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First published online June 29, 2007
Journal of Experimental Biology 210, 2481-2488 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.001909
Acoustic feature recognition in the dogbane tiger moth, Cycnia tenera
1 Department of Biology, University of Toronto at Mississauga, Mississauga,
Canada, L5L 1C6
2 Department of Neurobiology and Behavior, Cornell University, Ithaca, NY
14853, USA
* Author for correspondence (e-mail: jfullard{at}utm.utoronto.ca)
Accepted 17 April 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: bat echolocation, tiger moth, phonoresponse, defensive behaviour, Cycnia tenera
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
Insects are also capable of similar discrimination abilities
(Hoy, 1989;
Wyttenbach and Farris, 2004;
Schul and Sheridan, 2006) and
perform them with far fewer neurons. Of all insects, the ears of moths
represent the simplest auditory systems, possessing only one to four auditory
receptor cells (Eggers, 1919;
Yack, 2004). With some
exceptions (Conner, 1999),
moths use their ears solely to detect the echolocation calls of hunting bats
and evoke escape behaviours appropriate to the threat presented by the bat. To
determine what that threat is, the moth must acoustically estimate the
proximity of the bat as gauged by its echolocation calls, since other cues
(e.g. visual) are of presumably little or no use to these insects for bat
detection when flying at night (Fullard
and Napoleone, 2001; Soutar
and Fullard, 2004).
Griffin et al. categorized the echolocation calls of aerial hawking bats
into three phases based on changes in call duration, period (the time from the
start of one call to the start of the next) and frequency
(Griffin et al., 1960).
Search-phase calls are emitted first and are defined as having periods of 50
ms or more. It is assumed that during this phase, bats have not yet detected a
potential target. After a bat has detected a target
(Kick and Simmons, 1984;
Wilson and Moss, 2004) it
emits approach-phase calls that are shorter in duration and period
(10–50 ms) and are marked by an increase in their lowest frequencies
(Surlykke and Moss, 2000).
Once the bat has decided to complete its attack, it emits terminal
(buzz)-phase calls that are very short (
1–2 ms), have periods of
less than 10 ms (which increases the duty cycle – the percentage of time
that the bat is actively producing sound) and are of lower peak frequency than
either search or approach calls. While this three-phase heuristic has proved a
valuable tool for comparative analysis of bat species and hunting strategies
(e.g. Kalko, 1995;
Ratcliffe and Dawson, 2003),
it can be simplified from the perspective of the insect into two phases: (1)
search-phase calls that signify a bat before it has detected its target and
(2) attack-phase calls (approach + terminal) that signify a bat after it has
detected a target and has begun to actively pursue it. Insects react bimodally
to these calls: to search-phase calls with primary defences intended to
conceal them from the bat before it has detected them and to attack-phase
calls with secondary defences designed to rapidly evade the now-aware bat.
Roeder proposed that the bimodal defence response of noctuid moths is based
upon their perceived intensity of the bats' calls
(Roeder, 1966;
Roeder, 1974). According to
this theory, moths react to distant bats (i.e. faint calls) with directional
controlled flight away from the bat, a defensive behaviour evoked by the most
sensitive auditory receptor, the A1 cell. When confronted by near bats (i.e.
intense calls), moths switch to erratic flight or cease flying altogether,
responses elicited by the less sensitive A2 receptor cell. Skals and Surlykke
supported this hypothesis by concluding that flight cessation in the moth
Galleria mellonella was triggered by the rise in acoustic power (as
perceived by the moth) caused by increased duty cycle of the attack-phase
calls (hereafter the `acoustic power hypothesis')
(Skals and Surlykke, 2000).
While changing call intensity will provide a measure of the relative distance
of a searching distant bat (assuming it does not change its emitted level),
this cue may become unreliable to an erratically moving moth for a bat
beginning its attack. Temporal and spectral changes to the bat's calls, on the
other hand, present acoustic cues that should provide less ambiguous
information about the bat's switch from search to attack phase, and moths may
possess the ability to recognize such cues (hereafter the `acoustic
recognition hypothesis').
