|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online August 8, 2008
Journal of Experimental Biology 211, 2609-2616 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.019612
Phonotactic selectivity in two cryptic species of gray treefrogs: effects of differences in pulse rate, carrier frequency and playback level
Division of Biological Sciences, University of Missouri, Columbia, MO 6521, USA
e-mail: gerhardth{at}missouri.edu
Accepted 2 June 2008
 |
Summary |
|---|
 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Key words: phonotactic selectivity, tree frogs (Hylidae), pulse rate, carrier frequency, sound pressure level, interactive effects
|
INTRODUCTION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
). The spectral structure (number of spectral peaks and their
frequency and relative amplitudes) may also contribute to signal recognition,
and carrier frequency may provide reliable information about the size of the
signaler (Gerhardt and Huber,
2002). In most experimental studies of intraspecific acoustic
communication, the major spectral features (number of components and their
frequencies) of test stimuli are held constant while the temporal properties
are varied or vice versa. This design reflects two implicit
hypotheses: (1) that any frequency component or band to which the auditory
system is reasonably sensitive may serve as a carrier of information encoded
in the temporal properties of the signal; and (2) that receivers process and
make decisions based on fine-scale temporal properties independently of gross
differences in spectral properties and vice versa. Of course, changes
in the temporal properties of most signals inevitably affect the spectrum by
generating sidebands around the carrier frequency or frequencies. Such
differences are subtle when modulation rates are low as in the present study,
and there is evidence from experiments using amplitude-modulated noise that
such spectral differences are inconsequential (see Discussion)
(Gerhardt, 1978a). In this
study, I explicitly test the null hypothesis that receiver selectivity based
on pulse rate is independent of that based on the number or frequency of the
spectral peaks typical of conspecific calls.
Frogs and toads have served as important model systems for the study of
both evolution and auditory mechanisms because of their strong reliance on
acoustic communication (for reviews, see
Gerhardt and Huber, 2002;
Narins et al., 2006). The
anuran auditory system is specialized at the peripheral level by virtue of
having two inner ear organs with different frequency sensitivities and
physiological properties (for a review, see
Simmons et al., 2006). In
species in which the advertisement call has a bimodal spectrum, the frequency
of the high-frequency spectral peak usually matches the tuning of the basilar
papilla, whereas the frequency of the low-frequency peak usually matches the
tuning of relatively high-frequency-tuned neurons in the amphibian papilla
(for reviews, see Capranica and Moffat,
1983; Gerhardt and Schwartz,
2001).
In this study, I assessed the preferences of two cryptic species of North
American gray treefrogs (Anura: Hylidae). Cope's gray treefrog (H.
chrysoscelis Cope) is a diploid species in which males produce pulsed
advertisement calls with a relatively rapid pulse rate (about 35–70
pulses s–1 uncorrected for temperature). The second species
(H. versicolor Leconte) is a tetraploid species that has had three or
more independent origins (Ptacek et al.,
1994) from hybridization events involving H. chrysoscelis
and other extinct diploid species
(Holloway et al., 2006). The
pulsed advertisement calls of H. versicolor have a slower pulse rate
(about 10–35pulsess–1 uncorrected for temperature) than
the calls of H. chrysoscelis.
Whereas females of H. chrysoscelis base their choices on pulse
rate or, equivalently, on sequences of pulse periods (time between the onset
of two successive pulses), females of H. versicolor assess fine-scale
temporal properties in terms of pulse duration and the silent interval between
pulses (Schul and Bush, 2002).
I emphasize that in the calls of both species
(Gerhardt and Doherty, 1988)
and in the synthetic signals used in this study, pulse duration and the
interpulse interval vary in a dependent fashion with pulse rate so that the
durations of these properties are greater in a signal with a low pulse rate
than in a signal with a high pulse rate
(Fig. 1).
|
). Females of
both species preferred signals with bimodal spectra to signals having just one
of these spectral peaks (Gerhardt,
2005a) but surprisingly chose single-component calls of 1.1 or 1.2
kHz rather than alternatives of 2.2 or 2.4 kHz, respectively, at low playback
levels (65–75 dB). Females either did not show a preference (H.
chrysoscelis from most populations) or preferred the high-frequency
alternatives [H. versicolor; H. chrysoscelis from Minnesota
(M. A. Bee, unpublished data)] at playback levels of 85–90 dB sound
pressure level (SPL) (Gerhardt et al.,
2007). These intensity-dependent changes in preference serve to
emphasize that the auditory system often shows non-linear characteristics and
that female selectivity must therefore be assessed over a wide range of
playback levels.
Although differences in the tuning of the auditory organs suggest a
two-channel system, the situation is more complicated for two reasons: (1)
different kinds of receptors within the amphibian papilla have different
tuning properties and respond differently to two-tone stimulation; and (2)
inputs from the two inner organs already show some degree of convergence in
the very first auditory nucleus in the ascending pathway. Auditory neurons in
the ascending pathway show a bewildering diversity of response properties to
the spectral and fine-scale temporal properties of acoustic signals (e.g.
