Moth tails divert bat attack: Evolution of acoustic deflection

Abstract

Adaptations to divert the attacks of visually guided predators have evolved repeatedly in animals. Using high-speed infrared videography, we show that luna moths (Actias luna) generate an acoustic diversion with spinning hindwing tails to deflect echolocating bat attacks away from their body and toward these nonessential appendages. We pit luna moths against big brown bats (Eptesicus fuscus) and demonstrate a survival advantage of ∼47% for moths with tails versus those that had their tails removed. The benefit of hindwing tails is equivalent to the advantage conferred to moths by bat-detecting ears. Moth tails lured bat attacks to these wing regions during 55% of interactions between bats and intact luna moths. We analyzed flight kinematics of moths with and without hindwing tails and suggest that tails have a minimal role in flight performance. Using a robust phylogeny, we find that long spatulate tails have independently evolved four times in saturniid moths, further supporting the selective advantage of this anti-bat strategy. Diversionary tactics are perhaps more common than appreciated in predator-prey interactions. Our finding suggests that focusing on the sensory ecologies of key predators will reveal such countermeasures in prey.antipredator defense | bat-moth interactions | Lepidoptera | Saturniidae P redators are under pressure to perform incapacitating initial strikes to thwart prey escape. It is thought that prey, in turn, have evolved conspicuous colors or markings to deflect predator attack to less vulnerable body regions (1, 2). Eyespots are a wellknown class of proposed deflection marks (3), which are found in a variety of taxa, including Lepidoptera (3) and fishes (4), but only recently have experiments convincingly demonstrated that these color patterns redirect predatory assault. Eyespots on artificial butterfly (5) and fish (4) prey draw strikes of avian and fish predators. Eyespots on the wing margins of woodland brown butterflies (Lopinga achine) lure the attacks of blue tits (Cyanistes caeruleus) (6). Brightly colored lizard tails also divert avian predator attacks to this expendable body region (7).Deflection coloration is unlikely to be an effective strategy against echolocating bats, as these predators have scotopic vision and poor visual acuity unsuited for prey localization and discrimination (8). Most bats rely on echoes from their sonar cries to image prey and other objects in their environment-they live in an auditory world (9). Thus, we would expect a deflection strategy, effective against bats, to present diversionary acoustic signatures to these hearing specialists. Weeks (10) proposed that saturniid hindwing tails might serve to divert bat attacks from essential body parts. We hypothesized that saturniid tails, spinning behind a flying moth (Movie S1) and reflecting sonar calls, serve as either a highly contrasting component of the primary echoic target or as an alternative target. We predicted that bats would aim their attacks at moth tails, instead of the wings or body, durin...

Evolutionary escalation: the bat–moth arms race

“…The distinctive combination of echolocation and powered flight allowed bats to first exploit, then dominate the foraging niche of night-flying insects. Bat predation drove selection for both bat-detecting ears and non-auditory means of avoiding bats in a variety of insects, including moths and butterflies that never evolved ears and remain deaf to bats (Fullard and Napoleone, 2001;Barber et al, 2015).…”

Tempo and mode of antibat ultrasound production and sonar jamming in the diverse hawkmoth radiation

“…3, but also see ref. 10). Tiger moths can hear bat echolocation and have paired metathoracic tymbals that beam ultrasonic clicks back at bats (6,7).…”

Evolution of directional hearing in moths via conversion of bat detection devices to asymmetric pressure gradient receivers

“…(9) owing to available genetic resources, most acoustic insects are to be found in the Lepidoptera. Approximately 55% of lepidopteran species have tympanal ears (10), hearing evolved independently between 10-12 times in the order (11), and sound signaling-using ultrasound frequenciesfor mating communication is now known to occur in diverse species in several families, including those characterized by small body size (12). Because mates may need to be localized with the same precision as hosts, some degree of directional hearing is expected in moth species that communicate acoustically.…”