Behavioral Ecology Vol. 13 No. 3: 375-380
© 2002 International Society for Behavioral Ecology
Female greater wax moths reduce sexual display behavior in relation to the potential risk of predation by echolocating bats
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
Address correspondence to G. Jones. E-mail: gareth.jones{at}bris.ac.uk .
Received 9 February 2001; revised 16 July 2001; accepted 30 July 2001.
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ABSTRACT |
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Female greater wax moths Galleria mellonella display by wing fanning in response to bursts of ultrasonic calls produced by males. The temporal and spectral characteristics of these calls show some similarities with the echolocation calls of bats that emit frequency-modulated (FM) signals. Female G. mellonella therefore need to distinguish between the attractive signals of male conspecifics, which may lead to mating opportunities, and similar sounds made by predatory bats. We therefore predicted that (1) females would display in response to playbacks of male calls; (2) females would not display in response to playbacks of the calls of echolocating bats (we used the calls of Daubenton's bat Myotis daubentonii as representative of a typical FM echolocating bat); and (3) when presented with male calls and bat calls during the same time block, females would display more when perceived predation risk was lower. We manipulated predation risk in two ways. First, we varied the intensity of bat calls to represent a nearby (high risk) or distant (low risk) bat. Second, we played back calls of bats searching for prey (low risk) and attacking prey (high risk). All predictions were supported, suggesting that female G. mellonella are able to distinguish conspecific male mating calls from bat calls, and that they modify display rate in relation to predation risk. The mechanism (s) by which the moths separate the calls of bat and moth must involve temporal cues. Bat and moth signals differ considerably in duration, and differences in duration could be encoded by the moth's nervous system and used in discrimination.
Key words: bats, echolocation, mating behavior, moths, predation risk, ultrasound.
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INTRODUCTION |
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Animals may reduce courtship behavior under conditions of high predation risk, thus trading off investment in reproduction relative to the threat of predation (Magnhagen, 1991
).
Even animals with simple nervous systems need to distinguish between
opportunities for mating and threats from predators. Moths have simple ears
with one to four sensory neurons that show similar frequency responses at
different thresholds. Moth ears function mainly as bat detectors
(Fullard, 1998), though some
species also use ultrasound in intra-specific communication
(Conner, 1999). Moth species
that use ultrasound in courtship must therefore detect predators and listen
for mates. Correct identification of the signaler is crucial for the moth's
reproductive success and survival.
Distinguishing between the sounds of conspecifics and predators is clearly
important in the evolution of audition
(Faure and Hoy, 2000) and will
present the greatest challenges when conspecifics and predators produce
similar sounds. In the greater wax moth Galleria mellonella,
distinctions between mates and predators are potentially difficult to make.
Male G. mellonella attract females by releasing pheromones and by
producing short phrases of ultrasound
(Spangler, 1985). The
ultrasonic signals are brief (100-500 µs) with peak energy between 80 and
100 kHz, and they are emitted in approximately 0.5-s bursts at a repetition
rate of about 40 Hz by flexure of tymbal organs (Spangler,
1985,
1986,
1987). The pulses are produced
when a forewing strikes a tegular wing-coupler. Each wingbeat causes a tymbal
to buckle in and snap out, so two pulses are produced per wingbeat. If tymbal
buckling by both wingbeats is in phase, two pulses are produced per wingbeat
cycle. If buckling is out of phase, up to four pulses may be produced in a
pulse train. Trains produced by successive wingbeats form a phrase, and there
are on average four trains per phrase. Temporal characteristics of moth calls
are defined in Figure 1a. Male
calls promote wing fanning by females, which in turn elicits pheromone
production by males, finally leading to approach by the females prior to
copulation (Spangler, 1985,
1987).
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Greater wax moths are tympanate pyralid moths, with four sensory cells that
have similar frequency responses with different thresholds
(Skals and Surlykke, 2000).