Walkowiak, 1984; reviewed by
Rose and Gooler, 2006). Thus,
quantitative behavioral experiments, which explore the multi-variate acoustic
space of signals that best elicit responses from the whole animal, are an
important complementary step to understanding how auditory systems recognize
biologically significant signals [see Schmidt et al. for a recent study of
grasshoppers with the same perspective
(Schmidt et al., 2007)].
I show here that phonotactic selectivity based on differences in fine-scale temporal properties may be affected in significant ways by carrier frequency. Such effects were stronger in H. versicolor than in H. chrysoscelis. There were also significant interactions between preferences based on carrier frequency, the direction of the pulse-rate difference relative to that of the standard call, and playback level in H. versicolor but not H. chrysoscelis. Temporal selectivity was generally greater when the temporal information was carried by the low-frequency band than when it was carried by the high-frequency band. I propose that exceptions in H. versicolor may reflect differences in the way that females of this species assess fine-scale temporal patterns.
|
MATERIALS AND METHODS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
; Gerhardt,
2005b). Synthetic calls were made with custom-designed software
(written by J. J. Schwartz, Pace University) that created 8-bit or 16-bit
digital files with an output sampling rate of at least 20 kHz. The temporal
properties of standard synthetic calls were typical of calls produced by
conspecific males calling at about 20°C, which was also the temperature
(±2°C) at which females were tested. The bandwidths of spectral
peaks were narrower than in natural calls because the synthetic calls did not
incorporate the within-pulse frequency modulation typical of these species
(Fig. 1). In tests of H.
versicolor and H. chrysoscelis these standard calls were as
attractive as synthetic calls with frequency-modulated pulses, which, in turn,
were as attractive as typical pre-recorded natural calls
(Gerhardt, 1978b;
Gerhardt, 2005b). For the experiments described in this study, the two standard calls used to test H. chrysoscelis had a pulse rate of 50 pulses s–1 and a 50% pulse-duty cycle. One standard call had a single carrier frequency of 1.2 kHz, and the other a single carrier frequency of 2.4 kHz. Alternatives had one or other of these carrier frequencies and pulse rates of 40, 45, 65 or 75 pulses s–1; pulse duty cycle was always 50% (see examples in Fig. 1). The two standard calls used to test H. versicolor had a pulse rate of 20 pulses s–1 and a 50% duty cycle. One standard call had a single carrier frequency of 1.1 kHz, and the other a single carrier frequency of 2.2 kHz. Alternatives had one or the other of these carrier frequencies and pulse rates of 10, 15, 25, 30, 35 or 40 pulses s–1; pulse duty cycle was always 50% (examples in Fig. 1). In all tests, both the standard and the alternative call had the same carrier frequency and differed in pulse rate. Synthetic calls used to test H. chrysoscelis had 36 pulses, and calls used to test H. versicolor had 18 pulses; pulse number in alternatives was changed so that their call duration was approximately equal to that of the standard call. Call period was 4 s in stimuli presented to both species. The timing relationship of alternatives in any given test was fixed so that there were equal periods of silence between the end of one stimulus and the beginning of the alternative stimulus.
Females of H. versicolor and H. chrysoscelis were tested
in the semi-anechoic chamber described previously
(Gerhardt, 1994). Sounds were
amplified by Nagra DSM amplifiers (Nagra Audio, Lausanne, Switzerland) and
played back from two Analog-Digital-Systems 200 speakers (ADS, Vista, CA,
USA), which were separated by 2 m. Digital files were output from an
IBM-compatible personal computer using software specific to digital-to-analog
interfaces (Siliconsoft DacEditor 12AB, 16-bit; San Jose, CA, USA). Signal
amplitudes were adjusted and equalized at the female release point midway
between the speakers using a General Radio 1990 or Larson-Davis 720 sound
level meter (Provo, UT, USA). Most initial tests were conducted at a playback
level of 85 dB SPL in order to compare the results with those obtained at the
same level using stimuli with bimodal spectra
(Gerhardt, 2005a;
Gerhardt, 2005b). Tests were
also conducted at playback levels of 90, 75 and 65 dB SPL with both species.
Females of H. versicolor were less likely to respond at all at 65 dB
SPL than were females of H. chrysoscelis, so some tests of H.
versicolor were conducted at 69 dB SPL. Tests with sufficient data at
both levels indicated that there was no significant difference in choices at
these two intensities, so the results at these two levels were combined.
Experimental procedure
Female gray treefrogs were collected in amplexus at the localities
specified previously in Missouri, USA
(Gerhardt et al., 2007) and
refrigerated (about 4°C) to delay oviposition. Before testing (usually
within 3days of capture), each female was acclimated to the target test
temperature (20°C) for at least 30min. Each female was placed in a
circular, acoustically transparent (hardware or plastic cloth) cage, which was
located midway between the speakers. After each alternative stimulus had been
played back several times in an alternating fashion, the top of the cage was
removed remotely. Female movements were observed under infra-red illumination
with a closed-circuit video system. A response was tabulated when the female
showed phonotactic orientation behavior
(Rheinlaender et al., 1979)
and moved to within 10cm of one of the speakers. If a female did not begin
phonotaxis within 5min or hopped away from the testing area within the
chamber, the trial was recorded as a `no response'. Most responses occurred
within 3min of the female's release.
