Predator detection and evasion by flying insects

Predator detection and evasion by flying insectsDavid D Yager

Available online at www.sciencedirect.com

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 ([email protected])

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

IntroductionMany 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, grass-

hoppers, 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 exclu-

sively, 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

www.sciencedirect.com

‘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 eva-

sion against the costs in terms of energetics and, especi-

ally 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 systemInsect auditory systems are based on the standard pres-

sure-detector design with a vibrating membrane (tympa-

num) backed by an internal airspace for increased

sensitivity, and a transducing mechanism with as few

as one or as many as several thousand receptors (chordo-

tonal sensilla) depending on the species (reviewed in [7];

Figure 1). Sensitivity and tuning are determined primar-

ily 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]. Predator-

generated 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 com-

pared 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 processingRemarkably little is known about the ‘higher’ CNS pro-

cessing that controls ultrasound-based defensive beha-

viors. 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 tetti-

goniids, 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


mailto:[email protected]

http://dx.doi.org/10.1016/j.conb.2011.12.011

http://www.sciencedirect.com/science/journal/09594388

202 Neuroethology

Figure 1

(a)

(b)

500 µm

100 µm

(e)

(d)

(c)

Tympanum

Dorsal

N.7

Ganglion*

TSRostral

BS

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.


Ultrasound-triggered evasion and defenseMost responses to ultrasonic pulses involve a change in

flight path, and many eared insects have a repertoire of

defensive strategies depending on context and level of

risk [15�] (Figure 3). The strategies of: 1) getting out of


Hearing aerial predators Yager 203

Figure 2

90

80

70

60

5010 20 30 40 50 60

Frequency (KHz)

Miomantis sp.

Miomantis abyssinica

Sphodromantis aurea

Thr

esho

ld (

dB S

PL)

70 80 90 100 110 120 130


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 dom-

inates 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 Mullerian


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 out-

side 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 hipposi-

derid bats. This is above the most sensitive hearing range

for most insects, although some moths and praying man-

tises 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 insuffi-

cient time to respond effectively.

Ultrasound serves multiple functions for bats (hunting,

obstacle avoidance, intraspecific interactions; [28]), which


204 Neuroethology

Figure 3

(a) (b)

(c)

80

Strong dive

Moderate dive

Slight dive

Level tum

No response

1-3 m.85-74 dB

3-5 m.74-70 dB

5-7 m.70-67 dB

7-9 m.67-65 dB

9-10 m.65-64 dB

> 10 m.< 64 dB

60

Per

cent

age

of r

espo

nses

40

20

Before ultrasound

After ultrasound


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]. None-

theless, 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 character-

istics [32,33] and even an analog to vertebrate ‘auditory

stream segregation’ [34].

Economics of auditory predator detection andevasionPredator evasion is costly. It requires the maintenance of a

sensory detection and processing system, it requires


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, Tele-ogryllus 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



(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 pur-

poses 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], pre-

sumably 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 man-

tises, crickets, tachinid flies, and tettigoniids. Low inten-

sity ultrasonic pulses (a distant bat) trigger low intensity

behaviors, often deviations of the flight path to move

Figure 4

501-T3 spikes

50 ms.

Approach

Basis for risk assessment during bat attacks. Simultaneous recordings of b

ascending interneuron (501-T3) during a free-flight bat attack. Contact is the

progresses from ca. 20 pps during early approach phase (early attack) throug

>100 pps. The mantis’ evasive dive begins at 200–300 ms before contact w

involved in triggering the dive.Modified from [46].


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 deter-

mined 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 stereo-

typed changes in echolocation pulse rate as a capture

attempt progresses (Figure 4). For instance, arctiid moths

can distinguish between early and late attack echoloca-

tion call patterns based on rate alone [43]. Both arctiid and

pyralid moths alter their behavior (clicking rate and

pheromone signaling, respectively) depending on preda-

tion 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.

