Effects of age and size in the ears of gekkonomorph lizards: middle-ear sensitivity
2
1 Department of Otorhinolaryngology: Head and Neck Surgery, University of
Pennsylvania, PA 19104, USA
2 University of Chicago Pritzker School of Medicine, 924 E
57th Street, Chicago, IL 60637, USA
3 Department of Evolution, Systematics and Ecology, The Hebrew University of
Jerusalem, 91904 Jerusalem, Israel
* Author for correspondence (e-mail: yehudah_w{at}yahoo.com)
Accepted 7 August 2001
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Summary |
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Key words: lizard, gecko, middle ear, transfer function, age effect, size effect
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Introduction |
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In the present work we endeavoured to separate the effects of size and age
on the functioning of the tetrapod ear, as exemplified in geckos. Geckos,
lizards of the family-cluster Gekkonomorpha, are of special interest because
their vocal communication is more extensive and better known than in other
lizard groups (Frankenberg and Werner,
1992; Y. L. Werner, in
press
).
Our experimental design was comparative. We planned to compare ear function in samples making up a triad: adults of a relatively large species, adults of a smaller species that is closely related, preferably congeneric, and juveniles of the larger species, having the size of the latter. We hoped that repetitions with comparable triads of different species would give similar results, thus demonstrating a general phenomenon. We applied to each animal four methodological approaches for assessing ear function and structure. (i) Measurement of the velocity transfer function of the tympanic membrane. (ii) Generation of audiograms from VIIIth-nerve compound action potential responses. (iii) Description and quantification of the morphology of various middle-ear structures, to gain information on the extent of mechanical and hydraulic levers. (iv) Classifying and counting the hair cells of the basilar papilla, visualised by scanning electron microscopy, to check for possible effects of their variation on auditory sensitivity.
This report deals only with the first approach, assessment of the velocity
transfer function of the tympanic membrane (hereinafter termed `transfer
function'). But in addition to the analysis of the three sample-triads, we
explore the interspecific correlation of the characterising variables of the
transfer function (peak velocity and its frequency) with the relevant
morphological size variables (measurements of the tympanic membrane,
extracolumella, and whole body). Some of our data have been reported elsewhere
(Werner et al., 1998,
2001
;
Saunders et al., 2000
). The
relevant parts of the middle ear are shown in
Fig. 1 (see also
fig. 1 in
Werner and Igi
,
2002
).
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Materials and methods |
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The second triad consisted of adults and juveniles of Oedura
marmorata Gray, 1842 and adults of the smaller Oedura reticulata
Bustard, 1969 (Diplodactylinae). O. marmorata were collected by N.
Werner and Y. L. Werner from granite outcrops 6-8 km north of Mount Magnet
township, Western Australia, during SeptemberOctober 1993, and were
used in experiments during JuneJuly 1994. The mean RA of the adults
(N=5) was 96.3 mm (range 85-99 mm) and mass 23.7 g (20.0-28.7 g), and
for the juveniles (N=5) mean RA was 69.0 mm (64-74 mm), mass 8.2 g
(range 5.4-11.2 g). In this species, maturation takes 5 years and is
accompanied by coloration change (Cogger,
1957; Y. L. Werner, personal observation). Hence we can estimate
that, when captured, the adults were at least 4.5 years old, and the juveniles
were up to 2.5 years old. (Voucher specimens HUJ-R 18934-18944.) O.
reticulata (N=5) were collected by N. Werner and Y. L. Werner in
eucalyptus groves in the Bungalbin Hills area, approximately 100 km NE of
Southern Cross township, southern Western Australia, during 1-5 November 1993,
and were used during JulyAugust 1994; mean RA 60.8 mm (52-68 mm), mean
mass 6.2 g (4.1-10.0 g). (Voucher specimens HUJ-R 18949-18953.)
