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First published online November 28, 2008
Journal of Experimental Biology 211, 3808-3815 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.023978
Surviving cave bats: auditory and behavioural defences in the Australian noctuid moth, Speiredonia spectans
1 Department of Biology, University of Toronto, 3359 Mississauga Road,
Mississauga, Ontario, Canada L5L 1C6
2 Department of Zoology, University of Cape Town, Private Bag X3, Rondebosch
7701, South Africa
3 Biodiversity Conservation Division, Department of Natural Resources,
Environment and the Arts, P.O. Box 1120, Alice Springs, 0871 Australia
4 Queensland Museum, P.O. Box 3300, South Brisbane, 4101 Australia
5 Griffith School of Environment, Griffith University, Nathan, 4111
Australia
* Author for correspondence (e-mail: james.fullard{at}utoronto.ca)
Accepted 13 October 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: bat echolocation, moth ears, predator, prey, sensory ecology
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). This now
classic neuroethological story was originally set in the open skies where
free-flying bats locate and attack their prey by what is known as aerial
hawking. Further studies suggested that substrate-gleaning bats who find their
prey by orienting towards the prey's incidental sounds (e.g. wing fanning) may
be at an advantage in capturing eared moths owing to the reduced intensity as
well as to the higher frequency of their calls
(Fenton and Fullard, 1979;
Faure et al., 1990;
Faure et al., 1993). Roeder and
Fenton introduced another potential arena for the arms-race between these two
opponents, viz. subterranean roosts such as caves and mines in which bats and
moths co-habit (Roeder and Fenton,
1973). In a North American mine, the noctuid moth,
Scoliopteryx libatrix (Linnaeus) overwinters with hibernating bats
[Myotis spp and Eptesicus fuscus (Beauvois)] and although it
can hear the calls of these bats, it does not react behaviourally to them.
This apparent anomaly was explained by the possibility that this moth inhibits
its normal avoidance flight response to ultrasound to remain in the relative
safety of the roosts, protected from abiotic (e.g. freezing) and biotic
dangers (e.g. predation by birds). This study also reported that bats did not
appear to eat the moths, perhaps because of the physical inability of aerially
hawking bats to attack insects in the narrow confines of the mines.
Pavey and Burwell further developed this story of `lambs laying down with
lions' by describing the co-habitation of the Australian Granny's Cloak
noctuid moth, Speiredonia spectans Guenée, in subterranean day
roosts with insectivorous bats, including the Eastern horseshoe bat,
Rhinolophus megaphyllus Gray and the Little Bent-winged bat,
Miniopterus australis Tomes
(Pavey and Burwell, 2005).
S. spectans lives in large numbers with these bats [Pavey and Burwell
counted 1090 live moths in six sites
(Pavey and Burwell, 2005)] but
in contrast to Roeder and Fenton (Roeder
and Fenton, 1973), they found moth wings on the floors of the
roosts implying that co-habiting bats prey upon S. spectans. A report
of cave-foraging in bats by Lacki and Ladeur described the Big-eared bat,
Corynorhinus rafinesquii (Lesson) capturing moths in a cave in
Kentucky, USA by both aerially hawking them and by gleaning them from the
surface of the cave (Lacki and Ladeur,
2001). Pavey and Burwell suggested that in spite of the risk of
predation, S. spectans co-habits with bats by being able to detect
their echolocation calls and escaping to the walls of the day roosts
(Pavey and Burwell, 2005). The
echolocation calls of R. megaphyllyus and M. australis
contain frequencies of 60–70 kHz
(Jones and Corben, 1993;
Fenton et al., 1999;
Reinhold et al., 2001), which
although not frequency-matched (syntonic) are theoretically within the
bandwidth of sensitivity of tropical moths
(Fullard, 1988) and should be
detectable by S. spectans. By contrast, subterranean day roosts
occupied by the Dusky leafnosed-bat (Hipposideros ater Templeton)
contained S. spectans wings but no live moths
(Pavey and Burwell, 2005),
suggesting that the very high frequency of this bat's echolocation calls
[>150 kHz (Fenton, 1982;
Crome and Richards, 1988)]
renders them less audible (allotonic) to the moths and allows this bat to prey
more heavily on S. spectans.
