Cycnia Tenera Research Articles

Adaptive auditory risk assessment in the dogbane tiger moth when pursued by bats

Moths and butterflies flying in search of mates risk detection by numerous aerial predators; under the cover of night, the greatest threat will often be from insectivorous bats. During such encounters, the toxic dogbane tiger moth, Cycnia tenera uses the received intensity, duration and emission pattern of the bat's echolocation calls to determine when, and how many, defensive ultrasonic clicks to produce in return. These clicks, which constitute an acoustic startle response, act as warning signals against bats in flight. Using an integrated test of stimulus generalization and dishabituation, here we show that C. tenera is able to discriminate between the echolocation calls characteristic of a bat that has only just detected it versus those of a bat actively in pursuit of it. We also show that C. tenera habituates more profoundly to the former stimulus train (‘early attack’) than to the latter (‘late attack’), even though it was initially equally responsive to both stimuli. Matched sensory and behavioural data indicate that reduced responsiveness reflects habituation and is not merely attributable to sensory adaptation or motor fatigue. In search of mates in the face of bats, C. tenera's ability to discriminate between attacking bats representing different levels of risk, and to habituate less so to those most dangerous, should function as an adaptive cost–benefit trade-off mechanism in nature.

Tiger moths and the threat of bats: decision-making based on the activity of a single sensory neuron

Echolocating bats and eared moths are a model system of predator-prey interaction within an almost exclusively auditory world. Through selective pressures from aerial-hawking bats, noctuoid moths have evolved simple ears that contain one to two auditory neurons and function to detect bat echolocation calls and initiate defensive flight behaviours. Among these moths, some chemically defended and mimetic tiger moths also produce ultrasonic clicks in response to bat echolocation calls; these defensive signals are effective warning signals and may interfere with bats' ability to process echoic information. Here, we demonstrate that the activity of a single auditory neuron (the A1 cell) provides sufficient information for the toxic dogbane tiger moth, Cycnia tenera, to decide when to initiate defensive sound production in the face of bats. Thus, despite previous suggestions to the contrary, these moths' only other auditory neuron, the less sensitive A2 cell, is not necessary for initiating sound production. However, we found a positive linear relationship between combined A1 and A2 activity and the number of clicks the dogbane tiger moth produces.

Acoustic feature recognition in the dogbane tiger moth,Cycnia tenera

Certain tiger moths (Arctiidae) defend themselves against bats by phonoresponding to their echolocation calls with trains of ultrasonic clicks. The dogbane tiger moth, Cycnia tenera, preferentially phonoresponds to the calls produced by attacking versus searching bats, suggesting that it either recognizes some acoustic feature of this phase of the bat's echolocation calls or that it simply reacts to their increased power as the bat closes. Here, we used a habituation/generalization paradigm to demonstrate that C. tenera responds neither to the shift in echolocation call frequencies nor to the change in pulse duration that is exhibited during the bat's attack phase unless these changes are accompanied by either an increase in duty cycle or a decrease in pulse period. To separate these features, we measured the moth's phonoresponse thresholds to pulsed stimuli with variable versus constant duty cycles and demonstrate that C. tenera is most sensitive to echolocation call periods expressed by an attacking bat. We suggest that, under natural conditions, C. tenera identifies an attacking bat by recognizing the pulse period of its echolocation calls but that this feature recognition is influenced by acoustic power and can be overridden by unnaturally intense sounds.

TO CLICK OR NOT TO CLICK?

