Her odours make him deaf: crossmodal modulation of olfaction and hearing in a male moth
1 Department of Ecology, Lund University, SE-223 62 Lund, Sweden,
2 Department of Crop Science, Swedish University of Agricultural Sciences,
SE-230 53, Alnarp, Sweden
3 Center for Sound Communication, Institute of Biology, University of
Southern Denmark, DK-5230 Odense M, Denmark
* Author for correspondence at present address: Center for Sound Communication, Institute of Biology, University of Southern Denmark, DK-5230 Odense M, Denmark (e-mail: niels.skals{at}biology.sdu.dk)
Accepted 22 November 2004
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Summary |
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Key words: hearing in moth, moth olfaction, trade-off, sensory conflict, predation risk, crossmodal integration
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Introduction |
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At night male moths get aroused by long distance attractant sex pheromones
released by conspecific females, and will initiate flight and orient into the
pheromone plume (see review by Hansson,
1995). In a zigzagging flight pattern he will locate the calling
female, land and together they will initiate mating behaviour. The composition
of the pheromone blend as well as the amount is important for the mate finding
behaviour in male moths (Linn et al.,
1987
).
Nocturnal activity of moths is associated with the risk of predation by
echolocating insectivorous bats. Aerial hawking bats detect nocturnal insects
on the wing (Neuweiler, 1989),
while gleaning bats catch insects on the substrate
(Arlettaz et al., 2001
).
Gleaning bats may constitute about a third of all insectivorous species and
are especially common in tropic regions
(Arlettaz et al., 2001
). Moths
have evolved ears sensitive to bat cries and a repertoire of evasive
manoeuvres adapted to evade attacking bats
(Roeder, 1967
;
Miller and Surlykke, 2001
).
Airborne moths react to bat sound by diving towards the ground or steering
away from the bat. Non-aerial moths running on surfaces react by freezing all
movement (Werner, 1981
;
Greenfield and Weber, 2000
;
Jones et al., 2002
), since
this will protect them from detection by gleaners. Other defensive responses
to gleaning bats include falling silent in acoustic signalling insect species
(Belwood and Moris, 1987
;
Bailey and Haythornthwaite,
1998
; Jones et al.,
2002
; Greenfield and Baker,
2003
). Evasive manoeuvres and other anti-predator tactics, such as
`freezing', involve a cost in the form of reduced mating opportunities.
Despite countless studies of either modality (olfaction and hearing) in moths
very few studies have focused on how moths deal with simultaneously exposure
to sex odours from potential mates and predator sounds, although this often
occurs in nature. Exceptions from this are the studies by Baker and
Cardé (1977
), and
Acharya and McNeil (1998
),
which show that moth sexual behaviours associated with pheromone release, and
detection can be disrupted by ultrasound stimulation. However, they
(Baker and Cardé, 1977
;
Acharya and McNeil, 1998
) only
manipulated predation risk and did not investigate potential trade-off
mechanisms, which may occur when a moth receives incompatible sensory input.
In this study we manipulated both predation risk and the quality and quantity
of the pheromone to examine the hypothesis that moths will make a trade-off
between mating and predator avoidance, based on the relative intensity of the
two sensory inputs. The alternative hypothesis suggests that a moth should
respond to a predator cue every time it exceeds the hearing threshold. As a
model species we chose the noctuid moth, Spodoptera littoralis, since
the sex pheromone compounds are identified
(Kehat and Dunkelblum, 1993
),
and ultrasonic hearing in noctuids in general is well described. Noctuoid
moths have a pair of tympanic ears located dorsolateral on the thorax. Each
ear contains only two sensory cells
(Ghiradella, 1971
;
Surlykke and Miller, 1982
). We
discuss the ecological relevance of bimodal integration in moths.
