J. exp. Biol.

195, 329–343 (1994)

Printed in Great Britain © The Company of Biologists Limited 1994
329

THE LUNG–EARDRUM PATHWAY IN THREE TREEFROG AND

FOUR DENDROBATID FROG SPECIES: SOME PROPERTIES OF
SOUND TRANSMISSION

GÜNTER EHRET, ELKE KEILWERTH

Abteilung Vergleichende Neurobiologie, Universität Ulm, D-89069 Ulm, Germany
AND TSUTOMU KAMADA
Department of Oral Physiology, School of Dentistry, Hokkaido University,
Sapporo 060, Japan

Accepted 23 June 1994

Summary
Frequency–response curves of the tympanum and lateral body wall (lung area) were
measured by laser Doppler vibrometry in three treefrog (Smilisca baudini, Hyla cinerea,
Osteopilus septentrionalis) and four dendrobatid frog (Dendrobates tinctorius,
D. histrionicus, Epipedobates tricolor, E. azureiventris) species. The high-frequency cut-
off of the body wall response was always lower than that of the tympanum. The best
response frequencies of the lateral body wall were lower than those of the tympanum in
some species (S. baudini, O. septentrionalis, D. tinctorius), while in the others they were
rather similar. Best tympanic frequencies and best body wall response frequencies tended
to differ more with increasing body size.
Stimulation of the tympanum by sound transfer through 3.14 mm2 areas of the lateral
body wall showed that the lung–eardrum pathway can be in two states, depending on
breathing activity within the lungs: 44 % (in Smilisca), 39 % (in Hyla) and 31 % (in
Osteopilus) of the eardrum vibrations were 2.5–8 times (8–18 dB) larger when the frogs
were breathing with the lungs compared with non-breathing conditions.
The vibration amplitudes of the tympanum and lateral body wall of the treefrogs
followed the same dependence on sound intensity, only absolute amplitudes differed
between species.
Our results suggest that the lung–eardrum pathway attenuates high-frequency
components of species-specific calls and enhances low-frequency components. In
addition, an amplitude modulation is imposed on the low frequencies during the rhythm
of breathing.

Introduction
The lateral body wall overlying the lung of several species of frogs has been shown to
vibrate in response to sound at frequencies similar to, or lower than, those to which the
eardrum is sensitive (Narins et al. 1988; Jørgensen, 1991; Hetherington, 1992). The

Key words: amphibian hearing, auditory periphery, lung–eardrum pathway, tympanum vibration, frogs.
330 G. EHRET, E. KEILWERTH AND T. KAMADA
sound that enters the lungs passes through an internal pathway via the glottis, mouth
cavity and Eustachian tubes to the inner surface of the tympanum, where a vibrational
response occurs (Ehret et al. 1990; Jørgensen et al. 1991). This sound transmission from
the lung is one component of the pressure gradient established between the outer and
inner surfaces of the tympanum. Sounds directly impinging on the eardrum from outside
and from other internal sources, such as a pathway from the contralateral tympanum, also
contribute to the pressure gradient, so that the amplitude and phase of the tympanic
vibration is the result of a complex interaction of waves reaching the eardrum by various
routes (Chung et al. 1981; Feng and Shofner, 1981; Vlaming et al. 1984; Michelsen et al.
1986). Since pressure-gradient systems are inherently directionally sensitive, the
vibrational amplitude of the tympanum also depends on the angle of incidence of the
sound (Michelsen et al. 1986; Jørgensen, 1991; Jørgensen and Gerhardt, 1991; Jørgensen
et al. 1991). Thus, it has been suggested that the biological function of the multi-input
system to the frog tympanum is to provide the basis for the localization of sound, which is
remarkably accurate despite the tiny heads of some hylid and dendrobatid frogs (Feng
et al. 1976; Gerhardt and Rheinlaender, 1980; Rheinlaender et al. 1981; Klump and
Gerhardt, 1989).
Many questions remain concerning the actual contribution to the tympanic response of
each of the routes the sound can take before reaching the eardrum. In our present study,
we report eardrum and lateral body wall vibrations of seven frog species and thus broaden
the comparative basis for a discussion of the significance of this input to the ear.
Furthermore, we present data on the modulation of the effectiveness of sound
transmission via the lung and mouth cavity when the glottis is closed or open, and finally
measure the intensity-dependence of vibration amplitudes of the tympanum and body
wall, in order to estimate the relative influence of the lung on the tympanum at various
sound intensities.

