The adaptive function of tiger moth clicks against echolocating bats: an experimental and synthetic approach
Department of Zoology, University of Toronto at Mississauga, Toronto, Ontario, M5S 3G5, Canada
* Author for correspondence at present address: Department of Neurobiology and Behavior, Cornell University, Seeley G. Mudd Hall, Ithaca, NY 14853, USA (e-mail: jmr247{at}cornell.edu)
Accepted 12 October 2005
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Summary |
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Key words: aposematism, echolocation, Chiroptera, Arctiidae, coevolution, Myotis septentrionalis, Cycnia tenera
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Introduction |
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The clicks of arctiid moths have been proposed to function as acoustic
aposematic signals (Blest et al.,
1963; Dunning and Roeder,
1965
; Dunning,
1968
; Hristov and Conner,
2005a
) and as signals that interfere with information processing
facilitating escape, by startling the bat (deimatism) and/or jamming
echolocation (Bates and Fenton,
1990
; Fullard et al.,
1979
,
1994
;
Miller, 1991
;
Masters and Raver, 1996
;
Tougaard et al., 1998
,
2004
). These functional
hypotheses are not mutually exclusive although they are often portrayed as
such (e.g. Surlykke and Miller,
1985
; Fullard et al.,
1994
; Waters,
2003
; Hristov and Miller, 2005a). Until recently
(Hristov and Conner, 2005a
),
all laboratory studies had used (1) synthetic bat echolocation calls and
stationary moths, (2) synthetic arctiid clicks and stationary bats or (3)
free-flying bats capturing mealworms while synthetic clicks were broadcast
>1 m away from the prey trajectory (see
Waters, 2003
and
Hristov and Conner, 2005a
for
a review). In field studies (e.g. Dunning
et al., 1992
; Acharya and
Fenton, 1992
), predation on intact and muted arctiid moths has
been compared, but the sounds intact moths presumably produce were not
monitored and the numbers of bats sampled could not be accurately
determined.
The two dominant foraging strategies used by echolocating predatory bats
are substrate gleaning (taking prey from surfaces) and aerial hawking (taking
airborne prey) (Bell, 1982;
Norberg and Rayner, 1987
;
Arlettaz et al., 2001
). In
contrast to hawking, during substrate gleaning attacks bats attempt to capture
stationary or slow-moving prey from the ground, foliage or tree trunks and
bats should, arguably, have more opportunity to assess potential non-auditory
prey cues. To our knowledge, no study has investigated the efficacy of arctiid
clicks as defence against the gleaning attacks of bats.
The northern long-eared bat, Myotis septentrionalis, and the
sympatric dogbane tiger moth, Cycnia tenera, are good models for
investigating the influence of foraging strategy and signal design on
battiger-moth interactions. Brack and Whitaker
(2001) found that four wild
populations of M. septentrionalis fed predominantly on Lepidoptera.
Ecomorphology, flight behaviour and echolocation call design demonstrate that
M. septentrionalis is well adapted for both aerial hawking and
gleaning prey (Ratcliffe and Dawson,
2003
). Preferred foraging habitat and the presence of non-volant
arthropods in their diet suggests that M. septentrionalis gleans in
the wild (Brack and Whitaker,
2001
), while open field and over-water recordings of M.
septentrionalis echolocation attack sequences indicate aerial hawking
(Miller and Treat, 1993
; M. B.
Fenton, personal communication). C. tenera is active day and night
(Fullard and Napoleone, 2001
)
and has both conspicuous colouration and sound-producing tymbals
(Fullard and Fenton, 1977
).
This species sequesters and/or synthesizes a number of defensive chemical
compounds (Cohen and Brower,
1983
; Weller et al.,
1999
; Nishida,
2002
; Hristov and Conner,
2005b
); captive M. septentrionalis do not eat C.
tenera when presented together with non-arctiid moths (J.M.R. and J.H.F.,
unpublished data).