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Materials and methods |
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Neurophysiology
Individual audiograms of male moths were determined by extracellular
recording of nervous activity in the tympanic nerve when the moth ears were
exposed to sound at different frequencies. The moths were processed 1-2 days
after emerging. The tympanic nerve was exposed using a dorsal approach and
hooked onto a tungsten electrode. The preparation was placed 40 cm from the
loudspeaker. Tympanic nerve activity was bandpass filtered, amplified (custom
built equipment) and displayed on an oscilloscope and through an audio
monitor. Sound stimuli were 10 ms long pulses with a rise/fall time of 0.5 ms
repeated at 1 Hz. Threshold was defined as the sound pressure level (SPL) that
evoked at least 1-2 spikes in at least eight out of ten stimulations. The
hearing sensitivity was tested randomly in 5-10 kHz steps in the frequency
range from 5 to 125 kHz.
The acoustic pulses were generated with an oscillator (Wavetek model 186;
San Diego, CA, USA) controlled by a custom-built pulse generator that gave
shaped pulses with linear rise and fall times. The stimulus was amplified
(Xelex; Stockholm, Sweden) and broadcast through a tweeter (Technics EAS 10
TH400B; Secaucus, NJ, USA). The loudspeaker was calibrated before and after
the experiments by means of a inch microphone (G.R.A.S., Nærum,
Denmark) (with grid off) that was calibrated against a G.R.A.S. sound
calibrator (type 42AB).
The walking bioassay
Experiments were conducted in an open arena olfactometer (63 cm x 75
cm) (Schlyter et al., 1995) at
17-18°C. Air was pushed in through a baffle with spaced 2 mm holes. An
exhaust at the other end sucked out the odour-contaminated air. The
push-exhaust system created laminar airflow above the arena floor as
visualised with TiCl4 smoke. As a stimulus, 10 µl of a pheromone
solution was applied to a filter paper and placed upwind at the centre of the
arena 2 cm in front of the baffle and close to the table surface. Filter
papers were used for a maximum of 20 min. In the walking bioassay the moth
moves at relatively slow speed in a narrow path, which facilitates control of
the sound intensity at the moth's position. A male released downwind in the
olfactometer starts wing fanning upon detection of pheromone and walks toward
the pheromone source. [Anderson et al.
(2003
) compare walking and
flying moths, and find that their behavioural response to pheromone is
comparable.] Approximately halfway between the odour source and the release
site the moth was stimulated with bat-like ultrasound from a loudspeaker. A
walking moth responds to ultrasound by `freezing' and remaining stationary for
some time (see also Werner,
1981
; Rydell et al.,
2000
; Greenfield and Weber,
2000
). Moths were presented with sound stimuli of different
intensities and the behavioural thresholds to sound stimuli were determined at
different pheromone qualities and quantities.
Odour sources
The following chemical stimuli were used. Female extract: glands from
2-day-old virgin females were dissected 2 h into the scotophase and extracted
with hexane. One female equivalent (1FE) corresponds to the amount of
pheromone from one gland, which was analysed to be approximately 20 ng of the
major component. Major component: (Z9, E11)-tetradecadienyl
acetate (Z9E11-14:OAc) in 20 ng and 100 ng solutions. Two-component blend
[Z9E11-14:OAc and (Z9, E12)-tetradecadienyl acetate
(Z9E12-14:OAc)] in the proportions of 99.5:0.5 ng. This blend was previously
shown to be highly attractive to the species in the field
(Kehat and Dunkelblum,
1993).
Sound stimulus
The sound stimulus was a pulse train consisting of 20 pulses (4.7 ms long
with a carrier frequency of 30 kHz) with a repetition rate of 23 pulses
s-1. This stimulus elicited a consistent behavioural response. 30
kHz was chosen because it is within the moths' best frequency of hearing
(Fig. 1) and since many bats,
including gleaners, emit echolocation signals including 30 kHz. The temporal
structure of our stimuli corresponds roughly to the search phase of many bats
(Faure et al., 1993;
Neuweiler, 1990
;
Waters and Jones, 1995
).
Furthermore, these stimulus parameters evoke maximum silencing response in the
acoustic signalling moth, A. grisella
(Greenfield and Baker, 2003
).