A third triad comprised adults and one juvenile of Gehyra punctata (Fray, 1914) and somewhat smaller adult Gehyra variegata (Duméril and Bibron, 1836) (Gekkonidae: Gekkoninae). The G. punctata were collected by N. Werner and Y. L. Werner from a granite outcrop between Gallowa and Barnong Station, west-central Western Australia, on 17-18 September 1993 and used in June 1994. Mean RA of the adults (N=5) was 55.9 mm (51-61 mm) and mass 5.3 g (4.0-6.9). For the single juvenile, RA was 38 mm and mass 1.3 g. (Voucher specimens HUJ-R 18910-18917.) G. variegata (N=6) were collected by N. Werner and Y. L. Werner from granite outcrops 6-17 km north of Mount Magnet township, Western Australia, during SeptemberOctober 1993, and used in experiments in June 1994; mean RA 43.3 mm (38-47 mm) and mass 2.6 g (1.8-4.3 g). (Voucher specimens HUJ-R 18923-18927; 18929-18930.)
Biological and evolutionary background information on all species is given
in Rösler (1995) and
Bauer (1998
), and for the
Oedura and Gehyra species in Storr et al.
(1990
) and Cogger
(1992
).
Collecting in Australia and export to the USA were done under permits SF001105 from the Department of Conservation and Land Management of Western Australia, and PWS-P935483 from the Australian Nature Conservation Agency, Canberra, respectively. At the University of Pennsylvania, all geckos were maintained and tested under a protocol approved by the Institutional Animal Care and Use Committee of the University of Pennsylvania.
Between capture or receipt and testing (except during transportation) the animals were housed in small groups in glass terraria with shelters and access to water. They were fed mealworms, waxmoth larvae (in Australia) or crickets three times a week. The terraria were in rooms held at a constant 25°C under a 12h: 12h light:dark cycle.
Methods
Our methods were as described earlier (Werner et al.,
1998,
2001
) and are summarised as
follows. For anaesthesia we used a solution of 20% urethane in reptilian
saline (Wever, 1978
). The
initial dose was 0.012 ml g-1 and additional doses (each 20% of the
initial dose) were given to the smaller geckos, because small animals require
allometrically larger doses (Sedgwick,
1986
). Anaesthesia was judged by the elimination of any response
to pinching. We kept seasonal variation to a minimum among samples to be
compared (Köppl et al.,
1990
).
Tympanic membrane (TM) velocity and phase behavior were measured to a
constant pure tone intensity across all test frequencies (0.15-20.0 kHz) at
the TM surface (100 dB SPL). The velocity response was plotted to show only
the magnitude portion of the transfer function; phase behavior was the same as
previously reported (Werner et al.,
1998). Since the input sound stimulus at the TM was constant, the
velocity response directly indicates the transfer of sound vibrations from air
to the TM. The TM was surgically exposed by minimal removal of skin and soft
tissues surrounding the external ear opening. The animal was positioned on its
back on a metal plate, and the head and limbs were stabilized with modeling
clay, which also blocked the contralateral ear. The animal's mouth remained
closed but the throat was surgically opened, as for electrode access to the
round window, to enable later comparison of the results obtained from the two
methods. The metal plate was secured on a heavy-duty X-Y stage
resting on a large granite stone inside a sound-attenuated room. The tabletop
was isolated from the stone by vibration dampers. The X-Y stage
enabled the animal to be moved in these axes with micrometer precision.
Free-field acoustic stimulation was provided by a 14 cm midrange speaker
(model 405-8H, Altec Lansing Inc., Milford, PA, USA) suspended approximately
12 cm above the animal's head. Pure tone stimuli from the speaker were
generated with a computer-controlled frequency synthesiser (model System One,
Audio Precision Inc., Beaverton, OR, USA). The synthesiser was programmed to
step logarithmically through 141 frequencies between 0.15 and 20.0 kHz,
sequentially. The frequency range was extended beyond the 10.0 kHz limit that
is conventional when testing lizards, because some gecko vocalisations contain
ultrasound, even up to 60 kHz (Brown,
1985; Frankenberg and Werner,
1992
). A probe tube (50 mmx0.5 mm i.d.) leading to a 12.5 mm
condenser microphone was positioned with its tip at the perimeter of the TM.
The probe tube was calibrated in free field against a 3.13 mm condenser
microphone (Brüel and Kjaer, model 4138, Viby, Denmark). During
calibration of sound at the TM surface, the synthesiser stepped through all
test frequencies, while maintaining the voltage across the loudspeaker
constant. The output signal from the probe-tube microphone was led to the
analyser section of the synthesiser. The analyser section measured the voltage
of each test tone, as detected by the microphone. Low-frequency noise was
eliminated by a moving one-third octave filter centred about each test tone.