Each female provided a single datum for a test of a pair of alternatives at
a given playback level. There was a minimum time-out of 2min for females that
were used in more than one test. Control experiments have demonstrated that
female treefrogs (H. cinerea and H. versicolor) were not
biased for or against a stimulus they heard or responded to in a previous
two-stimulus test (Gerhardt,
1981; Gerhardt et al.,
2000). Although the different alternatives were switched
periodically between speakers within and between two-stimulus testing to
minimize the effects of possible side biases, no such biases were detected
(see also Gerhardt et al.,
2000). Most females were later released at the site of capture or
held in the animal care facilities and used for other studies. Facilities and
experimental procedures were approved by the University of Missouri Animal
Care and Use Committee.
Data analysis
Results are presented as the proportion of females that chose one of the
alternatives (Figs 2,
3,
4). The 95% exact confidence
limits were computed using the F-distribution method employed in SAS
version 9.1 (Statistical Analysis System Institute, Cary, NC, USA). If a
significant proportion chose one of the alternatives (two-tailed binomial,
P<0.05), only one-sided limits are shown. However, because the
sample size was not pre-determined, such significance tests are not strictly
valid, and I interpret the confidence limits as Bayesian credible intervals
whose validity is independent of a stopping rule. Bayesian credible intervals
correspond numerically to confidence limits when the prior distribution is
uniform, which is also the assumption of classical significance tests (see
Gerhardt, 1992, and references
therein). Note that credible intervals are interpreted differently from
confidence limits. The true proportion is assumed to have a 95% probability of
being within the 95% credible limits, whereas if many confidence limits are
computed, then 95% of them are expected to include the mean.
|
|
|
|
RESULTS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Choices for standard calls with the species-typical bimodal spectrum (data
from Gerhardt, 2005b) are
compared with those in tests using single-peaked calls in
Fig. 2; the alternative stimuli
were equalized at 85 dB SPL. In H. chrysoscelis, carrier frequency
had no significant effect on the proportions of females choosing the standard
call of 50 pulses s–1 relative to any of the alternatives
[main effect of frequency: likelihood ratio (LR) chi-square=2.47, d.f.=2,
P=0.29; interaction of frequency and pulse rate: LR chi-square=7.58,
d.f.=6, P=0.27). In H. versicolor, the interaction between
carrier frequency and the pulse rate of the alternative was highly significant
(LR chi-square=19.75, d.f.=7, P=0.006). Post-hoc comparisons
confirmed that a significantly higher proportion of females chose the standard
call of 20 pulses s–1 than the alternative of 30 pulses
s–1 when alternatives had a bimodal spectrum [difference in
least square means (DLSM): chi-square=13.13, d.f.=1, P=0.0003], or a
carrier frequency of 1.1 kHz (DLSM: chi-square=5.24, d.f.=1, P=0.022)
than when the carrier frequency of alternatives was 2.2 kHz. Significantly
higher proportions of females also chose the standard call with the bimodal
carrier frequency (DLSM: chi-square=5.98, d.f.=1, P=0.015) or with
the 2.2 kHz carrier frequency (DLSM: chi-square=4.07, d.f.=1,
P=0.044) than the alternative of 15 pulses s–1 when
it had a carrier frequency of 1.1 kHz
Fig. 3 shows the results of
tests in which pulse rate, carrier frequency and playback level were
systematically varied; pulse rates of alternatives had values (40 and 75
pulses s–1; hereafter referred to, respectively, as the low-
and high-cutoff values) that were less attractive than the standard call when
both alternatives had a bimodal carrier and a playback level of 85 dB
(Gerhardt, 2005b). In H.
chrysoscelis, the full model indicated that the only significant main
effect was carrier frequency (LR chi-square=24.85, d.f.=1,
P<0.0001). The general pattern seen in
Fig. 3A, however, is that
females were more selective for the standard call when the carrier frequency
was 1.2 kHz rather than 2.4 kHz. Although the interaction effects were
non-significant in this analysis and so no formal post-hoc test is
justified, the greatest difference in selectivity occurred in tests against
the alternative of 75 pulses s–1 at low SPLs. When two
additional alternatives (45 and 65pulsess–1) were included,
there were also significant effects of pulse rate and the interaction of pulse
rate and carrier frequency (see Fig.
4A and below).
