Predator detection and evasion by flying insects

Available online at www.sciencedirect.com
Predator detection and evasion by flying insects
David D Yager
Echolocating bats detect prey using ultrasonic pulses, and
many nocturnally flying insects effectively detect and evade
these predators through sensitive ultrasonic hearing. Many
eared insects can use the intensity of the predator-generated
ultrasound and the stereotyped progression of bat
echolocation pulse rate to assess risk level. Effective
responses can vary from gentle turns away from the threat (low
risk) to sudden random flight and dives (highest risk). Recent
research with eared moths shows that males will balance
immediate bat predation risk against reproductive opportunity
as judged by the strength and quality of conspecific
pheromones present. Ultrasound exposure may, in fact, bias
such decisions for up to 24 hours through plasticity in the CNS
olfactory system. However, brain processing of ultrasonic
stimuli to yield adaptive prey behaviors remains largely
unstudied, so possible mechanisms are not known.
Address
Department of Psychology and Neuroscience and Cognitive Science
Program, University of Maryland, College Park, MD 20742, United States
Corresponding author: Yager, David D (ddyager@umd.edu)
Current Opinion in Neurobiology 2012, 22:201–207
This review comes from a themed issue on
Neuroethology
Edited by Michael Dickinson and Cynthia Moss
Available online 7th January 2012
0959-4388/$ – see front matter
# 2011 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.conb.2011.12.011
Introduction
Many insects have tympanate ears that provide them with
sensitive hearing at frequencies from a few kHz to over
100 kHz depending on the species. There have been at
least 18 independent evolutions of pressure-sensitive
hearing yielding ears of diverse shapes, sizes, and
locations on the body [1,2]. Having two ears is the norm,
but most praying mantises have just one and a pneumorid
grasshopper has six pairs. Insects including crickets, grasshoppers, water bugs, cicadas, and some butterflies and
moths use hearing as part of intraspecific communication
systems [3]. A few — most notably parasitoid flies that
target singing male crickets as hosts — use hearing to find
prey [4]. Finally, many insects, additionally or exclusively, use their hearing to detect and evade predators,
which, for flying nocturnal insects means echolocating
bats. This is the well-known story of the coevolutionary
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‘arms race’ between hearing insects and bats [5], although
‘diffuse coevolution’ might better describe a system with
many species of prey and predator [6]. An emerging
theme in this story is behavioral and neural
economics — balancing the benefits of hunting and evasion against the costs in terms of energetics and, especially for the prey, of the disruption of other important
behaviors such as finding a mate. Thus, the assessment of
risk and of potential benefit along with the mechanisms of
decision-making have become key research topics.
The detection system
Insect auditory systems are based on the standard pressure-detector design with a vibrating membrane (tympanum) backed by an internal airspace for increased
sensitivity, and a transducing mechanism with as few
as one or as many as several thousand receptors (chordotonal sensilla) depending on the species (reviewed in [7];
Figure 1). Sensitivity and tuning are determined primarily in the periphery through bioacoustic characteristics of
the tympanum and associated structures (studied most
recently using scanning laser vibrometry; for instance, [8])
and/or properties of the receptor structures that are not
yet fully understood. The range of frequencies to which a
particular species is most sensitive is matched to the
dominant echolocation frequencies used by the sympatric
bat assemblage, typically 20–60 kHz, but sometimes
extending beyond 100 kHz (Figure 2) [5]. Predatorgenerated sounds outside that range will be relatively
inaudible to the insect. Sensitivity determines the
response time available to the prey. The echolocation
cries of aerial hawking bats are typically intense (>120 dB
SPL at 10 cm), so insects with minimum thresholds of 40–
60 dB SPL can detect on oncoming bat at >20 m compared to detection distance for bats of <12 m [9,10].
Considering typical insect and bat flight speeds, this
translates to an available response time of >1 s, more
than adequate for predator recognition and evasion [11].
Neural processing
Remarkably little is known about the ‘higher’ CNS processing that controls ultrasound-based defensive behaviors. Past studies have focused primarily on the afferent
side and the activities of a few key interneurons such as
AN2 of crickets, 501-T3 of mantises, the T-cell of tettigoniids, and IN533 and IN714 of locusts [12]. However, the
head is necessary for evasive behavior, at least in pyralid
moths, mantises, tettigoniids, tiger beetles, and crickets. In
the last of these, there are at least 20 ultrasound-sensitive
brain neurons, seven of which have descending axons [13].