Materials and methods

Animals
Six American treefrogs, two Hyla cinerea (body lengths 51 and 46 mm), three
Osteopilus septentrionalis (72, 72 and 65 mm) and one Smilisca baudini (59 mm), and ten
dendrobatid frogs, three Dendrobates tinctorius (37, 40 and 42 mm), three Dendrobates
histrionicus (25, 28 and 32 mm), two Epipedobates azureiventris, (23 and 27 mm) and
two Epipedobates tricolor (20 and 22 mm), were used. All frogs were adult males
captured at their natural habitats. The animals were kept in terraria
(23.5 cm324 cm334.5 cm) with plants and water basins in an air-conditioned room at the
University of Konstanz, Germany. Lights were on from 08:00 h to 20:00 h. Room
temperature was 22–24 ˚C during the day and 18–20 ˚C at night, humidity was 80–90 %.
All experiments were performed with fully awake, unrestrained animals between
09:00 h and 21:00 h. Prior to the measurements, the treefrogs were exercised by letting
them leap in the terrarium for several minutes. This tiring of the frogs markedly reduced
their tendency to move during data recording and increased the ventilation of the lungs.
Several procedures were attempted to keep the dendrobatid frogs sitting motionless for at
 Lung–eardrum sound transmission in frogs 331
least the several minutes necessary to obtain reproducible measurements. By leaving the
frogs as undisturbed as possible, we finally managed to obtain data under free-field sound
conditions. Stimulation with a closed-sound system, as carried out with the treefrogs, was
impossible for the dendrobatids.

Laser measurements
The apparatus and procedures have previously been described (Narins et al. 1988;
Ehret et al. 1990). A frog was placed on a vertical post (10 cm in diameter) in the centre of
a vibration-damped terrarium. A 5 mW He/Ne laser beam could be focused onto the
tympanum or any part of the frog’s body on the side directly exposed to the free-field
sound. Vibrations were recorded in the Doppler vibrometer mode of the laser (Disa 55x).
The analog signals of the laser output were bandpass-filtered (0.1–10 kHz, Kemo VBF/8,
48 dB per octave), amplified (Hewlett-Packard 465A) and stored either on channel 1 of a
four-channel tape recorder (Teac A-2340SX), for off-line analysis, or Fourier-
transformed (Nicolet spectrum analyzer 446A) and velocity or displacement spectra were
viewed on-line. Channel 2 of the tape recorder was used for storage of the sound signal,
channel 3 for stimulus synchronous trigger signals and channel 4 for vocal comment. The
precise spots of measurements on the frog’s body were recorded photographically
(Kodak Ektachrom 400ASA). During the laser measurements, breathing activity was
observed and movements of the body flank were noted on channel 4 of the tape recorder.

Acoustic stimulation
Continuous white noise was presented free-field in 20 s long bursts to all frog species. In
addition, the treefrogs were stimulated with bursts of two alternating tones, either free-field
or through a closed sound system. Tones of known frequency (Kontron counter 400B)
were produced in two generators (Wavetek 130 and 132) and each was passed through
attenuators (Hewlett-Packard 350D) into one channel of a two-channel electronic switch,
where they were formed into bursts (300 ms duration, 5 ms rise and fall times, 300 ms
inter-burst interval) and added to give an alternating series. The output of the switch was
amplified (Hewlett-Packard 467A) and passed to a dynamic loudspeaker (Transco HTF
80/5), for free-field stimulation, or to an electrostatic speaker (Machmerth et al. 1975) in a
closed sound system consisting of a metal headpiece with a 9.2 cm long metal tube (inside
diameter 2 mm, outside diameter 3 mm at its tip) screwed onto the speaker as a sound
outlet. At the base of the tube, a calibrated 6.35 mm condenser microphone (Bruel and
Kjaer 4135) connected to a measuring amplifier (Bruel and Kjaer 2606) was fitted into the
sound pathway to monitor the sound pressure level on-line (dB SPL re 20 mPa) in the tube.
During stimulation, the open end of the tube gently touched the frog’s skin and was sealed
to it with a film of silicone grease. With this arrangement, 3.14 mm2 areas of the frog’s
body could be stimulated with tone bursts of known sound pressure level (SPL).
Noise was produced in a generator (Wavetek 132) and passed through a filter (Kemo
VBF/8, bandpass 0.1–10 kHz, 48 dB per octave), attenuator (Hewlett-Packard 350D) and
amplifier (Hewlett-Packard 467A) to the free-field speaker. The spectral response of this
speaker was flat to within ±6 dB between 0.9 and 8.7 kHz (Fig. 1) measured at the
position of the experimental frog. Thus, the speaker characteristics reflect the response of
332 G. EHRET, E. KEILWERTH AND T. KAMADA
Relative average velocity