The stimulus was produced by multiplying signals from a pulse generator
(Berkeley Nucleonics Corporation 555, San Rafael, CA, USA) and a sine wave
generator (Agilent 33120A, Palo Alto, CA, USA) in a custom-built trapeze
modulator. The signal was attenuated (Kay 865 step attenuator, Lincoln Park,
NJ, USA), amplified (UltraSoundAdvice S55A, London, UK) and broadcast through
an electrostatic loudspeaker (UltraSoundAdvice S56). The loudspeaker was
positioned close to the ground almost perpendicular to the moths' path between
release point and pheromone source 25 cm downwind from the pheromone source.
The intensity of the sound was measured by a
inch microphone
(G.R.A.S., Nærum, Denmark) (with grid off) that was calibrated against a
G.R.A.S. sound calibrator (type 42AB). The sound pressure was measured at
several points in front of the loudspeaker at the floor level. From these
results an area in the middle of the arena was marked in which the sound
pressure did not vary by more than ±3 dB. Sound pressure levels (SPL)
are given in dB relative to 20 µPa rms.
|
Experimental protocol
In the behavioural experiments, 1-2 days old naïve male moths were
tested 1.5-4 h into the scotophase. For testing, moths in glass cylinders
covered with mesh net were introduced in the arena 60 cm downwind from the
odour source. The arena was illuminated by red light, 5-10 lux; the
temperature was 17-18°C, and relative humidity 30-50%. Pheromone
stimulation elicited activation (movement of the antennae), wing-fanning and
chemotaxis in this order. Males walked upwind towards the odour source, and
when they reached the test zone (approximately half way between release site
and odour source) the sound was switched on manually and the behavioural
response observed. The responses were only scored as either `stopped walking'
or `no response' although response to sound seemed to be graded. Cessation of
walking was always accompanied by cessation of wing fanning. However,
sometimes (especially when exposed to female extract) males would cease wing
fanning without cessation of walking as response to the sound. Likewise, at
lower sound intensities moths sometimes responded to the sound by turning away
from the sound source. We defined a behavioural walking stop response to sound
as a complete stop that lasted at least 1 s. We only used responses fulfilling
this criterion for threshold determination. The response duration was defined
by the time from stimulation until the males started walking again and was
only measured for the most intense sound stimuli (102 dB SPL). All reactions
lasting two or more minutes were arbitrarily calculated as 120 s. The sound
intensity at the position of the moth was varied in 6 dB steps from 72 dB SPL
to 102 dB SPL in experiments with odour stimulation, and from 60 to 102 dB SPL
in experiments with air. Moths that were exposed to air (i.e. no odour) did
not orient in a specific direction, consequently they were introduced in the
middle of the arena. After a gentle touch they started walking in a random
direction and were stimulated with sound when they entered the pre-defined
area. The number of animals that were available for behavioural experiments
each day (on average 30) was divided in five treatment groups (Air, 20 ng
Z9E11-14:OAc, 100 ng Z9E11-14:Oac, two-component blend and female extract)
with equal number in each group. Each day experiments were carried out in the
order of increasing pheromone load, thus starting with air and ending with
female extract. This order was chosen to minimise potential contamination of
the set-up. Experiments from consecutive days were pooled to minimise possible
day effects. All individuals were only tested once (i.e. one walk in the
bioassay) and then discarded to avoid habituation effects or pre-exposure
effects (see e.g. Anderson et al.,
2003). For every treatment we used 20-24 males.
Data analyses
The mean difference in sound intensity required for eliciting reaction at
50% level of selected combinations of odour and sound intensities was
calculated using a logistic fit (Table
1). Within odour type Spearman rank correlation between sound
intensity and reaction frequency were performed using SYSTAT (v7.0, SPSS).
Logistic regression fit (Hosmer and
Lemeshow, 1989) and pair-wise comparisons using dummy variables
were performed using SAS (rel. 8.2, SAS institute Inc.). The non-parametric
Kruskal-Wallis test (SAS rel. 8.2) were used for testing differences in odour
influence on the response duration, the subsequent multiple comparisons were
done by hand following a non-parametric Tukey test
(Zar, 1996
).