The purpose of the present study was to examine the auditory capability of
S. spectans to address the hypothesis proposed by Pavey and Burwell
(Pavey and Burwell, 2005) that
this moth can hear the echolocation calls of R. megaphyllus and
M. australis but not those of H. ater in underground roosts.
In addition, we examine the hypothesis that S. spectans avoids roost
predation by adjusting its flight activity to minimize encounters with bats by
testing the prediction that there will be an absence of flight overlap between
the cave exits of the moths and the bats.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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)
whose 108 kHz calls are readily distinguishable from those of H.
ater; however, this species was recorded only once in the Bramston Beach
site and is, therefore, not considered further in this study]. Bats and moths
were observed in the Camp Mountain sites by illuminating the mine shafts with
a near infra-red (NIR) light source (Extreme CCTV Surveillance Systems, model
EX12LED, Scottsdale, AZ, USA) at wavelengths of 850–940 nm, to which
Lepidoptera are insensitive (Horridge,
1977), and videotaping them with a NIR-sensitive camera (Swann
Communications Pty., Richmond, Victoria, Australia) as they flew in the
mine.
|
).
Bat echolocation
We characterized the acoustic environment of the mines with respect to bat
echolocation by remotely recording echolocation calls of bats as they flew in
the mines. We used an ultrasonic microphone (Avisoft condenser microphone type
CM16; frequency response, 10–200 kHz) and digitizer (Avisoft
UltrasoundGate 416, Avisoft Bioacoustics, Berlin, Germany; sampling rate, 16
bit, 500 kHz) to record the calls and then analyzed sequences of calls using
BatSound Pro software (v. 3.20, Pettersson Elektronik AB, Upsala, Sweden).
Although we cannot ascertain the actual number of individuals used in our
acoustic analyses, we believe that the massive exodus of the bats from the
caves at night effectively rules out the possibility of pseudoreplication.
Only one sequence from each file was selected for measurement and these
sequences were chosen on the following criteria: (1) only sequences with calls
with a high signal-to-noise ratio (i.e. oscilloscope signal from the bat was
at least three times stronger than the background noise as displayed on a
linear time-voltage window) were analyzed; (2) only calls that were not
saturated were analyzed (Fenton et al.,
2001); (3) only calls that did not overlap with other calls were
analyzed. For each call in a sequence, we measured the peak frequency (PF)
from the power spectrum (1024-point FFT), call duration, inter-pulse interval
(IPI) and inter-onset interval (time from the onset of one call to the onset
of the next call in the sequence) from the oscillogram, and minimum frequency
of the frequency modulated (FM) tails for R. megaphyllus and H.
ater from the spectrogram. Minimum frequency (which can be calculated by
subtracting the bandwidth from peak frequency in
Table 1) for M.
australis was taken as the value –20 dB below peak frequency
whereas for R. megaphyllus and H. ater, this was taken as
the lowest frequency of the FM component of the call as measured from the
BatSound Pro spectrogram (time/frequency plot, 512-point FFT, resolution=19.36
ms per plot). IPI was measured from the end of one call to the initiation of
the next call, and duty cycle was calculated by dividing pulse duration by the
inter-onset interval. Bandwidth was measured at ±20 dB below peak
frequency for M. australis whereas for R. megaphyllus and
H. ater, bandwidth was calculated by subtracting the minimum
frequency of the FM component from the frequency of the constant frequency
(CF) component. R. megaphyllus had an FM component at both the
beginning and the end of each call, as opposed to the single FM sweep at the
end of a call for H. ater. We, thus, used the first FM component when
calculating the bandwidth for R. megaphyllus as this FM sweep was
usually the longer of the two.
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Moth auditory analyses
Moths were collected during the day from either the mines or from
storm-water drains at the St Lucia campus of the University of Queensland and
were used no more than 24 h later. Following decapitation and thoracic
dissection, the action potentials of the A1 auditory receptor in the moths'
tympanic nerve (IIIN1b) (Nüesch,
1957) were recorded using a stainless steel hook electrode
referenced to another in the moths' abdomen
(Fullard et al., 2003). Neural
responses were amplified (Grass Instruments P-15 Pre-amplifier, Astro-Med,
West Warwick, RI, USA) and observed either on-line or stored in a laptop PC
using digital acquisition boards (ADC 212/3, sampling rate=3 MHz; Pico
Technology, St Neots, Cambridgeshire, UK or UltraSoundGate 416-200, 16 bit,
sampling rate=250 kHz channel–1) and oscilloscope-emulating
software (PicoScope 5.10.7 or Recorder 2.9, respectively). Spike records were
later analysed with a customized MATLAB (v. R2006b, The MathWorks Inc.,
Natick, MA, USA) application. In keeping with previous studies
(Roeder, 1964;
Fullard et al., 2003;
Nabatiyan et al., 2003;
Marsat and Pollack, 2006), we
report spike periods rather than mean rates (e.g. spikes s–1)
as a direct measure of the activity of the auditory receptors and their
likelihood to activate postsynaptic neural components
(Hedwig, 2006).