Our purpose was to determine which of C. tenera's putative
multiple sensory warning signals would be effective deterrents against M.
septentrionalis during aerial hawking and gleaning attacks. We predicted
that during all attacks M. septentrionalis would not use visual or
other non-acoustic signals prior to contact with C. tenera due to the
relatively reduced size of the visual and olfactory systems in myotid bats
(Bhatnagar, 1975). We did not
expect C. tenera to produce sounds in response to a gleaning attack
because the ears of C. tenera are less sensitive to sympatric bat
echolocation calls than those of catocaline (family Noctuidae) moths
(Fullard and Dawson, 1999
), to
which the gleaning attacks of M. septentrionalis are inaudible
(Faure et al., 1993
).
Therefore, we predicted that gleaning M. septentrionalis would attack
and contact both muted and intact C. tenera. We predicted that during
aerial hawking attacks the bats would use acoustic cues when available,
aborting attacks on intact C. tenera in response to the moth's
clicks. We expected that attacks on muted C. tenera would result in
contact with the moth. We also expected that C. tenera would be
unpalatable to the bats and that during gleaning and hawking trials intact and
muted C. tenera would be rejected rather than consumed.
In spite of the >40 years that scientists have investigated the acoustic
interactions between arctiid moths and bats, there has never been a documented
recording of the sounds emitted by these animals during an actual attack.
Based on reported click emission rates to a big brown bat (Eptesicus
fuscus) aerial hawking attack echolocation call sequence
(Fullard et al., 1994) and the
critical time window for degrading echolocation ranging ability
(Miller, 1991
), we predicted
that (1) the clicks of C. tenera would affect the echolocation
behaviour of M. septentrionalis, as revealed by increased time
between calls, and (2) at least some click modulation cycles would coincide
with echolocation calls in our recordings and thus provide indirect support
for the jamming hypothesis (Miller,
1991
; Tougaard et al.,
1998
,
2004
). The existence of
studies that support both jamming and aposematism implies that an `either/or'
approach to the function of arctiid clicks is incorrect and so we propose a
synthesis of the role that these unique sounds play in the defence of these
insects.
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Materials and methods |
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Dogbane tiger moths Cycnia tenera Hübner, were reared from eggs collected from wild specimens captured at QUBS during the summer of 2003, raised to pupae on milkweed and dogbane (Apocynum androsaemifolium and A. cannabinum, respectively) and stored in constant temperature rooms at 4°C with a 12 h:12 h light:dark photoperiod for approximately 78 months at the University of Toronto at Mississauga. Pupae were then transferred to constant temperature rooms at 25°C with a 16 h:8 h light:dark photoperiod at QUBS, and adults emerged 23 weeks later. Adults were allowed to mature for 2472 h. Of 113 individuals successfully reared, 37 were used as prey. Eleven more C. tenera were caught as adults from nearby fields (day) and light traps (night) during the summer of 2004.
The tymbals (modified metathoracic episterna) of 24 of the 48 C.
tenera used as prey in experiments were ablated under a dissecting
microscope using an insect pin. For ablation, moths were first cooled for 10
min in a refrigerator and then held by their wings using flat tweezers. Before
and after tymbal ablation, moths were stroked gently with a small brush over a
Holgate ultrasonic heterodyne detector tuned to 50 kHz, representing the peak
frequencies of the clicks (Fullard and
Dawson, 1999), to ensure moths had been completely muted. Intact
moths that did not respond to tactile stimulation (7) and moths that were
improperly ablated (18) were not used. We also tested for sound production in
all 48 C. tenera used in this study immediately before and after each
moth interacted with a bat (except in one instance when the moth was not
recovered).
All other moths used in this study were captured nightly from light traps
(mercury vapour incandescent and ultraviolet fluorescent) positioned around
QUBS. Moths were identified to family using criteria in Ward et al.