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Results |
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The lowest behavioural thresholds were found for moths in clean air. In the absence of pheromone stimulation most male moths ceased walking and froze to stimulus intensities above 66 dB SPL (Fig. 2). In all experiments the proportion of males that responded to sound increased with increasing sound intensity (Fig. 2). Conversely, at constant sound pressure the reaction to sound was successively reduced with increasing pheromone quality and concentration (Fig. 2). The most pronounced disregard to predator sound was found for males attracted to female extract, where only about 30% of the males responded to sound at the highest intensity (102 dB SPL) whereas the same sound pressure elicited more than 95% responses when exposed to 20 ng of the one-component odour or no odour at all. By logistic regression, we estimated response probability functions (Fig. 3), which allowed us to test for significant differences between selected pairs of odour treatments (Table 1). At the 50% level (Fig. 3) pair wise comparisons showed that all olfactory stimulations were significantly different (P<0.001) except one-component 100 ng vs two-component blend (P=0.648) (Table 1). Significantly more moths responded to sound stimuli when approaching a low amount of odour (20 ng) than a higher dose (100 ng) (Table 1). At 100 ng the threshold for eliciting walking stop in 50% of the cases was 12 dB higher than at 20 ng pheromone (Fig. 3, Table 1). Also, the pheromone quality (one component < blend of two components < female extract) affected the response to sound significantly (Fig. 3 and Table 1). Female extract increases the threshold for behavioural response compared with stimulation with pure air or synthetic pheromone. At the 50% probability level the increase is approximately 40 dB (Fig. 3). At 102 dB SPL 75% of the moths stopped when stimulated with the two-component blend (Z9E11-14:OAc and Z9E12-14:OAc) while only 40% reacted when the pheromone was female extract (Fig. 2). The difference in acoustic threshold between this blend and the female extract was 16 dB at the 50% reaction probability level.
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The time the moth remained motionless following sound stimulation was also affected by pheromone stimulation (Fig. 4). Among the tested odours the median response duration at 102 dB SPL was longest, 16 s, for 20 ng of the major pheromone component. The shortest median response duration, 2 s, was observed for female extract. Without pheromones, the response duration was significantly longer (100 s), than with pheromones (2-16 s) (P<0.01, Kruskal-Wallis followed by nonparametric Tukey test).
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Discussion |
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We used a walking-stop response as an indicator of an acoustic response.
Presumably, this behaviour would protect the moth from predation by gleaning
bats (Werner, 1981;
Arlettaz et al., 2001
;
Schnitzler and Kalko, 2001
;
Greenfield and Baker, 2003
),
and may correlate to the last chance manoeuvres of moths hunted on the wing by
aerial hawking bats. The advantage of the walking bioassay is that it allows
for a precise estimate of response thresholds to acoustic stimuli both with
and without odour stimulation, which would be very difficult to obtain for a
flying moth. However, a flying moth may be more vulnerable to bats than a
walking moth and, therefore, may pay relatively more attention to the predator
by exhibiting lower response thresholds to sound. Therefore, it is not
straightforward to extrapolate our data obtained from the walking bioassay to
flying moths, although several recent experiments indicate similar results for
moth in flight tunnels. Svensson et al.
(2004
) found that both noctuid
and pyralid moths respond less to sound when flying towards a high quality or
quantity of sex pheromone than when attracted to pheromone of minor quality or
quantity. No fundamental differences have been found in the attraction
behaviour to pheromones between walking and flying moths
(Anderson et al., 2003
). In
addition, threshold intensities for cessation of walking
(Fig. 2)
(Werner, 1981
) are in the same
range as for cessation of flight in moths in tethered flight
(Skals and Surlykke, 2000
;
Zhantiev, 1988
) without
pheromone exposure. The evidence therefore indicates that the general findings
in this study may also apply to flying moths.
The consequence for a male moth ignoring acoustic signals when engaged in
mate finding is that his reaction range to the predator signals is reduced
considerably. We used acoustic threshold data for the 50% reaction level from
Fig. 3 tocalculate approximate
reaction distances for moths exposed to bats emitting cries at 30 kHz with an
intensity of 90 dB peSPL at 1 m and assuming spherical spreading loss and
atmospheric attenuation of 0.7 dB m-1
(Lawrence and Simmons, 1982).