10 dB

0 2 4 6 8 10
Frequency (kHz)

Fig. 1. Frequency characteristics of the free-field loudspeaker in response to white noise

(bandpass 0.1–10 kHz) measured at the position of the experimental frog.

the sound-generating system and the acoustics of the apparatus. This speaker was
mechanically decoupled from the terrarium so that possible stimulation of the frog via
vibrations from the speaker was excluded. The distance between speaker and frog was
70 cm; the angle to the frog’s long axis was 90 ˚.
SPLs of the tone bursts and the free-field noise bursts were calibrated at the position of
the frog after every experiment with the condenser microphone and measuring amplifier
described above. The tone frequencies for stimulation of the treefrogs were selected
according to the frequency content of their calls. Hyla cinerea was stimulated at 0.9 and
2.7 kHz (Gerhardt, 1974; Oldham and Gerhardt, 1975), Smilisca baudini at 0.96 and
2 kHz (Duellmann, 1970) and Osteopilus septentrionalis at 1 and 2 kHz. These are the
main frequencies of calls of Osteopilus from a disc supplied with Rivero (1978); they
were analyzed with a sonagraph (Uniscan II).

Data analysis
The equipment for data recording and analysis was calibrated so that the vibration
measured by the laser and stored on tape could be calculated as absolute values for
velocity or displacement. The stored laser signal was Fourier-transformed by the
spectrum analyser (Nicolet 446A) and plotted (Nicolet 136a). Average velocity or
displacement spectra of the sound response at a given spot on a frog’s body were
calculated (N=128). The average background spectrum without sound stimulation taken
at the same spot on the frog’s body (N=128) was substracted from the average values in
response to sound. Single spectra of tone responses were also measured.
Before quantitative data were recorded, the body of each frog was scanned with the
laser to determine the area of the body wall with the largest vibrational amplitude. Fig. 2
 Lung–eardrum sound transmission in frogs 333
shows a typical example of the distribution of vibrational amplitudes at various points on
the body in comparison with those on the tympanum. It is evident that, besides the
eardrum, the lung area is most sensitive to sound and shows the best vibrational
responses. This was true for all species in our study.

Results
Frequency response ranges
Responses to free-field stimulation with the bandpassed white noise (total level 90 dB
SPL) were measured at the tympanum and the lateral body wall area (lung area), where
the highest vibrational amplitudes were recorded. Fig. 3 shows an average velocity
spectrum from one of each treefrog species; the spectra for the dendrobatid species are
given in Fig. 4. Frequency response ranges can be estimated as the bandpass between the
lowest and highest frequencies at which a vibration above the average background noise
becomes noticeable. Table 1 presents the maximum extensions of the frequency response
ranges combined from all the animals of each species used in this study. Frequency
response ranges of individual frogs can be smaller (compare Figs 3 and 4).
In all individuals tested, the high-frequency cut-off of the frequency response range of
the lung area was always lower than that of the tympanum. The low-frequency cut-off of
the lung area response was either lower or similar to that of the tympanum. There was no
common trend with regard to the best response range of the tympanum compared with
that of the lung area. In Smilisca baudini, there was no overlap of best response ranges.
The lung area maximum responsiveness was at much lower frequencies than that of the
tympanum (Table 1; Fig. 3A). In Osteopilus septentrionalis and Dendrobates tinctorius,
the lung area responded best at frequencies just lower than those leading to the best
responses of the tympanum (Table 1, Figs 3C, 4B). In the other four species (Hyla
cinerea, Dendrobates histrionicus, Epipedobates tricolor, Epipedobates azureiventris),
the best frequency response range of the lung largely overlapped with or lay within the
best response range of the tympanum (Table 1; Figs 3B, 4A,C,D).