Acoustic stimulation
Moth auditory preparations were exposed to pulsed synthetic sounds
generated by a MATLAB application running on a separate PC laptop, amplified
(Avisoft 70101) and broadcast from a speaker (ScanSpeak, Avisoft) mounted 30
cm from the moths. Intensities were recorded as voltages delivered to the
speaker and then converted to peak equivalent sound pressure levels (dB peSPL)
(r.m.s. re. 20 Pa) (Stapells et al.,
1982) from equal-amplitude continual tones as previously measured
with a Brüel & Kjær 4135 microphone and 2610 measuring
amplifier (Brüel & Kjær; Nærum, Denmark). The entire
system was calibrated before and after the study with a Brüel &
Kjær 4228 pistonphone. Auditory threshold curves (audiograms) were
derived using 20 ms sound pulses, 1 ms rise/fall times from 5 to 120 kHz
delivered 2 s–1 at randomly chosen 5 kHz intervals with A1
cell threshold determined as the stimulus intensity that evoked two receptor
spikes per stimulus pulse.
Bat playbacks
Digital recordings of bat echolocation calls were made in the absence of
human observers using the methods described above as the bats exited their day
roosts in the Camp Mountain site. Of these recordings, two files approximately
1.5 s in duration that contained no saturated signals or overlapping bat calls
were used as playbacks to seven auditory preparations of S. spectans
using the same equipment as for the auditory measurements. One of these files
contained 23 calls of R. megaphyllus and the other contained five
calls of M. australis. For each sequence, we set the highest
amplitude of each bat call to 70 dB peSPL by matching its voltage to that of a
continual 65 kHz tone (the frequency closest to that of the peak frequency for
both bats for which our speaker was calibrated) of known intensity as
generated using the set-up described above. We chose 70 dB as this intensity
would minimize the number of occurrences of the moth's A2 receptor cell, which
complicates the spike analysis. The echolocation sequence was played back five
times to each auditory preparation and neural responses recorded using the
UltraSoundGate 416-200 digitizer. From these playbacks, we isolated sections
using BatSound Pro that contained calls of only one or the other of the two
bat species and the moth's auditory nerve responses to those calls. We
analyzed the auditory receptor responses off-line with a customized MATLAB
application by measuring the number of A1 spikes per bat call and the
percentage of calls in the playback sequence that evoked A1 spikes. We also
applied Roeder's (Roeder,
1964) observation of 1.5–2.6 ms as the A1 spike period range
that evoked evasive flight responses in North American noctuids and counted
the percentage of spikes per bat call whose periods fell within this range. To
check for possible auditory responses to electronic static from the speaker,
the neural responses to the calls were compared with that of a 1.5 s playback
of a blank file (i.e. one whose signal was reduced to zero) that broadcast
only the output of the amplifier and speaker.
Our speaker was unable to reproduce the extremely high echolocation
frequencies of H. ater without generating electronic noise that
artifactually activated the moth's sensitive ear. This necessitated taking a
portable auditory neural preparation (Faure
et al., 1993) into the Bramston Beach day roost and allowing
free-flying bats to stimulate the moth's ear as they exited. One moth was
dissected and positioned near to the walls of the mine where H. ater
preferred to fly and its auditory nerve was continuously monitored and
recorded for 30 s every 15 min from 17:30 h until 19:00 h. All of the
previously described neurophysiological recording methodology was used except
that the USG digitizing board was set to an 8 bit, 500 kHz
channel–1 sampling mode to adequately capture the
echolocation calls of the bat. The auditory A1 receptor responses
(simultaneously recorded on a separate channel) to five different echolocation
sequences (presumably of different bats because bats were not observed
re-entering the mine once they had left) containing only H. ater
calls (a mean of 26 calls sequence–1) were then analyzed as
described above.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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To more precisely test for activity overlap, we examined each 1 minute bin as a discrete event and showed that the presence of bats excludes that of moths. By analysing bat and moth fly-bys as binomial events, moth activity is significantly more likely to occur during periods of bat inactivity (Fisher's Exact test, P<0.001). Fig. 2B shows the frequency of 1 minute bins where moths are active for each number of bat passes ranging from 0 to >10 and indicates that it was more likely to observe a moth in flight when no bats were present. The single recording we made of an entire night showed moths returning to the roost once bat activity had completely subsided.