When stimulated by the echolocation calls of an attacking bat, the dogbane
tiger moth (Cycnia tenera) phonoresponds with trains of ultrasonic
clicks generated by thoracic tymbals. These sounds warn the bat of its noxious
qualities [aposematism (Dunning and
Roeder, 1965; Hristov and
Conner, 2005)] and/or interfere with the bat's echolocation
[jamming (Fullard et al.,
1979; Fullard et al.,
1994; Miller
1991)]; aposematism and jamming may act synergistically because
negative-cue/negative-consequence associations should be readily made
(Ratcliffe and Fullard, 2005).
The phonoresponse is a stereotyped behaviour that can be used to examine
auditory perception in this moth and what cues it uses to evoke its acoustic
defence (Fullard, 1979;
Fullard, 1984;
Fullard et al., 1994;
Barber and Conner, 2006). Male,
and rarely female, Cycnia tenera also emit these sounds during mating
(Conner, 1987) but they are not
elicited as a phonoresponse to conspecific clicks
(Fullard and Fenton, 1977) and
social functions should not influence whatever acoustic cues it uses to evoke
this defensive behaviour. Fullard reported that C. tenera
preferentially phonoresponds to stimulus pulse periods that resemble those of
a bat's echolocation calls when it is in its attack phase and argued that
recognizing the pulse period of the bat's echolocation attack sequence reduces
the moth's chances of inappropriately clicking to sounds of pulse periods that
are either too high (e.g. searching bats) or too low (e.g. chorusing insects)
(Fullard, 1984).
The stimuli used by Fullard (Fullard,
1984) did not closely resemble bat calls in that they were of a
constant frequency and duration while real bats manipulate these acoustic
characteristics as they change from search to attack phase. Fullard et al.
(Fullard et al., 1994)
provided a more realistic stimulus to C. tenera by using the calls
recorded in a laboratory from a free-flying bat (Eptesicus fuscus) as
it attacked a target and again demonstrated that C. tenera times its
phonoresponse to attack calls. These results were confirmed in flight-cage
experiments with wild-caught, free-flying Myotis septentrionalis bats
(Ratcliffe and Fullard, 2005).
Barber and Conner (Barber and Conner,
2006) also reported the attack-stage phonoresponse of C.
tenera and demonstrated that other (but not all) tiger moths phonorespond
when the bat is less than a second from contact. While these studies confirm
that C. tenera is most sensitive to the calls of an attacking bat,
the question remains, does this insect recognize some specific signature (i.e.
frequency, duration, period) of these calls, as suggested by Fullard
(Fullard, 1984), or does it
simply respond to its perceived increase in the calls' acoustic power as the
bat closes (Skals and Surlykke,
2000)? In the current paper, we use the phonoresponse of C.
tenera and two auditory psychophysical methods [thresholds and
habituation/generalization (H/G)] to test for acoustic feature recognition in
this insect and interpret these results in the context of this animal's
defence against naturally hunting bats.
