The physics of sound propagation imposes fundamental constraints on sound localization: for a given frequency, the smaller the receiver, the smaller the available cues. Thus, the creation of nanoscale acoustic microphones with directional sensitivity is very difficult. The fly Ormia ochracea possesses an unusual 'ear' that largely overcomes these physical constraints; attempts to exploit principles derived from O. ochracea for improved hearing aids are now in progress. Here we report that O. ochracea can behaviourally localize a salient sound source with a precision equal to that of humans. Despite its small size and minuscule interaural cues, the fly localizes sound sources to within 2 degrees azimuth. As the fly's eardrums are less than 0.5 mm apart, localization cues are around 50 ns. Directional information is represented in the auditory system by the relative timing of receptor responses in the two ears. Low-jitter, phasic receptor responses are pooled to achieve hyperacute timecoding. These results demonstrate that nanoscale/microscale directional microphones patterned after O. ochracea have the potential for highly accurate directional sensitivity, independent of their size. Notably, in the fly itself this performance is dependent on a newly discovered set of specific coding strategies employed by the nervous system.

1. The courtship behavior of male field crickets, Gryllus bimaculatus (De Geer) and Teleogryllus oceanicus, is a complex, multimodal behavioral act that involves acoustic signals (a courtship song; Fig. 1A, B). The dominant frequency is 4.5 kHz for T. oceanicus song (Fig. 1A) and 13.5 kHz for G. bimaculatus (Fig. 1B). 2. When courting males are deprived of their courtship song by wing amputation, their courtship success declines markedly but is restored when courting is accompanied by tape-recordings of their courtship songs or a synthetic courtship song with only the dominant frequency of the natural song; other naturally occurring frequency components are ineffective for restoring mating success (Figs. 4, 5). 3. It has been suggested that an identified auditory interneuron, AN2, plays a critical role in courtship success. Chronic recordings of AN2 in an intact, tethered female show that AN2's response to the natural courtship song and synthesized songs at 4.5 and 13.5 kHz is similar in T. oceanicus. By contrast, in G. bimaculatus, AN2's response to the natural courtship song and synthesized song at 13.5 kHz, but not at 4.5 kHz, is similar (Fig. 2,3). 4. In behavioral experiments, playback of a 30 kHz synthetic courtship song in G. bimaculatus does not restore courtship success, yet this same stimulus elicits as strong a response from AN2 as does the normal courtship song (Fig. 6). Thus, contrary to earlier work by others, we conclude AN2 is not, by itself, a critical neural link in the courtship behavior of these two species of crickets.

Ormia ochracea is a parasitoid fly which lays its larvae on its hosts, the field crickets Gryllus integer and Gryllus rubens, in two distinct modes: (1) directly on the host and (2) around the host. In the field, 12.7% of male crickets were parasitized and 3.2% were superparasitized. Despite the disadvantages of parasitizing infested hosts, there was no evidence that O. ochracea avoided superparasitism. This and other experiments suggest that the host assessment ability of O. ochracea is less than that reported for many hymenopteran parasitoids. By manipulating the number of larvae in each cricket, we determined that four to five larvae per host resulted in the largest number of adult flies. However, as larval number per host increased from one to six, pupal size, and hence adult size, declined. In the field, hosts were found with a mean of 1.7 _+ 1.0 (SD) larvae per cricket, suggesting that there may be some selection pressure against larger clutch sizes. Nevertheless clutch sizes larger than the host can support were sometimes found in the field. During the first mode of larviposition, gravid flies deposited no more than three larvae directly onto the host. Larvae deposited directly on the host had a high probability of infesting it. During the second mode of larviposition, gravid flies laid a larger number of larvae around the host (6.1 _+ 5.2). Larvae that were laid around the host were less likely to infest a cricket than were larvae that were deposited directly onto it. O. ochracea is unique in that its two different modes of larviposition have different probabilities of larval success. Even though the success rate for larvae laid during the second mode of larviposition was low, the possibility of parasitizing more hosts appears to have selected for flies laying more larvae (e.g. increasing clutch size) than is optimal if all the larvae successfully entered a single host.

The development of novel microfabrication techniques for producing a directional microphone for hearing aids is here described. The mechanisms underlying both the structure and function of these unusual microphones were originally inspired by the ears of an inconspicuous insect, the parasitoid fly Ormia ochracea. The structure of Ormia’s ears inspired new approaches to design directional microphones that are more sensitive and have lower thermal noise than that typical of those using traditional approaches. The mechanisms for directional hearing in this animal are discussed along with the engineering design concepts that they have inspired, because they illustrate how basic research can inspire technology development–translational research. However, to realize the potential of bioexploitation this microphone diaphragm concept would have been very difficult to realize without the availability of new silicon microfabrication technologies. Thus, this report can be viewed as an example of what may be possible with the application of new fabrication methods to microphones. Challenges and opportunities provided by the use of silicon microfabrication technology for microphones are discussed.

Protective mimicry, in which a palatable species avoids predation by being mistaken for an unpalatable model, is a remarkable example of adaptive evolution. These complex interactions between mimics, models and predators can explain similarities between organisms beyond the often-mechanistic constraints typically invoked in studies of convergent evolution. However, quantitative studies of protective mimicry typically focus on static traits (e.g. colour and shape) rather than on dynamic traits like locomotion. Here, we use high-speed cameras and behavioural experiments to investigate the role of locomotor behaviour in mimicry by the ant-mimicking jumping spider Myrmarachne formicaria, comparing its movement to that of ants and non-mimicking spiders. Contrary to previous suggestions, we find mimics walk using all eight legs, raising their forelegs like ant antennae only when stationary. Mimics exhibited winding trajectories (typical wavelength = 5–10 body lengths), which resemble the winding patterns of ants specifically engaged in pheromone-trail following, although mimics walked on chemically inert surfaces. Mimics also make characteristically short (approx. 100 ms) pauses. Our analysis suggests that this makes mimics appear ant-like to observers with slow visual systems. Finally, behavioural experiments with predatory spiders yield results consistent with the protective mimicry hypothesis. These findings highlight the importance of dynamic behaviours and observer perception in mimicry.