Available online at www.sciencedirect.com

Predator detection and evasion by flying

David D Yager

Echolocating bats detect prey using ultrasonic pulses, and ‘arms race’ between hearing insects and bats [5], although

many nocturnally flying insects effectively detect and evade ‘diffuse coevolution’ might better describe a system with

these predators through sensitive ultrasonic hearing. Many many species of prey and predator [6]. An emerging

eared insects can use the intensity of the predator-generated theme in this story is behavioral and neural

ultrasound and the stereotyped progression of bat economics — balancing the benefits of hunting and eva-

echolocation pulse rate to assess risk level. Effective sion against the costs in terms of energetics and, especi-

responses can vary from gentle turns away from the threat (low ally for the prey, of the disruption of other important

risk) to sudden random flight and dives (highest risk). Recent behaviors such as finding a mate. Thus, the assessment of

research with eared moths shows that males will balance risk and of potential benefit along with the mechanisms of

immediate bat predation risk against reproductive opportunity decision-making have become key research topics.

as judged by the strength and quality of conspecific

pheromones present. Ultrasound exposure may, in fact, bias The detection system

such decisions for up to 24 hours through plasticity in the CNS auditory systems are based on the standard pres-

olfactory system. However, brain processing of ultrasonic sure-detector design with a vibrating membrane (tympa-

stimuli to yield adaptive prey behaviors remains largely num) backed by an internal airspace for increased

unstudied, so possible mechanisms are not known. sensitivity, and a transducing mechanism with as few

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

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

Department of Psychology and Neuroscience and Cognitive Science

Figure 1). Sensitivity and tuning are determined primar-

Program, University of Maryland, College Park, MD 20742, United States

ily in the periphery through bioacoustic characteristics of

the tympanum and associated structures (studied most

Corresponding author: Yager, David D ([email protected])

recently using scanning laser vibrometry; for instance, [8])

and/or properties of the receptor structures that are not

Current Opinion in Neurobiology 2012, 22:201–207

yet fully understood. The range of frequencies to which a

particular species is most sensitive is matched to the

This review comes from a themed issue on

Neuroethology dominant echolocation frequencies used by the sympatric

Edited by Michael Dickinson and Cynthia Moss bat assemblage, typically 20–60 kHz, but sometimes

extending beyond 100 kHz (Figure 2) [5]. Predator-

Available online 7th January 2012

generated sounds outside that range will be relatively

0959-4388/$ – see front matter inaudible to the insect. Sensitivity determines the

# 2011 Elsevier Ltd. All rights reserved.

response time available to the prey. The echolocation

cries of aerial hawking bats are typically intense (>120 dB

DOI 10.1016/j.conb.2011.12.011

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 ].

Introduction Considering typical insect and bat flight speeds, this

Many insects have tympanate ears that provide them with translates to an available response time of >1 s, more

sensitive hearing at frequencies from a few kHz to over than adequate for predator recognition and evasion [11].

100 kHz depending on the species. There have been at

least 18 independent evolutions of pressure-sensitive Neural processing

hearing yielding ears of diverse shapes, sizes, and Remarkably little is known about the ‘higher’ CNS pro-

locations on the body [1,2]. Having two ears is the norm, cessing that controls ultrasound-based defensive beha-

but most praying have just one and a pneumorid viors. Past studies have focused primarily on the afferent

has six pairs. Insects including crickets, grass- side and the activities of a few key interneurons such as

hoppers, water bugs, cicadas, and some butterflies and AN2 of crickets, 501-T3 of mantises, the T-cell of tetti-

moths use hearing as part of intraspecific communication goniids, and IN533 and IN714 of locusts [12]. However, the

systems [3]. A few — most notably parasitoid flies that head is necessary for evasive behavior, at least in pyralid

target singing male crickets as hosts — use hearing to find moths, mantises, tettigoniids, tiger beetles, and crickets. In

prey [4]. Finally, many insects, additionally or exclu- the last of these, there are at least 20 ultrasound-sensitive

sively, use their hearing to detect and evade predators, brain neurons, seven of which have descending axons [13].

which, for flying nocturnal insects means echolocating Cephalic ultrasound processing is brief (<20 ms; [13,14]).

bats. This is the well-known story of the coevolutionary Its role could simply be conditionally permissive, for

www.sciencedirect.com Current Opinion in Neurobiology 2012, 22:201–207 202 Neuroethology

Figure 1

(c) (a)