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Materials and methods |
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Acoustic stimulation
Individual moths were fastened by their descaled mesothoracic terga to the
head of a dissecting pin with a drop of molten Cenco Softseal Tackiwax (Cenco
Scientific, Chicago, IL, USA) and suspended 20 cm above a Technics EAS10TH400B
(Panasonic, Matsushita Electric Industrial Co. Ltd, Kadoma City, Japan)
speaker in a chamber lined with sound-attenuating foam. Moths were positioned
under red light and were then left in complete darkness for 20 min before
playbacks began. Continual tones produced by either a Wavetek (model 23)
(Willtek Communications, Ismaning, Germany) or Hewlett-Packard
(Hewlett-Packard, Palo Alto, CA, USA) signal generator (model 3311A) were
shaped with a 0.5 ms rise/fall time to various durations and periods
(Coulbourn S84-04; Coulbourn Instruments, Allentown, PA, USA), amplified
(National Semiconductor LM1875T; National Semiconductor Corp., Santa Clara,
CA, USA) and broadcast from the Technics speaker. Certain of the stimulus
trains were stored on a Racal Store 4D tape recorder (Racal Acoustics Ltd,
Harrow, UK) running at 76 cm s–1 (as internally
calibrated), while others were recorded as .wav files onto a PC laptop using a
500 kHz sampling rate PCMCIA card (DAQ Card-6062E; National Instruments,
Austin, TX, USA) controlled by the programme BatSound Pro v.3.30 (Pettersson
Elektronik AB, Uppsala, Sweden). Stimulus trains were either played back using
the Racal tape recorder or the playback feature of the BatSound Pro programme
and DAQ Card. Playback intensities were recorded as mV peak-to-peak and were
later converted to peak equivalent dB sound pressure level (peSPL) (re 20
µPa rms) from equal-amplitude continual tones using a Brüel and
Kjær (B&K) (Nærum, Denmark) type 4135 6.35 mm microphone and
type 2610 B&K measuring amplifier. The system was regularly calibrated
with a B&K type 4228 pistonphone. Stimuli were presented to the moth as
trains of pulses of different durations, frequencies and periods depending
upon the experiment.
Phonoresponse
The phonoresponse in C. tenera
(Fig. 1A) was generated by
exposing moths to acoustic stimuli as generated by the aforementioned methods.
Tymbal sounds are generated as trains of clicks [modulation cycles (MC)
(Blest et al., 1963)] that
result from the in and out buckling of the striated tymbal surface
(Fullard and Fenton, 1977) and
were recorded with the B&K microphone and measuring amplifier onto the
Racal tape recorder. Phonoresponse recordings were played at 
real-time tape speed into a data acquisition board (TL-2; Axon Instruments,
Molecular Devices Corporation, Sunnyvale, CA, USA) at a 20 kHz sampling rate
and stored on a PC, and files were subsequently analysed using the programme
AxoScope 8.1 (Axon Instruments). Certain trials were recorded using the DAQ
Card and stored and analysed as .wav files using BatSound Pro.
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Threshold trials
For neural examinations, we exposed the auditory nerves (IIIN1b)
(Nüesch, 1957) of male
and female C. tenera and recorded auditory receptor cell action
potentials with a stainless steel hook electrode referenced to another
electrode placed in the moth's abdomen
(Fullard et al., 1998).
Responses were amplified with a Grass Instruments P-15 pre-amplifier (Quincy,
MA, USA). Auditory threshold curves (audiograms) were derived for each moth
using trains of 20 ms acoustic pulses (produced as described above) with 500
ms periods at 5 kHz frequency increments randomly chosen from 5 to 100 kHz. A1
cell threshold was determined as the stimulus intensity that evoked two
receptor spikes per stimulus pulse.
For behavioural threshold trials, we positioned individual C. tenera above the speaker as described above and exposed them to trains of pulses of various durations, frequencies and periods. The intensity of the pulse trains was raised from zero to the point when the moth just began to phonorespond.
Habituation/generalization trials
We used a habituation/generalization (H/G) paradigm
(Thompson and Spencer, 1966)
to test whether C. tenera discriminated changes to various parameters
in the acoustic stimulation applied to them.
Fig. 1 describes the
stimulation regime applied to each moth; in all cases, response was measured
as the number of tymbal modulation cycles that the moth produced during the
stimulus trains (counting MCs was facilitated by treating the files to a 40
kHz high-pass filter that eliminates the stimulus pulses while preserving the
tymbal clicks). The first part of the trial began with the habituating
stimulus (Fig. 1B, top and
middle) consisting of a 95 dB peSPL [20 cm, equal to approximately 101 dB
source level (10 cm)] train of pulses of a particular frequency, duration and
period. This stimulus train was one second in duration and was repeated 20
times. Each trial was separated from the next by one second of silence. This
was followed one second later by the test stimulus, consisting of a single
train of pulses that differed from the habituating stimulus in a single
acoustic parameter (Fig. 1B,
bottom). Habituation was determined for each individual moth by applying a
linear regression to the raw response data and then testing for a
significantly negative departure from a slope of zero (F-test)
(Fig. 1C). Only moths that
habituated were used in subsequent analyses. To control for inter-individual
responsiveness, modulation cycle numbers were normalized as the percentage of
the response to the first pulse train. We tested for stimulus generalization
by comparing test stimulus responses (trial 21) to responses to the last
pre-test stimulus train (trial 20) by using paired-sample t-tests
(Zar, 1999).
