Very little is known about the acoustic landscape of long-gone environments, such as the Jurassic forests. The sounds made by dinosaurs and other charismatic vertebrates are not definitively known because their vocal organs rarely preserve well in fossils. Unlike tetrapod vocal cords, the sound-producing organs present in the sclerotized cuticle of some arthropods do fossilize well. For example, the stridulatory structures (file, plectrum) can be observed and measured in the fossilized forewings of male crickets and allies. These fossils incorporate a fingerprint of the acoustic signals they generated, offering a unique window into the soundscapes of the past. While call frequencies can be inferred from fossilized wings using phylogenetically informed predictions, the reconstruction of wing vibrations and the songs' temporal patterns from fossil material remains elusive. Integrating phylogenetics, laser Doppler-vibrometry, numerical simulations, and an AI-based approach, 20 ensiferan fossils (nine species) from a single location (Jiulongshan Formation, Inner Mongolia, China) were studied to recreate the acoustic landscape of the Middle Jurassic. These insects produced pure-tone calls, an adaptation to avoid localization by eavesdropping predators. They also exhibited rich diversity in their calling song frequencies and repertoires, facilitated by specialized file morphologies and wing-size variation. One species called above 20 kHz, suggesting that ultrasonic communication in insects was established long before the emergence of bats in the Eocene. Evolving mammalian hearing thresholds suggest early predators imposed acoustic pressures before bats. This arms race with singing ensiferans likely drove Jurassic insect song diversity and the evolution of mammalian and insect auditory systems.
Olfaction is a sensory modality common to most organisms. In insects, the primary olfactory organ is the antenna, where sensilla house olfactory receptor neurons adapted to detect volatile organic compounds (VOCs). Whilst olfaction is well-understood at molecular and neural levels, questions remain as to how, biophysically, airborne VOCs reach sensilla. Transport through passive diffusion and active antennal motion is empirically supported but cannot entirely explain the remarkably rapid VOC sampling rates. We present evidence that the insect antennae exploits electrostatic forces that amplify VOC transfer from bulk air to sensilla. In effect, charged antennae capture more ambient VOCs than neutral ones, also evoking an enhanced electrophysiological (EAG) response to VOCs. Experimentally altering the charge of isolated antennae modulates EAG responses and olfactory sensitivity. Multiphysics modelling incorporating electrostatic and fluid dynamic mechanisms supports empirical evidence. Altogether, this work reveals the existence of a previously unknown and complementary biophysical mechanism supporting olfaction. ### Competing Interest Statement The authors have declared no competing interest. Biotechnology and Biological Sciences Research Council, https://ror.org/00cwqg982, BB/Y512886/1, BB/X010953/1, BBS/E/RH/230003A European Research Council, ERC- ELECTROBEE 743093
A novel miniature (28 mm x 38 mm) shielded Faraday cup is described for quantifying picocoulomb charges on millimetre environmental objects, such as small insects or plants, droplets, dust particles or powders. The electrometer electronics is contained within the device, avoiding any transfer of low level signals to an external electrometer. It is calibrated using a voltage ramp - capacitor method, generating defined charge pulses without a reference electrometer. The device can fit within an acoustic levitator to provide non-contact, zero leakage suspension of small objects, measuring charge on their release. Convenience and simplicity of use open new environmental charge measurement opportunities.
Arthropods, including pollinators, respond to environmental electrical fields. Here, we show that electric field information can be decoded to reconstruct environmental features. We develop an algorithm capable of inferring the shapes of polarisable flowers from the electric field generated by a nearby charged bee. We simulated electric fields arising from bee flower interactions for flowers with varying petal geometries. These simulated data were used to train a deep learning UNet model to recreate petal shapes. The model accurately reconstructed diverse flower shapes including more complex flower shapes not included in training. Reconstruction performance peaked at an optimal bee flower distance, indicating distance-dependent encoding of shape information. These findings show that electroreception can impart rich spatial detail, offering insights into arthropod environmental perception.
