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

Lead Research Organisation: University of Bristol
Department Name: Biological Sciences


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.

Technical Summary

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.


10 25 50
Description Key achievements per work package:
• WP1: We developed a measurement-based perceptual space model, and applied it to a community of 15 UK noctuid moth and 5 aerial-hawking bat species. Quantitative predictions were verified by measured real-world detection ranges. Most significantly, the model predicts a novel stealth hunting strategy, which we indeed discovered in the rare UK barbastelle bat.
• WP2: We related moth evasive manoeuvres to the neural activity elicited by bat calls during attack. Confirming Roeder's prediction, the onset of the A2 cell activity matched the onset of evasive manoeuvres in all noctuid moth species studied. Manoeuvres were stereotypic rather than unpredictable, yet proved highly successful.
• WP3: We linked tympanal mechanics to neural coding in moths. Tympanum displacement determined neural thresholds independent of frequency, and tympanal mechanics was unaffected by dissection. Thus we validated standard neurophysiological approaches, and propose laser vibrometry as non-invasive alternative for threshold analysis
Exploitation Route Methods used and developed by us were also used by our colleagues Aaron Corcoran from Wake Forest University in North Carolina in the publication in Science on Sonar Jamming in November 2014 in Science
Sectors Aerospace, Defence and Marine,Environment

Description By researchers in the field of biological and man-made sonar and radar. New collaboration with Dr Alessio Balleri, Centre for Electronic Warfare, Cranfield Defence and Security
First Year Of Impact 2010
Sector Aerospace, Defence and Marine,Environment
Description Dryland Research - Specific Support Action (SSA)
Amount ‏93,000 ₪ (ILS)
Organisation Ben-Gurion University of the Negev 
Department Jacob Blaustein Centre for Scientific Cooperation
Sector Academic/University
Country Israel
Start 06/2008 
End 09/2008
Description RCUK National Science & Engineering Week Awards 2010
Amount £1,309 (GBP)
Organisation Research Councils UK (RCUK) 
Sector Public
Country United Kingdom
Start 07/2010 
End 09/2010
Title Data from: Neural representation of bat predation risk and evasive flight in moths: a modelling approach 
Description Most animals are at risk from multiple predators and can vary anti-predator behaviour based on the level of threat posed by each predator. Animals use sensory systems to detect predator cues, but the relationship between the tuning of sensory systems and the sensory cues related to predator threat are not well-studied at the community level. Noctuid moths have ultrasound-sensitive ears to detect the echolocation calls of predatory bats. Here, combining empirical data and mathematical modelling, we show that moth hearing is adapted to provide information about the threat posed by different sympatric bat species. First, we found that multiple characteristics related to the threat posed by bats to moths correlate with bat echolocation call frequency. Second, the frequency tuning of the most sensitive auditory receptor in noctuid moth ears provides information allowing moths to escape detection by all sympatric bats with similar safety margin distances. Third, the least sensitive auditory receptor usually responds to bat echolocation calls at a similar distance across all moth species for a given bat species. If this neuron triggers last-ditch evasive flight, it suggests that there is an ideal reaction distance for each bat species, regardless of moth size. This study shows that even a very simple sensory system can adapt to deliver information suitable for triggering appropriate defensive reactions to each predator in a multiple predator community. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
Description Cranfield PhD co-supervision 
Organisation Cranfield University
Country United Kingdom 
Sector Academic/University 
PI Contribution Co-supervision and project development for a PhD on adaptive radar signal design.
Collaborator Contribution Provide radar measurement facilities, host PhD student
Impact Two publications in 2014 alone.
Start Year 2013
Description IS 
Organisation Ben-Gurion University of the Negev
Department Mitrani Department of Desert Ecology
Country Israel 
Sector Academic/University 
PI Contribution Conducting field research in IS, equipment and experimental expertise, data collection, training of local staff
Collaborator Contribution Hosting us for research visits, providing infrastructural support, access to laboratories, transportation, general research logistics
Impact One joint PhD student on a related project (now finished) - including twp publications One joint MSc by Research student (starting in spring 2015) Annual research visits
Start Year 2009
Description Bot 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact the talk and interactive activities sparked interactions and started a collaboration with the botanical gardens

The botanical gardens now grow plants in their main exhibit that have links to bat echolocation, active strategy to expand such plant species in their collection
Year(s) Of Engagement Activity 2009
Description FN 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Many interactions with visitors at our interactive displays, sparked discussions, inspired future students

One of my PhD students manning these stalls has subsequently been employed by one of the main contributors to the Festival of Nature,
Year(s) Of Engagement Activity 2009,2010
Description NBC 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Gave talk, received great responses from the community of bat consultants

several short-term collaborations as a consequence, including co-supervision of UG student projects and research into bat detector calibration
Year(s) Of Engagement Activity 2008
Description NSEW 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? Yes
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Interactive displays during the week, hundreds of visitors, excitement

Raise local and regional perception and profile of UoB, in particular regarding recruiting from the WP market
Year(s) Of Engagement Activity 2010