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Results |
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) and behaviourally
(Fullard, 1984). The moth
reveals a uniform sensitivity for frequencies between 30 and 50 kHz. This
bandwidth was used in habituation/test of stimulus generalization trials to
determine if the moth would discriminate between pulse trains of different
frequencies.
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Stimulus duration
H/G trials
We first ran a series of 5 ms/10 ms H/G trials in which we compared
habituated and test stimuli responses to pulse trains of equal (10%/10%) and
unequal (10%/20%) duty cycles. The results are illustrated in
Fig. 3 and indicate that C.
tenera generalizes (i.e. does not differentiate) between a 5 ms increase
or decrease in pulse duration when duty cycles are maintained at 10%. When
pulse train duty cycles were doubled, moths generalized to pulse durations
that were twice the duration but if this increase in duty cycle was
accompanied by a halving of pulse period, moths exhibited a vigorous
re-initiation of clicking to shortened pulses.
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Stimulus period
Threshold trials
When stimulus pulses were delivered using variable duty cycles
(Fig. 5A, top), moths exhibited
a maximum sensitivity to a pulse train period of 20 ms (i.e. 50 pulses
s–1) with increased thresholds to shorter and longer pulse
periods (i.e. the response was tuned). The duty cycle at 20 ms for a 2 ms
pulse duration was 10% so we ran another series of threshold trials using duty
cycles below (6.7%) and above (20%) this value to determine if acoustic power
would account for the tuning. To hold the duty cycles constant we had to
change the pulse durations for each period used.
Fig. 5A (middle) illustrates
the pulse period tuning curve for a duty cycle of 6.7% and shows that the
moths exhibited no particular tuning. However, when the duty cycle was
increased to 20%, the moth's response exhibited less sensitivity displayed a
high-pass filter at pulse periods of 20–40 ms
(Fig. 5A, bottom).
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H/G trials
To separate the effect of pulse period from that of duty cycle in C.
tenera's phonoresponse tuning we ran a series of H/G trials using pulse
trains that simulated a typical bat's search and terminal echolocation phases.
For pulse periods, we used the call parameters as described by Surlykke and
Moss' analyses of wild Eptesicus fuscus foraging in an open area
(Surlykke and Moss, 2000) and
picked search- and attack-phase examples that shared the same duty cycle
(Fig. 6). This bat represents a
common (Fullard et al., 1983;
Brooks and Ford, 2005;
Kurta and Baker, 1990)
sympatric, moth-feeding species that should form a significant part of this
moth's natural predation potential. The pulse train sequences that matched
these criteria had pulse durations of 15 ms (search) versus 1.5 ms
(terminal) and equal duty cycles of 7% (pulse periods of 215 and 21.5 ms,
respectively). The results from these trials indicate that when C.
tenera is first habituated to search-phase calls it vigorously responds
to terminal calls but does not respond when exposed to the opposite sequence
of terminal to search calls (Fig.
5B).
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Frequency
Surlykke and Moss observed that searching Eptesicus fuscus raise
the minimum frequencies of their calls by 3–4 kHz as they begin their
approach phase (Surlykke and Moss,
2000) and we suggest that this shift would be a reliable spectral
cue to insects capable of frequency discrimination. Based on physiological
evidence, authors have predicted that moths cannot frequency discriminate
(Suga, 1961;
Roeder, 1966) and our study
behaviourally supports this conclusion (but see
Spangler, 1984). While moths
may be tone-deaf, the Pacific field cricket, Teleogryllus oceanicus,
categorically perceives sound frequencies representing diametrically opposed
signals (mating versus bat sounds)
(Wyttenbach et al., 1996) and
could use spectral cues to identify an attacking bat. Crickets discriminate
frequencies by using a range-fractionated auditory receptor array
(Imaizumi and Pollack, 2005)
that reserves approximately 25% of its cells for the ultrasonic calls of bats.
