William E. Conner

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.

Courtship pheromone production and body size as correlates of larval diet in males of the arctiid moth,Utetheisa ornatrix

Hydroxydanaidal, the corematal courtship pheromone of maleUtetheisa ornatrix, shows pronounced quantitative variation in natural populations of the moth. Males that, as larvae, fed on seed-bearing rather than immature food plants (Crotalaria spectabilis orC. mucronata) produce higher levels of hydroxydanaidal. Such males also have higher systemic loads of pyrrolizidine alkaloid, the known metabolic precursor of hydroxydanaidal, whichUtetheisa sequester from their larval diet and which is concentrated in the seeds ofCrotalaria. Males raised on seed-bearing plants also achieve higher adult weight. In the context of sexual selection, therefore, femaleUtetheisa could, through assessment of male hydroxydanaidal levels, gauge both the alkaloid content and body weight of their suitors.

Acoustic mimicry in a predator–prey interaction

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 Müllerian 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.

Heteropteran chemical repellents identified in the citrus odor of a seabird (crested auklet: Aethia cristatella): evolutionary convergence in chemical ecology.

Abstract. The exogenous application of chemical repellents is widespread in birds, but endogenous production is exceedingly rare. We herein report a new class of avian defensive compounds isolated from the feathers and volatile odor of the crested auklet (Aethia cristatella). Mass spectra indicate that n-hexanal, n-octanal, n-decanal, Z-4-decenal and a 12-carbon unsaturated aldehyde comprise the auklet odorant. Octanal and hexanal are also secreted in the repugnant metasternal gland emissions of heteropteran insects and are known to be potent invertebrate repellents. We suggest that the auklet odorant functions as an ectoparasite repellent and a signal of mate quality. This would represent a rare and direct link between vigor, quality and parasite resistance, one of several putative bases for mate selection. This is the first report of defensive compounds produced by a seabird or colonial bird and one of the few examples of chemical defense in a polar or subpolar marine vertebrate.

Effectiveness of tiger moth (Lepidoptera, Arctiidae) chemical defenses against an insectivorous bat (Eptesicus fuscus)

Summary.Adult tiger moths exhibit a wide range of palatabilities to the insectivorous big brown bat Eptesicus fuscus. Much of this variation is due to plant allelochemics ingested and sequestered from their larval food. By using a comparative approach involving 15 species from six tribes and two subfamilies of the Arctiidae we have shown that tiger moths feeding on cardiac glycoside-containing plants often contain highly effective natural feeding deterrents. Feeding on pyrrolizidine alkaloid-containing plants is also an effective deterrent to predation by bats but less so than feeding on plants rich in cardiac glycosides. Moths feeding on plants containing iridoid glycosides and/or moths likely to contain biogenic amines were the least deterrent. By manipulating the diet of several tiger moth species we were able to adjust their degree of palatability and link it to the levels of cardiac glycosides or pyrrolizidine alkaloids in their food. We argue that intense selective pressure provided by vertebrate predators including bats has driven the tiger moths to sequester more and more potent deterrents against them and to acquire a suite of morphology characteristics and behaviors that advertise their noxious taste.

Courtship sounds of the polka-dot wasp moth,Syntomeida epilais

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Chemical Odorant of Colonial Seabird Repels Mosquitoes

Abstract The crested auklet, Aethia cristatella, emits a class of aldehydes shown to be potent invertebrate repellents when used by heteropterans against their predators. Our aim was to determine the efficacy of these aldehydes against mosquitoes in the laboratory. Synthetic analogues of the auklet odorant were strongly repellent to mosquitoes in controlled laboratory trials. Furthermore, the efficacy was similar to previous reports for commercial mosquito repellents. These results, in combination with a previously published study, show that constituents of the aldehyde odorant are broad spectrum in efficacy against ectoparasitic arthropods of birds. Our report is the first empirical evidence for an endogenous mosquito repellent in birds.