Dive starts Contact

TerminalBuzz


at echolocation pulses (lower trace) and a mantis ultrasound-sensitive

time of capture with no evasion. The stereotyped pattern of bat pulses

h 55 pps when 501-T3 stops tracking the pulses to the terminal buzz with

hen the echolocation pulse rate is 50–60 pps. The interneuron may be


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 phero-

mone. 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 phero-

mone 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] phero-

mone 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 walk-

ing females, which increases the male’s copulation success

[53�,54]. Svensson et al. [55] noted that disruption of

pheromone tracking by ultrasound could considerably out-

last 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.

ConclusionsWe 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 cross-

modal studies linking olfaction and hearing point us toward

lines of research into the least studied aspects of hearing in


insects — processing and plasticity in the brain control

systems for bat evasive behaviors.

AcknowledgmentPreparation of this paper was supported by National Science FoundationGrant #IOS-0746037.

References and recommended readingPapers of particular interest, published within the period of review,have been highlighted as:

� of special interest

�� of outstanding interest

1. Yager DD: Structure, development, and evolution of insectauditory systems. Microsc Res Tech 1999, 47:380-400.

2. Yack JE, Dawson JW: Insect ears. In The Senses: AComprehensive Reference, vol 3. Edited by Hoy RR, Sheperd GM,Basbaum AI, Kaneko A, Westheimer G. Elsevier; 2008:35-54.

3. Robert D, Hoy RR: Auditory systems in insects. In InvertebrateNeurobiology. Edited by North G, Greenspan RJ. Cold SpringHarbor Press; 2007:155-184.

4. Muller P, Robert D: A shot in the dark: the silent quest of a free-flying phonotactic fly. J Exp Biol 2001, 204:1039-1052.

5. Fullard JH: The sensory coevolution of moths and bats. InComparative Hearing: Insects. Edited by Hoy RR, Popper AN, FayRR. Springer-Verlag; 1998:279-326.

6. Rydell J, Jones G, Waters D: Echolocating bats and hearingmoths: who are the winners. Oikos 1995, 73:419-424.

7. Yack JE: The structure and function of auditory chordotonalorgans. Microsc Res Tech 2004, 63:315-337.

8. Windmill JFC, Fullard JH, Robert D: Mechanics of a ‘simple’ ear:tympanal vibrations in noctuid moths. J Exp Biol 2007,210:2637-2648.

9. Surlykke A, Kalko EKV: Echolocating bats cry out loud to detecttheir prey. PLoS One 2008, 3(4) e2036(1)–e2036(10).

10.�

Goerlitz HR, ter Hofstede HM, Zeale MRK, Jones G, Holderled M:An aerial-hawking bat uses stealth echolocation to countermoth hearing. Curr Biol 2010, 20:1-5.

This study supports the idea of predator–prey coevolution by presenting aclear example of a common echolocation hunting strategy modified speci-fically to circumvent the prey’s defensive capabilities. It includes an excellentdiscussion of the determinants of available escape time for hearing insects.

11. Schulze W, Schul J: Ultrasound avoidance behavior in thebushcricket Tettigonia viridissima (Orthoptera: Tettigoniidae).J Exp Biol 2001, 204:733-740.

12. Hennig RM, Franz A, Stumpner A: Processing of auditoryinformation in insects. Microsc Res Tech 2004, 63:351-374.

13. Brodfuerher PD, Hoy RR: Ultrasound sensitive neurons in thecricket brain. J Comp Physiol A 1990, 166:651-662.

14. Baden T, Hedwig B: Front leg movements and tibialmotorneurons underlying auditory steering in the cricket(Gryllus bimaculatus deGeer). J Exp Biol 2008, 211:2123-2133.

15.�

Conner WE, Corcoran AJ: Sound strategies: the 65-million-yearold battle between bats and insects. Annu Rev Entomol 2012,57:21-39.

An excellent review broadly covering bat insect interactions, but alsolaying out the most recent experiments resolving controversy about thefunctions of arctiid moth clicking.

16. Triblehorn JD, Ghose K, Bohn K, Moss CF, Yager DD: Free-flightencounters between praying mantids (Parasphendale agrionina)and bats (Eptesicus fuscus). J Exp Biol 2008, 211:555-562.

17. Clare EL, Fraser EE, Braid HE, Fenton MB, Hebert PDN: Specieson the menu of a generalist predator, the eastern red bat(Lasiurus borealis): using a molecular approach to detectarthropod prey. Mol Ecol 2009, 18:2532-2542.