When a bat is cruising around looking for its next meal it sends out its ultrasonic pulses and listens carefully to the tell-tale echoes of a moth fluttering by. Despite the sophistication of a bat's echolocation system,moths have a few defences of their own. The dogbane tiger moth responds to a bat's attacking clicks with clicks of its own when the bat gets too close,either interfering with the bat's echolocation or warning the bat that it faces a bitter mouthful. However the moth has to choose very carefully when to click at a bat; too early draws unnecessary attention to itself, and leaving it too late is very risky. James Fullard and colleagues at the University of Toronto and Cornell University investigated which aspects of a bat's calls the moths use to decide whether to defend themselves or not (p. 2481).A bat can vary many of the characteristics of its echolocating calls, such as the frequency or intensity of the calls. It also alters the duration of the individual pulses or the time between the start of each pulse, known as pulse period, which in turn affect the duty cycle, which is the percentage of the total time a calling bat is making a sound. A moth could use any of these characteristics to identify an attacking bat, but the question is, which one?First the team recorded from the moths' auditory neurons to test their response to different frequency sounds, and find their auditory threshold. They found while moths' auditory neurons are sensitive between 30 and 50 kHz,they didn't show any difference in their clicking behaviour to different frequencies, showing that moths are essentially tone deaf.Having ruled out frequency, they turned to a technique which allowed them to test if moths could tell the difference between two sets of bat calls. They attached the moths to a pin with wax and suspended them above a speaker in a dark room, before repeatedly playing a sequence of bat pulses to them and recording their clicking response. Once the moths had habituated –stopped responding to the bat signals – they changed one or more aspects of the signal to see whether the moths could tell the difference and start clicking again.They found that once the moths had habituated to a particular signal, they had to change the duty cycle by 60% or more before the moths started responding again. Next they tested to see how the moths responded to varying duty cycles, and found that they were most sensitive to pulse periods of 20 ms. They were less sensitive to longer and shorter pulse periods, showing that the response was tuned.Finally to show that pulse period was the primary parameter that the moths were responding to, they habituated the moths to `searching' bat signals and then tested them with `attacking' bat signals. Both signals had the same duty cycle, but the pulse period changed as the bats switched from searching to attacking. They found that the moths responded very strongly to the switch between a searching and attacking bat, showing that pulse period is the defining feature they use to identify when they are in danger. However they also found that their response was influenced by the intensity of the signal. If an attacking bat is pulsing to another insect 30 m away, then the moth is not going to respond because the intensity is too low, and it doesn't want to draw attention to itself. But if the intensity is right, and the bat is bearing down on the moth and bombarding it with high intensity, short period signals, it will click to avoid being snatched and eaten.

The adaptive function of tiger moth clicks against echolocating bats: an experimental and synthetic approach

We studied the efficiency and effects of the multiple sensory cues of tiger moths on echolocating bats. We used the northern long-eared bat, Myotis septentrionalis, a purported moth specialist that takes surface-bound prey (gleaning) and airborne prey (aerial hawking), and the dogbane tiger moth, Cycnia tenera, an eared species unpalatable to bats that possesses conspicuous colouration and sound-producing organs (tymbals). This is the first study to investigate the interaction of tiger moths and wild-caught bats under conditions mimicking those found in nature and to demand the use of both aerial hawking and gleaning strategies by bats. Further, it is the first to report spectrograms of the sounds produced by tiger moths while under aerial attack by echolocating bats. During both aerial hawking and gleaning trials, all muted C. tenera and perched intact C. tenera were attacked by M. septentrionalis, indicating that M. septentrionalis did not discriminate C. tenera from palatable moths based on potential echoic and/or non-auditory cues. Intact C. tenera were attacked significantly less often than muted C. tenera during aerial hawking attacks: tymbal clicks were therefore an effective deterrent in an aerial hawking context. During gleaning attacks, intact and muted C. tenera were always attacked and suffered similar mortality rates, suggesting that while handling prey this bat uses primarily chemical signals. Our results also show that C. tenera temporally matches the onset of click production to the ;approach phase' echolocation calls produced by aerial hawking attacking bats and that clicks themselves influence the echolocation behaviour of attacking bats. In the context of past research, these findings support the hypotheses that the clicks of arctiid moths are both an active defence (through echolocation disruption) and a reliable indicator of chemical defence against aerial-hawking bats. We suggest these signals are specialized for an aerial context.

Auditory encoding during the last moment of a moth's life.

The simple auditory system of noctuoid moths has long been a model for anti-predator studies in neuroethology, although these ears have rarely been experimentally stimulated by the sounds they would encounter from naturally attacking bats. We exposed the ears of five noctuoid moth species to the pre-recorded echolocation calls of an attacking bat (Eptesicus fuscus) to observe the acoustic encoding of the receptors at this critical time in their defensive behaviour. The B cell is a non-tympanal receptor common to all moths that has been suggested to respond to sound, but we found no evidence of this and suggest that its acoustic responsiveness is an artifact arising from its proprioceptive function. The A1 cell, the most sensitive tympanal receptor in noctuid and arctiid moths and the only auditory receptor in notodontid moths, encodes the attack calls with a bursting firing pattern to a point approximately 150 ms from when the bat would have captured the moth. At this point, the firing of the A1 cell reduces to a non-bursting pattern with longer inter-spike periods, suggesting that the moth may no longer express the erratic flight used to escape very close bats. This may be simply due to the absence of selection pressure on moths for auditory tracking of bat echolocation calls beyond this point. Alternatively, the reduced firing may be due to the acoustic characteristics of attack calls in the terminal phase and an acoustic maneuver used by the bat to facilitate its capture of the moth. Although the role of less sensitive A2 cell remains uncertain in the evasive flight responses of moths it may act as a trigger in eliciting sound production, a close-range anti-bat behaviour in the tiger moth, Cycnia tenera.