(1974), Covell
(1984
) and Riotte
(1992
). Some of the moth
species used for experiments (families Arctiidae, Noctuidae, Notodontidae,
Lymantriidae and Geometridae) had ears while others (family Lasiocampidae)
were earless (Fullard and Napoleone,
2001
). All moths used, including C. tenera, had a body
length of 1.52.5 cm and, for gleaning trials, were kept at
510°C until presented to the bats.
Flight room and experimental design
Experiments one and two were run in a large, screened (ceiling and roof)
flight room (9.14x3.66x3.66 m, length x width x
height; see Fig. 1 in Ratcliffe and
Dawson, 2003) built in a small glade within a mixed temperate
forest (canopy intact), mimicking a cluttered habitat where the only light
available was that from the moon and stars. Experiments were run two weeks
after the emergence of adult C. tenera in the wild
(Ward et al., 1974
; J.M.R.,
personal observation). Bats were observed using an infrared-sensitive night
vision scope with a built-in infrared LED light source (Night Owl Explorer
NOCX3; JNL Trading Company, Aurora, IL, USA). We released individual M.
septentrionalis into the flight room and presented each bat with 10 live
moths positioned on substrate or tethered (described below) to simulate
foraging conditions, demanding substrate gleaning or aerial hawking,
respectively. One trial entailed one presentation of a single moth followed by
an attempt at capture (Ratcliffe and
Dawson, 2003
). To control for possible ordering effects within and
between subjects, moths were presented to each bat in pseudorandomized order
such that C. tenera of the same sound-producing class (intact or
muted) were never presented one after another and such that no more than two
C. tenera were presented in unbroken sequence. For each successive
trial, moths were placed at different positions on the trellis for gleaning
trials and at slightly different heights and distances from the long walls of
the flight room when tethered. Bats were hand-fed three mealworms before being
introduced to the flight room to ensure they were ready to eat while at the
same time not starving. After having hunted in the flight room, bats were fed
to satiation and released at point of capture.
High-frequency sound recording
Call sequences emitted during foraging trials were recorded using two D 980
Ultrasound Detectors (Pettersson Elektronik AB, Uppsala, Sweden) using the
high-frequency output. The D 980 (hereafter `the microphone') output was
passed through a F2000 Control/Filter Unit (Pettersson Elektronik AB) with
gain set to `low' before input to a computer (Dell Notebook C800, Pentium III
800 MHz processor, 512 MB RAM) using a DAQCard-6062E (National Instruments,
Austin, TX, USA) as interface. Data were stored as .wav files using BatSound
Pro v. 3.30 (Pettersson Elektronik AB) software in high-speed sampling mode
(500 kHz sampling frequency, circular buffer, 10-second storage time, 150 kHz
external anti-aliasing filter).
Experiment one: gleaning trials
Six M. septentrionalis, 24 C. tenera (12 intact, 12
muted) and 36 non-arctiid moths served as subjects in experiment one. These
animals did not serve as subjects in experiment two. Myotis
septentrionalis were introduced individually into the flight room and
presented with a moth on substrate. The gleaning substrate was a trellis
(1x1.5 m, width x height) covered with matt black canvas to
maximize contrast between C. tenera and background. During trials (10
trials per bat), the bat was allowed to fly and perch freely in the room. At
the beginning of the trial, the moth was not placed into position until the
bat was either perched at one end of the room or was flying at one end of the
room away from the moth's ultimate position. Between trials, we varied the
position of the moth at one of five almost equidistant screen windows
fashioned into the canvas (each 3 cm2, 30 cm apart). A
microphone was positioned 10 cm behind this screen window. For M.
septentrionalis, fluttering sounds are necessary for the detection of
perched moths (Ratcliffe and Dawson,
2003
). Therefore, we held a second moth between the microphone and
the trellis such that one fluttered against the screening. Moths used as lures
included arctiid moths.