The moths show low thresholds to frequencies between 30 and 120 kHz, with
greatest sensitivity at 60 kHz (Skals and
Surlykke, 2000). The best threshold may not be the same as the
frequency of most energy in the male's call (75 kHz:
Spangler, 1986; 86 kHz: this
study) because the moths must listen also for the echolocation calls of bats,
which often contain lower frequencies
(Fenton et al., 1998). Hearing
in G. mellonella may therefore represent a compromise between
predator and mate detection. The ultrasonic signals of males that elicit wing
fanning in females have some spectral and temporal similarities with the
echolocation calls of many bat species. Many species of bats that emit
frequency-modulated (FM) signals call at frequencies that are highly audible
to G. mellonella. We studied Daubenton's bat Myotis
daubentonii, which in the laboratory calls between 90 and 30 kHz,
sometimes with a pulse repetition rate similar to that of male G.
mellonella. The calls of M. daubentonii are typical of small
Myotis bats in being broadband and of short duration. Many bats that
use similar calls (e.g., M. evotis:
Faure and Barclay, 1994; M.
septentrionalis: Faure et al.,
1993) hunt by gleaning, and so may represent a real threat to
displaying moths, which they could detect by listening for sounds made by
their movement. G. mellonella often displays on the outside of
beehives (Spangler, 1988a),
where it would be at risk from predation by gleaning bats.
Nonflying moths cease movement when subjected to artificial ultrasonic
pulses (Werner, 1989). Many
gleaning bats are sensitive to the sounds made by moving prey
(Bell, 1982;
Coles et al., 1989;
Fuzessery et al., 1993), and
cessation of wing fanning in response to the threat of bat predation is
adaptive. Can the relatively simple nervous system of G. mellonella
distinguish the calls of a potential mate from those of a potential predator,
allowing the moth to behave accordingly?
Given that the calls of echolocating bats should select for cessation of
wing fanning, and calls of male conspecifics should select for wing fanning
(to induce pheromone production), we related the extent of wing fanning in
female G. mellonella to the potential level of threat from
echolocating bats. We first predicted that female G. mellonella will
wing fan in response to playbacks of male calls (as previously shown for
synthetic pulsed ultrasound by Spangler,
1988b), but will not wing fan in response to bat echolocation
calls. We then predict that females will invest more in wing fanning when
predation risk from echolocating bats is lower. We elicited wing fanning in
female moths by playbacks of male calls, and simultaneously varied predation
risk by manipulating the intensity of bat calls to mimic a near and distant
bat and by playing back calls of bats that were searching for prey (lower
risk) and attacking prey (higher risk).
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METHODS |
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Animal husbandry
Three male M. daubentonii were kept under license from English Nature in a 3 x 3 x 2.2 m room under a 14 h light: 10 h dark photoperiod. The bats were allowed free flight in the room. Water was available at all times, and the bats were fed daily with mealworms dusted with multivitamin powder. Bats were released at the site of capture within 3 weeks of capture. Moths were reared in 800-ml glass jars at 28-31°C and 65% relative humidity under a 16 h light: 8 h dark photoperiod. Larvae were fed on a mixture of 300 ml clear honey and 400 ml glycerol, mixed with 200 ml milk powder, 200 g whole-meal coarse flour, 100 g dried brewer's yeast, 100 g wheatgerm, and 400 g bran (recipe from D. A. Waters). Pupae were removed in small groups and placed in 50-ml vials to reduce numbers emerging in a container on any day. If moths of two sexes emerged in a vial in one day, the moths were discarded, as we required virgin moths for experimentation.
Recording bats
We recorded search phase and feeding buzz (i.e., terminal phase;
Griffin et al., 1960)
echolocation calls from three M. daubentonii flying in a 3 x 3
x 2 m room. Search-phase calls are emitted by bats during orientation
and while searching for prey; feeding buzzes involve increases in pulse
repetition rate and decreases in interpulse interval and pulse duration
immediately before prey capture. Recordings were made with a QMC S200 bat
detector (QMC Instruments, London; frequency response ± 3 dB, 20-120
kHz) linked to a Portable Ultrasound Processor (PUSP; Ultra Sound Advice
[USA], London) which time-expanded 2 s of sound 10X at a sampling rate of 448
kHz. Recordings were downloaded onto metal tapes in a Sony WM D6C Professional
Walkman cassette recorder (Sony Corporation, Tokyo). Search-phase calls were
recorded as the bats flew around the room. Feeding buzz calls were recorded by
placing the microphone 10 cm behind a tethered mealworm, which was attacked by
the bats. We obtained 20 search phase and feeding buzz sequences spread evenly
over the three bats (7, 7, and 6 from each bat respectively), and used a
different sequence for each playback. We were unable to record 20 bats because
of licensing restrictions. No sequences contained overloaded signals, and
echoes and interference were minimal.