Selective stimulation of the lung area

While recording vibrations of the tympanum in response to selective stimulation of a
spot of the lung area with the closed sound system, we noted that the frogs did not breathe
regularly with the lungs. Bouts of breathing activity were separated by periods during
which we did not see any movement of the body flank. We found that the amplitudes of
tympanic responses to a single tone burst (single spectra) were either large or small
(Fig. 5), but rarely intermediate, when the frog was breathing with the lungs, but only
small when the frog was not breathing. During breathing activity, large amplitudes were
found in 44 % (N=85) of all observations of Smilisca, 39 % (N=139) of Hyla and 31 %
(N=237) of Osteopilus. The difference between large and small amplitudes was between
8 and 18 dB (2.5–8.0 times; see Fig. 5). A statistical analysis of the distributions of
amplitude values during breathing activity in all treefrogs at all sound intensities used
showed that 19 out of 22 distributions were not normally distributed (x2-test; Sachs,
1974). Response amplitudes measured in single spectra (as shown in Fig. 5) were divided
 334 G. EHRET, E. KEILWERTH AND T. KAMADA

a h

k
c

d
Relative average velocity

b
a c k
e f l
g m
d n
h
e i

1 cm
l

g
n

10 dB

0 1 2 3 4 5 0 1 2 3 4 5
Frequency (kHz) Frequency (kHz)

Fig. 2
 Lung–eardrum sound transmission in frogs 335
Fig. 2. Average relative velocity in response to 1 and 2 kHz tones measured at the eardrum (a)
and various spots on the body wall (b–n) of an alert Osteopilus septentrionalis. The response
amplitudes are largest in the lung area (e–g, shown shaded).

into classes of equal width using the algorithm: (max2min)/√N = class width, where max
or min are the maximum or minimum measured amplitudes, N is the number of measured
amplitudes and √N is the number of classes (Sachs, 1974; Ramm and Hofmann, 1987).
The results are bimodal distributions such as those shown in Fig. 6, i.e. small (class 1) and
large (class 4) amplitudes dominated. These bimodal distributions of vibrational
amplitudes of the tympanum show that the pathway from the lung to the tympanum can
be in two functional states while the frog is breathing with the lungs.

Table 1. Frequency ranges of vibrational responsiveness measured at the tympanum and

lung area of the lateral body wall and main frequencies of advertisement calls of seven
frog species
Frequency range (kHz)
Call frequencies
Tympanum Lung (kHz)
Smilisca baudini ≈0.1+21
Range 0.7–4.5 0.7–2.1
Best response 2.0–2.8 0.7–0.9
Hyla cinerea 0.9+2.7+3.02
Range 0.2–5.3 0.2–3.2
Best response 1.2–3.5 1.4–2.2
Osteopilus septentrionalis ≈1+2
Range 0.3–4.6 0.3–3.0
Best response 1.0–3.2 0.7–1.4
Dendrobates histrionicus 2.7–3.93
Range 1.0–4.4 1.0–3.5
Best response 1.7–3.4 1.7–2.6
Dendrobates tinctorius 3–44
Range 1.7–5.5 1.0–3.1
Best response 2.0–3.4 1.6–2.1
Epipedobates tricolor 3.5–4.73
Range 0.3–8.2 0.1–6.8
Best response 3.0–6.0 3.3–4.6
Epipedobates azureiventris 2.8–5.05
Range 0.2–8.0 0.2–3.7
Best response 2.0–5.2 1.8–2.8

The ranges given are the maximum extensions of the frequency response ranges combined from all
animals of each species.
The best response indicates the frequency range in which the peaks of the response curves of all
animals of a given species are located (compare Figs 3 and 4).
1Duellmann (1970); 2Oldham and Gerhardt (1975); Gerhardt (1974); 3Zimmermann and Rahmann

(1987); Zimmermann (1990); 4Zimmermann and Zimmermann (1988); 5Myers and Daly (1976).
336 G. EHRET, E. KEILWERTH AND T. KAMADA

A
Relative average velocity

L 10 dB

0 1 2 3 4 5

B
Relative average velocity

L
10 dB

0 1 2 3 4 5

C
Relative average velocity

10 dB
L

0 1 2 3 4 5
Frequency (kHz)

Fig. 3. Frequency response characteristics of the tympanum (T) and the best response area of
the lateral body wall (L) of one individual each of (A) Smilisca baudini, (B) Hyla cinerea and
(C) Osteopilus septentrionalis.
 Lung–eardrum sound transmission in frogs 337