Cephalic ultrasound processing is brief (<20 ms; [13,14]).
Its role could simply be conditionally permissive, for
Current Opinion in Neurobiology 2012, 22:201–207
202 Neuroethology
Figure 1
(c)
(a)
*
Ganglion
N.7
Dorsal
TS
Rostral
(d)
BS
*
m
anu
p
Tym
100 µm
(b)
(e)
*
*
500 µm
Current Opinion in Neurobiology
An example of insect ear structure showing the fundamental components of a pressure-sensitive ear. (a) The ear of the praying mantis Sphodromantis
sp. is located in the midline between the metathoracic legs. (b) The ear (inside the dashed oval) has hard cutilical knobs at the rostral end (black
asterisk in b, c, and d) and a deep auditory chamber (opening marked with yellow asterisk) that contains the tympana. The auditory chamber increases
sensitivity and shapes tuning. (c) A cutaway view shows a portion of the large tracheal sac apposed to the inner surface of the tympanum (TS). Nerve 7
(N.7) carries signals from the tympanal organ (dark oval structure) and the two chordotonal sensilla an auditory sensory structure, the bifid sensillum
(black dot) to the CNS (ganglion). (d) A midsagittal section through the ear shows one of the tympana in the wall of the auditory chamber. The white dot
shows the attachment location of the tympanal organ. BF: bifid sensillum. (e) Laser vibrometry shows maximum vibration at the center of the
tympanum (outlined with white line) and at the bifid sensillum. a–e: (Yager, unpublished data). e: (Yager, Michelsen, unpublished data). The illustration
in c was done by John Norton.
example, if the flight CPG is active AND ultrasound is
present to initiate evasive behavior controlled by thoracic
circuitry. Alternatively, the cephalic ganglia may play a
more ‘hands on’ role. The data are not yet available to
distinguish among these and other possibilities.
Current Opinion in Neurobiology 2012, 22:201–207
Ultrasound-triggered evasion and defense
Most responses to ultrasonic pulses involve a change
flight path, and many eared insects have a repertoire
defensive strategies depending on context and level
risk [15] (Figure 3). The strategies of: 1) getting out
in
of
of
of
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Hearing aerial predators Yager 203
Figure 2
90
Sphodromantis aurea
Miomantis sp.
Threshold (dB SPL)
80
Miomantis abyssinica
70
60
50
10
20
30
40
50
70
80
60
Frequency (KHz)
90
100
110
120
130
Current Opinion in Neurobiology
Different insect auditory frequency ranges in different ecological contexts. Physiological tuning curves for three praying mantis species.
Sphodromantis aurea is a large mantis with best sensitivity in the dominant frequency range used by many insectivorous bats with FM echolocation
calls (left green bar). The Miomantis species are small/medium sized animals sympatric with bat species using much higher frequency CF and CF-FM
echolocation calls (right green bar). Their tuning curves suggest that they could respond effectively to bats that use both low and high frequency calls
(Yager, unpublished data).
the way before detection, and/or 2) disrupting the bat’s
attack through some combination of startle and sudden,
random flight path changes serve hearing insects well. In
the few cases for which it has been measured in free-flight
bat-insect encounters (noctuid moths, green lacewings, and
praying mantises), sound-triggered evasion confers a 40–
50% survival advantage over nonhearing conspecifics [16].
It is worth noting that dietary analysis for some bat species
shows a high percentage of hearing insects (for instance
[17]). However, without accompanying data about relative
abundance of size-appropriate hearing and nonhearing prey
or direct observations of capture success rates, it is not
possible to infer the effectiveness of auditory defenses.
Tiger moths (Arctiidae) implement the unusual strategy of
producing intense ultrasonic clicks when they hear pulsed
ultrasound [18]. Faced with an oncoming bat, clicking
arctiids do not alter their flight path and yet survive because
the bats break off their attack [19]. The long-standing
question of how the clicking works to deter bats has been
resolved through an elegant series of experiments using
naive bats and several species of arctiids having different
ecologies. In fact, all of the traditional rival hypotheses —
advertising distastefulness, startling the bat, and jamming
the echolocation system — are correct. Which one dominates depends on the moth species and its ecology and on
the past experience of the bat [15]. Flying tiger beetles,
some of which are distasteful, also click in response to
ultrasound, opening the possibility of intricate Müllerian
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and Batesian mimicry complexes among sympatric beetles
and moths [20,21].
