Aaron J. Corcoran

Sound Strategies: The 65-Million-Year-Old Battle Between Bats and Insects

The intimate details regarding the coevolution of bats and moths have been elucidated over the past 50 years. The bat-moth story began with the evolution of bat sonar, an exquisite ultrasonic system for tracking prey through the night sky. Moths countered with ears tuned to the high frequencies of bat echolocation and with evasive action through directed turns, loops, spirals, drops, and power dives. Some bat species responded by moving the frequency and intensity of their echolocation cries away from the peak sensitivity of moth ears, and the arms race was on. Tiger moths countered by producing anti-bat sounds. Do the sounds advertise moth toxicity, similar to the bright coloration of butterflies; do they startle the bat, giving the moth a momentary advantage in their aerobatic battle; or do they jam the sonar of the bat? The answer is yes. They do all and more in different situations and in different species. Any insect that flies at night must deal with bat predation. Beetles, mantids, true crickets, mole crickets, katydids, green lacewings, and locusts have anti-bat strategies, and we have just scratched the surface. In an exciting new twist, researchers are taking the technologies developed in the laboratory back into the field, where they are poised to appreciate the full richness of this remarkable predator-prey interaction.

Sonar jamming in the field: effectiveness and behavior of a unique prey defense

SUMMARY Bats and insects provide a model system for integrating our understanding of predator–prey ecology, animal behavior and neurophysiology. Previous field studies of bat–insect interactions have been limited by the technological challenges involved with studying nocturnal, volant animals that use ultrasound and engage in battles that frequently last a fraction of a second. We overcame these challenges using a robust field methodology that included multiple infrared cameras calibrated for three-dimensional reconstruction of bat and moth flight trajectories and four ultrasonic microphones that provided a spatial component to audio recordings. Our objectives were to document bat–moth interactions in a natural setting and to test the effectiveness of a unique prey defense – sonar jamming. We tested the effect of sonar jamming by comparing the results of interactions between bats and Grote’s tiger moth, Bertholdia trigona, with their sound-producing organs either intact or ablated. Jamming was highly effective, with bats capturing more than 10 times as many silenced moths as clicking moths. Moths frequently combined their acoustic defense with two separate evasive maneuvers: flying away from the bat and diving. Diving decreased bat capture success for both clicking and silenced moths, while flying away did not. The diving showed a strong directional component, a first for insect defensive maneuvers. We discuss the timing of B. trigona defensive maneuvers – which differs from that of other moths – in the context of moth auditory neuroethology. Studying bat–insect interactions in their natural environment provides valuable information that complements work conducted in more controlled settings.

How moths escape bats: predicting outcomes of predator–prey interactions

ABSTRACT What determines whether fleeing prey escape from attacking predators? To answer this question, biologists have developed mathematical models that incorporate attack geometries, pursuit and escape trajectories, and kinematics of predator and prey. These models have rarely been tested using data from actual predator–prey encounters. To address this problem, we recorded multi-camera infrared videography of bat–insect interactions in a large outdoor enclosure. We documented 235 attacks by four Myotis volans bats on a variety of moths. Bat and moth flight trajectories from 50 high-quality attacks were reconstructed in 3-D. Despite having higher maximum velocity, deceleration and overall turning ability, bats only captured evasive prey in 69 of 184 attacks (37.5%); bats captured nearly all moths not evading attack (50 of 51; 98%). Logistic regression indicated that prey radial acceleration and escape angle were the most important predictors of escape success (44 of 50 attacks correctly classified; 88%). We found partial support for the turning gambit mathematical model; however, it underestimated the escape threshold by 25% of prey velocity and did not account for prey escape angle. Whereas most prey escaping strikes flee away from predators, moths typically escaped chasing bats by turning with high radial acceleration toward ‘safety zones’ that flank the predator. This strategy may be widespread in prey engaged in chases. Based on these findings, we developed a novel geometrical model of predation. We discuss implications of this model for the co-evolution of predator and prey kinematics and pursuit and escape strategies. Summary: Three-dimensional reconstructions of bat–insect interactions reveal that prey survive chases by escaping into ‘safety zones’ that flank predators.