A B
T
T

L L
Relative average velocity

G 10 dB
g
0 1 2 3 4 5 0 1 2 3 4 5
0 2 4 6 8 10
C D
T T

T
L

L G 10 dB
g
0 2 4 6 8 10 0 1 2 3 4 5
Frequency (kHz)

Fig. 4. Frequency response characteristics of the tympanum (T) and the best response area of
the lateral body wall (L) of one individual each of (A) Dendrobates histrionicus, (B) D.
tinctorius, (C) Epipedobates tricolor and (D) E. azureiventris. In D, the upper x-axis scale is
related to the upper tympanum curve, which shows the whole frequency response range of the
tympanum; the lower x-axis scale is related to the lower tympanum and body wall curves
showing the tympanum and lung response with higher resolution.

Class 4
Relative displacement

Class 1

10 dB 10 dB

1 2 3 4 5 1 2 3 4 5
Frequency (kHz)

Fig. 5. An example showing a small (class 1) and large (class 4) response of the tympanum of
Smilisca baudini to selective stimulation via the lung area of the body wall.
338 G. EHRET, E. KEILWERTH AND T. KAMADA

14 10
A B
12
8
10
Number

8 6
6 4
4
2
2
0 0
1 2 3 4 1 2 3 4

16
C
12
Number

0
1 2 3 4
Class

Fig. 6. Division of displacement amplitudes of the tympanum into four classes (see Results);
class 1, small; class 4, large; classes 2, 3, intermediate. The tympanic displacements were
caused by selective tone stimulation via the lung area of the body wall while the frog was
breathing. Example distributions are shown for (A) Smilisca baudini, (N=20), (B) Hyla cinerea
(N=17) and (C) Osteopilus septentrionalis (N=19). Number, number of values in each sample.

Intensity-dependence of vibration amplitudes

The intensity-dependencies of the displacement amplitudes at the tympanum to free-
field and selective lung area stimulation and at the lung area to free-field stimulation are
presented in Fig. 7 for the three treefrog species. Of 36 investigated functions, 31 (those
shown in Fig. 7) showed a linear (in the double logarithmic plots) and statistically
significant relationship between displacement amplitude and sound pressure level
(0.001<P<0.05). Since the slopes of all significant correlations do not differ much (range
0.038–0.056), the relationship between displacement amplitude and sound intensitiy is
comparable among species and across conditions of stimulation and measurement. Only
the absolute amplitude of vibration of the tympanum and the lung area may be different.
The relationship between sound intensity and displacement amplitude was not significant
for the remaining five functions. These functions concerned some measurements of free-
field and selective lung area stimulation in both individuals of Hyla and two individuals
of Osteopilus.
At the stimulation frequencies examined, the tympanum always showed the largest
displacement amplitudes when stimulated free-field. The displacement values in response
to the lower frequencies tested for each species (0.96, 0.9, 1.0 kHz) were between 1.5 and
2 times larger than those of the lung area. The differences were even larger (between 20
 Lung–eardrum sound transmission in frogs 339

100 100 B
A
Displacement amplitude (nm)

10 10

1 1
40 60 80 100 40 60 80 100

100 C
Displacement amplitude (nm)

10

1
40 60 80 100
Sound pressure level (dB)

Fig. 7. Intensity-dependence of average displacement amplitudes for (A) Smilisca baudini,

(B) Hyla cinerea and (C) Osteopilus septentrionalis. Measurements from all individual
treefrogs are shown. Regression lines indicate statistically significant correlations. Tympanum
(filled circles) and lateral body wall (open circles) by free-field stimulation at 0.96 kHz
(Smilisca), 0.9 kHz (Hyla) or 1 kHz (Osteopilus). Tympanum (filled triangles) and lateral body
wall (open triangles) by free-field stimulation at 2 kHz (Smilisca, Osteopilus) or 2.7 kHz
(Hyla). Class 4 response (filled squares) and class 1 response (filled diamonds) of the
tympanum by selective stimulation at the respective lower frequencies mentioned above are
also given (see also Results and Fig. 5).

and 53 times) for the higher frequencies tested (2.0 and 2.7 kHz). In Smilisca and two
individuals of Osteopilus, the vibrational amplitudes of the lung area in response to free-
field stimulation with the lower frequencies were comparable to the displacements
measured at the tympanum when the lung area was selectively stimulated with the closed
sound system and the frog was breathing with the lungs. This indicates a very effective
coupling between lung and tympanum vibrations.