Experiment two: aerial hawking trials
An additional six M. septentrionalis, 24 C. tenera (12
intact, 12 muted) and 36 non-arctiid moths served as subjects in experiment
two. M. septentrionalis were introduced individually into the flight
room and presented with a live moth that was tethered (for details and diagram
of set-up, see Ratcliffe and Dawson,
2003). Most moths, but never C. tenera, were tethered
approximately in the centre of the flight room (within 1 m to the right and
left of centre) to the end of a 0.2 mm-diameter black cotton thread, 12
m long, by passing a threaded sewing needle through the anterior portion of
the abdomen. The thread, which was unknotted, extended on average 1 cm below
the moth's body. All C. tenera and eight of the non-arctiid moths
were attached to this same thread using a drop of beeswax on the centre of the
dorsal thorax rather than by passing a needle through their abdomen.
Moths flew vigorously within the limits of the thread and frequently
changed direction and altitude. During trials (10 trials per bat), the bat was
allowed to fly and perch freely in the room. At the beginning of the trial,
the moth was tethered but not placed into position until the bat was either
perched at one end of the room or was flying at one end of the room away from
the moth's ultimate position. The moth was then hoisted into position,
allowing the bat to discover and interact with it. Based on a previous study
(Ratcliffe and Dawson, 2003),
we predicted that M. septentrionalis would typically initiate its
aerial attacks from the back of the room and fly towards our position at the
front of the room. Accordingly, we positioned one microphone approximately 1 m
in front of and 50 cm below the tail of the tether's resting position and
another microphone 50 cm to the side of and 50 cm below the tail of the
tether, near to the closest wall.
For both gleaning and aerial-hawking trials, bats typically attacked moths well within 30 s of being made available. However, bats would sometimes roost for several minutes after a trial. When this happened, we would leave the flight room for approximately 20 min; upon returning we found the bats once again ready to hunt. For gleaning trials, the maximum distance from the bat (if at the back wall) to the moth was approximately 8 m; for aerial hawking trials, this distance was never more than 5 m.
Sound analysis
Using BatSound Pro v. 3.30, we high-pass filtered .wav files at 12 kHz
(filter type, Butterworth; filter order, 8). We analyzed one echolocation call
sequence (from first visually discernible search phase call through to calls
emitted after completing or aborting attack) for each moth class for each
foraging condition for each bat; sequences were selected on the basis of the
quality of the sound recordings (i.e. high signal-to-noise ratio). We measured
onset and duration of echolocation calls and tymbal click cycles using the
oscillograms (while referencing the spectrograms for aberrations). For
gleaning trials, we also measured time elapsed from last call emitted (or
recorded) to the bat's initial contact with substrate from spectrograms and
oscillograms (the bat hitting the trellis produced sound more intense than
either fluttering moth wings or an echolocation call). We used these data to
calculate period and duty cycle of echolocation sequences and the timing of
tymbal clicks with respect to period and duty cycle.
Statistical analysis
For both gleaning and aerial hawking trial data, we ran approximate
randomization tests (Noreen,
1989; 1000 shuffles per test) to identify potential relationships
between three moth classes (intact C. tenera, muted C.
tenera and non-arctiid moth) and three attack classes (aborted attack;
moth attacked but left undamaged; moth attacked and mortally injured/killed).
Approximate randomization tests were conducted using a custom program (written
in Visual Basic). This distribution-free analysis, aside from being free of
the assumptions of conventional statistics (e.g. data need not constitute a
random sample), is more powerful than the chi-squared test because unexpected
departures from the null model can be distinguished from expected departures,
and it does not assume that such departures are normally distributed
(Noreen, 1989
). A positive
test statistic refers to the number of cases (e.g. moth class/condition class)
that deviated from expectations under the null hypothesis (equal distribution
of moth classes among condition classes) in the direction expected under the
alternative hypothesis: the larger the value of the test statistic the
stronger the evidence for this departure
(Noreen, 1989
). The P
value then refers to the percentage of shuffles for which the test statistic
for the shuffled data was as large or larger than the original test statistic
(Noreen, 1989
).