The closed-loop nature of the tymbal response in the dogbane tiger moth, Cycnia tenera (Lepidoptera, Arctiidae).

The dogbane tiger moth, Cycnia tenera, emits ultrasonic sounds by rhythmically buckling a pair of tymbals when stimulated by pulsed sounds resembling bat echolocation. We monitored the central pattern generator governing this response by recording the motor output of the tymbal branch of the metathoracic leg nerve. The rhythm of the tymbal motor pattern can be altered midway (500 m/sec from its initiation) by changing the period and, to a lesser degree, the intensity of the stimulus. The tymbal response of C. tenera is therefore closed-looped to stimulus pulse period and intensity. Our results suggest that C. tenera relies less on the changes in an attacking bat's echolocation intensity when responding with this behaviour because this acoustic parameter may be a more unreliable indicator of the proximity of the bat than its echolocation call period.

Jamming Bat Echolocation: the Dogbane Tiger Moth Cycnia Tenera Times Its Clicks to the Terminal Attack Calls of the Big Brown Bat Eptesicus Fuscus

Certain tiger moths emit high-frequency clicks to an attacking bat, causing it to break off its pursuit. The sounds may either orient the bat by providing it with information that it uses to make an attack decision (aposematism) or they may disorient the bat by interrupting the normal flow of echo information required to complete a successful capture (startle, jamming). At what point during a bat's attack does an arctiid emit its clicks? If the sounds are aposematic, the moth should emit them early in the attack echolocation sequence in order to allow the bat time to understand their meaning. If, however, the sounds disrupt the bat's echo-processing behaviour, one would expect them to be emitted later in the attack to maximize their confusion effects. To test this, we exposed dogbane tiger moths (Cycnia tenera) to a recording of the echolocation sequence emitted by a big brown bat (Eptesicus fuscus) as it attacked a stationary target. Our results demonstrate that, at normal echolocation intensities, C. tenera does not respond to approach calls but waits until the terminal phase of the attack before emitting its clicks. This timing is evident whether the moth is stationary or flying and is largely independent of the intensity of the echolocation calls. These results support the hypothesis of a jamming effect (e.g. 'phantom echoes') and suggest that, to determine experimentally the effects of arctiid clicks on bats, it is important that the bats be tested under conditions that simulate the natural context in which this defence operates.

Ultrasound: its role in the courtship of the arctiid moth,Cycnia tenera

MaleCycnia tenera (Lepidoptera: Arctiidae) were shown to produce ultrasonic clicks during courtship. The ultrasound enhances male courtship success, but only in the absence of male-produced pheromonal cues.

Calling behaviour in arctiid moths: The effects of temperature and wind speed on the rhythmic exposure of the sex attractant gland

Female arctiid moths rhythmically extrude their ovipositors and thereby rhythmically expose their sex pheromone glands while calling. In Utetheisa ornatrix this behaviour results in concentration-modulated or pulsed pheromone release. The ovipositor protrusion frequencies were determined for 15 arctiid species: U. ornatrix, Haploa clymene, H. colona, H. lecontei, Pyrrarctia isabella, Estigmene acrea, Spilosoma congrua, S. virginica, Ecpantheria scribonia, Phragmatobia fuliginosa, Apantesis nais, A. arge, Pareuchaetes insulata, Cycnia tenera, and Euchaetes egle. Moth species that call early in the scotophase extrude their ovipositors at high frequencies (up to 170.9 ± 24.9 extrusions/min at 25°C) while moth species that call late in scotophase extrude their ovipositors at low frequencies (down to 68.3 ± 5.4 extrusions/min at 25°C). In all species tested, the ovipositor extrusion frequencies were shown to be temperature sensitive with a mean Q 10 of 2.0 ± 0.1. In one species, U. ornatrix, the ovipositor extrusion frequency varies with wind speed. In still air the ovipositor extrusion frequency is 70.1 ± 8.4 extrusions/min and at a wind speed of 120 cm/s the ovipositor extrusion frequency is 142.1 ± 8.3 extrusions/min. Suggested functions for rhythmic ovipositor extrusion during calling are discussed.

Listening for bats: pulse repetition rate as a cue for a defensive behavior inCycnia tenera (Lepidoptera:Arctiidae)

The tympanate, arctiid moth,Cycnia tenera responds to pulsed, 30 kHz acoustic stimuli resembling bat echolocation signals by emitting trains of clicks. This phonoresponse was used to determine that this moth is maximally sensitive to stimulus pulse repetition rates of 30–50 pulses/s, rates typically emitted by bats shortly before they close with their targets. At rates both above and below this optimum moths exhibit higher thresholds and reduced responsiveness. These data suggest thatC. tenera is capable of using the repetition rate emitted by an approaching bat as a cue in determining the relative proximity of the bat. The use of repetition rate information should allow this moth both an unambiguous indication of a bat at very close range as well as the ability to distinguish sources of nocturnal, high-frequency sounds not emitted by predators.