Discussion
Frequency response characteristics
The general physics of sound receptor systems (Fletcher and Thwaites, 1979) predicts
that the frequency response ranges and resonance frequencies of the lateral body wall
340 G. EHRET, E. KEILWERTH AND T. KAMADA
4.5
4
3.5
Best frequency (kHz)

3
2.5 T
2
1.5
1 L
0.5
0
15 25 35 45 55 65 75
Body length (mm)

Fig. 8. Relationship between body length and the best response frequency of the tympanum T
(filled circles) and lung area of the body wall L (open squares) of all 16 individual frogs
investigated (for equations, see Discussion).

depend on the lung volume and the stiffness of the vibrating structures, mainly of the skin
covering the lung area. The tympanic frequency response is determined by the size, mass
and stiffness of the tympanic membrane and the middle ear ossicles and by the middle ear
volume (Dallos, 1973). Thus, the frequency response of the tympanic membrane and
body wall must not be the same. In harmony with previous studies on frogs and toads
(Narins et al. 1988; Jørgensen, 1991; Jørgensen et al. 1991; Hetherington, 1992), the
frequency response range of the lateral body wall always has the high-frequency cut-off
at lower frequencies than the tympanum (Figs 3, 4; Table 1). The frequencies of the best
body wall response, however, are not always lower than those of the best tympanic
response. Fig. 8 shows the relationship between best frequencies and body size for the
individuals in the present study. Best frequencies (BF) decreased significantly (P<0.005)
with increasing body length (S): lnBF=a2bS. The slope (b) is about twice as large for the
lung area of the body wall (b=0.023) as for the tympanum (b=0.01). The constants (a) in
the equation are similar (tympanum, a=1.32; lung area of body wall, a=1.56). This
indicates that the resonance frequency of the body wall vibration depends much more on
the size of the frog, and thus on the area of the skin covering the lung, than does the best
frequency of the eardrum. The best frequency response ranges of the tympanum and
lateral body wall may be similar only when the frogs are small, like the small
dendrobatids, or have a smooth and rather stiff skin covering the lungs, like hylid and
some ranid frogs (Figs 3, 4, 8; Table 1; see also Jørgensen, 1991). In this context, the very
low best frequency of the body wall of the Smilisca (Fig. 3A) can be explained by the
structure of its skin, which is rather coriaceous and covered with little warty swellings.
In general, Fig. 8 shows that a coincidence of best frequency responses of the
tympanum and lateral body wall is more likely in small than in larger frogs. This suggests
that during postmetamorphic growth the best frequency response of the eardrum and
lateral body wall may change from being similar to being different, which means that the
 Lung–eardrum sound transmission in frogs 341
contribution of the lung pathway to the frequency response pattern of the tympanum may
vary with age.

The magnitude of the influence of the lung on tympanic vibration

A 15–20 dB enhancement of the sound from the lung to the eardrum by an open glottis
has been reported in the Puerto-Rican treefrog Eleutherodactylus coqui by Jørgensen
et al. (1991). It has also been shown that the greater is the degree of inflation of the lungs,
the larger is the effect of the lung pathway on the eardrum (Jørgensen, 1991). Our present
results suggest a similar influence of the lung on the eardrum response. If the lungs are
ventilated by breathing (through an open glottis), the sound propagates up to eight times
(18 dB) better from the lung to the tympanum than when the frog is not breathing
(possibly with its glottis closed). Thus, the sound propagation from the lung to the
eardrums is highly variable and depends on breathing activity. An actively moving or
calling frog with high energetic demands will be more likely to ventilate its lungs than a
resting one, so that the lung pathway is expected to make the greatest contribution to
hearing in frogs when they are active, e.g. in male–male or female–male interactions
during the breeding season.
When the frogs were breathing with their lungs, we recorded about 30–40 % of the
large response amplitudes at the tympanum, while the lung was stimulated with tone
bursts. If large amplitudes are related to a glottis-open condition, this suggests that the
glottis in our frogs may have been open for 30–40 % of the breathing cycle, which is
comparable to about 25 % in the resting treefrog Eleutherodactylus coqui (Narins et al.
1988). Thus, the lung input seems to be a source of amplitude modulation, by 15–20 dB,
of tympanic vibrations in the rhythm of breathing.
Furthermore, a change in the angle of incidence of a sound wave can attenuate the
tympanic response at certain frequencies by up to 40 dB if the glottis is open (Jørgensen
et al. 1991; Jørgensen, 1991). This induction of a highly directional frequency response
of the tympanum, by coupling it with the lung, suggests that the lung pathway of sound
may play a role in the sound localization of frogs. Behavioural tests of directional hearing
in the grey treefrog (Hyla versicolor), however, do not support this suggestion, because
this species locates a sound source less well when the sound contains frequencies to
which the eardrum response shows its maximum directionality (Jørgensen and Gerhardt,
1991). Instead of having a positive influence on the ability to localize sound, the lung
pathway seems to have a deleterious effect. Whether this result can be generalized has yet
to be evaluated in further studies.