We observed no instances of predation by bats, either by aerially hawking or by gleaning in the 50 h of video recordings and saw only four in-flight interactions between bats and moths. In these instances, moths exhibited evasive flight manoeuvres in response to passing bats by either diving to the ground (one of four) or landing on the wall of the mine (three of four).
Bat echolocation
The number of files per species that we analyzed was: R.
megaphyllus, four files; M. australis, five files; H.
ater, four files. H. ater produced CF/FM calls of higher peak
frequency and bandwidth than the FM/CF/FM calls emitted by R.
megaphyllus; however, the latter emitted calls of much higher call
duration and IPI resulting in their duty cycles being similar
(Table 1). The peak frequency
of the FM calls of M. australis was similar to that of R.
megaphyllus but the call duration of the former is much shorter and the
IPI much longer giving M. australis a lower duty cycle. The broad
bandwidth of the H. ater calls means that the FM sweep drops to a
mean frequency of 123.3±2.2 kHz.
|
Comparing the median audiogram in Fig. 3 with the frequency spectra of typical echolocation calls that were recorded in the same mines where the moths day-roosted, we predicted that S. spectans should be able to detect the calls of M. australis and R. megaphyllus (in fact, there appears to be a specific increased sensitivity at the fundamental frequency of R. megaphyllus) but would be unlikely to hear the calls of H. ater, although this is uncertain as our speakers could not reproduce frequencies higher than 120 kHz.
Bat playbacks
Figs 4 and
5 illustrate the responses of
S. spectans' A1 auditory receptor to the calls of R.
megaphyllus and M. australis. The neural traces demonstrate that
the ears of this moth responds to the calls of both bats, although the long
calls of R. megaphyllus evoke a significantly greater number of A1
spikes per call than do the shorter calls of M. australis
(Fig. 5A). In addition, the
percentage of bat calls that evoked any A1 spikes in auditory preparations of
S. spectans was significantly higher for R. megaphyllus than
for M. australis (Fig.
5B). R. megaphyllus calls also elicited significantly
more A1 spikes per call with periods that have been reported previously as
evoking evasive flight (Roeder,
1964) (Fig.
5C).
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|
As previously described, the inability of our speakers to reproduce the
calls of H. ater necessitated the field exposure of a moth auditory
preparation to these bats as they exited their day roost.
Fig. 4 illustrates the S.
spectans' maximum A1 cell response to one of the calls of this bat and
suggests that although the moth is completely deaf to the initial CF portion
of the call, it can detect the lower frequencies contained in the FM portion.
In spite of this detection ability, only 16% of the calls of H. ater
recorded elicited any A1 activity compared with 98% and 66% for R.
megaphyllus and M. australis, respectively
(Fig. 5B). Although the single
moth sample size for the H. ater exposure trials prohibits
statistical comparisons, the few calls of H. ater that were
detectable by S. spectans produced a surprisingly similar number of
A1 spikes as those produced by M. australis
(Fig. 5B) and with a similar
percentage of periods (Fig. 5C)
that meet Roeder's criterion of evoking evasive flight
(Roeder, 1964).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Fullard,
2006) and rival those of moths from other areas of high bat
abundance and diversity [Côte d'Ivoire
(Fenton and Fullard, 1979),
South Africa (Fullard et al.,
2008), Zimbabwe (Fullard and
Thomas, 1981)]. By contrast, the ears of the most sensitive
Canadian and Danish noctuids analysed possess thresholds of 30–40 dB at
their best frequencies, which rapidly increase above 50 kHz becoming
functionally deaf at 80–100 kHz
(Surlykke et al., 1999). The
sensitive ears of S. spectans probably arise from two conditions.
