In response to sonar-guided attacking bats, some tiger moths make ultrasonic clicks of their own. The lepidopteran sounds have previously been shown to alert bats to some moths' toxic chemistry and also to startle bats unaccustomed to sonic prey. The moth sounds could also interfere with, or "jam," bat sonar, but evidence for such jamming has been inconclusive. Using ultrasonic recording and high-speed infrared videography of bat-moth interactions, we show that the palatable tiger moth Bertholdia trigona defends against attacking big brown bats (Eptesicus fuscus) using ultrasonic clicks that jam bat sonar. Sonar jamming extends the defensive repertoire available to prey in the long-standing evolutionary arms race 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.
The night sky is the venue for an ancient arms race. Insectivorous bats with their ultrasonic sonar exert an enormous selective pressure on nocturnal insects. In response insects have evolved the ability to hear bat cries, to evade their hunting maneuvers, and some, the tiger moths (Arctiidae), to utter an ultrasonic reply. We here determine what it is that tiger moths "say" to bats. We chose four species of arctiid moths, Cycnia tenera, Euchaetes egle, Utetheisa ornatrix, and Apantesis nais, that naturally differ in their levels of unpalatability and their ability to produce sound. Moths were tethered and offered to free-flying naive big brown bats, Eptesicus fuscus. The ability of the bats to capture each species was compared to their ability to capture noctuid, geometrid, and wax moth controls over a learning period of 7 days. We repeated the experiment using the single arctiid species E. egle that through diet manipulation and simple surgery could be rendered palatable or unpalatable and sound producing or mute. We again compared the capture rates of these categories of E. egle to control moths. Using both novel learning approaches we have found that the bats only respond to the sounds of arctiids when they are paired with defensive chemistry. The sounds are in essence a warning to the bats that the moth is unpalatable-an aposematic signal.
Mimicry of visual warning signals is one of the keystone concepts in evolutionary biology and has received substantial research attention. By comparison, acoustic mimicry has never been rigorously tested. Visualizing bat-moth interactions with high-speed, infrared videography, we provide empirical evidence for acoustic mimicry in the ultrasonic warning sounds that tiger moths produce in response to echolocating bats. Two species of sound-producing tiger moths were offered successively to naïve, free-flying red and big brown bats. Noctuid and pyralid moth controls were also offered each night. All bats quickly learned to avoid the noxious tiger moths first offered to them, associating the warning sounds with bad taste. They then avoided the second sound-producing species regardless of whether it was chemically protected or not, verifying both Mü llerian and Batesian mimicry in the acoustic modality. A subset of the red bats subsequently discovered the palatability of the Batesian mimic, demonstrating the powerful selective force these predators exert on mimetic resemblance. Given these results and the widespread presence of tiger moth species and other sound-producing insects that respond with ultrasonic clicks to bat attack, acoustic mimicry complexes are likely common components of the acoustic landscape.aposematism ͉ Arctiidae ͉ bats V isual mimicry has played an important role in evolutionary theory (1, 2) since Bates (3) and Müller (4) first proposed that mimics benefit through deception if they are palatable or through spreading the cost of educating predators if they are also noxious. Recent reviews of warning signals and mimicry (5, 6) make no mention of the acoustic domain despite the widespread use of sound as an aposematic signal in animals (7). Decades of anecdotal observations (8-12) have suggested acoustic mimicry among groups ranging from viperid snakes (12) to honey bees and droneflies (9). Perhaps the best studied of these is the purported model/mimic complex involving rattlesnakes and burrowing owls (13).Here, we report definitive experimental evidence for acoustic mimicry. Tiger moths answer the echolocation attack of bats with ultrasonic clicks broadcast from bilateral metathoracic structures called tymbals (Fig. 1) [to view the tymbal in action, see supporting information (SI) Movie 1]. Vigorous debate (14) over the functions of these sounds has produced three non-mutually exclusive hypotheses: startle, jamming, and warning. Although some evidence exists for both startle (15) and jamming (16,17) effects, recent work (18) confirmed one critical assumption of the warning model: naïve big brown bats (Eptesicus fuscus) failed to learn to avoid chemically protected moths unless those moths also provided an acoustic warning. Acoustic aposematism is a defensive strategy that is clearly open to mimicry.We trained naïve, lab-raised bats to hunt tethered moths, on the wing, in view of two high-speed video cameras, allowing three-dimensional visualization of interactions that occurred in fractions of a ...
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