18. Corcorah AJ, Conner WE, Barber JB: Anti-bat tiger mothsounds: form and function. Curr Zool 2010, 56:358-369.

19. Ratcliffe JM, Fullard JH: The adaptive function of tiger mothclicks against echolocating bats: an experimental andsynthetic approach. J Exp Biol 2005, 208:4689-4698.

20. Yager DD, Spangler HG: Behavioral response to ultrasound bythe tiger beetle Cicindela marutha Dow combinesaerodynamic changes and sound production. J Exp Biol 1997,200:649-659.

21. Barber JR, Conner WE: Acoustic mimicry in a predator–preyinteraction. Proc Natl Acad Sci USA 2007, 104:9331-9334.

22. Fullard JH, Ratcliffe JM, Guignion C: Sensory ecology ofpredator–prey interactions: responses of the AN2 interneuronin the field cricket, Teleogryllus oceanicus, to the echolocationcalls of sympatric bats. J Comp Physiol A 2005, 191:605-618.

23. ter Hofstede HM, Killow J, Fullard JH: Gleaning bat echolocationcalls do not elicit antipredator behavior in the Pacific fieldcricket, Teleogryllus oceanicus (Orthoptera: Gryllidae). JComp Physiol A 2009, 195:769-776.

24. Schoeman MC, Jacobs DS: Support for the allotonic frequencyhypothesis in an insectivorous bat community. Oecologia 2003,134:154-162.

25. Pavey CR, Burwell CJ, Milne DJ: The relationship betweenecholocation call frequency and moth predation of a tropicalbat fauna. Can J Zool 2006, 84:425-433.

26. Jacobs DS, Ratcliffe JM, Fullard JH: Beware of bats, beware ofbirds: the auditory responses of eared moths to bat and birdpredation. Behav Ecol 2008, 19:1333-1342.

27. Surlykke A, Pedersen SB, Jakobsen L: Echolocating bats emit ahighly directional sonar sound beam in the field. Proc R Soc B2009, 276:853-860.

28. Schnitzler H-U, Moss CF, Denzinger A: From spatial orientationto food acquisition in echolocating bats. Trends Ecol Evol 2003,18:386-394.

29. Waters DA: Bats and moths: what is there left to learn? PhysiolEntomol 2003, 28:237-250.

30. Schoeman MC, Jacobs DS: The relative influence ofcompetition and prey defenses on the trophic structure ofanimalivorous bat ensembles. Oecologia 2011, 166:493-506.

31. Rodriguez RL, Greenfield MD: Behavioural context regulates dualfunction of ultrasonic hearing in lesser wax moths: batsavoidance and pair formation. Physiol Entomol 2004, 29:159-168.

32. Hobel G, Schul J: Listening for males and bats: spectralprocessing in the hearing organ of Neoconocephalusbivocatus (Orthoptera: Tettigoniidae). J Comp Physiol A 2007,193:917-925.

33. Nakano R, Takanashi T, Fujii T, Skals N, Surlykke A, Ishikawa Y:Moths are not silent, but whisper ultrasonic courtship songs. JExp Biol 2009, 212:4072-4078.

34. Schul J, Sheridan RA: Auditory stream segregation in an insect.J Neurosci 2006, 138:1-4.

35. Pollack GS, Martins R: Flight and hearing: ultrasound sensitivitydiffers between flight-capable and flight-incapable morphs of awing-dimorphic cricket species. J Exp Biol 2007, 210:3160-3164.

36. Fullard JH, Dawson JW, Otero LD, Surlykke A: Bat deafness inday-flying moths (Lepidoptera, Notodontidae, Dioptinae). JComp Physiol A 1997, 181:477-483.

37. Yack JE, Kalko EKV, Surlykke A: Neuroethology of ultrasonichearing in nocturnal butterflies (Hedyloidea). J Comp Physiol A2007, 193:577-590.

38.�

Fullard JH, ter Hofstede HM, Ratcliffe JM, Pollack GS, Brigidi GS,Tinghitella RM, Zuk M: Release from bats: genetic distance andsensoribehavioural regression in the Pacific field cricket,Teleogryllus oceanicus. Naturwissenschaften 2010, 97:53-61.

