Mechanosensory hairs in bumblebees (Bombus terrestris) detect weak electric fields.

Bumblebees (Bombus terrestris) use information from surrounding electric fields to make foraging decisions. Electroreception in air, a nonconductive medium, is a recently discovered sensory capacity of insects, yet the sensory mechanisms remain elusive. Here, we investigate two putative electric field sensors: antennae and mechanosensory hairs. Examining their mechanical and neural response, we show that electric fields cause deflections in both antennae and hairs. Hairs respond with a greater median velocity, displacement, and angular displacement than antennae. Extracellular recordings from the antennae do not show any electrophysiological correlates to these mechanical deflections. In contrast, hair deflections in response to an electric field elicited neural activity. Mechanical deflections of both hairs and antennae increase with the electric charge carried by the bumblebee. From this evidence, we conclude that sensory hairs are a site of electroreception in the bumblebee.

Auditory sensitivity, spatial dynamics, and amplitude of courtship song in Drosophila melanogaster.

Acoustic communication is an important component of courtship in Drosophila melanogaster. It takes the form of courtship song produced by males through the unilateral extension and vibration of a wing. Following the paradigm of sender-receiver matching, song content is assumed to match tuning in the auditory system, however, D. melanogaster audition is nonlinear and tuning dependent upon signal amplitude. At low stimulus amplitudes or in the absence of sound the antenna is tuned into song frequency, but as amplitude increases the antenna's resonance is shifted up by hundreds of Hertz. Accurate measurements of song amplitude have been elusive because of the strong dependency of amplitude upon the spatial geometry between sender and receiver. Here, D. melanogaster auditory directional sensitivity and the geometric position between the courting flies are quantified. It is shown that singing occurs primarily from positions resulting in direct stimulation of the female antenna. Using this information, it is established that the majority of song is louder than theoretically predicted and at these sound levels the female antenna should not amplify or be tuned into song. The study implies that Drosophila hearing, and, in particular, its active mechanisms, could function in a broader context than previously surmised.

Impacts of regular and random noise on the behaviour, growth and development of larval Atlantic cod (Gadus morhua).

Anthropogenic noise impacts behaviour and physiology in many species, but responses could change with repeat exposures. As repeat exposures can vary in regularity, identifying regimes with less impact is important for regulation. We use a 16-day split-brood experiment to compare effects of regular and random acoustic noise (playbacks of recordings of ships), relative to ambient-noise controls, on behaviour, growth and development of larval Atlantic cod (Gadus morhua). Short-term noise caused startle responses in newly hatched fish, irrespective of rearing noise. Two days of both regular and random noise regimes reduced growth, while regular noise led to faster yolk sac use. After 16 days, growth in all three sound treatments converged, although fish exposed to regular noise had lower body width-length ratios. Larvae with lower body width-length ratios were easier to catch in a predator-avoidance experiment. Our results demonstrate that the timing of acoustic disturbances can impact survival-related measures during development. Much current work focuses on sound levels, but future studies should consider the role of noise regularity and its importance for noise management and mitigation measures.

Active auditory mechanics in female black­horned tree crickets (Oecanthus nigricornis).

The acoustic signalling behaviour of many tree cricket species is easily observed and has been well described. Very little is known, however, about the receivers in these communication loops. The exception to this is a single Indian species (Oecanthus henryi) which employs active auditory mechanics to enhance female sensitivity to quiet sounds at male calling frequencies. In most species, male calls have been described, but whether or not sender­receiver matching is present is uncertain. Here we investigate auditory mechanics in females of the North American black-horned tree cricket (Oecanthus nigricornis). The response of the anterior tympanal membrane is nonlinear, exhibiting a lack of tuning at high amplitudes (60 dB and above) but as stimulus amplitude decreases, the membrane becomes tuned to around 4.3 kHz. The tuning of the membrane falls within the frequency range of male calls indicating sender­receiver matching at low amplitudes, which could aid localisation of the highly directional calls of males. The extent of active auditory mechanics in tympanal insects is not yet known, but this paper provides an indication that this may indeed be widespread in at least the Oecanthinae.