Bats foster false negatives in the insect defensive system.
First, echolocation frequencies and intensities outside the
insect’s detection capabilities could achieve this. Bats
that take prey from a substrate (gleaners) often use very
low intensity pulses that their insect prey cannot hear as
shown by neural recordings [22,23]. An aerial insectivore,
Barbastella barbastella, uses echolocation frequencies of
30–40 kHz, but at amplitudes 20–40 dB lower that other
aerial insectivores. It is highly successful at capturing
eared moths [10]. Echolocation calls at frequencies outside an insect’s hearing range could also work [24–26].
Several studies have found a high proportion of eared
moths in the diets of bat species using frequencies
>70 kHz like the Old World rhinolophid and hipposiderid bats. This is above the most sensitive hearing range
for most insects, although some moths and praying mantises have extended their ranges to >100 kHz (Figure 2).
Secondly, at least some bats project their calls in a
relatively narrow cone of sound that they sweep across
the immediate environment [27]. This strategy greatly
reduces their detectability. Even an insect with sensitive
hearing could be surprised by the bat and have insufficient time to respond effectively.
Ultrasound serves multiple functions for bats (hunting,
obstacle avoidance, intraspecific interactions; [28]), which
Current Opinion in Neurobiology 2012, 22:201–207
204 Neuroethology
Figure 3
(a)
Before ultrasound
(b)
(c)
Strong dive
Percentage of responses
Moderate dive
80
Slight dive
Level tum
No response
60
40
20
After ultrasound
1-3 m.
85-74 dB
3-5 m.
74-70 dB
5-7 m.
70-67 dB
7-9 m.
9-10 m.
67-65 dB 65-64 dB
> 10 m.
< 64 dB
Current Opinion in Neurobiology
An example of ultrasound-triggered evasive responses. (a) Ultrasound elicits a complex, multi-component behavior in the praying mantis
Parasphendale agrionina that starts 45–85 ms after stimulation. (b) The change in flight path starts 150–250 ms after stimulation and ranges from
simple turns and dives to looping power dives. The direction of the response is random relative to the bat position. (c) The types and strength of the
mantis’s response varies with distance to the source (normally a bat). Data are from mantis free-flight experiments using a stationary sound source
producing 40 kHz pulses at 60 pulses/s.
a, b, c: Modified from [41].
can make it difficult to attribute the primary driving force
for particular echolocation call design features exclusively
to countering evasion capabilities of prey [6,29]. Nonetheless, an ecological approach studying bat assemblages
in southern Africa suggests that dealing with prey
defenses is a significant contributor to bat community
structure via common echolocation parameters [30].
Although less common, some insects use their ultrasonic
hearing for a second function, reproductive signaling. The
functions are decoded by context [31], signal characteristics [32,33] and even an analog to vertebrate ‘auditory
stream segregation’ [34].
Economics of auditory predator detection and
evasion
Predator evasion is costly. It requires the maintenance of a
sensory detection and processing system, it requires
Current Opinion in Neurobiology 2012, 22:201–207
energy expenditure, and it diverts effort and time from
other crucial activities like eating and mating.
The costs for insects to maintain an auditory system for
bat evasion have been addressed indirectly in many
studies comparing auditory structure and function in
morphs of a single species [35] and in closely related taxa
differing in their history of exposure to bats. Some taxa of
moths that have become diurnal have lost high-frequency
hearing [36]. The few species of butterflies that have
become nocturnal have evolved ultrasonic hearing [37].
Fullard and colleagues [38] combined genetic data with
neurophysiological and behavioral results among multiple
geographic populations of a single cricket species, Teleogryllus oceanicus, living under a range of bat predation
pressures. Populations with no history of predation
showed both reduction of defensive behavior and
reduction in the activity of the interneuron neuron
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Hearing aerial predators Yager 205
(AN2) necessary and sufficient to elicit it. In many species
of praying mantis, males fly at night and have sensitive
ultrasonic hearing, but the females are flightless with
reduced or absent ears [39]. Although there are some
counterexamples, the general picture is that the benefit of
ultrasonic hearing is very high, but the cost is must be
significant as well.