In H. versicolor, by contrast, there was a significant three-way interaction among the variables [pulse rate (low- and high-cutoff values of 15 and 30 pulses s–1, respectively), carrier frequency and playback level; LR chi-square=10.30, d.f.=3, P=0.016]. The main effects of pulse rate and carrier frequency and their interaction were also statistically significant as was the interaction between frequency and playback level. Post-hoc comparisons indicated that in all except two tests, there was a significant difference in the proportions of females choosing the alternative with the standard pulse rate that depended on carrier frequency (Fig. 3B shows the significance levels in terms of DSLMs). At all four playback levels, significant proportions of females chose the standard call of 20 pulses s–1 rather than the alternative of 30 pulses s–1 when the carrier frequency was 1.1 kHz but not when the carrier frequency was 2.2 kHz. When the alternative had a pulse rate of 15 pulses s–1, significant proportions of females chose the standard call when the carrier frequency was 2.2 kHz at all four playback levels; females showed no preference when the carrier frequency was 1.1 kHz at playback levels of 85 and 90 dB SPL.
Fig. 4A shows the choices of
H. chrysoscelis in additional tests of alternatives with pulse-rate
differences that did not result in preferences for either alternative when
tested with calls with bimodal spectra at a playback level of 85 dB SPL
(Gerhardt, 2005b). There was a
significant effect of pulse rate (LR chi-square=15.28, d.f.=2,
P=0.0005) and of the interaction between pulse rate and carrier
frequency (LR chi-square=8.67, d.f.=1, P=0.003). When these data were
combined with those plotted in Fig.
3A, there were also highly significant effects of pulse rate (LR
chi-square=50.47, d.f.=3, P<0.0001), carrier frequency (LR
chi-square=12.73, d.f.=1, P=0.0004) and the interaction of these two
variables (LR chi-square=20.43, d.f.=3, P=0.0001). Carrier-frequency
effects were significant at pulse rates of 40 pulses s–1
(DLSM chi-square=4.39, d.f.=1, P=0.036), 65pulsess–1
(DLSM chi-square=14.75, d.f.=1, P=0.0001) and 75 pulses
s–1 (DLSM chi-square=6.03, d.f.=1, P=0.014), and
there was a strong trend at 45pulsess–1 (DLSM
chi-square=3.43, d.f.=1, P=0.064). In summary, females were more
likely to choose the standard call when the carrier frequency was 1.2 kHz
rather than 2.4 kHz and the pulse rate of the alternative was higher. The
effect of carrier frequency was weak or absent when the pulse rate of the
alternative was lower.
Fig. 4B shows the choices of H. versicolor in additional tests of alternatives with different pulse rates at all four playback levels. Because not all pulse-rate alternatives were tested with both carrier frequencies, the data were not analyzed with the Genmod procedure. There were no statistically significant effects of playback level for any of the four sets of tests (P-values of log-likelihood estimates of 2x4 tables were all >0.1). These results reinforce the fact that females showed poor selectivity over a wide range of playback levels when the carrier frequency was 2.2 kHz and alternatives had pulse rates even higher than 30 pulses s–1. Only when the pulse rate of the alternative was increased to 40 pulses s–1 did significant proportions of females choose the standard call, and this choice was far from unanimous. By contrast, even though most females did not choose the standard call of 20 pulses s–1 with a carrier frequency of 1.1 kHz in preference to an alternative with the same carrier frequency and a pulse rate of 15 pulses s–1 at playback levels of 90 and 85 dB SPL, significantly higher proportions of females chose the standard call at all four playback levels when the pulse rate of the alternative was reduced to 10 pulses s–1.
|
DISCUSSION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
)]. First, although any change in a temporal
property also affects the spectrum of nearly all signals, an exception is the
long-term spectrum of broadband noise, which is independent of amplitude
modulation (Rice, 1955). I
exploited this characteristic of noise to show that in another species of
North American treefrog (H. cinerea), females discriminated between
unmodulated and pulsed (50 pulses s–1) signals (noise bursts)
based on the difference in the amplitude–time waveform alone
(Gerhardt, 1978a).
Amplitude-modulated noise has often been used for the same purpose in
neurophysiological studies of temporal-pattern selectivity in anurans and
other animals (e.g. Rose and Capranica,
1985). Second, many auditory neurons in both the low- and
high-frequency channels of the anuran auditory system show reliable temporal
encoding (phase locking to each pulse in a train of pulses) pulse rates higher
than those of any stimulus used in these experiments (Rose and Gooler,
2007).
Temporal selectivity was usually greater when the carrier frequency of both
alternatives was low (1.1 or 1.2 kHz) rather than high (2.2 or 2.4 kHz).
Effects were much less pronounced in H. chrysoscelis, in which
selectivity was comparable to that occurring in experiments in which both
spectral peaks were present (at least as 85 dB SPL;
Gerhardt, 2005b), than in
H. versicolor. In the latter species there were significant
interactions among carrier frequency, the direction of the pulse-rate
difference vis-à-vis that of the standard call, and playback
level.
