Bats and moths in the real world: neuronal responses as adaptations to predation

Interactions between bats and insects have long fascinated evolutionary biologists. Bats use echolocation to detect and track nocturnal insects, and about 70% of bat species worldwide eat insects. In defence, insects in at least 7 orders have evolved ears that pick up the ultrasonic frequencies emitted by echolocating bats. These ears are often simple in structure, but highly effective for triggering escape behaviours that reduce the risk of the insect being eaten. Ears have been most studied in moths, where 1-4 sensory cells send signals to the central nervous system, which can then trigger a range of behavioural responses ranging from flight away from the signal source to unpredictable complex looping manoeuvres. Interactions between bats and moths are often viewed as an evolutionary arms race, with adaptations in the echolocation calls of bats driving adaptations in the hearing responses of insects, which in turn shape the further evolution of echolocation signals in bats. To date, most work on interactions between bats and moths has taken place in the laboratory. We aim to study these interactions in nature, and this is important because bat echolocation calls differ substantially in field and laboratory conditions. We will therefore use moths as biological microphones, recording responses of auditory neurones along the flight paths of bats. We will test whether the distance at which moths detect the echolocation calls of bat species (with differing frequency, time and intensity parameters) depends on signal design. We can quantify detection distances accurately because we can pinpoint the bat's position accurately in 3-dimensions by measuring time-of-arrival differences at an array of microphones. We can also calculate the intensity of the bat calls at known positions by using a measuring microphone, allowing us to measure the sound pressure level that triggers a neural response in the moth. We will also quantify the evasive manoeuvres used by moths in the dark by recording their flight paths using two video cameras and infrared lighting. We can then categorise the escape manoeuvres used by moths, and relate these to signal designs used by bats. These methods will allow us to test the hypothesis that moths fly away from distant bats, and only perform unpredictable escape manoeuvres when bats are close by (and hence emitting more intense signals). Our first video recording of a moth evading a bat attack has shown it to use a manoeuvre previously described as a method to avoid attack in dogfights by aircraft! We will take our knowledge from the field into the laboratory to test our predictions under more controlled conditions. We will play back some of the attack sequences emitted by bats to moth preparations. Our recent work, published in Current Biology, suggests that moths can change their hearing responses in relation to the intensity of the sound source. At low sound intensities, moth ear membranes are sensitive to low frequencies, at higher intensities they become more sensitive to higher frequencies. Such changes in hearing sensitivity were totally unexpected. The changes make perfect sense from an adaptive perspective however / bats often use higher frequencies when they home in on insects than when they are searching for them. Our field recordings will give an accurate picture of how signal design changes in prey capture, and by monitoring responses of the eardrum (by laser vibrometry) we can establish whether simultaneous responses operate at the neural level by recording from the auditory nerve. We believe that understanding predator-prey interactions can best advance by performing studies in natural conditions. Our work will determine how moth hearing responds to bat echolocation in the field, how moths respond behaviourally to bat calls of known structure and intensity, and whether moths can adjust their auditory responses to best detect bats in an active manner.

Moths evolved ears primarily to detect bats. On hearing calls, many moths fly away from the sound or initiate escape manoeuvres, yet it is largely unknown how complex acoustic scenes are translated into estimates of predation pressure to release an appropriate behavioural response. We aim to quantify this process in nature using novel techniques. Stereo-videogrammetry allows us to reconstruct aerial bat-moth interactions in 3D. We will quantify reaction distances, timing and strategies of last ditch evasive responses. Simultaneously, we will record bat calls with a calibrated microphone. Because we know the bat's and the moth's positions, accurate on-axis reconstructions of the acoustic scene experienced by the moth are possible, which will then allow us to relate flight manoeuvres and reaction distances to acoustic information available to the moth, in particular to sound pressure levels. We will use moths as biological microphones to quantify neuronal responses to bat predation in the field. A calibrated microphone will allow us to relate neural reactions to call source levels. At the same time we will track the bats' positions with a microphone array, which evaluates differences in the time of arrival of its calls, to measure detection distances directly. Finally, we will replay reconstructed acoustic scenes in the lab while recording tympanal responses from moths. We will also use a scanning laser vibrometer to study the role and mechanism of the recently discovered dynamic auditory tuning in moth ears. The study is innovative because it relates moth auditory responses to bat flight trajectories. It will be the first study to measure the intensity of bat calls at the same time as documenting neural responses of moths. It will be the first attempt to quantify escape manoeuvres of moths, and to test the 'graded response' hypothesis of escape behaviour. Most importantly, we will investigate dynamic auditory tuning in response to realistic bat call sequences.