Recording moths
We placed male moths in a 5 x 7 x 21 cm foam chamber with three
mated female moths. Mated females were used because they are less receptive to
male courtship than are virgins, and so male signaling is rarely interrupted
by copulation. We recorded signals from 20 virgin male moths placed
individually 2.5 cm from the microphone of the S200 bat detector and used the
same equipment described for recording bat calls. All recordings and playback
experiments were performed under illumination from two 40-W red incandescent
lamps, which facilitated observations while keeping light levels minimal.
Sound analysis
We analyzed time-expanded sounds using BatSound v2.1 (Pettersson Elektronik
AB, Uppsala, Sweden) on a personal computer with 16-bit A:D and D:A converters
at a sampling rate of 44.1 kHz. We set the threshold level at 16 in BatSound
and used an FFT size of 512 points. We measured maximum frequency and minimum
frequency of the fundamental harmonic of the call from spectrograms, and
frequency of most energy from a power spectrum. Pulse duration and interpulse
interval were measured from waveform displays.
Preparation of playback signals
Calls were manipulated in MATLAB (version 5.3.1, Mathworks, Natick,
Massachusetts). We applied a bandpass filter so that sound below 20 kHz and
above 150 kHz was largely removed. We manipulated the amplitudes of all
sequences so that the signal of maximal amplitude was of equal magnitude
across sequences. This allowed us to use a fixed gain level on the ultrasound
amplifier to standardize the intensity of playbacks. Five-second sequences of
time-expanded ultrasound were repeated by cutting and pasting in BatSound to
produce sequences 20 s long. These 20-s sequences were then recompressed by
the PUSP in playbacks to produce 2-s sequences of ultrasound. Waveforms and
sonagrams of representative playback sequences are shown in
Figure 1. The number of pulse
trains in each moth call phrase varied between 1-13
(Spangler, 1985, found 1-18).
We used the phrase containing the most pulse trains from each moth in our
playback, selected the phrase and the following interphrase interval, and
repeated it to produce 20 s of time-expanded recordings. Playback sequences
were downloaded from computer onto metal cassette tapes. Control sound
sequences consisted of time-expanded background sound from the rooms in which
recordings were made.
Playback experiments
We measured amplitude levels of playbacks using a Larson Davis 2520
0.25-inch microphone (with protective grid off) and preamplifier (Larson
Davis, Provo, Utah) attached to a Gould 500 Digital Storage Oscilloscope
(Gould Instrument Systems, Valley View, Ohio). As some of the sound sequences
that we used were of very short duration, we used root mean square (RMS)
voltage values in our measurements. Initial calibration was performed by using
an acoustic calibrator (D-1411E, R. S. Components Ltd., Corby, UK). To avoid
nearfield distortion of moth calls, we broadcast calls at 90.3 dB SPL at 40 cm
from the test subjects, so that calls would reach the subject at 72.3 dB SPL
at 5 cm, the peak signal intensity measured by Spangler
(1985).
Playbacks of bat echolocation calls were made at 90 dB SPL and 76 dB SPL at
a moth's ear. Rydell et al.
(1999) measured call intensity
of free-living M. daubentonii as 108 dB SPL at 10 cm, so our playback
levels would represent a bat 80 cm away (high predation risk) and 320 cm
distant (low predation risk). These playback levels are of greater amplitude
than the thresholds that elicit neural responses and flight-stop behavior in
G. mellonella (Skals and
Surlykke, 2000), although the audiograms in that study were
obtained from responses to 50-ms pure tones. The playback intensities used
would mimic a gleaning bat species (which use lower call intensities) at
closer range. For example, the gleaning bat Plecotus auritus calls at
89-97 dB peSPL at 10 cm in free-flight in the laboratory
(Waters and Jones, 1995), so a
gleaning bat might be 15 cm and 80 cm distant in our high- and low-intensity
simulations. Playbacks were made through two USA USL5 loudspeakers (frequency
response ± 4 dB, 20-120 kHz), powered by USA S55 amplifiers.