The link between form and function of an organism's morphology is usually apparent or intuitive. However, some clades of organisms show remarkable diversity in their form, often exhibiting extreme morphologies, but with no obvious functional explanation. Treehoppers (Membracidae) are a family of insects that exemplify this, displaying an astounding morphological diversity, resulting in a plethora of extreme forms. The function of these morphological extremities and the reasons for their evolution have thus far remained largely enigmatic. However, this mystery can be considered in light of the capacity of many animals to detect electric fields in air via electrostatic actuation of mechanosensory structures on their body. Importantly, the strength of the electric field experienced by these mechanosensory structures is expected by physics to depend on the animal's geometry, with sharp and elongated features producing the highest electric fields. Therefore, we hypothesize that the extreme morphologies of treehoppers increase their electrical sensitivity. Here, we show that treehoppers, along with their predators and mutualists, produce electric fields and that the treehopper Poppea capricornis can detect electric fields, responding behaviorally. We also demonstrate that predatory wasps and mutualist bees differ significantly in their electrostatic profiles, pointing to the sophistication of electrical information potentially available to treehoppers. Biophysical, computational, and mathematical techniques are then utilized to provide evidence that the pronotum of treehoppers is the site of electroreception and that its extreme shapes may enhance its sensitivity to electricity.
Increasing empirical evidence suggests that many terrestrial arthropods, such as bees, spiders and butterflies, sense electric fields in their environments. This relatively newly discovered sense may play a unique role within their broader sensory ecology, alongside other fundamental senses such as vision, hearing, olfaction, and aero-acoustic sensing. Deflectable hairs are the primary candidate for the reception of electrical stimuli. With each hair individually innervated, the arthropod can transduce environmental information through the deflection of such hairs. However, it is unclear what information an animal can elicit from hair receptors and how it relates to their environment. This paper explores how an arthropod can ascertain geometric and electrical information about its environment through the multiple observations and several deflecting hairs. Using two-dimensional models, we explore the possibility of electroreceptive object recognition and reconstruction via hair deflections. We analyse how the number of hairs, the observed shape, and the observation path taken alter the accuracy of the reconstructed representations. The results herein indicate the formidable possibility that geometric information about the environment can be electro-mechanically measured and acquired at a distance.
Predators and prey benefit from detecting sensory cues of each other’s presence. As they move through their environment, terrestrial animals accumulate electrostatic charge. Because electric charges exert forces at a distance, a prey animal could conceivably sense electrical forces to detect an approaching predator. Here, we report such a case of a terrestrial animal detecting its predators by electroreception. We show that predatory wasps are charged, thus emit electric fields, and that caterpillars respond to such fields with defensive behaviors. Furthermore, the mechanosensory setae of caterpillars are deflected by these electrostatic forces and are tuned to the wingbeat frequency of their insect predators. This ability unveils a dimension of the sensory interactions between prey and predators and is likely widespread among terrestrial animals.
Electroreception is the capacity of living organisms to detect the presence of electricity, usually studied in the aquatic environment. Electroreception in air, however, has received much less attention until relatively recently. Understanding how and why aerial electroreception may work requires a multidisciplinary framework, anchored in both the physics of static electricity and the ecology of sensory biology. In essence, the novel challenge arises from the fact that air is a much less conductive medium than water. Yet, recent research on terrestrial arthropods, including bees, flies, spiders, worms and caterpillars, has unveiled sensitivity to electric fields in different sensory ecological contexts. For each aerial organism considered thus far, filiform hairs and/or the antennae have been proposed to be the specialised sensory structures enabling detection based on both empirical and theoretical evidence. This newfound sensory modality reveals a previously unrecognised source of information, a new informational ecological niche integral to diverse life histories and navigational abilities, which remarkably involves animals, plants and atmospheric electricity (Figure 1). Understanding aerial electroreception in arthropods opens avenues for exploring their behaviour and ecology in diverse environments and sheds light on the evolution of sensory adaptations in terrestrial organisms. Because, as is known today, humans are not sensitive to weak electric fields, challenges arise in our comprehension of the elusive and discrete nature of aerial electric fields, and how they could be detected and used by terrestrial organisms.