At 85 dB SPL, which corresponds to a distance of 1–2 m from a typical
calling male and to the playback level that has been most commonly used in
studies of these species, females of H. chrysoscelis showed the same
selectivity for pulse-rate differences regardless of whether the carrier
frequency was 1.2 kHz, 2.4 kHz or the usual bimodal spectrum
(Fig. 2A). Generalizing these
results by varying the playback level, however, indicated that temporal
selectivity was sometimes weaker or absent at lower playback levels when the
2.4 kHz carrier was used (Figs
3 and
4). By contrast, when the
carrier frequency of both alternatives was 1.2 kHz, more than 80% of the
females chose the standard call of 50 pulses s–1 over
alternatives with pulse rates of 40 and 75 pulses s–1 at all
four playback levels (Fig. 3A).
Females even preferred the standard call to an alternative of 65 pulses
s–1 [a value less than the high-cutoff value in tests with
the bimodal carrier (Gerhardt,
2005b)] at playback levels of 90 and 75 dB SPL
(Fig. 4A).
In H. versicolor, striking and complex effects of carrier
frequency on the temporal preferences of females were already evident in the
initial tests at 85 dB SPL (Fig.
2B). Females failed to discriminate against an alternative of 30
pulses s–1 when the carrier frequency was 2.2 kHz. This
result is surprising because this is the dominant frequency band in their
advertisement call, and females preferred an alternative with a 2.2 kHz
carrier frequency to an alternative with a carrier frequency of 1.1 kHz at 85
dB SPL when both alternatives had the standard pulse rate of 20 pulses
s–1 (Gerhardt,
2005a). Furthermore, the alternative pulse rate of 30 pulses
s–1 falls within the range of variation of H.
chrysoscelis, a genetically incompatible species that often breeds at the
same time and place. The absence of a preference for the standard call was
also observed at the three other playback levels
(Fig. 3B), and other tests
showed that discrimination against alternatives of 35 and 40 pulses
s–1 was also weak or absent when the carrier frequency was
2.2 kHz (Fig. 4B).
A second unexpected result seemingly runs counter to the previous indication that selectivity was generally high when the low-frequency carrier was used. That is, there was no preference for the standard call when the carrier frequency was 1.1 kHz and the alternative had a pulse rate of 15 pulses s–1 at 85 and 90 dB SPL (Fig. 2B, Fig. 3B). Strong preferences for the standard call did occur, however, at playback levels of 65 and 75 dB SPL in the same test, and females chose the standard call at all playback levels when the pulse rate was decreased to 10 pulses s–1 (Fig. 4B).
Interpretation and hypotheses
The general superiority of the low-frequency peak in mediating phonotactic
selectivity based on fine-scale temporal properties was anticipated by a
previous study of pulse-shape selectivity in H. versicolor
(Gerhardt and Schul, 1999).
When pulse rate was held constant at 20 pulses s–1 (25 ms
pulse duration and 25 ms interpulse interval, as in the standard call used in
the present study), females discriminated between calls with a rise-time
difference of 5ms when the carrier frequency was either 1.1 or 2.2 kHz at a
playback level of 85 dB SPL. However, when the playback level was lowered to
75 dB SPL, females discriminated only when the low-frequency carrier was used.
Gerhardt and Schul hypothesized that pulse rise-time selectivity is
accomplished by the low-frequency channel and that preferences observed at 85
dB SPL with the 2.2 kHz carrier frequency occurred because of cross-talk
(Gerhardt and Schul, 1999).
That is, at such high levels, substantial numbers of receptors and auditory
neurons in the low-frequency channel would also be excited. The same kind of
argument may explain patterns of intensity-dependent selectivity of females of
H. chrysoscelis in tests of alternatives with higher pulse rates than
that of the standard call. Alternatively, neurons in the high-frequency
channel may be generally less sensitive than those in the low-frequency
channel and hence require higher stimulus levels in order to resolve
fine-scale time differences. The underlying mechanism could reflect, in part,
the better phase-locking ability of auditory nerve fibers innervating the
amphibian papilla (low-frequency-tuned inner ear organ) than auditory nerve
fibers innervating the basilar papilla (high-frequency-tuned inner ear organ)
(Dunia and Narins, 1989;
Simmons et al., 1993),
although even high-frequency-tuned fibers should still be able to phase-lock
reliably to pulses repeated at rates of 75 pulses s–1 or
less.
An explanation based on frequency-dependent phase locking and cross-talk
between the two inner ear organs is, however, inadequate to explain the
pattern of selectivity shown by females of H. versicolor. First, when
the high-frequency carrier was used there was no improvement in selectivity in
tests of alternatives of higher-than-standard pulse rates when the playback
level was increased to 85 and 90 dB SPL. Second, females did not prefer the
standard call when the carrier frequency was 1.1 kHz and the alternative was
15 pulses s–1 at playback levels of 90 and 85 dB SPL. I now
re-emphasize that because pulse duty-cycle (the ratio of pulse duration to
pulse period) was held constant (the natural pattern in the calls of both
species) in the present study, the absolute values of pulse duration and pulse
interval were longer in synthetic calls with pulse rates lower than the
standard pulse rate; the values of these properties were shorter in synthetic
calls with pulse rates higher than the standard (see
Fig. 1). It follows that the
absolute values of pulse duration and intervals were longer in the majority of
stimuli presented to H. versicolor than those presented to H.
chrysoscelis. Another variable that differed between species was the
shape and rise-time of the pulses, which affects the selectivity of females of
H. versicolor (Diekamp and
Gerhardt, 1995; Gerhardt and
Schul, 1999). Females of H. chrysoscelis were unselective
with regard to pulse shape differences over the normal range of
conspecific-call variation in pulse duration.