Time-expanded sequences of calls were replayed from tape, and recompressed by
either the PUSP or by a USA S-350 ultrasound processor.
We placed 1-day-old virgin female moths in a 15-cm3 gauze arena,
and experiments were conducted within the first 2 h of darkness, when moths
are most active (Spangler,
1986). Females were placed in test cages 1 h before experiments so
they could habituate to their new surroundings. Five males were shaken in
individual containers and placed in the test cage 1 min before playbacks, so
that they would release pheromones to excite females. Experiments were
conducted in a 1.2 x 2.3 x 2.4 m room lined with sound-absorbing
foam. Each moth was subject to eight playback sequences in a repeated-measures
design, and treatment order was randomized. In five treatments male moth (MM)
signals were broadcast from one speaker. The other speaker broadcast either
control sound (control & MM), high-intensity feeding buzzes (HIFB &
MM), low-intensity feeding buzzes (LIFB & MM), high-intensity search-phase
calls (HISP & MM), or low-intensity search-phase calls (LISP & MM).
These experiments allowed us to obtain a background measure of female display
rate in relation to male calling (first treatment) and then to measure how
display rate was modified in relation to different levels of perceived
predation risk. Further treatments consisted of control sound from one
speaker, low-intensity feeding buzzes from the other (control & LIFB), and
control sound from one speaker, low-intensity search phase calls from the
other (control & LISP). These treatments allowed us to measure female
display in relation to playbacks of bat echolocation calls alone. We only used
low-intensity playbacks to investigate female responses to echolocation calls
alone to minimize the number of treatments that each moth was subjected to,
hence reducing the risk of habituation. We reasoned that if display rate were
reduced in relation to low-intensity playbacks, it would be reduced even more
to high-intensity ones. The final treatment involved playbacks of control
sound from both speakers (control & control) to control for any wing
fanning produced in response to recording conditions. Our hypotheses,
treatment comparisons, and predictions are summarized in
Table 1.
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We measured the amount of time a female spent wing fanning during a 5-min
playback session. Wing fanning was timed with a stopwatch by one observer who
was blind to the nature of the playbacks. The same observer also prepared the
moths for the experiments and was again blind to the playback treatment. A
second person broadcast 0.5-s sound sequences every 5 s. These time periods
represent the duration of bursts of sounds and intervals between them produced
by male G. mellonella (Spangler,
1986) and those used experimentally by Spangler
(1988b). The timing of the
0.5-s sound bursts from one speaker relative to the other was random (selected
using random numbers for 1-5 s after the beginning of the playback from the
other speaker), so that only in one-sixth of all playbacks were bursts of bat
and moth calls broadcast during the same time block. This situation minimizes
signal masking from the output of the two speakers and may be a realistic
reflection of nature, where echolocation calls may occur between bursts of
male moth calling. The katydid Neoconocephalus ensinger only ceases
calling in response to batlike ultrasound when the calls are played in the
window of silence between stridulatory syllables
(Faure and Hoy, 2000).
None of our results were normally distributed, so we used nonparametric statistics throughout. Because we used a repeated-measures design, we investigated differences among all treatments by using a Friedman test. A posteriori differences among treatments were investigated by Wilcoxon signed-ranks tests (n = 20 females), with p adjusted by Bonferroni corrections. We therefore assigned significance to p values of.025 for two,.017 for three, and.0125 for four comparisons in a posteriori tests.
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RESULTS |
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Signal parameters
Signal parameters for moth calls, search-phase echolocation calls, and feeding buzz calls are summarized in Table 2. Moth calls had higher values of frequency parameters than both search phase and feeding buzz echolocation calls of bats. Moth calls were also shorter in duration and had lower duty cycles.
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Playback experiments
Female G. mellonella showed different median levels of wing
fanning in the different playback treatments (Friedman Test,
S7 = 51.2, p <.001;
Figure 2). Females wing fanned
at the highest rate (median 12.2 s in 5 min) in response to playback of male
moth calls with no bat echolocation calls broadcast during the test period (MM
& control). The median wing fanning response when both speakers broadcast
background sound (control & control) was only 0.15 s, so females clearly
responded to playbacks of male moth calls. Hence hypothesis 1
(Table 1) was supported.