First, it is a large species [mean forewing length 39.5 mm (36–42.1 mm,
N=20) (C.J.B., personal observations)] and larger moths possess
greater auditory sensitivity due to the fact that they provide more detectable
echoes to searching bats (Surlykke et al.,
1999). Second, S. spectans occurs in the wet–dry
tropics of the Top End of the Northern Territory and the wet tropics of north
Queensland south to southern New South Wales
(Common, 1990)
(Fig. 1) – areas that
contain a rich diversity and abundance of echolocating bats
(Crome and Richards, 1988;
Law and Chidel, 2002;
Rhodes, 2002;
Pavey et al., 2006). Fullard
suggested that the broad tuning of moth ears is the evolutionary result of the
need of these insects to detect the acoustic assemblage of all of the bats
that hunt them, therefore, moths exposed to diverse bat communities typically
found in the tropics will possess ears with greater sensitivity across more
frequencies (Fullard, 1982;
Fullard, 1988). Regardless of
the total auditory sensitivity, it is the moth's audiogram peak sensitivity
that identifies the frequencies [i.e. bats, assuming that bat-detection is the
main use for these ears (Fullard,
1988)] from which the moth receives the greatest selection
pressure. From this theory, bats that emit syntonic echolocation frequencies
(those matched to the moth's peak sensitivity) form the heaviest predation
potential on moths compared with those that emit allotonic
(frequency-mismatched) calls. Paradoxically, allotonic bats should be expected
to consume more moths (i.e. present a greater selection pressure) as a result
of their reduced detectability. The explanation to this apparent conundrum is
the relative scarcity of allotonic bats, compared with the syntonic predatory
community, allowing them to exploit the sensory equilibrium that exists
between moths and sympatric bats [i.e. they are `cheaters' in an evolutionary
stable acoustic relationship (Faure et al.,
1993)]. To examine this, we created composite spectra of the peak
frequencies of the calls emitted by the species of Australian bats sympatric
with S. spectans for which acoustic data are available [Anabat files
(D. J. Milne, unpublished data) and analysed with AnalookW (v. 3.5 m,
www.hoarybat.com)].
These spectra were weighted with the relative abundances (C.R.P. and D. J.
Milne, unpublished data) of each bat species as estimated in the three
locations that encompass the distribution of the moth: Top End Northern
Territory, north Queensland (including the Bramston Beach study site) and
south-east Queensland (including the Camp Mountain study site).
Fig. 6 illustrates the three
echolocation assemblages compared with the mean audiogram of S.
spectans. These figures indicate that the heaviest predation potential on
moths arises from bats that echolocate in a bandwidth of 20–60 kHz,
predicting that common bats emitting these frequencies and preferring moths in
their diets [e.g. Chaerephon jobensis (Miller), Chalinolobus
gouldii (Gray) (Churchill,
1998)] form the greatest predatory threat for S.
spectans. Fig. 6 further
indicates that higher frequency echolocators such as R. megaphyllus
and M. australis are less common hunters of S. spectans but
still form a significant predation potential [R. megaphyllus feeds
extensively on moths over a wide geographical range
(Pavey and Burwell, 2004)].
Finally, Fig. 6 indicates that
the allotonic calls of uncommon bats such as H. ater fall
considerably outside of the sensitivity of S. spectans, and predicts
that while these bats will take large numbers of moths in their diets [a
prediction supported by data for H. ater at Bramston Beach where
91.7% of prey items were noctuid moths
(Pavey and Burwell, 1998)]
they are, nevertheless, rare predators of moths across the entire geographical
range of S. spectans and, therefore, impart little selective force on
its auditory design. Faced with the need to detect the greater number of bats
echolocating at lower frequencies, the moth's high frequency insensitivity
constitutes a sensory constraint that cannot be overcome by its limited
auditory hardware. The general similarity of the echolocation assemblages
among the three locations also predicts that the ears of S. spectans
will not exhibit auditory signs of local adaptation. To verify this prediction
would require testing moths from the three locations sympatric with the local
community of bats.
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Why does S. spectans co-habit with R. megaphyllus and M. australis?
S. spectans exists by the hundreds in subterranean roosts occupied
by R. megaphyllus and M. australis and should be a valuable
prey for these bats, a prediction supported by the observations of Pavey and
Burwell of wings left on the floors of day roosts
(Pavey and Burwell, 2005). The
question is therefore, how in the face of predation from these bats does
S. spectans defend itself when sharing its day roosts? Edmunds
defines primary and secondary defences as those that operate before and after,
respectively, a predator is aware of its intended prey
(Edmunds, 1974). We suggest
that S. spectans employs both types of defence to allow it to exploit
the relative safety of subterranean roosts from diurnal predators such as
birds. Regarding primary defence, Soutar and Fullard
(Soutar and Fullard, 2004)
examined how earless moths could protect themselves against bats, such as by
flying less (Roeder, 1974).
For S. spectans, the simplest defence could be that they do not fly
when the bats are active in their day roosts and this is borne out by our
observations that the activity of S. spectans within the roosts is
greater in the absence of bats. Although it is possible that other factors
(e.g. metabolic condition) may contribute to the evening flight patterns of
these moths, we believe that the most likely reason that moths do not fly when
bats do, is that they are acoustically aware of the bats and remain
perched.