This filter was a built-in function of the analyser. A look-up table was
created (under software control) with test frequency and voltage in adjacent
columns. The software then calculated corrections for each frequency so that
the voltage delivered to the speaker by the generator portion of the
synthesiser would produce a constant SPL of 100 dB at the surface of the TM.
All measurements in dB were referenced against 20 µPa.
Once the sound level at the TM surface was calibrated, the interferometer laser beam was focused on the TM. The optical head of the laser interferometer was mounted on an x-y-z micromanipulator 20 cm from the TM. Either the animal or the laser head could be moved in order to align the laser beam with the desired point on the TM.
Glass microbeads, 15-30 µm diameter (5-10 ng), were placed at two, or
sometimes three, locations on the external surface of the TM
(Bigelow et al., 1996). These
microbead positions, chosen for repeatability and representing locations to
show the mechanical leverage and the input to the ossicular chain, were (A)
opposite the junction of the extracolumellar shaft with the extracolumellar
processes radiating on the inside of the TM, (B) at the tips of pars inferior
of the extracolumella (TPI) and, sometimes (C) on the free TM, approximately
midway between the TPI and the anterior rim of the TM
(Fig. 1). The tip of a single
human body hair was used to deposit the microbead on the TM surface. The beads
adhered to the TM, presumably because of the cerumen on the TM surface
(Cohen et al., 1992
). The glass
beads increased the reflectance of the laser beam by >300% compared with
the reflectance of the TM surface itself. The alignment of the laser beam with
the bead was adjusted for maximum signal strength. These procedures
significantly improved the signal-to-noise ratio of the velocity signal
received by the interferometer. The velocity transfer function of the TM was
measured at each bead location.
The synthesiser then stepped through the series of test frequencies, each presented at 100 dB SPL. The output signal from the interferometer was connected to the analyser section of the synthesiser and, as each tone was presented, a voltage signal for the velocity of the TM was stored in the computer memory and transferred to a disk file.
Each experiment was performed on a group of 4-6 animals (with the exception of the single Gehyra punctata juvenile). At each frequency the mean velocity response and standard error of the mean (S.E.M.) were calculated for the group. The resulting TM-response plots underwent a smoothing procedure, which calculated a running average over a moving window of six test frequencies. This smoothing procedure moderated local perturbations due to minor anomalies of calibration or unique responses of the TMs.
Temperature affects reptilian auditory sensitivity such that optimal
audiograms are obtained at the ecologically preferred body temperature of the
species (Campbell, 1969;
Werner, 1976
). Although a
minor contributing effect on the middle ear has been indicated
(Werner, 1983
), the main
effect is at the level of the inner ear
(Eatock and Manley, 1981
). Our
experiments were conducted at stable room temperature, 20-22°C, well
within the normal efficient activity range of the subjects, as all these
species are nocturnal foragers.
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Results |
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However, the four morphological measures differed a little in their effects on the velocity transfer function variables. Maximum velocity was most strongly correlated with RA (Fig. 2). The frequency at maximum velocity was most strongly negatively correlated with the extracolumellar anchorage length and the length of pars inferior (Fig. 3). The octave bandwidth of the velocity function was, again, most strongly negatively correlated with RA (Fig. 4). Maximum velocity strongly and significantly negatively correlated with its frequency. However, the correlation of maximum velocity and of peak frequency with octave bandwidth was not significant.
Next we applied stepwise regression analysis in order to view each of the
three physiological variables as a function of the four size measurements
(Draper and Smith, 1998). The
results matched the above in principle but indicated stricter restriction of
the factors affecting the physiology. Statistically, maximum velocity was
determined by RA alone (r2adj=0.743,
P<0.01). The frequency at maximum velocity was determined only by
pars inferior length (r2adj=0.599,
P<0.01). The octave bandwidth was determined by RA alone
(r2adj=0.613, P<0.01).