My speculative explanation for the puzzling results in H.
versicolor is based on the acoustic differences just discussed, species
differences in the acoustic criteria whereby females evaluate pulsed calls,
and on recent studies of how different classes of temporally selective neurons
respond to different kinds of pulsed signals. Females of H.
chrysoscelis use pulse rate (largely independent of pulse duty cycle) as
the main criterion for fine-scale temporal discrimination
(Schul and Bush, 2002). Female
selectivity is well correlated with the response properties of a class of
auditory neurons found in the anuran torus semicircularis (midbrain) that show
sharp band-pass selectivity for relatively fast rates of amplitude modulation
(Rose and Gooler, 2006). These
integration-type neurons require some minimum number of correct interpulse
intervals, do not synchronize to the pulses within a stimulus, and are
relatively unaffected by duty cycle (pulse duration) (Adler and Rose,
2000).
Females of H. versicolor require a minimum pulse duration and
tolerate some maximum silent interval between pulses
(Schul and Bush, 2002). In
other words, their temporal selectivity is not based on pulse rate per
se. Thus, fine-scale pattern recognition in H. versicolor might
be limited at least in part by how well primary auditory neurons and
temporally selective neurons in the ascending pathway encode pulse duration
rather than by how well phasic neurons synchronize to each pulse (for a
review, see Rose and Gooler,
2006). Indeed, a subset of about 20% of neurons in the torus
semicircularis of three anuran species show selectivity for pulse duration
(for a review, see Rose and Gooler,
2006). More recently another class of duration-selective neurons
have been found to respond only when pulses exceed some minimum duration or
when some minimum number of shorter pulses are rapidly repeated
(Leary et al., 2008). Such
`long-pass' neurons, therefore, show integrating (interval-counting)
properties (Edwards et al.,
2005) and could also play a role over some ranges of pulse
duration and rise-time. Whatever the mechanism, it must explain the poor and
intensity-independent selectivity observed when the high-frequency carrier was
used and the alternatives had a higher pulse rate, and the even more
problematic, intensity-dependent selectivity observed when the low-frequency
carrier was used and the alternatives had a pulse rate of 15 pulses
s–1. Long-interval-selective neurons may be involved in the
latter phenomenon. At SPLs substantially above threshold, the dominance of
inhibition can decrease the response levels of temporally selective neurons
(G. J. Rose, personal communication). Thus, the decreased behavioral
selectivity at high amplitudes and low carrier frequency might have resulted
from an inhibition-related attenuation of responses to the 20 pulses
s–1 (standard) stimulus, which was more attractive at lower
SPLs.
General mechanisms of temporal selectivity and future directions
One emerging perspective is that a wide variety of mechanisms that underlie
temporal selectivity probably depend on within-cell interactions between
inhibition and excitation rather than, or in addition to, convergence of the
outputs of lower-order neurons with various filtering processes (e.g.
Casseday et al., 2000;
Edwards et al., 2007;
Bush and Schul, 2005).
Moreover, neural modeling suggests that, in general, single neurons can be
expected to respond in fundamentally different ways to pulse trains with
different values of pulse duration and intervals (e.g.
Izhikevich, 2001).
Given the diversity of potential auditory mechanisms, it is perhaps not
surprising that a species like H. versicolor shows such complex
patterns of frequency- and intensity-dependent preferences. Not only do
females have to deal with a wide range of pulse rates
(9–32pulsess–1) and pulse durations (15–55ms)
found in conspecific calls over the normal range of breeding temperatures
(Gayou, 1984), but also the
longer absolute durations of pulses are likely to engage auditory neurons that
selectively respond to relatively long pulses. The closely related bird-voiced
treefrog (Hyla avivoca Viosca) produces calls with pulses and
interpulse intervals that are even longer than those in the calls of H.
versicolor. The results of preliminary behavioral tests indicate that
females of H. avivoca also assess pulse duration and intervals rather
than pulse rate per se (C. C. Martínez-Rivera and H. C.
Gerhardt, unpublished data). Moreover, unlike the gray treefrogs the
advertisement call of this species has a single spectral peak of relatively
high frequency (Gerhardt,
2001). Could it be that a shift from low-frequency- or
high-frequency-mediated, pulse-rate discrimination (as shown by H.
chrysoscelis) to primarily high-frequency-mediated, pulse-duration
discrimination occurs in species that must correctly identify signals with
relatively long pulses, which also allow for the discrimination of pulse
shape? The pulse-duration dependence of discrimination of pulse shape by
females of H. chrysoscelis also supports this concept. Females did
not prefer pulses with the conspecific pulse shape unless pulse duration was
increased to values greater than those produced by conspecific males so that
rise-time differences became comparable to those discriminated by females of
H. versicolor (Gerhardt,
2005b). As pointed out by Adler and Rose, neurons with the
potential for dealing with a variety of pulse durations, pulse forms and rates
probably occur in most species (Adler and Rose, 2000), and other models, such
as those involving resonance mechanisms, indicate that dramatic differences in
response properties can be achieved by small changes in membrane potential
(Bush and Schul, 2005).