The frequency non-fractionating, two-celled receptor organ of the noctuoid
moth ear appears to preclude a similar ability for these insects.
Tone-deafness appears to extend to more complex moth ears, as demonstrated in
the four auditory-celled pyralid Galleria mellonella
(Skals and Surlykke,
2000).
Duration
Once a searching bat enters its attack phase, it shortens the duration of
its echolocation calls, and if C. tenera recognizes such a temporal
change it could use this as a trigger to elicit its phonoresponse. Our H/G
trials demonstrate that C. tenera does not respond differentially to
a 5 ms increase or decrease in stimulus pulse duration when duty cycles are
held constant (Fig. 3),
suggesting that changes to duration alone will not trigger a phonoresponse.
However, a real attacking bat differentially decreases its pulse period as
well as its duration, resulting in an increase in duty cycle
(Kalko, 1995). Using the data
of Surlykke and Moss (Surlykke and Moss,
2000) (Fig. 6), the
echolocation duty cycle increases from an average of 7% during E.
fuscus' search phase to an average of 11% during its attack phase (i.e.
an increase of 57%). This value is similar to the 60% increase that appears to
be the minimum required to re-elicit C. tenera's phonoresponse
(Fig. 4), suggesting that
increasing duty cycle could serve as a natural cue in telling the moth that
the bat has entered its attack phase, as predicted by an acoustic power
hypothesis (Skals and Surlykke,
2000). This hypothesis would predict, however, that given the same
increase in duty cycle, the moth would show an equal degree of differential
responsiveness whether the pulse duration was increased or decreased. This,
however, was not the case, with the moth exhibiting a more than sevenfold
increase in responsiveness when the pulse duration was decreased by 5 ms
compared with when it was increased by the same amount
(Fig. 3). To obtain an equal
doubling of duty cycles with shorter pulse durations, we were required to
change the pulse train pulse periods. Whereas the pulse period was the same
(50 and 50 ms) in the equal duty cycle trials, it had to be reduced to 25%
(100 and 25 ms) for the unequal duty cycle trials. The dramatic increase in
phonoresponse suggests the primary role that pulse period plays in eliciting
C. tenera's behaviour.
Period
If C. tenera recognizes an attacking bat's echolocation call
period we should expect to see its phonoresponse tuned to a specific period,
with reduced sensitivity to lower and higher values. By contrast, if the moth
responds to an increase in acoustic power arising from changing duty cycle
(Skals and Surlykke, 2005), the phonoresponse threshold will decrease
regardless of period. Our threshold trials using increasing duty cycles
(Fig. 5A, top) show that C.
tenera exhibits maximum sensitivity to pulse periods of 20 ms
(Fullard, 1984). These pulse
periods simulate the echolocation calls of E. fuscus after it has
detected its intended prey and is approaching for an attack
(Kick and Simmons, 1984;
Surlykke and Moss, 2000) and
are similar to values that initiate the phonoresponse in laboratory
experiments (Fullard et al.,
1994; Barber and Conner,
2006). Our results also demonstrate that C. tenera's
phonoresponse thresholds are not linearly related to the duty cycles of the
pulse trains but instead exhibit a tuned response to the preferred period
value of 20 ms. When pulse train duty cycles were maintained at 6.7%, a value
representing natural search calls (Fig.
5A, middle), intensity thresholds decreased as pulse periods
decreased, which would be predicted by an acoustic recognition hypothesis. As
shown by its response to pulse train duty cycles of 20%, those in excess of a
natural terminal phase (Fig.
5A, bottom), C. tenera discriminates against pulse
periods below 20 ms, suggesting an adaptive function for its period tuning.