Abstract Flying insect pollinators are electrically charged. As bumblebees (Bombus terrestris) and honeybees (Apis mellifera) are almost always positively charged, they present a static electric field that is modulated by the harmonic motion of their wings. Previous research has demonstrated that as a bee approaches a flower, there is a change in the stem potential of the plant, even before the bee lands, suggesting a capacity for flowers to sense the approaching bee through its electric field. Using a combination of laboratory and field studies, we explore the potential for flowers to act as receiving antennas for electrical signals, and to transmit these signals to neighbouring plants. Results show that flowers can detect non-contact electric stimuli, presumably by charge induction, and appear not to be tuned to a specific frequency. In the field, non-contact electric stimuli can also be detected in neighbouring flowers that did not receive the aerial stimulus. This evidence demonstrates the ability of flowers to capture local, aerial electrical signals, and the plant to then transmit signals through the soil to neighbouring plants. This work highlights the significance of environmental electric fields in pollination biology.
Animals, most notably insects, generally seem to accumulate electrostatic charge in nature. These electrostatic charges will exert forces on other charges in these animals’ environments and therefore have the potential to attract or repel other objects, for example, pollen from flowers. Here, we show that butterflies and moths (Lepidoptera) accumulate electrostatic charge while in flight. Then, using finite element analysis, we demonstrate that when within millimetres of a flower, the electrostatic charge of a lepidopteran generates an electric field in excess of 5 kV m −1 , and that an electric field of this magnitude is sufficient to elicit contactless pollen transfer from flowers across air gaps onto the body of a butterfly or moth. Furthermore, we see that phylogenetic variations exist in the magnitude and polarity of net charge between different species and families and Lepidoptera. These phylogenetic variations in electrostatic charging correlate with morphological, biogeographical and ecological differences between different clades. Such correlations with biogeographical and ecological differences may reflect evolutionary adaptations towards maximizing or minimizing charge accumulation, in relation to pollination, predation and parasitism, and thus we introduce the idea that electrostatic charging may be a trait upon which evolution can act.
The recent discovery that some terrestrial arthropods can detect, use, and learn from weak electrical fields adds a new dimension to our understanding of how organisms explore and interact with their environments. For bees and spiders, the filiform mechanosensory systems enable this novel sensory modality by carrying electric charge and deflecting in response to electrical fields. This mode of information acquisition opens avenues for previously unrealised sensory dynamics and capabilities. In this paper, we study one such potential: the possibility for an arthropod to locate electrically charged objects.We begin by illustrating how electrostatic interactions between hairs and surrounding electrical fields enable the process of location detection. After which we examine three scenarios: (1) the determination of the location and magnitude of multiple point charges through a single observation, (2) the learning of electrical and mechanical sensor properties and the characteristics of an electrical field through several observations, (3) the possibility that an observer can infer their location and orientation in a fixed and known electrical field (akin to "stellar navigation").To conclude, we discuss the potential of electroreception to endow an animal with thus far unappreciated sensory capabilities, such as the mapping of electrical environments. Electroreception by terrestrial arthropods offers a renewed understanding of the sensory processes carried out by filiform hairs, adding to aero-acoustic sensing and opening up the possibility of new emergent collective dynamics and information acquisition by distributed hair sensors.