In any event, the results of the present study suggest that the carrier
frequency of the temporal information is another factor that should be
considered in studies of the neural mechanisms of fine-scale temporal
selectivity. For example, are there any biases in the frequency tuning of
recovery-type, integrative-type and duration-selective cells in the frog torus
semicircularis that might also depend on the pulse rates (interpulse
intervals) to which they are most selective? Finally, changes in intensity had
non-linear effects on frequency preferences in the two species of gray
treefrogs (Gerhardt et al.,
2007), and so it is hardly surprising that many of the choices
demonstrated in this paper were also intensity dependent. Another task for
behavioral biologists is to generalize their results over a reasonably wide
range of sound intensities because only by doing so can we provide a set of
useful specifications for studies of auditory mechanisms as well as gaining
insights about how these animals recognize biologically important sounds at
different distances in their natural environment.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Alder, T. B. and Rose, G. J. (2000). Integration and recovery processes contribute to the temporal selectivity of neurons in the midbrain of the northern leopard frog, Rana pipiens.J. Comp. Physiol. A 186,923 -937.[CrossRef][Medline]
Bradbury, J. W. and Vehrencamp, S. L. (1998). Principles of Animal Communication. Sunderland, MA: Sinauer Associates.
Bush, S. L. and Schul, J. (2005). Pulse-rate recognition in an insect: evidence for a role of oscillatory neurons. J. Comp. Physiol. A 192,113 -121.[Medline]
Capranica, R. R. and Moffat, A. J. M. (1983). Neurobehavioral correlates of sound communication in anurans. In Advances in Vertebrate Neuroethology (ed. J. P. Ewert, R. R. Capranica and D. J. Ingle), pp. 701-730. New York: Plenum Press.
Casseday, J. H., Ehrlich, D. and Covey, E.
(2000). Neural measurements of sound duration: control by
excitatory-inhibitory interactions in the inferior colliculus. J.
Neurophysiol. 84,1475
-1487.
Diekamp, B. M. and Gerhardt, H. C. (1995). Selective phonotaxis to advertisement calls in the gray treefrog, Hyla versicolor: Behavioral experiments and neurophysiological correlates. J. Comp. Physiol. A 177,173 -190.[Medline]
Dunia, R. and Narins, P. M. (1989). Temporal resolution in frog auditory-nerve fibers. J. Acoust. Soc. Am. 85,1630 -1638.[CrossRef][Medline]
Edwards, C. J., Alder, T. B. and Rose, G. J.
(2005). Pulse rise time but not duty cycle affects the temporal
selectivity of neurons in the anuran midbrain that prefer slow AM rates.
J. Neurophysiol. 93,1336
-1341.
Edwards, C. J., Leary, C. J. and Rose, G. J.
(2007). Counting on inhibition and rate-dependent excitation in
the auditory system. J. Neurosci.
27,13384
-13392.
Gayou, D. C. (1984). Effects of temperature on the mating call of Hyla versicolor. Copeia 1984,733 -738.[CrossRef]
Gerhardt, H. C. (1978a). Mating call
recognition in the green treefrog (Hyla cinerea): significance of
some fine-temporal properties. J. Exp. Biol.
74, 59-73.
Gerhardt, H. C. (1978b). Temperature coupling
in the vocal communication system of the gray treefrog Hyla versicolor.Science 199,992
-994.
Gerhardt, H. C. (1981). Mating call recognition in the green treefrog (Hyla cinerea): importance of two frequency bands as a function of sound pressure level. J. Comp. Physiol. A 144,9 -16.[CrossRef]
Gerhardt, H. C. (1992). Conducting playback experiments and interpreting their results. In Playback and Studies of Animal Communication: Problems and Prospects (ed. P. MacGregor), pp. 59-77. New York: Plenum Press.
Gerhardt, H. C. (1994). Reproductive character displacement of female mate choice in the grey treefrog H. chrysoscelis.Anim. Behav. 47,959 -969.[CrossRef]
Gerhardt, H. C. (2001). Acoustic communication in two groups of closely related treefrogs. In Advances in the Study of Behavior (ed. P. J. B. Slater, J. S. Rosenblatt, C. T. Snowdon and T. J. Roper), pp. 99-167. New York: Academic Press.