The possession of sensitive ears should allow S. spectans, when
inside the roosts, to employ its secondary defence of detecting the bats'
echolocation calls and thereby either remaining perched when a bat flies by or
by avoiding the bat if the moth is already in flight. S. spectans
characteristically rests with its wings elevated from the surface of the cave
wall thus exposing its ears and increasing its ability to hear approaching
bats. Pavey and Burwell reported that S. spectans flying in mines
responded to the attacks of bats, as well as to the ultrasonic sounds of dog
whistles, by immediately lighting upon the walls
(Pavey and Burwell, 2005).
They, as we, did not observe any incidence of bats landing on the walls to
capture moths (i.e. gleaning) and it may be that R. megaphyllus and
M. australis infrequently, if ever, glean their prey, thus allowing
the moth enough protection to successfully co-habit with these bats.
Alternatively, R. megaphyllus, like other rhinolophids, may require
that perched prey be moving their wings
(Siemers and Ivanova, 2004) to
localize them; hearing this bat would allow S. spectans the
opportunity to remain still. The rarity of observed captures of S.
spectans by bats while in the roosts suggests that the majority of the
wings on the floors of the roosts originate from captures outside of the mines
and that little predation takes place during the day or the evening as the
moths begin to exit. The sensitivity of its ears, therefore, allows S.
spectans to monitor the presence of bats in flight and remain motionless
on the cave walls until there is a break in bat activity. Being acoustically
`pinned down' by bat echolocation calls may confer an immediate survival
advantage to these moths but may delay the evening emergence of moths and
leave some trapped inside the cave for the entire night. These predictions
could be tested by comparing the exit activity of S. spectans in day
roosts with and without co-habiting bats.
Why does S. spectans not co-habit with H. ater?
Pavey and Burwell suggested that H. ater uses the allotonic nature
of its calls as an acoustic counter-manoeuvre to increase its foraging success
on S. spectans to the point of excluding them from subterranean
roosts (Pavey and Burwell,
2005). If S. spectans could adequately hear H.
ater we would expect to find some moths co-habiting with this bat but
this is not the case (Pavey and Burwell,
2005). Although the extraordinary sensitivity of S.
spectans allows it to detect the FM portion of some of H. ater's
calls, the low percentage of calls that the moth did detect compared with
those of R. megaphyllus and M. australis, suggests that this
bat is functionally inaudible to the moth or only detectable at very short
distances. We suggest that the chance of S. spectans escaping H.
ater would depend on the distance at which the moth first hears the bat
and whether or not H. ater can glean. Some hipposiderid bats,
including Australian species, are able to glean prey from surfaces
(Bell and Fenton, 1984;
Pavey and Burwell, 2000) and
H. ater may share this trait. A gleaning H. ater would be
able to take a moth that, unable to hear the bat until late in its attack
sequence, had landed on the wall and was still moving its wings [hipposiderid
bats require movement to detect their prey
(Link et al., 1986)].
Alternatively, as mentioned above, a perched moth vibrating its wings in
preparation for flight might detect a bat homing in on it but not in time to
stop moving and deny the bat its localization cue.
What if H. ater does not glean
(Pavey and Burwell, 2000)?
Allotonic echolocation in combination with other factors that influence a
bat's dietary composition [e.g. flight ability, prey preference
(Jacobs et al., 2008)] may
explain a non-gleaning H. ater's success at capturing S.
spectans. H. ater is a small bat with a relatively high wing-aspect ratio
(Crome and Richards, 1988),
which should allow it to better negotiate the physically and acoustically
cluttered confines of its day roosts. The percentage of moths in the diet of
individuals in a population of the African hipposiderid, Hipposideros
ruber, was positively correlated with aspect ratio and wingspan
(Jones et al., 1993)
suggesting that bats with agile flight may be better suited to capture moths.
A non-gleaning H. ater could, therefore, combine flight
manoeuvrability with allotonic calls to enhance its chances of catching flying
S. spectans in the day roosts. Differences in flight manoeuvrability
may also explain why H. ater includes more moths in its diet than the
larger Hipposideros cervinus (Gould) (CF: 145 kHz) despite both using
allotonic echolocation frequencies (Pavey
and Burwell, 2000). In this respect, the moth-preference of H.
ater is of special interest as this bat may actually restrict the cave
and mine dwelling distributions of S. spectans in northern Australian
locations where H. ater and similar bats are abundant.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Bell, G. P. and Fenton. M. B. (1984). The use of Doppler-shifted echoes as a flutter detection and clutter rejection system: the echolocation and feeding behavior of Hipposideros ruber (Chiroptera: Hipposideridae). J. Comp. Physiol. A 15,109 -114.[Medline]
Churchill, S. (1998). Australian Bats. Sydney: New Holland.