Finally, we asked whether juveniles differ from adults in the relationship
of the measured properties of the TM transfer function to the morphological
variation. We performed linear regressions, using only the size measurements
that significantly affected the physiological variables. The two age
categories were included as dummy variables
(Draper and Smith, 1998). To
correct for size differences between adults and juveniles, the measurements
were taken on a relative scale; the maximum measurements for each age category
were used as an anchor point and given the value of one. All other size
measurements were scaled relative to them. An Arcsine transformation was used
on the relative size values in order to adjust their distribution to a normal
one (y=arcsin
p, where p is the relative size
value) (Sokal and Rohlf,
1997
). The transformations performed on the data did not allow for
analysis of the intercept. No significant differences were found in all
analyses of juvenile and adult responses.
Size and age effects within species-triads
The results from the three triads of species are graphically summarised in
Figs
5,6,7,
in each of which the averaged TM transfer functions of the three samples
comprising the triad are superimposed. Because the point of measurement
(glass-bead location) affected the sensitivity of the transfer function, i.e.
the velocity attained, but not its shape
(fig. 6 in
Werner et al., 1998; fig. 2.18
in Saunders et al., 2000
), we
present for each triad the results from one location only (location A,
opposite the columellaextracolumella shaft). From Figs
5,6,7
it can be seen that in each of the triads the general shape of the transfer
functions is relatively similar for the two functions representing the
juveniles of the larger species and the similarly sized adults of the smaller
species. Both together differ from the more sharply tuned transfer function of
the adults of the larger species. We now consider these visual observations in
Figs
5,6,7
more quantitatively.
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Rather than complicate Figs
5,6,7
with the S.E.M. values on each curve at each test frequency, we present a
separate example of the amount of variation.
Fig. 5A shows a transfer
function averaged from the raw data, without the smoothing procedure, with
S.E.M. values calculated from the raw data. The variability shown in
Fig. 5A is typical of that seen
in all the transfer functions that we report here (except for one curve based
on a single animal) and elsewhere (figs
3,4,5,6
in Werner et al., 1998; fig.
2.18 in Saunders et al., 2000
;
fig. 2 in
Werner et al., 2001
).
The nine transfer functions measured opposite the columella (Figs 5,6,7) or at the TPI (Table 1) may be compared in quantitative terms by determining for each the greatest velocity, the frequency at the point of peak velocity, and the octave bandwidth. Table 1 shows that (at the TPI) in the eublepharid triad the TM attains a much higher velocity in the large adults than in the juveniles and small adults, which resemble each other. Similarly, the octave bandwidth of the velocity function in the large adults is less than half those of the juveniles and small adults, which resemble each other. However, the peak frequency of the small adults resembles that of the large adults (compare with Fig. 5). In the diplodactyline triad the small adults resembled the juveniles and differed from the large adults both in the best frequency and in octave bandwidth. In TM velocity the small adults were intermediate between the two other groups (compare with Fig. 6). Finally, in the gekkonine triad the peak frequency and the octave bandwidth are similar in the small adults and the juveniles, and together different from the large adults. The peak velocity of the juvenile is intermediate between the two adult groups (compare with Fig. 7).
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Discussion |
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The surgical window in the throat was shown by Werner et al.
(2001), using
Eublepharis as a model, to have little effect on the results except
at the lowest (<0.5 kHz) and highest (>8.0 kHz) frequencies. The effect
above 8.0 kHz is discussed below.
Although the contralateral ear was blocked with plasticine, the open sound system could stimulate the ipsilateral TM from both sides because of the fenestrated throat. However, the acoustic pathway through the throat was complicated and we have no evidence that it would allow a stimulus of sufficient intensity to effectively stimulate the inner surface of the TM. Moreover, if there was an effect, it was probably uniform across all the subjects being compared. Any effects of the varying relationship of sound wavelength to head size can be discounted because the transfer function shape correlated with animal size within triads rather than among triads; the adult Gehyra punctata had a transfer function shape like the adults of Eublepharis maculartius and Oedura marmorata but a body size like their juveniles or their respective small adults (Table 1). The size effect thus seems to occur independently in parallel within the genera or subfamilies (see below).
Comments on the results
The TM transfer functions in Figs
5 and
6 reveal irregularities in the
highest frequencies, although the plots represent group means. These `jumps'
in the velocity-frequency functions may well be due to the fenestration of the
throat (Werner et al., 2001).