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Female moths discriminated between male moth calls and bat calls (hypothesis 2, Table 1). Wing fanning almost ceased in tests involving playback of bat echolocation calls (Figure 2). Median responses to playbacks of low-intensity searchphase calls (LISP & control, median time wing-fanning 1.6 s) and low-intensity feeding buzzes (LIFB & control, median 1.2 s) were more than 10 s shorter than to playbacks of male moth calls (MM & control; Wilcoxon signed-rank tests W = 182, p <.025 and W = 210, p <.025, respectively).
When females were subjected to broadcasts of male moth calls and bat echolocation calls during the same time block, they wing fanned less than in response to male moth calls alone (Figure 2). Three of the four playbacks of bat calls reduced display rate in comparison with male moth calls alone (comparisons with control & MM: LISP & MM, p <.0125; LIFB & MM, W = 210, p <.0125; HIFB & MM, W = 202, p <.0125). When call intensity was varied, display rates were higher during playback of low-intensity echolocation calls at least for feeding buzzes (LISP & MM vs. HISP & MM, W = 51, p =.08, ns with Bonferroni correction; LIFB & MM vs. HIFB & MM, W = 33, p <.025; Figure 2). Female moths stimulated by male calls also displayed less when we broadcast feeding buzz sequences than search-phase calls of a given intensity (LIFB & MM vs. LISP & MM, W = 38, p <.025; HIFB & MM vs. HISP & MM, W = 20, p <.025; Figure 2). Thus females moderated their response in relation to perceived predation risk, and hypothesis 3 (Table 1) was supported.
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DISCUSSION |
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Moth hearing probably evolved largely in response to predation pressure from echolocating bats. Males of several moth species, including G. mellonella, exploited the bat-detecting ears of females to evolve ultrasonic courtship signals (Conner, 1999
). Their relatively simple ears must therefore distinguish
between similar sounds that signal courtship and predation threat. It seems
that G. mellonella females are able to make this distinction and,
moreover, that they vary display rate in relation to perceived predation risk
(varied by independent manipulations in call intensity and repetition rate).
Males of some moth species abort flights to pheromone plumes, cease pheromone
release when the echolocation calls of bats are broadcast, and reduce mating
behavior under conditions of high predation risk
(Acharya and McNeil, 1998).
Female G. mellonella fan their wings in response to playbacks of
male moth calls. Spangler
(1985) showed similar
responses to pulsed synthetic ultrasound at 72 kHz. Although the time spent
displaying by females is short, any reduction in wing fanning is likely to be
adaptive, especially as some bats can detect prey from echoes of single
wingbeats (Link et al.,
1986).
We found that display rate was reduced when male moth calls and bat
echolocation calls were broadcast to female G. mellonella during the
same time block in comparison with playbacks of male calls alone. Several
studies have shown that male insects cease calling in the presence of bat
echolocation calls. Male lesser wax moths (Achroia grisella) and bush
katydids (Insara covilleae) cease their ultrasonic calling when bats
fly over or when subjected to playbacks of 60 kHz ultrasonic pulses
(Spangler, 1984). Male
katydids Neoconocephalus ensinger also cease calling or insert pauses
in their song when pure tones of pulsed ultrasound between 20 and 100 kHz are
broadcast (Faure and Hoy,
2000).
We argue that the ability to distinguish bat and moth calls allows G.
mellonella to moderate display rate in relation to predation risk.
Masking of male calls by bat calls is unlikely to cause a reduction in wing
fanning by females for two reasons. First, there was little temporal overlap
in our playback sequences of bat and moth calls in each 5-min block when both
sequences were broadcast, yet large reductions in display rate in comparison
with playbacks of male moth calls alone occurred. Second, Greenfield and Weber
(2000) could not inhibit
female lesser wax moths from responding to male calls in the presence of
continuous white noise: females showed the same amount of orientation toward
moth calls plus white noise (20-90 kHz) as they did to moth calls alone.