Cardenolide sequestration by the dogbane tiger moth (Cycnia tenera; Arctiidae)

Cycnia tenera adults, reared as larvae onAsclepias humistrata, had 10 times higher cardenolide concentrations, and contained 15 times more total cardenolide, than did moths reared onA. tuberosa. Thin-layer chromatography confirmed that each individual cardenolide visualized in the adult moths reared on the former host plant corresponds to one present in the plant, thus demonstrating that the insects' cardenolides are indeed derived from the larval food. Adult weights were significantly greater when the larvae had been fed upon the higher cardenolide plant species,A. humistrata. Similar results for other milkweed-feeding insects have been interpreted by some authors as evidence against a metabolic cost of handling cardenolides. However, such interpretations confound cardenolide differences among milkweed species with other differences in plant primary and secondary chemistry that affect insect growth and development. While the cooccurrence inC. tenera of other noxious chemicals (e.g., alkaloids) is not precluded, cardenolides sequestered from larval host plants have probably contributed to the evolution of visual and auditory aposematism in this species. As the eggs are laid in large clutches and larvae are gregarious, such aposematism may have evolved via kin selection.

Cephalic influences on a defensive behaviour in the dogbane tiger moth, Cycnia tenera

ABSTRACT. The dogbane tiger moth (Cycnia tenera Hübner; Arctiidae) responds to ultrasonic, artificial bat echolocation signals by emitting stereotyped trains of high‐frequency, rapidly repeated clicks. By comparing this response in intact and headless moths, the role of protocerebral auditory inter‐neurones suggested by other studies was examined. Individual moths were tested intact and decapitated, and their response differences analysed. Response latency and threshold (dB) did not alter with the removal of the head but response duration and responsiveness to stimulus trains were significantly reduced in headless moths. These data are interpreted as suggesting the existence of a reflex arc connecting the moth's tympanic organ (ear) with its sound‐producing structure (tymbal), and as providing preliminary evidence that the role of higher‐order interneurones is primarily that of response reinforcement.

Behavioral analyses of auditory sensitivity inCycnia tenera H�bner (Lepidoptera: Arctiidae)

The auditory characteristics of the arctiid moth,Cycnia tenera were examined using two behavioral criteria, sound production and flight cessation. The majority of the individuals tested indicated a maximum sensitivity to frequencies between 30 and 50 kHz although there is a substantial degree of interindividual variation.

Abundance of Herbivores on Six Milkweed Species in Illinois

To aid the understanding of the role of insect herbivores as selective agents in the evolution of their host plants a survey of herbivore abundance and impact was undertaken in central Illinois on the six milkweed species: Asclepias incarnata, A. sullivantii, A. syriaca, A. verticillata, A. amplexicaulis, and A. tuberosa. These species occur in this order on a moisture gradient from wet to dry soil conditions. This survey revealed that 12 species occurred at an abundance of at least one individual per 100 host stems in 1 plot-year on one host species: Oncopeltus fasciatus*, Lygaeus kalmii*, Aphis nerii*, Labidomera clivicollis*, Tetraopes tetrophthalmus*, T. femoratus, T. quinquemaculatus, Rhyssomatus, lineaticollis*, Danaus PlexipPus, Cycnia tenera*, Euchaetias egle and a leafminer. All but L. kalmii are specific to milkweeds in Illinois. Seven of these species, marked with asterisks, were abundant enough to act as major selective forces on the life history patterns of the milkweed species, populations and clones concerned. Results support the hypothesis that major differences in herbivore species and abundance on milkweeds are largely a result of (1) differences in the environments that milkweeds successfully colonize and (2) morphological (allocational) differences between milkweeds. This hypothesis related to differences in herbivores between milkweed species, populations within a species and clones within a population. The herbivores were very patchily distributed on milkweed species; and, of all the possible herbivore-host plant relationships, in only 17% of the pair-wise comparisons in the 12 x 6 matrix were herbivores abundant on host plants. When all plot-years and all pair-wise comparisons were considered, in only 10% of the 252 possible situations in the 12 x 21 matrix were herbivores abundant on host plants. Such patchiness of herbivores supports recent theory on plant defense strategies, which argues that early successional plants, such as the milkweeds studied, are hard to find by specialized herbivores.