Interspecific Differences in Aethia Spp. Auklet Odorants and Evidence for Chemical Defense Against Ectoparasites

The true auklets (Genus Aethia) are small planktivorous seabirds of the Bering Sea and North Pacific. Two species, the crested and whiskered auklets produce volatile citrus-like odorants. We here show that the whiskered auklet odorant is composed predominantly of two odd-numbered aldehydes (heptanal and nonanal) with no detectable unsaturated aldehydes. By comparison the crested auklet odorant is dominated by even-numbered aldehydes, both saturated and monounsaturated, ranging in size from 6 to 12 carbons. This is evidence of species-specific acquisition or biosynthetic pathways. We clarify the chemistry of the crested auklet odorant. We cite evidence that the C-12:1 aldehyde in crested auklets is actually two isomers, (Z)-4-dodecenal and (Z)-6-dodecenal. We also report on experimental evidence that aldehyde constituents kill and repel ectoparasites. Efficacy of the aldehydes may increase when they are combined in a mixture. The repellency of the mixture increases with chemical concentration. This suggests that individuals with higher chemical production are likely to repel ectoparasites more effectively.

Courtship Behavior in Empyreuma affinis Roths. (Lepidoptera, Arctiidae, Ctenuchinae): Acoustic Signals and Tympanic Organ Response

Correspondence to: M.V. Sanderford Field and laboratory observations of the mating behavior ofEmpyreuma affinis show that ultrasonic signals consistently produced by the males and occasionally by the females are a distinctive feature of the courtship of this insect. The sounds produced by males and females show a significant sexual dimorphism, most dramatically in their modulation cycle rates. Moreover, males produce two distinct types of emissions that differ in modulation cycle rate. Electrophysiological recordings of spike activity at the tympanic nerve of males and females were carried out, and the responses to prerecorded intraspecific acoustic signals emitted during courtship behavior are shown. The results predict that the main informational content of these signals is in the modulation cycle rate, which is followed faithfully by the receptor cells. In 1864 Laboulbene suggested that acoustic signals play a role in the reproductive behavior of the Arctiidae [1]. Peter [2] later described the use of sound by a day-flying Alpine arctiid moth in its mating behavior, and more recently ultrasonic emissions associated with reproductive behavior have been described for an additional three arctiid species [3, 4]. The first ctenuchine moth to be implicated in acoustic mating behavior was Empyreuma affinis (E. pugione, in earlier references), the “scarlet-winged wasp moth,” a day-flying moth endemic to the Caribbean [5–7]. Since the initial (1983) publication on the ears and sound emission organs of E. affinis [8, 9] additional information has been gathered revealing characteristics which appear to adapt it for acoustic intraspecific communication: (a) Males and females produce sounds with striated and partially denuded tymbals which resemble those of other acoustically active arctiids [10]. (b) The acoustic signals of E. affinis consist of ultrasonic clicks composed of frequencies from 14 to 64 kHz with a major peak at 34 kHz [11] with signal sound pressure levels approaching 80 dB at 2 cm [10]. (c) Audiograms of the A1 and A2 receptor cells of males and females show a close frequency match of auditory sensitivity with the power spectrum of the sound emitted, and an overlap of the Q10 dB bandwidth of sound reception and emission [11]. (d) The auditory organ of this species can detect directional information over an intensity range of at least 60 dB [11]. Also behavioral studies [12] have shown that the time spent in courtship behavior and mating was significantly reduced when either the male or female was deafened. These data suggest that E. affinis engages in acoustic courtship communication, and that both sexes emit acoustic signals during courtship [13]. Our results confirm that sound emission in males (in all the successful matings observed) and in females (in some cases) is indeed present during its courtship. Audition in moths has been often studied in the context of bat/moth interactions [14–17]. Acoustic stimuli resembling bat echolocation signals, and in a few cases natural bat cries have been used to stimulate the tympanic organs [18–21] or central auditory neurons of moths [22]. The use of conspecific moth sounds to evoke tympanal responses has been limited [18, 23, 24]. We here show the responses of lepidopteran auditory receptors to intraspecific acoustic courtship signals.

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.