Most terrestrial animals naturally accumulate electrostatic charges, meaning that they will generate electric forces that interact with other charges in their environment, including those on or within other organisms. However, how this naturally occurring static electricity influences the ecology and life history of organisms remains largely unknown.1 Mammals, birds, and reptiles are known to carry appreciable net electrostatic charges, equivalent to surface potentials on the order of hundreds to tens of thousands of volts.1-7 Therefore, we hypothesize that their parasites, such as ticks, are passively attracted onto their surfaces by electrostatic forces acting across air gaps. This biophysical mechanism is proposed by us to assist these ectoparasites in making contact with their hosts, increasing their effective "reach"because they are otherwise incapable of jumping. Herein, experimental and theoretical evidence show that the tick Ixodes ricinus (Figure 1A) can close the gap to their hosts using ecologically relevant electric fields. We also find that this electrostatic interaction is not significantly influenced by the polarity of the electric field, revealing that the mechanism of attraction relies upon induction of an electrical polarization within the tick, as opposed to a static charge on its surface. These findings open a new dimension to our understanding of how ticks, and possibly many other terrestrial organisms, find and attach to their hosts or vectors. Furthermore, this discovery may inspire novel solutions for mitigating the notable and often devastating economic, social, and public health impacts of ticks on humans and livestock.8-15
Recruitment of coral larvae on reefs is crucial for individual survival and ecosystem integrity alike. Coral larvae can detect and respond to a wide range of biotic and abiotic cues, including acoustic cues, to locate suitable sites for settlement and metamorphosis. However, the acoustic ecology of coral larvae, including how they perceive auditory cues, remains poorly understood. In this mini-review we consider both ex situ physiology and behavior, and in situ ecological and behavioral studies, to first provide an updated overview of the abiotic and biotic cues used by coral larvae to guide settlement. We then explore in detail the use of acoustic cues and the current literature on behavioral responses to acoustic stimuli. Finally, we discuss gaps in our understanding of the mechanisms by which coral larvae detect acoustic cues, highlighting a novel application of technology to explore these sensory capabilities. We also address how larval phonotaxis, i.e., the ability to orient to a sound cue, can be applied to coral reef conservation. Current research suggests that acoustic cues are likely used at small spatial scales, and that coral larvae may have directional acoustic sensitivity enabling phonotactic behavior. Recruitment of coral larvae on reefs is significantly influenced by habitat-specific soundscape variation and likely affected by anthropogenic disturbance. We propose a novel application of the remote sensing technology, micro-scanning laser Doppler vibrometry (LDV), to quantify the micromechanical responses of putative acoustically sensitive epidermal microstructures. We then highlight the potential for incorporation of acoustic enrichment techniques in coral reef conservation and restoration interventions.
With increasing evidence of electroreception in terrestrial arthropods, an understanding of receptor level processes is vital to appreciating the capabilities and limits of this sense. Here, we examine the spatio-temporal sensitivity of mechanoreceptive filiform hairs in detecting electrical fields. We first present empirical data, highlighting the time-varying characteristics of biological electrical signals. After which, we explore how electrically sensitive hairs may respond to such stimuli. The main findings are: (i) oscillatory signals (elicited by wingbeats) influence the spatial sensitivity of hairs, unveiling an inextricable spatio-temporal link; (ii) wingbeat direction modulates spatial sensitivity; (iii) electrical wingbeats can be approximated by sinusoidally modulated DC signals; and (iv) for a moving point charge, maximum sensitivity occurs at a faster timescale than a hair's frequency-based tuning. Our results show that electro-mechanical sensory hairs may capture different spatio-temporal information, depending on an object's movement and wingbeat and in comparison with aero-acoustic stimuli. Crucially, we suggest that electrostatic and aero-acoustic signals may provide distinguishable channels of information for arthropods. Given the pervasiveness of electric fields in nature, our results suggest further study to understand electrostatics in the ecology of arthropods and to reveal unknown ecological relationships and novel interactions between species.
Plants are not exactly known to be great conversationalists. In this issue of Cell, a new study highlights that when stressed by desiccation or cutting injury, tomato and tobacco plants can produce airborne ultrasonic emissions. These sounds are loud enough to be heard by insects and can be analytically categorized using trained neural networks, pointing to their potential informative value.