* Ganglion

N.7

Dorsal

TS Rostral

(d) BS

*

Tympanum

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 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 Ultrasound-triggered evasion and defense

present to initiate evasive behavior controlled by thoracic Most responses to ultrasonic pulses involve a change in

circuitry. Alternatively, the cephalic ganglia may play a flight path, and many eared insects have a repertoire of

more ‘hands on’ role. The data are not yet available to defensive strategies depending on context and level of



distinguish among these and other possibilities. risk [15 ] (Figure 3). The strategies of: 1) getting out of

Current Opinion in Neurobiology 2012, 22:201–207 www.sciencedirect.com

Hearing aerial predators Yager 203

Figure 2

90

Sphodromantis aurea Miomantis sp. 80 Miomantis abyssinica

70 Threshold (dB SPL) 60

50 10 20 30 40 50 60 70 80 90 100 110 120 130 Frequency (KHz)

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 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 and Batesian mimicry complexes among sympatric beetles

attack through some combination of startle and sudden, and moths [20,21].

random flight path changes serve hearing insects well. In

the few cases for which it has been measured in free-flight Bats foster false negatives in the insect defensive system.

bat-insect encounters (noctuid moths, green lacewings, and First, echolocation frequencies and intensities outside the

praying mantises), sound-triggered evasion confers a 40– insect’s detection capabilities could achieve this. Bats

50% survival advantage over nonhearing conspecifics [16]. that take prey from a substrate (gleaners) often use very

It is worth noting that dietary analysis for some bat species low intensity pulses that their insect prey cannot hear as

shows a high percentage of hearing insects (for instance shown by neural recordings [22,23]. An aerial insectivore,

[17]). However, without accompanying data about relative Barbastella barbastella, uses echolocation frequencies of

abundance of size-appropriate hearing and nonhearing prey 30–40 kHz, but at amplitudes 20–40 dB lower that other

or direct observations of capture success rates, it is not aerial insectivores. It is highly successful at capturing



possible to infer the effectiveness of auditory defenses. eared moths [10 ]. Echolocation calls at frequencies out-

side an insect’s hearing range could also work [24–26].

Tiger moths (Arctiidae) implement the unusual strategy of Several studies have found a high proportion of eared

producing intense ultrasonic clicks when they hear pulsed moths in the diets of bat species using frequencies

ultrasound [18]. Faced with an oncoming bat, clicking >70 kHz like the Old World rhinolophid and hipposi-

arctiids do not alter their flight path and yet survive because derid bats. This is above the most sensitive hearing range

the bats break off their attack [19]. The long-standing for most insects, although some moths and praying man-

question of how the clicking works to deter bats has been tises have extended their ranges to >100 kHz (Figure 2).

resolved through an elegant series of experiments using Secondly, at least some bats project their calls in a

naive bats and several species of arctiids having different relatively narrow cone of sound that they sweep across

ecologies. In fact, all of the traditional rival hypotheses — the immediate environment [27]. This strategy greatly

advertising distastefulness, startling the bat, and jamming reduces their detectability. Even an insect with sensitive

the echolocation system — are correct. Which one dom- hearing could be surprised by the bat and have insuffi-

inates depends on the moth species and its ecology and on cient time to respond effectively.



the past experience of the bat [15 ]. Flying tiger beetles,

some of which are distasteful, also click in response to Ultrasound serves multiple functions for bats (hunting,

ultrasound, opening the possibility of intricate Mu¨llerian obstacle avoidance, intraspecific interactions; [28]), which

www.sciencedirect.com Current Opinion in Neurobiology 2012, 22:201–207 204 Neuroethology

Figure 3

(a) Before ultrasound (b)

(c) Strong dive Moderate dive Slight dive 80 Level tum No response 60

40 Percentage of responses Percentage 20

After ultrasound 1-3 m. 3-5 m. 5-7 m. 7-9 m. 9-10 m. > 10 m. 85-74 dB 74-70 dB 70-67 dB 67-65 dB 65-64 dB < 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 energy expenditure, and it diverts effort and time from

for particular echolocation call design features exclusively other crucial activities like eating and mating.

to countering evasion capabilities of prey [6,29]. None-

theless, an ecological approach studying bat assemblages The costs for insects to maintain an auditory system for

in southern Africa suggests that dealing with prey bat evasion have been addressed indirectly in many

defenses is a significant contributor to bat community studies comparing auditory structure and function in

structure via common echolocation parameters [30]. morphs of a single species [35] and in closely related taxa

Although less common, some insects use their ultrasonic differing in their history of exposure to bats. Some taxa of

hearing for a second function, reproductive signaling. The moths that have become diurnal have lost high-frequency

functions are decoded by context [31], signal character- hearing [36]. The few species of butterflies that have

istics [32,33] and even an analog to vertebrate ‘auditory become nocturnal have evolved ultrasonic hearing [37].