The bat species that pose the biggest threat to displaying female wax moths
are gleaners. How realistic are our playbacks of bat calls in mimicking
predation threat from gleaning bats? M. daubentonii is a trawling bat
that often captures prey from the water surface by using its tail membrane and
large feet (Jones and Rayner,
1988; Kalko and Schnitzler,
1989). Many gleaning bats switch off echolocation before capturing
prey and do not produce feeding buzzes when taking prey from surfaces
(Anderson and Racey, 1991;
Faure and Barclay, 1992,
1994;
Faure et al., 1993). Most
gleaning bat species also hunt by aerial hawking, however, and produce feeding
buzzes during aerial attacks (e.g., Faure
and Barclay, 1994). We argue, therefore, that playbacks of feeding
buzzes will represent increased predation risk compared with playbacks of
search-phase calls because they provide information that bats are feeding in
the vicinity. Gleaning bats emit calls that are usually shorter, lower in
intensity, and higher in frequency than the calls of aerial-hawking species
(Fenton, 1990). We used
recordings of M. daubentonii, a trawling species, recorded in the
laboratory to mimic calls of gleaning bats because calls in the laboratory are
shorter, higher frequency, and lower intensity than field recordings (see
Jones and Rayner, 1988;
Kalko and Schnitzler, 1989).
The echolocation calls of M. daubentonii recorded in the laboratory
are similar in their broadband frequency-time course to those of gleaning
species such as M. bechsteinii
(Parsons and Jones, 2000;
Vaughan et al., 1997).
Therefore, our playbacks are reasonably representative of predation risks
experienced by moths in nature.
How do moths distinguish bat calls from moth calls, and feeding buzzes from
search-phase calls? The ear of G. mellonella has four sensory cells
with similar frequency responses but different thresholds
(Skals and Surlykke, 2000), so
the moths are tone deaf. Frequency differences will not therefore be used in
discrimination of moth calls from bat calls. Greenfield and Weber
(2000) suggested that female
lesser wax moths A. grisella discriminate male moth calls from bat
echolocation calls by the faster pulse rate of the moth calls. However,
because the repetition rate of male moth calls is similar to that of feeding
buzz calls produced by bats, pulse repetition rate is unlikely to be used as a
discriminatory cue. Moth calls are shorter in duration than bat calls, and
they are emitted at a lower duty cycle. Skals and Surlykke
(2000) concluded that the
distinction between bats and conspecifics must be based on temporal cues. The
threshold for flight cessation (presumably to escape from bats) in G.
mellonella decreases with increasing pulse repetition rate, but
repetition rate has no effect when duty cycle is held constant
(Skals and Surlykke, 2000).
Skals and Surlykke (2000)
suggest that G. mellonella responds to signal power rather than to
repetition rate per se. The lesser wax moth A. grisella can
discriminate 126- from 208-µs pulses
(Jang and Greenfield, 1996),
so discrimination of bats from moths by pulse duration may occur in G.
mellonella. Inhibition of running in female A. grisella only
occurs in response to synthetic pulses that resemble bat echolocation calls
both in repetition rate and pulse duration
(Greenfield and Weber, 2000).
Perhaps the grouping of moth calls into trains may also facilitate
discrimination. Two or more pulses emitted over very short intervals would
then signal "moth," whereas more regular, longer intervals between
pulses would signal "bat." Discrimination of conspecifics from
bats may become more difficult when several males are chorusing.
Female preferences for male signal parameters have been studied in A.
grisella by Jang and Greenfield
(1996). Females show
preferences for signals with longer durations and higher repetition rates (up
to 71 Hz). It would be interesting to determine if female preferences were
reversed at durationst that approach those of bat calls (tests were restricted
to signals < 250 µs), in which case predator detection may place a
ceiling on female preferences for signals that might otherwise signal male
quality (longer signals have more energy and may be more costly for males to
produce).
Few studies have measured how mating behavior varies in relation to
experimental manipulation of predation risk
(Acharya and McNeil, 1998;
Fuller and Berglund, 1996;
Mathis and Hoback, 1997).
Natural selection will result in animals trading off reduced mating
opportunities against an increased threat of predation. Our results suggest
that pyralid moths with relatively simple nervous systems can distinguish
between the ultrasonic calls of mates and those of predators and that
differences in the durations of signals of the two may provide the basis for
discriminations.
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ACKNOWLEDGEMENTS |
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We thank Rob Houston for assistance with intensity calibrations, Annemarie Surlykke for permission to use unpublished results, Arjan Boonman for help with recording bats that he held in captivity, and Ian Tew of the University of Wales at Swansea for supplying the moth cultures.
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REFERENCES |
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