This is the most thorough study to date documenting the effects ofvarying levels of bat predation pressure on the maintenance of auditorystructure, ultrasound CNS processing, and evasive behavior.


39. Yager DD, Svenson GJ: Patterns of praying mantis auditorysystem evolution based on morphological, molecular,neurophysiological, and behavioural data. Biol J Linn Soc 2008,94:541-568.

40. Ghose K, Triblehorn JD, Bohn K, Yager DD, Moss CF: Behavioralresponses of big brown bats to dives by praying mantises. JExp Biol 2009, 212:693-703.

41. Yager DD, May ML, Fenton MB: Ultrasound-triggered, flight-gated evasive maneuvers in the praying mantisParasphendale agrionina. J Exp Biol 1990, 152:17-39.

42. Ratcliffe JM, Fullard JH, Arthur BJ, Hoy RR: Tiger moths and thethreat of bats: decision-making based on the activity of asingle sensory neuron. Biol Lett 2009, 5:368-371.

43. Ratcliffe JM, Fullard JH, Arthur BJ, Hoy RR: Adaptive auditoryrisk assessment in the dogbane tiger moth when pursued bybats. Proc R Soc B 2010, 278:364-370.

44. Jones G, Barabas A, Elliott W, Parsons S: Female greater waxmoths reduce sexual display behavior in relation to thepotential risk of predation by echolocating bats. Behav Ecol2002, 13:375-380.

45. Nolen TG, Hoy RR: Initiation of behavior by single neurons: therole of behavioral context. Science 1984, 226:992-994.

46. Triblehorn JD, Yager DD: Implanted electrode recordings from apraying mantis auditory interneuron during flying bat attacks.J Exp Biol 2002, 205:307-320.

47. Triblehorn JD, Yager DD: Timing of praying mantis evasiveresponses during simulated bat attack sequences. J Exp Biol2005, 208:1867-1876.

48. Hartbauer M, Radspieler G, Romer H: Reliable detection ofpredator cues in afferent spike trains of a katydid under highbackground noise levels. J Exp Biol 2010, 213:3036-3046.

49. Svensson GP, Lofstedt C, Skals N: The odor makes thedifference: male moths attracted by sex pheromones ignorethe threat by predatory bats. Oikos 2004, 104:91-97.

50. Skals N, Anderson P, Kanneworff M, Lofstedt C, Surlykke A: Herodours make him deaf: crossmodal modulation of olfactionand hearing in a male moth. J Exp Biol 2005, 208:595-601.

51. Gillam EH, Westbrook JK, Schleider PG, McCracken GF: Virtualbats and real insects: effects of echolocation on pheromone-tracking behavior of male corn earworm moths, Helicoparvazea. Southwestern Nat 2011, 56:103-107.

52.�

Brunel-Pons O, Alem S, Greenfield MD: The complex auditoryscene at leks: balancing antipredator behavior andcompetitive 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 madeby a moth that produces ultrasound to attract mates, but must do this in acompetitive 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 mothsassist 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 ultrasoundin moth intraspecific communication than previously thought. This is thefirst report of male moths mimicking bats to elicit defensive behavior inconspecific females.

54. Nakano R, Takanashi T, Skals N, Surlykke A, Ishikawa Y: Tofemales of a noctuid moth, male courtship songs are nothingmore than bat echolocation calls. Biol Lett 2011, 6:582-584.

55. Svensson GP, Lofstedt C, Skals N: Listening in pheromoneplumes: disruption of olfactory-guided mate attraction in amoth by a bat-like ultrasound. J Insect Sci 2007, 7:1536-2442.

56.�

Anton S, Evengaard K, Barrozo RB, Anderson P, Skals N: Briefpredator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect. ProcNatl Acad Sci USA 2011, 108:3401-3405.

This study provides the first neural evidence of brain plasticity induced byultrasound that could bias cost–benefit decisions at a much later time.


Predator detection and evasion by flying insects

Documents

Transcript of Predator detection and evasion by flying insects