Because the bat auditory system is used for other purposes as well [28], the costs of echolocation specifically for
hunting are primarily energetic. This can work to the
prey’s advantage. For example, a mantis executing an
evasive power dive from >5 m above the ground, a
common flight altitude in the field, could rarely escape
a bat in a prolonged chase because of the latter’s greater
flight speed and adaptive targeting strategies [40]. Yet
bats often break off the chase before capture [41], presumably because an extended pursuit can be costly in
time, energy, and in the risk of collision with vegetation or
the ground. To survive, the mantis does not have to be
impossible to catch, only too expensive.
Auditory risk assessment can reduce cost for insects by
minimizing false positives and by allowing the level of
defensive response to be tailored to the threat. A simple
version of risk assessment based on the intensity of
ultrasound is well documented in moths, praying mantises, crickets, tachinid flies, and tettigoniids. Low intensity ultrasonic pulses (a distant bat) trigger low intensity
behaviors, often deviations of the flight path to move
away from the threat, that do not seriously interrupt the
ongoing behavior. In the same animals, high intensity
ultrasound triggers a ‘last ditch’ response including rapid
erratic flight, steep dives, or complete flight cessation
(dropping). Recently, Ratcliffe and colleagues [42] have
suggested an intensity-based two-threshold mechanism
in moths with low versus high intensity behavior determined by combined spike number of the A1 and the
higher threshold A2 receptors. Some insects make a more
nuanced risk assessment taking advantage of the stereotyped changes in echolocation pulse rate as a capture
attempt progresses (Figure 4). For instance, arctiid moths
can distinguish between early and late attack echolocation call patterns based on rate alone [43]. Both arctiid and
pyralid moths alter their behavior (clicking rate and
pheromone signaling, respectively) depending on predation risk, defined as a combination of intensity and pulse
pattern of ultrasonic stimuli [43,44]. If the same threat
parameters elicit spike repetition rates above a threshold
level of 180/s in the cricket auditory interneuron Int-1
(=AN2) the animal initiates a evasive turn [45]. In praying
mantises (Figure 4), the initiation of the full power dive
corresponds to an echolocation pulse rate of 50–55 pps,
which typically occurs at the transition from approach to
terminal phase of the attack, 250–350 ms before potential
capture [46,47]. Hartbauer and colleagues [48] have
demonstrated a novel thoracic neuronal mechanism in
a katydid that allows bat threat assessment based on
repetition rate even in the face of intense ultrasonic
background noise.
Figure 4
501-T3 spikes
Dive starts
Contact
50 ms.
Approach
Terminal
Buzz
Current Opinion in Neurobiology
Basis for risk assessment during bat attacks. Simultaneous recordings of bat echolocation pulses (lower trace) and a mantis ultrasound-sensitive
ascending interneuron (501-T3) during a free-flight bat attack. Contact is the time of capture with no evasion. The stereotyped pattern of bat pulses
progresses from ca. 20 pps during early approach phase (early attack) through 55 pps when 501-T3 stops tracking the pulses to the terminal buzz with
>100 pps. The mantis’ evasive dive begins at 200–300 ms before contact when the echolocation pulse rate is 50–60 pps. The interneuron may be
involved in triggering the dive.Modified from [46].
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Current Opinion in Neurobiology 2012, 22:201–207
206 Neuroethology
Increasing evidence, especially from eared moths, shows
that insects can use auditory risk assessment in a cost/
benefit ‘decision’ balancing predator evasion against a
reproductive opportunity. Male moths flying toward a
pheromone source (a female in the wild or an artificial
source in a wind tunnel) respond less vigorously or less
often to ultrasonic pulses than controls without the pheromone. Svensson and colleagues [49] showed that not only
the presence but the quality of the pheromone matters in
determining the reduction of ultrasound-triggered evasive
dives by flying males. Skals et al. [50] were able to titrate the
intensity of ultrasound against the concentration of pheromone to determine production of defensive behavior. In
fact, it can be a dual system because some pyralid moth
females regulate pheromone production based on level of
bat predation risk [44]. In a recent field study [51] pheromone trap catch rates of a nocuid moth were not affected by
ultrasound broadcast continuously over a crop field. This
could imply cost/benefit favoring immediate mating, but
could also indicate habituation to the constant ultrasound.