Relationship of the frequency response range of the lungs to frequency spectra of calls
In Table 1, the best frequency response ranges of the tympanum and lateral body wall
over the lungs are shown together with the main frequency components of the
advertisement calls of the species investigated. With the exceptions of Osteopilus and
Epipedobates tricolor, the best response range of the lung area does not overlap with the
major frequencies of the calls. The frequencies leading to the maximum displacement of the
lateral body wall lie either between (Smilisca, Hyla) or below (D. histrionicus, D. tinctorius,
E. azureiventris) the main call frequencies. A similar incongruity between call frequencies
342 G. EHRET, E. KEILWERTH AND T. KAMADA
and best frequency response ranges of the body wall has been found in other treefrogs, such
as Eleutherodactylus coqui (Narins et al. 1988), Hyla gratiosa and Hyla versicolor
(Jørgensen, 1991; Gerhardt, 1981, 1982), in which the maximum body wall response
always occurs between low and high call frequencies. This mismatching of frequency
ranges, however, does not necessarily mean that the sound pathway via the lung is of little
importance to call perception in frogs. The available data on E. coqui, H. versicolor,
H. gratiosa and Rana temporaria (Jørgensen, 1991; Jørgensen et al. 1991) indicate that the
lung input to the eardrum contributes to the maximum directional response by attenuation of
the eardrum vibration at or above the frequency of maximum displacement of the lateral
body wall. For Hyla cinerea, the frequency range of attenuation may lie between 1.5 and
2.5 kHz (see Fig. 3). However, the lung input also leads to a maximum amplification of
eardrum vibrations below the frequency of the maximum body wall response. Thus,
eardrum vibrations in response to the low-frequency components of the advertisement calls
of H. cinerea (0.9 kHz), H. gratiosa, H. versicolor and E. coqui may be optimally amplified
by the sound pathway through the lungs. At the same time, higher-frequency components
are attenuated by the lung pathway, the magnitude of attenuation depending on the angle of
incidence of the sound. The lowpass filter of the lung pathway could lead to considerable
attenuation of high-frequency call components or even entire advertisement calls for some
species in addition to an attenuation of high-frequency noise from the environment. In
conclusion, the few data available suggest that the major functional contribution of the lung
input to the hearing of treefrogs, at least, is the enhancement of the perception of low-
frequency components of advertisement calls. This hypothesis could be tested by measuring
the ability of animals in the presence of various background noises to detect a conspecific
caller against the noise, with and without a contribution of the lung pathway to the
eardrums. When the lungs are involved, the detection of a calling frog should require a
smaller signal-to-noise ratio than when there is no input from the lung.
In the dendrobatids, such as D. histrionicus, where the frequency range of the
advertisement calls is above the best response range of the lateral body wall (Table 1), the
lungs may play a role in detecting conspecific territorial (aggressive), courtship and
release calls, all of which may have a spectrum with more low-frequency components
(1.2–4 kHz in D. histrionicus) than the advertisement call (Zimmermann, 1990;
Zimmermann and Zimmermann, 1982). Hence, the comparison of species characteristics
suggests that the sound pathway through the lungs may contribute to auditory behaviour
in different ways depending on the frequency response patterns of the tympanum and
lateral body wall and the main frequencies of the species’ calls.

This study was supported by grants of the Deutsche Forschungsgemeinschaft. We

thank Dr T. Breithaupt, Dr B. Schmitz and Dr J. Tautz for their support during the course
of this study.

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