The atmosphere hosts multiple sources of electric charge that influence critical processes such as the aggregation of droplets and the removal of dust and aerosols. This is evident in the variability of the atmospheric electric field. Whereas these electric fields are known to respond to physical and geological processes, the effect of biotic sources of charge has not hitherto been considered. Here, we combine theoretical and empirical evidence to demonstrate that honeybee swarms directly contribute to atmospheric electricity, in proportion to the swarm density. We provide a quantitative assessment of this finding, by comparing the electrical contribution of various swarming insect species with common abiotic sources of charge. This reveals that the charge contribution of some insect swarms will be comparable with that of meteorologically induced variations. The observed transport of charge by insects therefore demonstrates an unexplored role of biogenic space charge for physical and ecological processes in the atmosphere.
In noise control applications, a perfect metasurface absorber would have the desirable traits of not only mitigating unwanted sound, but also being much thinner than the wavelengths of interest. Such deep-subwavelength performance is difficult to achieve technologically, yet moth wings, as natural metamaterials, offer functionality as efficient sound absorbers through the action of the numerous resonant scales that decorate their wing membrane. Here, we quantify the potential for moth wings to act as a sound-absorbing metasurface coating for acoustically reflective substrates. Moth wings were found to be efficient sound absorbers, reducing reflection from an acoustically hard surface by up to 87% at the lowest frequency tested (20 kHz), despite a thickness to wavelength ratio of up to 1/50. Remarkably, after the removal of the scales from the dorsal surface the wing's orientation on the surface changed its absorptive performance: absorption remains high when the bald wing membrane faces the sound but breaks down almost completely in the reverse orientation. Numerical simulations confirm the strong influence of the air gap below the wing membrane but only when it is adorned with scales. The finding that moth wings act as deep-subwavelength sound-absorbing metasurfaces opens the door to bioinspired, high-performance sound mitigation solutions.
The celestial mechanics of the Sun, Moon, and Earth dominate the variations in gravitational force that all matter, live or inert, experiences on Earth. Expressed as gravimetric tides, these variations are pervasive and have forever been part of the physical ecology with which organisms evolved. Here, we first offer a brief review of previously proposed explanations that gravimetric tides constitute a tangible and potent force shaping the rhythmic activities of organisms. Through meta-analysis, we then interrogate data from three study cases and show the close association between the omnipresent gravimetric tides and cyclic activity. As exemplified by free-running cyclic locomotor activity in isopods, reproductive effort in coral, and modulation of growth in seedlings, biological rhythms coincide with temporal patterns of the local gravimetric tide. These data reveal that, in the presumed absence of rhythmic cues such as light and temperature, local gravimetric tide is sufficient to entrain cyclic behaviour. The present evidence thus questions the phenomenological significance of so-called free-run experiments.
The use of agrochemicals is increasingly recognized as interfering with pollination services due to its detrimental effects on pollinators. Compared to the relatively well-studied chemical toxicity of agrochemicals, little is known on how they influence various biophysical floral cues that are used by pollinating insects to identify floral rewards. Here, we show that widely used horticultural and agricultural synthetic fertilizers affect bumblebee foraging behavior by altering a complex set of interlinked biophysical properties of the flower. We provide empirical and model-based evidence that synthetic fertilizers recurrently alter the magnitude and dynamics of floral electrical cues, and that similar responses can be observed with the neonicotinoid pesticide imidacloprid. We show that biophysical responses interact in modifying floral electric fields and that such changes reduce bumblebee foraging, reflecting a perturbation in the sensory events experienced by bees during flower visitation. This unveils a previously unappreciated anthropogenic interference elicited by agrochemicals within the electric landscape that is likely relevant for a wide range of chemicals and organisms that rely on naturally occurring electric fields.