Common, I. F. B. (1990). Moths of Australia. Melbourne: Melbourne University Press.
Crome, F. H. J. and Richards, G. C. (1988). Bats and gaps: microchiropteran community structure in a Queensland rainforest. Ecology 69,1960 -1969.[CrossRef]
Edmunds, M. (1974). Defence in Animals: A Survey of Antipredator Defences. New York: Longman.
Faure, P. A., Fullard, J. H. and Barclay, R. M. R. (1990). The response of tympanate moths to the echolocation calls of a substrate gleaning bat, Myotis evotis. J. Comp. Physiol. A 166,843 -849.
Faure, P. A., Fullard, J. H. and Dawson, J. W. (1993). The gleaning attacks of the northern long-eared bat, Myotis septentrionalis, are relatively inaudible to moths. J. Exp. Biol. 178,173 -189.[Abstract]
Fenton, M. B. (1982). Echolocation calls and patterns of hunting and habitat use of bats (Microchiroptera) from Chillagoe, north Queensland. Aust. J. Zool. 30,417 -425.[CrossRef]
Fenton, M. B. and Fullard, J. H. (1979). The influence of moth hearing on bat echolocation strategies. J. Comp. Physiol. 132,77 -86.[CrossRef]
Fenton, M. B., Rydell, J., Vonhof, M. J., Eklöf, J. and Lancaster, W. C. (1999). Constant-frequency and frequency-modulated components in the echolocation calls of three species of small bats (Emballonuridae, Thyropteridae, and Vespertilionidae). Can. J. Zool. 77,1891 -1900.[CrossRef]
Fenton, M. B., Bouchard, S., Vonhof, M. J. and Zigouris, J. (2001). Time-expansion and zero-crossing period meter systems present significantly different views of echolocation calls of bats. J. Mamm. 82,721 -727.[CrossRef]
Fullard, J. H. (1982). Echolocation assemblages and their effects on moth auditory systems. Can. J. Zool. 60,2572 -2576.[CrossRef]
Fullard, J. H. (1988). The tuning of moth ears. Experientia 44,423 -428.[CrossRef]
Fullard, J. H. (2006). The evolution of hearing in moths: the ears of Oenosandra boisduvalii (Noctuoidea: Oenosandridae). Aust. J. Zool. 54, 51-56.[CrossRef]
Fullard, J. H. and Thomas, D. W. (1981). Detection of certain African, insectivorous bats by sympatric tympanate moths. J. Comp. Physiol. 143,363 -368.[CrossRef]
Fullard, J. H., Dawson, J. W. and Jacobs, D. S.
(2003). Auditory encoding during the last moment of a moth's
life. J. Exp. Biol. 206,281
-294.
Fullard, J. H., Ratcliffe, J. M. and Jacobs, D. S. (2008). Ignoring the irrelevant: auditory tolerance of audible but innocuous sounds in the bat-detecting ears of moths. Naturwissenschaften 95,241 -245.[CrossRef][Medline]
Hedwig, B. (2006). Pulses, patterns and paths: neurobiology of acoustic behaviour in crickets. J. Comp. Physiol. A 192,677 -689.[CrossRef][Medline]
Horridge, G. A. (1977). Compound eye of insects. Sci. Am. 237,108 -118.[Medline]
Jacobs, D. S., Ratcliffe, J. M. and Fullard, J. H.
(2008). Beware of bats, beware of birds: the auditory responses
of eared moths to bat and bird predation. Behav. Ecol.
doi:10.1093/beheco/arn071
Jones, G. and Corben, C. (1993). Echolocation calls from six species of microchiropteran bats in southeastern Queensland. Aust. Mammal. 16,35 -38.
Jones, G., Morton, M., Hughes, P. M. and Budden, R. M. (1993). Echolocation, flight morphology and foraging strategies of some West African hipposiderid bats. J. Zool. (Lond.) 230,385 -400.