For echolocation sequences of aerial attacks on intact C. tenera,
we ran a repeated-measures ANOVA using SPSS/PC 12 to compare call
period for the two calls preceding the first C. tenera click, the
call period during which the first click was recorded and the subsequent call
period (where clicks were never detected). We also determined whether the
first complete tymbal modulation cycle coincided with an echolocation call and
whether subsequent modulation cycles coincided with echolocation calls before
the bat aborted or completed its attack (i.e. contacted the moth). Calls
produced with greater than 50 ms between calls are designated as `search
phase' calls; calls with less than 50 ms but more than 10 ms between them are
designated as `approach phase' calls; calls with less than 10 ms between them
are designated as `buzz phase' calls
(Griffin et al., 1960).
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Results |
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The bats ate all 36 non-arctiid moths (i.e. mortally injured/killed). Eleven of the 12 muted C. tenera were rejected: seven were mortally injured/killed, four were undamaged. Although we never observed any bat eating C. tenera, we were unable to locate one muted moth after the attack (this moth was scored as mortally injured/killed). All of the 12 intact C. tenera were rejected: five were mortally injured, seven were undamaged. The bats killed significantly fewer C. tenera than non-arctiid moths (N=60; test statistic=32.6, P<0.001), but intact C. tenera did not have significantly lower mortality rates than muted C. tenera (N=24; test statistic=3.6, P=0.20). These results show that M. septentrionalis differentiated C. tenera from non-arctiid moths based on chemical cues. See Table 1 for percentage breakdown of these results.
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Sound analysis
All intact C. tenera produced sounds detected by our microphone
when handled by the bats; none produced sounds prior to contact with the bats
(Fig. 1).
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The bats never ate C. tenera (muted or intact), and three of the four intact moths and eight of the 11 muted moths were alive and presumably reproductively viable (i.e. wings and body intact, still able to fly and produce clicks) after the bats' attacks. The remaining four C. tenera had crushed body parts and/or were missing wings (or were simply dead). The bats killed significantly fewer C. tenera than non-arctiid moths (N=60; test statistic=51.2, P<0.001). The bats made contact with significantly fewer intact C. tenera than muted C. tenera (N=24; test statistic=11.6, P<0.003), but for those contacted, intact C. tenera did not have significantly lower mortality rates than muted C. tenera (N=15; test statistic=0.6, P=0.77). These results suggest that after capture, the chemical defences, but not the tymbal clicks, of C. tenera are at least partially effective against bats. See Table 1 for percentage breakdown of these results.
Sound analysis
We were confident, based on the position of the moth with respect to the
microphones, that we would have detected most, if not all, of the clicks
produced by the intact C. tenera for at least one of the two trials
recorded for each bat. Visual inspection of spectrograms and oscillograms
supported this impression. For these six trials, intact C. tenera
never produced clicks until the bats had switched from producing search phase
calls (call period >50 ms) to approach phase calls (mean call period, 31.6
ms; range, 643.3 ms; Figs
2,
3,
4,
5).
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The bats paused significantly longer between calls at the onset of the first click: the call period immediately before and following the period in which the first click fell was significantly lower (repeated-measures ANOVA; N=6, F=8.87, P=0.006; Fig. 2). The first tymbal modulation cycle produced overlapped with an echolocation call in only one of six attacks, but at least one complete tymbal modulation cycle (and as many as three) overlapped with echolocation calls produced during attack for five of six trials analyzed.
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Discussion |
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Gleaning
As predicted, during gleaning attacks C. tenera did not produce
clicks in response to echolocation call sequences of M.
septentrionalis but did produce clicks upon tactile stimulation (i.e.