Fullard observed that auditory receptor response in C. tenera
decreases with pulse period until continual firing occurs to periods of less
than approximately 10 ms (Fullard,
1984), implying that the moth treats these sounds as continuous
and non-threatening (Fullard et al.,
2003). Similar neural responses have been reported by Waters
(Waters, 1996) and Coro et al.
(Coro et al., 1998) in
sound-producing arctiids and silent noctuids. Roeder reported that continuous
sounds were less effective than pulsed sounds in evoking evasive manoeuvres in
flying noctuid moths (Roeder,
1964). That pulsing is an essential element in evoking the
defensive behaviour of flying noctuid moths is not surprising since these are
the types of sounds that hunting bats emit, but these results suggest that
continual tones are actively ignored, perhaps since they represent
non-dangerous stimuli (e.g. chorusing insects).
Skals and Surlykke concluded that echolocation pulse period is not used by
G. mellonella to evoke its defence against near bats and suggested
instead that the increased acoustic power from an attacking bat's echolocation
calls triggers the moth's defences (Skals
and Surlykke, 2000). The duty cycle of the pulse trains used in
their experiments (35%) is approximately seven times higher than values
reported for typical vespertilionid bats
(Kalko, 1995;
Surlykke and Moss, 2000;
Ratcliffe and Fullard, 2005),
and we suggest that the high stimulus power delivered by Skals and Surlykke
(Skals and Surlykke, 2000) to
the G. mellonella masked the effect of pulse period in triggering
this particular moth's defensive behaviour. Furthermore, Skals and Surlykke's
acoustic power hypothesis (Skals and
Surlykke, 2000) depends upon a reliable increase in the received
intensity of sound pulses, something not likely experienced in nature by
erratically flying moths whose wings would already be attenuating the
intensities of the bat calls by frequently obscuring their ears
(Payne et al., 1966).
Our H/G trials using simulated natural search and attack echolocation pulse
trains (Fig. 5B) of equal duty
cycles indicate that the sequence of calls as encoded by pulse period is
important for evoking C. tenera's natural phonoresponse. The first
set of pulse trains (search – attack) simulates the situation where an
insect would naturally hear the approach of a bat that has detected its target
and is attacking, while the second set (attack – search) represents a
bat that has missed its intended target and has reverted to searching. It is
expected that C. tenera would not generalize the first pair of pulse
train stimuli since waiting until the bat is within a metre or so represents
the optimal time for the moth's clicks to have their deterrent effect
(Ratcliffe and Fullard, 2005).
On the other hand, phonoresponding to a bat that is departing would not serve
the moth any useful purpose since the bat had already passed and might, in
fact, draw that bat's attention or that of eavesdropping bats
(Balcombe and Fenton, 1987).
Since duty cycles and intensities were held constant in these trials, the only
cue available to C. tenera for its response would be the pulse period
of the calls.
Intensity
While C. tenera exhibits preferences for particular pulse trains,
it readily phonoresponds to unnatural stimuli if the intensity is great enough
[e.g. jingling keys (Fullard and Fenton,
1977)]. This suggests that, if an acoustic recognition mechanism
exists in C. tenera, it can be overridden by stimulus intensities and
cautions an appreciation of the natural relevance of the sounds used as
stimuli in these experiments. To evoke phonoresponses in C. tenera,
Fullard et al. (Fullard et al.,
1994) used pre-recorded echolocation calls with source level
intensities (i.e. dB @ 10 cm) that were matched to those produced by the bat,
which resulted in an increase in the intensity at the moth's ear as the bat
began its terminal phase. An increase in attack call intensity (as received by
the target) was also reported for the bat Myotis daubentonii
(Boonman and Jones, 2002) from
approximately 80 to 95 dB. By contrast, Holderied et al.