Lacki, M. J. and Ladeur, K. M. (2001). Seasonal use of lepidopteran prey by Rafinesque's big-eared bats (Corynorhinus rafinesquii). Am. Midl. Nat. 145,213 -217.[CrossRef]
Law, B. and Chidel, M. (2002). Tracks and riparian zones facilitate the use of Australian regrowth forest by insectivorous bats. J. App. Ecol. 39,605 -617.[CrossRef]
Link, A., Marimuthu, G and Neuweiler, G. (1986). Movement as a specific stimulus for prey catching behaviour in rhinolophid and hipposiderid bats. J. Comp. Physiol. A 159,403 -413.[CrossRef]
Marsat, G. and Pollack, G. S. (2006). A
behavioral role for feature detection by sensory bursts. J.
Neurosci. 26,10542
-10547.
Nabatiyan, A., Poulet, J. F. A., de Polavieja, G. G. and Hedwig,
B. (2003). Temporal pattern recognition based on
instantaneous spike rate coding in a simple auditory system. J.
Neurophysiol. 90,2484
-2493.
Nüesch, H. (1957). Die morphology des thorax von Telea polyphemus Cr. (Lepid.). II. Nervensystem. Zool. Jahr. (Anat.) 75,615 -642.
Pavey, C. R. and Burwell, C. J. (1998). Bat predation on eared moths: a test of the allotonic frequency hypothesis. Oikos 81,143 -151.[CrossRef]
Pavey, C. R. and Burwell, C. J. (2000). Foraging ecology of three species of hipposiderid bats in tropical rainforest in north-east Australia. Wildl. Res. 27,283 -287.[CrossRef]
Pavey, C. R. and Burwell, C. J. (2004). Foraging ecology of the horseshoe bat, Rhinolophus megaphyllus (Rhinolophidae), in eastern Australia. Wildl. Res. 31,403 -413.[CrossRef]
Pavey, C. R. and Burwell, C. J. (2005). Cohabitation and predation by insectivorous bats on eared moths in subterranean roosts. J. Zool. 265,141 -146.[CrossRef]
Pavey, C. R., Burwell, C. J. and Milne, D. J. (2006). The relationship between echolocation call frequency and moth predation of a tropical bat fauna. Can. J. Zool. 84,425 -433.[CrossRef]
Reinhold, L., Law, B., Ford, G. and Pennay, M. (2001). Key to the bat calls of south-eat Queensland and north-east New South Wales. Forest Ecosystem Research and Assessment technical paper #2001-07. Department of Natural Resources and Mines, Queensland.
Rhodes, M. P. (2002). Assessment of sources of variance and patterns of overlap in microchiropteran wing morphology in southeast Queensland, Australia. Can. J. Zool. 80,450 -460.[CrossRef]
Roeder, K. D. (1964). Aspects of the noctuid tympanic nerve response having significance in the avoidance of bats. J. Insect Physiol. 10,529 -546.[CrossRef]
Roeder, K. D. (1967). Nerve Cells and Insect Behavior. Cambridge, MA: Harvard University Press.
Roeder, K. D. (1974). Acoustic sensory responses and possible bat-evasion tactics of certain moths. In Proceedings of the Canadian Society of Zoologists Annual Meeting: June 2-5 (ed. M. D. B. Burt), pp. 71-78. Frederick: University New Brunswick Press.
Roeder, K. D. and Fenton, M. B. (1973). Acoustic responsiveness of Scoliopteryx libatrix L. (Lepidoptera: Noctuidae), a moth that shares hibernacula with some insectivorous bats. Can. J. Zool. 51,681 -685.[CrossRef]
Siemers, B. M. and Ivanova, T. (2004). Ground gleaning in horseshoe bats: comparative evidence from Rhinolophus blasii, R. euryale and R. mehelyi. Behav. Ecol. Sociobiol. 56,464 -471.
Soutar, A. and Fullard, J. H. (2004). Nocturnal
anti-predator adaptations in eared and earless Nearctic Lepidoptera.
Behav. Ecol. 15,1016
-1022.
Stapells, D. R., Picton, T. W. and Smith, A. D. (1982). Normal hearing thresholds for clicks. J. Acoust. Soc. Am. 72,74 -79.[CrossRef][Medline]
Surlykke, A. and Fullard, J. H. (1989). Hearing in the Australian whistling moth, Hecatesia thyridion.Naturwissenschaften 76,132 -134.[CrossRef]
Surlykke, A., Filskov, M., Fullard, J. H. and Forrest, E. (1999). Auditory relationships to size in noctuid moths: bigger is better. Naturwissenschaften 86,238 -241.[CrossRef]
van Dyck, S. M. and Strahan, R. (2008).The Mammals of Australia. 3rd edn. Sydney: Reed New Holland.
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