Hence an investigation of the high-frequency capacity of gecko ears,
interesting because of the enigmatic high-frequency components in some of
their vocalizations (Brown,
1985
; Frankenberg and Werner,
1992
), should preferably employ methods that exclude such
fenestration. But our data do carry a lesson. From our data, as shown in Figs
5 and
6, in the smaller animals the
jumps occur at higher frequencies. In Fig.
7, representing even smaller species, only for the group of large
adults does the clear onset of a jump occur at the upper extremity of the
frequency range; in the curves of the juvenile and small adults there are only
marginal indications of a jump. This dependence of the frequency at which the
disturbance occurs on animal size (which could be expected) means that when
testing even larger lizards the fenestration could also cause disturbance at
lower frequencies. Additional, minor peaks in the transfer functions (e.g. in
Fig. 5, notably at 0.4 and 1
kHz) cannot yet be interpreted and may deserve attention in future
research.
Our analysis of interspecific correlations showed that statistically both the peak velocity of the TM (in mm s-1) and the octave bandwidth of the transfer functions were determined by body size. The frequency at which velocity peaked was determined by the pars inferior length. The difference between these two determining factors is small: among the three variables describing ear size, it is the extracolumellar anchorage length that shows the strongest correlation with RA (r=0.966) but the correlation of the pars inferior was similar (r=0.964; Table 2). Body length (RA) may be described as representing the three middle-ear size descriptors as follows. We performed a multiple regression of RA over the three ear-size measurements, using the stepwise method. The function used only the anchorage length as an explaining variable. The whole model was significant (radj2=0.925; P<0.001), but when testing the significance of the regression, only the slope was significantly different from zero (P<0.001). Since when ear size approaches zero, initial body size has no meaning, we excluded the intercept from the equation. Thus the best body size description as function of ear size is: RA=31.499xanchorage length.
In the above considerations, we note that the three juvenile samples did not differ significantly from the adults. Since the samples were few, we can only conclude that we could show no difference.
As outlined in the Introduction, we had hoped that any differences among the samples comprising a triad would be similar in all three triads, enabling an unambiguous conclusion to be made about whether age effects are distinct from size effects, and if so, in what way. This hope has been fulfilled only to a small extent. Graphically, in each of the three triads the general shape of the transfer functions is relatively similar for the two functions representing the juveniles of the larger species and the similarly sized adults of the smaller species. Both have a relatively broad velocity peak, and together differ from the more sharply tuned transfer function of the adults of the larger species. In quantitative terms, we may consider the bandwidth that achieved at least half the peak velocity. For the adults of the large species in all three triads, mean bandwidth = 0.66 octaves (range 0.53-0.78 octaves). In contrast, for the juveniles of the same three species, mean bandwidth = 2.13 octaves (1.65-2.85 octaves), and for the adults of the smaller species of the three triads, mean bandwidth = 1.60 octaves (0.84-1.88 octaves).
We applied the Tukey's multiple-comparisons test to analyze whether the
three categories juveniles, small adults and big adults differ
in their mean octave ranges (Sokal and
Rohlf, 1997). The juveniles differed from the large-adults group
(P<0.05), but neither of these two groups differed significantly
from the small-adults group.
In principle, our finding that the larger animals (individuals or species)
have more sensitive TM responses parallels the findings of Rosowski et al.
(1984,
1988
) in the alligator lizard
and the findings of Huang
(1999
) in the cat family.
We may interpret the size-related variation observed here in the TM
transfer function, in light of the physics of mammalian middle-ear function as
elucidated by Relkin (1988)
and Rosowski (1994
; pp. 217).
In our data obtained for geckos, in accordance with the mammalian model,
increases in body size and ear size are accompanied by at least three changes
in middle-ear function.
First, peak TM velocity increases, perhaps due to decreased damping in TMs
with a larger surface area, accompanied by the increased hydraulic ratio due
to the columellar footplate not growing as much as the TM
(Werner et al., 1998).
Rosowski (1994
) raised the
possibility that a disproportional enlargement of the TM in mammals could lead
to `overmatching', which would result in a reduction in middle-ear sound
transmission efficiency. Nevertheless, the situation in these two animal
classes differs. In mammals there is a general trend for interspecific
uniformity in the hydraulic ratio
(Rosowski 1994
), while in
reptiles (or at least geckos) the norm is interspecific variation, with the
larger species having a higher ratio
(Werner and Igi
,
2002
).