These calculations show that a 40 dBreduction in auditory threshold
corresponds to reduction in reaction distance from approximately 8 m to
<0.2 m, which leaves the moth a very short time in which to react. These
calculations represent a best-case scenario for the moths, since we used sound
frequencies in the optimal hearing range (30 kHz) to establish the behavioural
threshold. The situation for the moth in the field may be worse, if it
encounters bats using frequencies outside the moth's best frequency range of
hearing and perhaps temporal parameters that are more difficult to detect as
they approach their target (Fullard et
al., 2003
). Thus male moths may appear functionally deaf when they
are exposed to a strong pheromone signal. Rydell et al.
(2000
) found that flying male
moths (Gynaephora groenlandica) reacted to ultrasound even at close
range to the female, which at first sight may seem to contradict our findings.
However, these moths were exposed to a very intense stimulus from an
electronic dog whistle (110 dB SPL at 1 m corresponding to 20 dB higher than
the maximum out put of our loudspeaker at 30 cm). Hence if we extrapolate the
curve for female extract in Fig.
3 by 20 dB then the expected response probability will be close to
100%. Therefore our results are in good accordance flying moths in the field
as observed by Rydell et al.
(2000
). The two-component
synthetic pheromone blend used in this study, was previously found to attract
moths very effectively in the field (Kehat
and Dunkelblum, 1993
). However, we found that female extract was
significantly better than the two-component blend in blocking the acoustic
response. Hence, our results strongly indicate that the two-component blend is
not optimal, and that female extract contains more hitherto un-identified
compounds. In future studies the reaction to ultrasound in an experimental
set-up as used here may serve as a sensitive behavioural assay to evaluate
pheromone quality in moths.
It is well known from mammalian psychophysics that input from one sensory
modality might alter the processing of information in another (e.g.
Stein et al., 1993; for review
see Calvert et al., 2004
). This
is especially well studied in humans where many cases have shown how
information from various sensory systems (e.g. acoustic, visual, somatosensory
and proprioceptive) is integrated (Driver
and Spence, 1998
). When animals receive concurrent sensory
information they may attend to one stimulus by ignoring other stimuli, which
is referred to as stimulus-selective attention
(Dukas, 2002
) or crossmodal
selective attention (Spence et al.,
2000
). The moth model as presented here may be used for studying
crossmodal selective attention. However, in our experiments, we cannot tell if
the moths actually choose not to react to the sound stimulus when the
pheromone stimulus is on (endogenous controlled attention) or whether the
acoustic system is turned off by the olfactory system by for example
inhibition at higher level, which may be interpreted as exogenous selective
attention (see Spence and Driver,
2004
).
It has been suggested that acoustic stimuli are dominant over attractive
odours (Agee, 1988). However,
our results do not support sensory dominance or that the sensory modalities
are organised in a hierarchal structure. Instead we suggest that integration
of information from different sensory modalities requires complex dynamic
comparisons by higher-order neurons, which implies that behavioural thresholds
are dynamic and depend on the behavioural context. Therefore behavioural
thresholds estimated under unimodal conditions in the lab may be far from the
relevant thresholds in the animal's habitat. Studies on the trade-off between
acoustic and chemical stimuli in the moth, offers an interesting model for
studies on how dynamic integration of bimodal sensory information is processed
by the CNS.
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Acknowledgments |
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References |
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---|
Acharya, L. and McNeil, J. N. (1998). Predation risk and mating behaviour: the responses of moths to bat-like ultrasound. Behav. Ecol. 9,552 -558.[Abstract]
Agee, H. R. (1988). How do acoustic inputs to the central nervous system of the bollworm moth control its behaviour? Fla. Entomol. 71,393 -400.
Anderson, P., Sadek, M. M. and Hansson, B. S.
(2003). Pre-exposure modulates attraction to sex pheromone in a
moth. Chem. Senses 28,285
-291.
