2 .

Wever, E. G., and E.

A.

Peterson 1963 Audi- ___ 1960 'The problem of hearing in snakes.

tory sensitivity in three iguanid lizards.

J.

Audi-

tory Res., 3 : 205-212.

Comp.

Physiol., 50: 33-340.

J. Auditory Res.,

1 ;

77-83.

amphisbaenia

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