(Holderied et al., 2005)
report approach/terminal echolocation call source intensities in Eptesicus
bottae of 105–115 dB, equating to much lower target received
intensities of 75–85 dB [assuming a distance from the bat of 3 m when it
begins its approach (Kick and Simmons,
1984) and not accounting for excess atmospheric attenuation]. The
range of reported approach/terminal call intensities serves as a further
warning that unnaturally high stimulus intensities may result in artifactual
responses. In our present study, habituating and test pulse trains were
delivered at a constant received sound level intensity of 95 dB, resulting in
unnaturally intense search sequences, which may explain C. tenera's
phonoresponse to these otherwise sub-threshold pulse train periods
(Fig. 5A, top). The observed
maximum phonoresponse sensitivity to terminal pulse periods of 20 ms at 95 dB
suggests that this represents the closest simulation of the combination of
temporal and intensity variables that naturally evokes C. tenera's
defensive behaviour.
As the bat closes on its target, the combination of changing pulse
intensities and duty cycles, counteracted by decreasing pulse durations [and
their concurrent effects due to the temporal integration of the moth's ear
(Tougaard, 1998)], results in
a complex transformation of the acoustic energy received by C.
tenera. The neural simplicity of the moth ear provides the unique
opportunity to empirically examine how these acoustic changes are encoded.
Fullard et al. (Fullard et al.,
2003) examined the responses of C. tenera's two auditory
receptor neurons to the same echolocation sequence they had used previously
(Fullard et al., 1994) and
reported that, at intensities evoking phonoresponse, both of C.
tenera's auditory receptor neurons reduce their firing as the
bat enters its terminal phase. This indicates that the total acoustic power
received by C. tenera's ear decreases as the bat nears its
target, further reducing its natural role as a cue activating its
phonoresponse.
The precise point at which C. tenera phonoresponds to an attacking
bat may be a result of the species of bat it is facing. While C.
tenera begins its phonoresponse to the terminal calls of a lab-reared
Eptesicus fuscus (Fullard et al.,
1994), experiments with free-flying wild Myotis
septentrionalis indicate that C. tenera phonoresponds earlier,
during this bat's approach-phase calls
(Ratcliffe and Fullard, 2005).
If wild-flying bats emit louder echolocation calls than lab-confined animals
(Surlykke and Moss, 2000),
these behavioural variations may be related to the different intensities of
the two bats. Fullard et al. showed that increasing the intensity of the
attack sequence of E. fuscus results in C. tenera beginning
its phonoresponse earlier in the bat's attack sequence
(Fullard et al., 1994).
Praying mantids also exhibit an advance in their anti-bat flight responses
when confronted by higher intensities
(Triblehorn and Yager,
2005).
Conclusion
Our original belief was that the situation-specific behavioural response of
C. tenera to attacking bats would support either an acoustic power
hypothesis (Skals and Surlykke,
2000) or an acoustic recognition hypothesis
(Fullard, 1984), but our
results suggest that both mechanisms play a role in the moth's natural
behaviour. The ability of C. tenera to discriminate searching from
attacking bats may exist by means of a pulse period identification mechanism
(e.g. a central nervous system template) but this template is influenced and
can be overridden by the acoustic power of the stimuli reaching it. Recent
work on pulse period recognition in singing insects (reviewed by
Hedwig, 2006) suggests that
such a template could exist as pattern-specific (oscillatory) neurons
(Bush and Schul, 2006) matched
to the same period as the calls of an attacking bat. This template (or others
running with different periods) could also account for the flight patterns
exhibited by other noctuoid moths when exposed to similar rates
(Roeder, 1964). Decreasing
pulse periods also trigger flight reaction in lacewings
(Miller and Olesen, 1979) and
praying mantids (Triblehorn and Yager,
2005) and we suggest that pulse period recognition is an auditory
feature shared by many flying, nocturnal insects that have to avoid hungry
bats.
|
Acknowledgments |
|---|
) and
for her helpful comments. This project was funded from a Discovery Grant
(J.H.F.) from the Natural Sciences and Engineering Research Council of Canada
(NSERC), a post-graduate NSERC scholarship (J.M.R.) and from undergraduate
research support provided by UTM. |
References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Barber, J. R. and Conner, W. E. (2006). Tiger
moth responses to a simulated bat attack: timing and duty cycle. J.
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