For ultrasound-producing tettigoniids and lekking pyralid
moth males, determining the balance is even more complex
because they are surrounded by other calling conspecifics
[34,52]. The interaction of reproductive and evasive
demands is taken to an ironic extreme by male corn borer
moths. They emit ultrasonic clicks at intensities sufficient
to elicit defensive behavior (immobility) in receptive walking females, which increases the male’s copulation success
[53,54]. Svensson et al. [55] noted that disruption of
pheromone tracking by ultrasound could considerably outlast the stimulus, and some males failed to resume tracking
at all. This suggests that in addition to an immediate
mechanism based in rapid neural processing, ultrasound
can induce longer term plasticity in the nervous system.
Using naive male noctuid moths, Anton and colleagues
[56] found that a single 10-min exposure to bat-like
ultrasound or to nonpulsed ultrasound induced changes
in sensitivity to pheromone of neurons in the primary
olfactory processing area of the brain measured 24 hours
postexposure. However, only the bat-like ultrasound
caused changes in a walking assay of pheromone tracking
behavior the next day. The implication is that the exposure
to ‘bats’ created a bias affecting later decisions between
following a pheromone plume and a defensive response,
thus shifting the titration point toward reproduction.
Conclusions
We continue to uncover intricacies and adaptations in the
special predator–prey relationship between eared insects
and echolocating bats. Emerging lines of research combine
bioacoustic, neural, behavioral, and ecological strands and
show that the relationship is far more complicated than just
capture or escape. We are seeing risk assessment and cost–
benefit analyses and beginning to glimpse some of their
neural underpinnings. In particular, the results of crossmodal studies linking olfaction and hearing point us toward
lines of research into the least studied aspects of hearing in
Current Opinion in Neurobiology 2012, 22:201–207
insects — processing and plasticity in the brain control
systems for bat evasive behaviors.
Acknowledgment
Preparation of this paper was supported by National Science Foundation
Grant #IOS-0746037.
References and recommended reading
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47. Triblehorn JD, Yager DD: Timing of praying mantis evasive
responses during simulated bat attack sequences. J Exp Biol
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48. Hartbauer M, Radspieler G, Römer H: Reliable detection of
predator cues in afferent spike trains of a katydid under high
background noise levels. J Exp Biol 2010, 213:3036-3046.
49. Svensson GP, Löfstedt C, Skals N: The odor makes the
difference: male moths attracted by sex pheromones ignore
the threat by predatory bats. Oikos 2004, 104:91-97.
50. Skals N, Anderson P, Kanneworff M, Löfstedt C, Surlykke A: Her
odours make him deaf: crossmodal modulation of olfaction
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51. Gillam EH, Westbrook JK, Schleider PG, McCracken GF: Virtual
bats and real insects: effects of echolocation on pheromonetracking behavior of male corn earworm moths, Helicoparva
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52. Brunel-Pons O, Alem S, Greenfield MD: The complex auditory
scene at leks: balancing antipredator behavior and
competitive signaling in an acoustic moth. Anim Behav 2011,
81:231-239.
This is the first study of the multi-factor cost–benefit decisions to be made
by a moth that produces ultrasound to attract mates, but must do this in a
competitive social setting (lek) under predation pressure by bats.
53. Nakano R, Takanashi T, Skals N, Surlykke A, Ishikawa Y:
Ultrasonic courtship songs of male Asian corn borer moths
assist copulation attempts by making the females motionless.
Physiol Entomol 2010, 35:76-81.
One of a series of three papers showing much broader use of ultrasound
in moth intraspecific communication than previously thought. This is the
first report of male moths mimicking bats to elicit defensive behavior in
conspecific females.
54. Nakano R, Takanashi T, Skals N, Surlykke A, Ishikawa Y: To
females of a noctuid moth, male courtship songs are nothing
more than bat echolocation calls. Biol Lett 2011, 6:582-584.
55. Svensson GP, Löfstedt C, Skals N: Listening in pheromone
plumes: disruption of olfactory-guided mate attraction in a
moth by a bat-like ultrasound. J Insect Sci 2007, 7:1536-2442.
56. Anton S, Evengaard K, Barrozo RB, Anderson P, Skals N: Brief
predator sound exposure elicits behavioral and neuronal longterm sensitization in the olfactory system of an insect. Proc
Natl Acad Sci USA 2011, 108:3401-3405.
This study provides the first neural evidence of brain plasticity induced by
ultrasound that could bias cost–benefit decisions at a much later time.
Current Opinion in Neurobiology 2012, 22:201–207