Arlettaz, R., Jones, G. and Racey, P. A. (2001). Effect of acoustic clutter on prey detection by bats. Nature 414,742 -745.[CrossRef][Medline]
Bailey, W. J. and Haythornthwaite, S. (1998). Risks of calling by the field cricket Teleogryllus oceanicus; potential predation by Australian long-eared bats. J. Zool. 244,505 -513.[CrossRef]
Baker, T. C. and Cardé, R. T. (1977). Disruption of Gypsy moth male sex pheromone behaviour by high frequency sound. Env. Entomol. 7,45 -52.
Belwood, J. J. and Morris, G. K. (1987). Bat predation and its influence on calling behavior in neotropical katydids. Science 238,64 -67.
Bernays, E. A. (2001). Neural limitations in phytopgagous insects: Implications for diet breadth and evolution of host affiliation. Annu. Rev. Entomol. 46,703 -727.[CrossRef][Medline]
Calvert, G. A., Spence, C. and Stein, B. E. (eds) (2004). The Handbook of Multisensory Processes. Cambridge, London: MIT Press.
Dicke, M. and Grostal, P. (2001). Chemical detection of natural enemies by arthropods: an ecological perspective. Annu. Rev. Ecol. Syst. 32, 1-23.[CrossRef]
Driver, J. and Spence, C. (1998). Crossmodal attention. Curr. Opin Neurobiol. 8, 245-253.[CrossRef][Medline]
Dukas, R. (2002). Behavioural and ecological consequences of limited attention. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357,1539 -1547.[CrossRef][Medline]
Farkas, S. R. and Shorey, H. H. (1974). Chemical trail-following by flying insects: a mechanism for orientation to a distant odour source. Science 178, 67-68.
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.
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.
De Gelder, B. and Bertelson, P. (2003). Multisensory integration, perception and ecological validity. Trends Cog. Sci. 7,460 -467.[CrossRef][Medline]
Ghiradella, H. (1971). Fine structure of the noctuid moth ear. J. Morph. 134, 21-46.[Medline]
Greenfield, M. D. and Baker, M. (2003). Bat avoidance in non-aerial insects: the silence response of signalling males in an acoustic moth. Ethology 109,427 -442.[CrossRef]
Greenfield, M. D. and Weber, T. (2000). Evolution of ultrasonic signalling in wax moths: discrimination of ultrasonic mating calls from bat echolocation signals and the exploitation of an anti-predator receiver bias by sexual advertidement. Ethol. Ecol. Evol. 12,259 -279.
Hansson, B. S. (1995). Olfaction in Lepidoptera. Experientia 51,1003 -1027.
Hinks, C. F. and Byers, J. R. (1976). Biosystematics of the genus Euxoa (Lepidoptera; Noctuidae). V. Rearing procedures and life cycles of 36 species. Can. Entomol. 108,1345 -1357.
Hölldobler, B. (1999). Multimodal signals in ant communication. J. Comp. Physiol. A 184,129 -141.
Hosmer, D. W. and Lemeshow, S. (1989). Applied Logistic Regression. New York, USA: Wiley.
Jones, G., Barabas, A. B. and Parsons, S.
(2002). Female greater wax moths reduce sexual display behaviour
in relation to the potential risk of predation by echolocating bats.
Behav. Ecol. 13,375
-380.
Kehat, M. and Dunkelblum, E. (1993). Sex pheromones: achievements in monitoring and mating disruption on cotton pests in Israel. Arch. Insect Biochem. Physiol. 22,425 -431.
Kennedy, J. S., Ludlow, A. R. and Sanders, C. J. (1980). Guidance systems used in moth sex attraction. Nature 288,475 -477.[CrossRef]
Lawrence, B. D. and Simmons, J. A. (1982). Measurements of atmospheric attenuation at ultrasonic frequencies and the significance for echolocation by bats. J. Acoust. Soc. Am. 71,585 -590.[Medline]
Linn, C. E., Campbell, M. G. and Roelofs, W. L. (1987). Pheromone components and active spaces: what do moths smell and where do they smell it? Science 237,650 -652.