handling by bat). The short-duration, low-intensity, broad-bandwidth,
high-frequency calls used by gleaning M. septentrionalis
(Faure et al., 1993;
Ratcliffe and Dawson, 2003
)
are inaudible to the ears of the most sensitive sympatric noctuid moths
(Faure et al., 1993
) and would
therefore be unheard by the less-sensitive ears of C. tenera
(Fullard and Dawson, 1999
). We
suggest that calls with these features serve at least two adaptive functions:
(1) to discriminate prey from background clutter, by reducing call-echo
overlap (Schnitzler and Kalko,
2001
), reducing self deafening
(Fenton et al., 1995
) and
increasing resolution (Ratcliffe and
Dawson, 2003
; Siemers and
Schnitzler, 2004
), and (2) for undetected approach leading to
capture of eared prey from substrate
(Faure et al., 1993
;
Fenton and Ratcliffe, 2004
;
present study). Gleaning attacks may be an insurmountable problem for moths
and, perhaps, most substrate-bound prey, palatable or not
(Faure et al., 1993
).
Aerial hawking
As predicted, intact, sound-producing C. tenera were attacked
significantly less than muted C. tenera, supporting the hypothesis
that clicks serve a defensive function against aerial hawking bats not served
by other sensory cues. Our results support earlier reports that C.
tenera clicks in response to echolocation calls at intensities greater
than those required for detection at the sensory level
(Fullard, 1979;
Fullard and Dawson, 1999
). For
echolocation calls within C. tenera's range of frequency sensitivity,
we suggest that thresholds for call intensity at the moth's ear
(Fullard, 1984
;
Fullard and Dawson, 1999
) and
call period (mean, 31.6 ms; range, 643.3 ms;present study) must both be
crossed to elicit defensive clicking behaviour. This is corroborated by data
from gleaning trials: pulse rate had exceeded required threshold but call
intensity at the moth's ear had presumably not
(Faure et al., 1993
;
Fig. 1). During aerial hawking
attacks, our results indicate that C. tenera first produces clicks in
response to close-range approach-phase calls of actual attacking bats: bats
that are a very real threat to the moth.
Based on observed changes in call emission, wing gait and flight speed,
Wilson and Moss (2004) suggest
that aerial hawking M. septentrionalis generate a motor plan for prey
capture approximately 400 ms before contact with prey. Wilson and Moss
(2004
) also found an
approximately 25-ms pause between the last buzz call and contact with prey. In
the context of these results and our own, C. tenera appears to click
at approximately the same moment as the bat decides to attack it. Therefore,
clicks are not produced until approximately the same time as an attack has
been initiated, a characteristic atypical of most aposematic signals, which
are continuously displayed (e.g. brightly coloured and contrasting wings of
monarch butterflies, the persistent buzz of the wings of wasps and bees;
Edmunds, 1974
;
Ruxton et al., 2005
). However,
from the perspective of the predator, non-continuous prey-generated cues can
be timed to act as deimatic and/or aposematic signals so long as there is
still time available for the attack to be aborted
(Edmunds, 1974
;
Endler, 1991
).
C. tenera clicks are within the same frequency spectrum as the
ultrasonic echolocation calls of sympatric bats
(Fullard and Fenton, 1977) and
should be easily detected by bats against almost non-existent background noise
at these frequencies (estimated from spectrograms). The change in echolocation
call emission upon the onset of the clicks indicates that the bats did notice
these sounds. While overlap between call and click was not necessary to
influence call emission rate (i.e. first clicks produced overlapped with an
echolocation call in only one of six attacks), for five of the six aerial
attack sequences analyzed, one complete tymbal modulation cycle, and as many
as three, overlapped with echolocation calls. Given that, within a modulation
cycle, clicks are produced, on average, once every 1.3 ms (14 clicks
cycle1; mean cycle length, 18 ms;
Fullard and Fenton, 1977
;
present study), clicks would have fallen within the window required for
degrading accuracy in echolocation range discrimination
(Miller, 1991
;
Masters and Raver, 1996
;
Tougaard et al., 1998
,
2004
) at least once during
five of the six attacks analyzed. Therefore, our results suggest that the
clicks of C. tenera may indeed interfere with bat echolocation and
result in target-ranging miscalculations in the wild. Further, even without
synchronization, clicks might degrade attack accuracy simply by forcing the
bats to process two streams of information concurrently
(Barber et al., 2003
).