stream segregation’ [34]. Fullard and colleagues [38 ] combined genetic data with

neurophysiological and behavioral results among multiple

geographic populations of a single cricket species, Tele-

Economics of auditory predator detection and ogryllus oceanicus, living under a range of bat predation

evasion pressures. Populations with no history of predation

Predator evasion is costly. It requires the maintenance of a showed both reduction of defensive behavior and

sensory detection and processing system, it requires reduction in the activity of the interneuron neuron

Current Opinion in Neurobiology 2012, 22:201–207 www.sciencedirect.com

Hearing aerial predators Yager 205

(AN2) necessary and sufficient to elicit it. In many species away from the threat, that do not seriously interrupt the

of praying mantis, males fly at night and have sensitive ongoing behavior. In the same animals, high intensity

ultrasonic hearing, but the females are flightless with ultrasound triggers a ‘last ditch’ response including rapid

reduced or absent ears [39]. Although there are some erratic flight, steep dives, or complete flight cessation

counterexamples, the general picture is that the benefit of (dropping). Recently, Ratcliffe and colleagues [42] have

ultrasonic hearing is very high, but the cost is must be suggested an intensity-based two-threshold mechanism

significant as well. in moths with low versus high intensity behavior deter-

mined by combined spike number of the A1 and the

Because the bat auditory system is used for other pur- higher threshold A2 receptors. Some insects make a more

poses as well [28], the costs of echolocation specifically for nuanced risk assessment taking advantage of the stereo-

hunting are primarily energetic. This can work to the typed changes in echolocation pulse rate as a capture

prey’s advantage. For example, a mantis executing an attempt progresses (Figure 4). For instance, arctiid moths

evasive power dive from >5 m above the ground, a can distinguish between early and late attack echoloca-

common flight altitude in the field, could rarely escape tion call patterns based on rate alone [43]. Both arctiid and

a bat in a prolonged chase because of the latter’s greater pyralid moths alter their behavior (clicking rate and

flight speed and adaptive targeting strategies [40]. Yet pheromone signaling, respectively) depending on preda-

bats often break off the chase before capture [41], pre- tion risk, defined as a combination of intensity and pulse

sumably because an extended pursuit can be costly in pattern of ultrasonic stimuli [43,44]. If the same threat

time, energy, and in the risk of collision with vegetation or parameters elicit spike repetition rates above a threshold

the ground. To survive, the mantis does not have to be level of 180/s in the cricket auditory interneuron Int-1

impossible to catch, only too expensive. (=AN2) the initiates a evasive turn [45]. In praying

mantises (Figure 4), the initiation of the full power dive

Auditory risk assessment can reduce cost for insects by corresponds to an echolocation pulse rate of 50–55 pps,

minimizing false positives and by allowing the level of which typically occurs at the transition from approach to

defensive response to be tailored to the threat. A simple terminal phase of the attack, 250–350 ms before potential

version of risk assessment based on the intensity of capture [46,47]. Hartbauer and colleagues [48] have

ultrasound is well documented in moths, praying man- demonstrated a novel thoracic neuronal mechanism in

tises, crickets, tachinid flies, and tettigoniids. Low inten- a katydid that allows bat threat assessment based on

sity ultrasonic pulses (a distant bat) trigger low intensity repetition rate even in the face of intense ultrasonic

behaviors, often deviations of the flight path to move 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].

www.sciencedirect.com Current Opinion in Neurobiology 2012, 22:201–207

206 Neuroethology

Increasing evidence, especially from eared moths, shows insects — processing and plasticity in the brain control

that insects can use auditory risk assessment in a cost/ systems for bat evasive behaviors.

benefit ‘decision’ balancing predator evasion against a

reproductive opportunity. Male moths flying toward a Acknowledgment

Preparation of this paper was supported by National Science Foundation

pheromone source (a female in the wild or an artificial

Grant #IOS-0746037.

source in a wind tunnel) respond less vigorously or less

often to ultrasonic pulses than controls without the phero-

References and recommended reading

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 of special interest

dives by flying males. Skals et al. [50] were able to titrate the

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37. Yack JE, Kalko EKV, Surlykke A: Neuroethology of ultrasonic

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sensoribehavioural regression in the Pacific field cricket,  predator sound exposure elicits behavioral and neuronal long-

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This is the most thorough study to date documenting the effects of Natl Acad Sci USA 2011, 108:3401-3405.

varying levels of bat predation pressure on the maintenance of auditory This study provides the first neural evidence of brain plasticity induced by

structure, ultrasound CNS processing, and evasive behavior. ultrasound that could bias cost–benefit decisions at a much later time.

www.sciencedirect.com Current Opinion in Neurobiology 2012, 22:201–207