Magnhagen, C. (1991). Predation risk as a cost of reproduction. Trends Ecol. Evol. 6, 183-186.[CrossRef]
Miller, L. A. and Surlykke, A. (2001). How some insects detect and avoid being eaten by bats: tactics and counter tactics of prey and predator. Bioscience 51,570 -581.
Neuweiler, G. (1989). Foraging ecology and audition in echolocating bats. Trends Ecol. Evol. 4, 160-166.[CrossRef]
Neuweiler, G. (1990). Auditory adaptations for
prey capture in echolocating bats. Physiol. Rev.
70,615
-641.
Partan, S. and Marler, P. (1999). Communication
goes bimodal. Science
283,1272
-1273.
Pashler, H. E. (1998). The Psychology of Attention. Cambridge, MA: MIT Press.
Roeder, K. D. (1962). The behaviour of free flying moths in the presence of artificial ultrasonic pulses. Anim. Behav. 10,300 -304.[CrossRef]
Roeder, K. D. (1967). Nerve Cells and Insect Behaviour. Cambridge, MA: Harvard University Press.
Rydell, J., Roininen, H. and Philip, K. W. (2000). Persistence of bat defence reactions in high Arctic moths (Lepidoptera). Proc. R. Soc. Lond. B Biol. Sci. 267,553 -557.[CrossRef][Medline]
Schlyter, F., Löfqvist, J. and Jakus, R. (1995). Green leaf volatiles and verbenone modify attraction of European Tomicus, Hylurgops and Ips bark beetles. In Behavior, Population Dynamics and Control of Forest Insects (ed. F. P. Hain, S. S. Salom, W. F. Ravlin, T. L. Payne and K. F. Raffa), pp.29 -44. Proceedings of a Joint IUFRO Working Party Conference - February 1994, Ohio State Univ., OARDC, Wooster 1995.
Schnitzler, H. U. and Kalko, E. K. V. (2001). Echolocation by insect-eating bats. BioScience 51,557 -569.
Skals, N. and Surlykke, A. (2000). Hearing and evasive behaviour in the greater wax moth, Galleria mellonella (Pyralidae). Physiol. Entomol. 25,354 -362.[CrossRef]
Small, D. M. (2004). Crossmodal integration - insights from the chemical senses. Trends Neurosci 27,120 -122.[CrossRef][Medline]
Spence, C. and Driver, J. (2004). Crossmodal Space and Crossmodal Attention. Oxford, UK: Oxford University Press.
Spence, C., Ranson, J. and Driver, J. (2000). Crossmodal selective attention: on the difficulty of ignoring sounds at the locus of visual attention. Percept. Psychophys. 62,410 -424.[Medline]
Stein, B. E., Meredith, M. A. and Wallace, M. T. (1993). The visual responsive neuron and beyond: multisensory integration in cat and monkey. Progr. Brain Res. 95, 79-90.[Medline]
Surlykke, A. and Miller, L. A. (1982). Central branchings of three sensory axons from a moth ear (Agrotis segetum, Noctuidae). J. Insect Physiol. 28,357 -364.[CrossRef]
Svensson, G., Löfstedt, C. and Skals, N. (2004) The odour makes the difference: male moths attracted by sex pheromones ignore the threat by predatory bats. OIKOS 104,91 -97.[CrossRef]
Vickers, N. J. and Baker, T. C. (1997). Flight of Heliothis virescens males in the field in response to sex pheromone. Phys. Entomol. 22,277 -285.
Waters, D. A. and Jones G. (1995). Echolocation call structure and intensity in 5 species of insectivorous bats. J. Exp. Biol. 198,475 -489.[Medline]
Werner, T. (1981). Responses of nonflying moths to ultrasound: the threat of gleaning bats. Can. J. Zool. 59,525 -529.
Zar, J. H. (1996). Biostatistical Analysis, 3rd edn. London, UK: Prentice-Hall.
Zhantiev, R. D. (1988). Response of lepidoptera to ultrasound signals. Zoologiskij Zurnal (in Russian) 67,995 -1001.
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