Recently, Hristov and Conner
(2005a), using naïve bats
in the laboratory, supported an aposematic function for C. tenera
clicks against aerial hawking attacks by Eptesicus fuscus and
suggested that the major impetus behind the evolution of arctiid clicks was to
serve as a warning of unpalatability. However, Hristov and Conner's results
also suggest a nonaposematic function of clicking: 20% of attacks on clicking
but not chemically defended tiger moths were repeatedly terminated by
naïve bats (i.e. bats that had never experienced a noxious tiger moth)
(see figs 1 and 2 in Hristov and Conner,
2005a
). Further, although laboratory results suggest that bats
habituate to the putatively startling effect of arctiid moth clicks
(Miller, 1991
;
Bates and Fenton, 1990
;
Hristov and Conner, 2005a
),
habituation and extinction rate is affected by time elapsed between successive
exposures and context, both of which vary dramatically in the wild but tend to
be uniform in the laboratory
(Shettleworth, 1998
). Evidence
that habituation occurs under controlled conditions is thus not sufficient to
posit that flying, hunting bats habituate to arctiid clicks in the wild.
Therefore, under natural conditions we assert that the clicks of the dogbane
tiger moth, C. tenera, are alone aversive signals to echolocating
bats.
Delineating startle, jamming and warning into three distinct
characteristics does not accurately describe either the ultimate or proximate
functions of these signals. Summers and Clough
(2001), using phylogenetically
independent contrasts, found that in poison frogs (Dendrobatidae)
conspicuousness and toxicity are positively correlated. In C. tenera,
we hypothesize that a similar parallel process shaped both signal and
secondary chemical defence. Furthermore, given the proposed negative qualities
of C. tenera clicks on echoic information processing
(Miller, 1991
; Fullard et al.,
1979
,
1994
; Tougaard et al.,
1998
,
2004
) in bats (as a result of
affecting echolocation behaviour when first produced and overlapping
temporally with calls during most aerial hawking attacks), these signals are
not only conspicuous and possibly reliable indicators of further defence
(sensu Sherratt,
2002
; Sherratt and Beatty,
2003
) but also especially effective signals of negative
consequences in particular (sensu
Etscorn, 1973
).
Synthesis
Warning signals function by informing potential predators that the sender
is unprofitable as prey (Servedio,
2000; Summers and Clough,
2001
; Sherratt,
2002
). During the aerial hawking attacks of insectivorous
echolocating bats, tiger moth tymbal clicking is of considerable survival
value (i.e. bats abort attacks), while visual and chemical cues are not
effective in deterring the predator before contact. During aerial hawking
attacks, the clicks of C. tenera are effective warning signals
(Hristov and Conner, 2005a
).
However, aposematism is a phenomenon typically defined by an always
conspicuous, but harmless cue (warning) and a negative consequence (defence)
(Edmunds, 1974
;
Servedio, 2000
;
Speed, 2000
;
Summers and Clough, 2001
;
Ruxton et al., 2005
).
We have demonstrated that C. tenera clicks are produced only when
attack is imminent or underway and serve as both defence in and of themselves
(as argued above) and as warning of further defence (Hristov and Miller,
2005a). Clicks are, in these respects, more analogous to the bitter and/or
sour flavours of plants containing even more toxic compounds
(Etscorn, 1973;
Chambers, 1990
;
Cipollini and Levey, 1997
;
Ratcliffe et al., 2003
) than
to the bright but benign colours and patterns of defended or mimetic animals
(Schuler and Hesse, 1985
;
Roper and Redston, 1987
). We
predict that for aerial-hawking echolocating bats, these acoustic signals are
more readily associated with unpalatability than visual and/or olfactory
signals and, more than this, that dogbane tiger moth clicks are more readily
associated with unpalatability than would be equally detectable, but otherwise
undisruptive, acoustic signals.
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Acknowledgments |
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References |
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