Second, the downward frequency shift in the transfer function velocity peak might arise from increased mass, or perhaps also decreased stiffness, in the conducting structures of the middle-ear system of the larger animals. At the moment, we lack any data to support the latter possibility.
Third, the shape of the transfer function changes. As body size increases,
the function becomes more sharply tuned (i.e. the octave bandwidth is
reduced), as predicted for a system dominated by the effects of mass (fig. 10
in Relkin, 1988). A decrease
in the damping factor of the conducting apparatus could also produce a more
sharply tuned function. Again, data in support of this mechanism remain to be
identified.
These suggestions on the roles of damping, mass and stiffness should not be lumped as an oversimplified holistic explanation of the effects of size. In view of the complexity of the middle ear, they only indicate the types of mechanisms that may contribute to the size-related differences among the TM transfer functions.
Although the characteristics of the TM transfer function did not differ statistically between the juveniles of the large species and the adults of the small species, scrutiny of Figs 5,6,7 indicates a possible qualitative difference. In each of the three triads, the very top of the function appears to be broadest in the juveniles. Because these functions are somewhat irregular in the relevant range, this phenomenon is not readily quantified but it warrants further investigation.
The relevance of these observations to the stimulation of the inner ear will be further discussed elsewhere when reporting on the audiograms derived from the same animals, based on VIIIth-nerve compound action potentials.
Conclusions
In gekkonomorph lizards, the transfer function of the tympanic membrane
velocity, as seen under constant-sound stimulation, varies with animal size as
follows. (i) The maximum velocity response is most strongly correlated with
animal (rostrum-anus) length. (ii) The frequency at which maximum velocity
occurs is most strongly negatively correlated with the pars inferior length.
(iii) The octave bandwidth is most strongly negatively correlated with animal
length.
Among the morphological measurements of the middle ear, the one with which body length is most closely correlated is the extracolumellar anchorage length.
Among the physiological variables, the maximum velocity is strongly and significantly negatively correlated with the frequency at which it occurs.
The dependence of the physiological variables of the tympanic membrane velocity transfer function on animal and ear size, is similar whether the comparison is among age classes within a species, or among adults of species of different size. Thus the age effects are largely due to size effects but the possibility of a separate age effect needs further research.
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Acknowledgments |
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References |
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Bauer, A. M. (1998). Lizards. In Encyclopedia of Reptiles and Amphibians, 2nd edition (ed. H. G. Cogger, and R. G. Zweifel), pp. 126-173. San Diego: Academic Press.
Bigelow, D. C., Swanson, P. H. and Saunders, J. C. (1996). The effect of tympanic membrane perforation size on umbo velocity in the rat. Laryngoscope 106, 71-76.[Medline]
Brown, A. M. (1985). Ultrasound in gecko distress calls (Reptilia: Gekkonidae). Israel J. Zool. 33, 95-101.
Campbell, H. W. (1969). The effect of temperature on the auditory sensitivity of lizards. Physiol. Zool. 42,183 -210.
Cogger, H. G. (1957). Investigations in the gekkonid genus Oedura Gray. Proc. Linn. Soc. NSW 82,167 -179.
Cogger, H. G. (1992). Reptiles and Amphibians of Australia, edition 5. Chatswood, NSW: Reed; Ithaca, NY: Cornell University Press.
Cohen, Y. E., Rubin, D. M. and Saunders, J. C. (1992). Middle ear development. I. Extra-stapedius response in the neonatal chick. Hear. Res. 58, 1-8.[Medline]
Draper, N. R. and Smith, H. (1998). Applied Regression Analysis, 3rd edition. New York: Wiley-Interscience.
Eatock, R. A. and Manley, G. M. (1981). Auditory nerve fibre activity in the tokay gecko. II. Temperature effects on tuning. J. Comp. Physiol. A 142,219 -226.
Frankenberg, E. and Werner, Y. L. (1992). Vocal communication in the Reptilia facts and questions. Acta Zool. Lilloana 41,45 -62.
Huang, G. T. (1999). Measurements of middle-ear acoustic function in intact ears: application to size variation in the cat family. PhD thesis, Department of Electrical Engineering and Computer Science, Massachusetts Institute of Technology, USA.