The importance of invertebrates when considering the impacts of anthropogenic noise.

Anthropogenic noise is now recognized as a major global pollutant. Rapidly burgeoning research has identified impacts on individual behaviour and physiology through to community disruption. To date, however, there has been an almost exclusive focus on vertebrates. Not only does their central role in food webs and in fulfilling ecosystem services make imperative our understanding of how invertebrates are impacted by all aspects of environmental change, but also many of their inherent characteristics provide opportunities to overcome common issues with the current anthropogenic noise literature. Here, we begin by explaining why invertebrates are likely to be affected by anthropogenic noise, briefly reviewing their capacity for hearing and providing evidence that they are capable of evolutionary adaptation and behavioural plasticity in response to natural noise sources. We then discuss the importance of quantifying accurately and fully both auditory ability and noise content, emphasizing considerations of direct relevance to how invertebrates detect sounds. We showcase how studying invertebrates can help with the behavioural bias in the literature, the difficulties in drawing strong, ecologically valid conclusions and the need for studies on fitness impacts. Finally, we suggest avenues of future research using invertebrates that would advance our understanding of the impact of anthropogenic noise.

Directional cues in Drosophila melanogaster audition: structure of acoustic flow and inter-antennal velocity differences.

Drosophila melanogaster have bilateral antisymmetric antennae that receive the particle velocity component of an acoustic stimulus. Acoustic communication is important in their courtship, which takes place in the acoustic near-field. Here, the small size of the dipole sound source (the male wing) and the rapid attenuation rate of particle velocity produce a spatially divergent sound field with highly variable magnitude. Also, male and female D. melanogaster are not usually stationary during courtship, resulting in a variable directionality of the acoustic stimulus. Using both particle image velocimetry and laser Doppler vibrometry, we examined the stimulus flow around the head of D. melanogaster to identify the actual geometry of the acoustic input to the antennae and its directional response. We reveal that the stimulus changes in both magnitude and direction as a function of its angle of incidence. Remarkably, directionality is substantial, with inter-antennal velocity differences of 25 dB at 140 Hz. For an organism whose auditory receivers are separated by only 660 ± 51 µm (mean ± s.d.), this inter-antennal velocity difference is far greater than differences in intensity observed between tympanal ears for organisms of similar scale. Further, the mechanical sensitivity of the antennae changes as a function of the angle of incidence of the acoustic stimulus, with peak responses along axes at 45 and 315 deg relative to the longitudinal body axis. This work indicates not only that the flies are able to detect differential cues in signal direction, but also that the male song structure may not be the sole determinant of mating success; his spatial positioning is also crucial to female sound reception and therefore also perhaps to her decision making.

Electric Fields Elicit Ballooning in Spiders.

When one thinks of airborne organisms, spiders do not usually come to mind. However, these wingless arthropods have been found 4 km up in the sky [1], dispersing hundreds of kilometers [2]. To disperse, spiders "balloon," whereby they climb to the top of a prominence, let out silk, and float away. The prevailing view is that drag forces from light wind allow spiders to become airborne [3], yet ballooning mechanisms are not fully explained by current aerodynamic models [4, 5]. The global atmospheric electric circuit and the resulting atmospheric potential gradient (APG) [6] provide an additional force that has been proposed to explain ballooning [7]. Here, we test the hypothesis that electric fields (e-fields) commensurate with the APG can be detected by spiders and are sufficient to stimulate ballooning. We find that the presence of a vertical e-field elicits ballooning behavior and takeoff in spiders. We also investigate the mechanical response of putative sensory receivers in response to both e-field and air-flow stimuli, showing that spider mechanosensory hairs are mechanically activated by weak e-fields. Altogether, the evidence gathered reveals an electric driving force that is sufficient for ballooning. These results also suggest that the APG, as additional meteorological information, can reveal the auspicious time to engage in ballooning. We propose that atmospheric electricity adds key information to our understanding and predictive capability of the ecologically important mass migration patterns of arthropod fauna [8]. VIDEO ABSTRACT.