Gerhardt, H. C. (2005a). Acoustic spectral preferences in two cryptic species of grey treefrogs: implications for mate choice and sensory mechanisms. Anim. Behav. 70, 39-49.[CrossRef]
Gerhardt, H. C. (2005b). Advertisement-call preferences in diploid-tetraploid treefrogs (Hyla chrysoscelis and Hyla versicolor): implications for mate choice and the evolution of communication systems. Evolution 59,395 -408.[CrossRef][Medline]
Gerhardt, H. C. and Doherty, J. A. (1988). Acoustic communication in the gray treefrog, Hyla versicolor: evolutionary and neurobiological implications. J. Comp. Physiol. A 162,261 -278.[CrossRef]
Gerhardt, H. C. and Huber, F. (2002). Acoustic Communication in Insects and Frogs: Common Problems and Diverse Solutions. Chicago: University of Chicago Press.
Gerhardt, H. C. and Schul, J. (1999). A quantitative analysis of behavioral selectivity for pulse-rise time in the gray treefrog, Hyla versicolor. J. Comp. Physiol. A 185, 33-40.[CrossRef][Medline]
Gerhardt, H. C. and Schwartz, J. J. (2001). Auditory tuning and frequency preferences in Anurans. In Anuran Communication (ed. M. J. Ryan), pp.73 -85. Washington: Smithsonian Institution Press.
Gerhardt, H. C., Tanner, S. D., Corrigan, C. M. and Walton, H.
C. (2000). Female preference functions based on call duration
in the gray treefrog (Hyla versicolor). Behav.
Ecol. 11,663
-669.
Gerhardt, H. C., Martínez-Rivera, C. C., Schwartz, J. J.,
Marshall, V. T. and Murphy, C. G. (2007). Preferences based
on spectral differences in acoustic signals in four species of treefrogs
(Anura: Hylidae). J. Exp. Biol.
210,2990
-2998.
Holloway, A. K., Cannatella, D. C., Gerhardt, H. C. and Hillis, D. M. (2006). Polyploids with different origins and ancestors form a single polyploidy species. Am. Nat. 167,E88 -E101.[CrossRef][Medline]
Izhikevich, E. M. (2001). Resonate-and-fire neurons. Neural Netw. 14,883 -894.[CrossRef][Medline]
Leary, C. J., Edwards, C. J. and Rose, G. J.
(2008). Midbrain auditory neurons integrate excitation and
inhibition to generate duration selectivity: an, in vivo, whole-cell patch
study in anurans. J. Neurosci.
28,5481
-5493.
Narins, P. M., Feng, A. S., Fay, R. R. and Popper, A. N. (2006). Hearing and Sound Communication in Amphibians. New York: Springer Science+Business Media.
Ptacek, M. B., Gerhardt, H. C. and Sage, R. D. (1994). Speciation by polyploidy in treefrogs: multiple origins of the tetraploid, Hyla versicolor. Evolution 48,898 -908.[CrossRef]
Rheinlaender, J., Gerhardt, H. C., Yager, D. and Capranica, R. R. (1979). Accuracy of phonotaxis in the green treefrog (Hyla cinerea). J. Comp. Physiol. 133,247 -255.[CrossRef]
Rice, E. O. (1955). Mathematical analysis of random noise. In Selected Papers on Noise and Stochastic Processes (ed. N. Was). New York: Dover Press.
Rose, G. J. and Capranica, R. R. (1985).
Sensitivity to amplitude modulated sounds in the anuran auditory system.
J. Neurophysiol. 53,446
-465.
Rose, G. J. and Gooler, D. M. (2006). Function of the amphibian central auditory system. In Hearing and Sound Communication in Amphibians (ed. P. M. Narins, A. S. Feng, R. R. Fay and A. N. Popper), pp. 250-290. New York: Springer Science+Business Media.
Schmidt, A., Ronacher, B. and Hennig, R. M. (2007). The role of frequency, phase and time for processing of amplitude modulated signals by grasshoppers. J. Comp. Physiol. A 194,221 -233.[Medline]
Schul, J. and Bush, S. L. (2002). Non-parallel coevolution of sender and receiver in the acoustic communication system of treefrogs. Proc. R. Soc. Lond., B, Biol. Sci. 269,1847 -1852.[Medline]
Simmons, A. M., Reese, G. and Ferragamo, M. (1993). Periodicity extraction in the anuran auditory nerve. II: Phase and temporal fine structure. J. Acoust. Soc. Am. 93,3374 -3389.[CrossRef][Medline]
Simmons, D. D., Meenerink, W. F. and Vassilakis, P. N. (2006). Anatomy, physiology, and function of auditory end-organs in the frog inner ear. In Hearing and Sound Communication in Amphibians (ed. P. M. Narins, A. S. Feng, R. R. Fay and A. N. Popper), pp. 184-220. New York: Springer Science+Business Media.
Walkowiak, W. (1984). Neuronal correlates of the recognition of pulsed sound signals in the grass frog. J. Comp. Physiol. A 155,57 -66.[CrossRef]
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
Related articles in JEB:
This article has been cited by other articles:
|
|
 |
|
  K. Phillips FEMALE FROGS PREFER DEEP CROAKS J. Exp. Biol., August 15, 2008; 211(16): iii - iii. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