Johnstone, B. M. and Werner, Y. L. (2001). Hearing in some Australian geckos (Reptilia: Sauria: Gekkonomorpha). Herpetol. Nat. Hist. 8,49 -56.
Köppl, C., Manley, G. A. and Johnstone, B. M. (1990). Peripheral auditory processing in the bobtail lizard Tiliqua rugosa. V. Seasonal effects of anaesthesia. J. Comp. Physiol. A 167,139 -144.
Manley, G. A. (1990). Peripheral Hearing Mechanisms in Reptiles and Birds. Berlin: Springer.
Manley, G. A. (2000). The hearing organ of lizards. In Comparative Hearing: Birds and Reptiles (ed. R. J. Dooling, R. R. Fay and A. N. Popper), pp.139 -196. New York: Springer-Verlag.
Relkin, E. M. (1988). Introduction to the analysis of middle-ear function. In Physiology of the Ear (ed. A. F. Jahn and J. Santos-Sacchi), pp.103 -123. New York: Raven Press.
Rösler, H. (1995). Geckos der Welt, alle Gattungen. Leipzig: Urania.
Rosowski, J. J. (1994). Outer and middle ears. In Comparative Hearing: Mammals (ed. R. Fay and A. N. Popper), pp. 172-247. New York: Springer.
Rosowski, J. J., Peake, W. T. and Lynch, T. J. (1984). Acoustic inputimpedance of the alligator-lizard ear: nonlinear features. Hear. Res. 16,205 -223.[Medline]
Rosowski, J. J., Ketten, D. R. and Peake, W. T. (1988). Allometric correlations of middle-ear structure and function in one species the alligator lizard. Assn Res. Otolaryngol., Abstract.
Saunders, J. C., Duncan, R. K., Doan, D. E. and Werner, Y. L. (2000). The middle ear of reptiles and birds. In Comparative Hearing: Birds and Reptiles (ed. R. J. Dooling, R. R. Fay and A. N. Popper), pp. 13-69. New York: Springer-Verlag.
Sedgwick, C. J. (1986). Chemical immobilization of wildlife. Semin. vet. Med. Surg. (Small Animals) 1, 215-233.
Sokal, R. R. and Rohlf, F. J. (1997). Biometry, 3rd edition. New York: W. H. Freeman and Company.
Storr, G. M., Smith, L. A. and Johnstone, R. E. (1990). Lizards of Western Australia III. Geckos and Pygopods. Perth: Western Australian Museum.
Werner, Y. L. (1971). Some suggestions on the standard expression of measurements. Syst. Zool. 20,249 -252.
Werner, Y. L. (1976). Optimal temperatures for inner-ear performance in gekkonoid lizards. J. Exp. Zool. 195,319 -352.[Medline]
Werner, Y. L. (1983). Temperature effects on cochlear function in reptiles: a personal review incorporating new data. In Hearing and Other Senses: Presentations in Honor of E. G. Wever (ed. R. R. Fay and G. Gourevitch), pp.149 -174. Groton, CT: Amphora Press.
Werner, Y. L. Vocal communication in geckos: new facts and old problems. Proceedings of the Third Asian Herpetological Meeting, Almaty, September 1998. Rus. J. Herp., in press.
Werner, Y. L. and Igi, P. G. (2002).
The middle ear of gekkonoid lizards: interspecific variation of structure in
relation to body size and to auditory sensitivity. Hear.
Res. 167,33
-45.[Medline]
Werner, Y. L., Igi, P. G. and Saunders, J. C.
(2001). Effects of surgery and other experimental factors on the
evaluation of ear function in gekkonomorph lizards. Hear.
Res. 160,22
-30.[Medline]
Werner, Y. L., Montgomery, L. G., Safford, S. D., Igi,
P. G. and Saunders, J. C. (1998). How body size affects
middle-ear structure and function and auditory sensitivity in gekkonoid
lizards. J. Exp. Biol.
201,487
-502.
Wever, E. G. (1974). The lizard ear: Gekkonidae. J. Morphol. 143,121 -165.[Medline]
Wever, E. G. (1978). The Reptile Ear. Princeton, NJ: Princeton University Press.