Optimal Predator Risk Assessment by the Sonar-Jamming Arctiine Moth Bertholdia trigona

Nearly all animals face a tradeoff between seeking food and mates and avoiding predation. Optimal escape theory holds that an animal confronted with a predator should only flee when benefits of flight (increased survival) outweigh the costs (energetic costs, lost foraging time, etc.). We propose a model for prey risk assessment based on the predators stage of attack. Risk level should increase rapidly from when the predator detects the prey to when it commits to the attack. We tested this hypothesis using a predator – the echolocating bat – whose active biosonar reveals its stage of attack. We used a prey defense – clicking used for sonar jamming by the tiger moth Bertholdia trigona– that can be readily studied in the field and laboratory and is enacted simultaneously with evasive flight. We predicted that prey employ defenses soon after being detected and targeted, and that prey defensive thresholds discriminate between legitimate predatory threats and false threats where a nearby prey is attacked. Laboratory and field experiments using playbacks of ultrasound signals and naturally behaving bats, respectively, confirmed our predictions. Moths clicked soon after bats detected and targeted them. Also, B. trigona clicking thresholds closely matched predicted optimal thresholds for discriminating legitimate and false predator threats for bats using search and approach phase echolocation – the period when bats are searching for and assessing prey. To our knowledge, this is the first quantitative study to correlate the sensory stimuli that trigger defensive behaviors with measurements of signals provided by predators during natural attacks in the field. We propose theoretical models for explaining prey risk assessment depending on the availability of cues that reveal a predators stage of attack.

Sensing in a noisy world: lessons from auditory specialists, echolocating bats

ABSTRACT All animals face the essential task of extracting biologically meaningful sensory information from the ‘noisy’ backdrop of their environments. Here, we examine mechanisms used by echolocating bats to localize objects, track small prey and communicate in complex and noisy acoustic environments. Bats actively control and coordinate both the emission and reception of sound stimuli through integrated sensory and motor mechanisms that have evolved together over tens of millions of years. We discuss how bats behave in different ecological scenarios, including detecting and discriminating target echoes from background objects, minimizing acoustic interference from competing conspecifics and overcoming insect noise. Bats tackle these problems by deploying a remarkable array of auditory behaviors, sometimes in combination with the use of other senses. Behavioral strategies such as ceasing sonar call production and active jamming of the signals of competitors provide further insight into the capabilities and limitations of echolocation. We relate these findings to the broader topic of how animals extract relevant sensory information in noisy environments. While bats have highly refined abilities for operating under noisy conditions, they face the same challenges encountered by many other species. We propose that the specialized sensory mechanisms identified in bats are likely to occur in analogous systems across the animal kingdom. Summary: Researchers use echolocating bats – with their adaptations for sound production and reception – as models for understanding how animals sense and communicate in noisy environments.

Inconspicuous echolocation in hoary bats (Lasiurus cinereus)

Echolocation allows bats to occupy diverse nocturnal niches. Bats almost always use echolocation, even when other sensory stimuli are available to guide navigation. Here, using arrays of calibrated infrared cameras and ultrasonic microphones, we demonstrate that hoary bats (Lasiurus cinereus) use previously unknown echolocation behaviours that challenge our current understanding of echolocation. We describe a novel call type (‘micro’ calls) that has three orders of magnitude less sound energy than other bat calls used in open habitats. We also document bats flying close to microphones (less than 3 m) without producing detectable echolocation calls. Acoustic modelling indicates that bats are not producing calls that exceed 70–75 dB at 0.1 m, a level that would have little or no known use for a bat flying in the open at speeds exceeding 7 m s−1. This indicates that hoary bats sometimes fly without echolocation. We speculate that bats reduce echolocation output to avoid eavesdropping by conspecifics during the mating season. These findings might partly explain why tens of thousands of hoary bats are killed by wind turbines each year. They also challenge the long-standing assumption that bats—model organisms for sensory specialization—are reliant on sonar for nocturnal navigation.

Bats (Tadarida brasiliensis) jam conspecifics in food competition

We here describe field experiments testing whether bats adaptively produce sounds to interfere with (“jam”) the echolocation of other bats. Visual observations, low-light videography, and ultrasound recording with microphone arrays allowing reconstruction of bat flight paths were used to document interactions between Mexican free-tailed bats (Tadarida brasiliensis) at two foraging locations in southern Arizona and New Mexico. We tested three sets of predictions based on the jamming hypothesis and two competing hypotheses—cooperative foraging and food patch defense. Bats produced putative jamming calls (termed sinFM calls) that overlapped temporally and spectrally with “feeding buzz” calls made by conspecifics when attacking insects. Bat capture success decreased by 400% when sinFM calls were present compared to when they were absent. Behavioral sequences consisted of two or more bats sequentially making feeding buzzes within a restricted area while another bats made sinFM calls. After making sinFM calls b...