Perception and the Characteristics of the Response of Honey Bees,Paper Wasps,and Red Wood Ants to a Low-Frequency Electric Field

Bees, wasps, and ants have no specialized receptors for the perception of an electric field. An appropriate response to naturally occurring electric fields in bees and ants is associated with atmospheric exposure, amplified by the approach of the front of a thunderstorm. The primary transducers of mechanoreceptors that respond to displacement are related to the perception of low-frequency electric fields of high intensity by insects. The non-specific mechanism of perception of electric fields is based on irritation by induced currents that flow in the locations of their contact with each other and/or conductive surfaces. The frequency dependence of the electric field sensitivity is determined mainly by the magnitude of the current induced by it and the intensity of its contact action. The magnitude of the current induced in the outer part of the insect body is non-linearly related to the frequency of the electric field. The region with the highest sensitivity to electric fields is close to 500 Hz, which is consistent with the maximum magnitude of the induced current. At the same time, the threshold of the sensitivity to an electric field in wasps is approximately 0.04 kV/m, while in bees it is 0.45 kV/m. Ants react to the action of an electric field of 7–10 kV/m by slowing their movement. Magnetic fields and ionization, which accompany the generation of an electric field whose intensity reaches 15–20 kV/m, do not stimulate changes in the behavior of insects.

     

Electric field detection in sawfish and shovelnose rays

In the aquatic environment, living organisms emit weak dipole electric fields, which spread in the surrounding water. Elasmobranchs detect these dipole electric fields with their highly sensitive electroreceptors, the ampullae of Lorenzini. Freshwater sawfish, Pristis microdon, and two species of shovelnose rays, Glaucostegus typus and Aptychotrema rostrata were tested for their reactions towards weak artificial electric dipole fields. The comparison of sawfishes and shovelnose rays sheds light on the evolution and function of the elongated rostrum ('saw') of sawfish, as both groups evolved from a shovelnose ray-like ancestor. Electric stimuli were presented both on the substrate (to mimic benthic prey) and suspended in the water column (to mimic free-swimming prey). Analysis of around 480 behavioural sequences shows that all three species are highly sensitive towards weak electric dipole fields, and initiate behavioural responses at median field strengths between 5.15 and 79.6 nVcm(-1). The response behaviours used by sawfish and shovelnose rays depended on the location of the dipoles. The elongation of the sawfish's rostrum clearly expanded their electroreceptive search area into the water column and enables them to target free-swimming prey.     

On the electrodetection threshold of aquatic vertebrates with ampullary or mucous gland electroreceptor organs

Reinterpretation of research on the electric sense in aquatic organisms with ampullary organs results in the following conclusions. The detection limit of limnic vertebrates with ampullary organs is 1 microV cm(-1), and of marine fish is 20 nV cm(-1). Angular movements are essential for stimulation of the ampullary system in uniform d.c. fields. Angular movements in the geomagnetic field also generate induction voltages, which exceed the 20 nV cm(-1) limit in marine fish. As a result, marine electrosensitive fish are sensitive to motion in the geomagnetic field, whereas limnic fish are not. Angular swimming movements generate a.c. stimuli, which act like the noise in a stochastic resonance system, and result in a detection threshold in marine organisms as low as 1 nV cm(-1). Fish in the benthic space are exposed to stronger electric stimuli than fish in the pelagic space. Benthic fish scan the orientation plane for the maximum potential difference with their raster of electroreceptor organs, in order to locate bioelectric prey. This behaviour explains why the detection threshold does not depend on fish size. Pelagic marine fish are mainly exposed to electric fields caused by movements in the geomagnetic field. The straight orientation courses found in certain shark species might indicate that the electric sense functions as a simple bisensor system. Symmetrical stimulation of the sensory raster would provide an easy way to keep a straight course with respect to a far-field stimulus. The same neural mechanism would be effective in the location of a bioelectric prey generating a near-field stimulus. The response criteria in conditioning experiments and in experiments with spontaneous reactions are discussed.     

Maternal Defence of a Leaf Beetle is not Effective against Parasitoids but is against Pedestrian Predators

Females of the subsocial leaf beetle Gonioctena sibirica attend their broods on the willow Salix bakko. Females with broods settle on the underside of the basal part of leaves and face towards the base of the shoots. If other arthropods approach such attendant females, the females show aggressive behaviour against the intruder. The effectiveness of maternal care on offspring survival against pedestrian predators and against a parasitoid wasp was evaluated in field experiments using three groups: broods from which parent females were experimentally removed, those from which females were removed and pedestrian predators were excluded by tanglefoot treatments, and control broods. These experiments showed that maternal care was highly effective against pedestrian predators, but parasitism was not affected by the presence of females. Offspring mortality by predation or by parasitism was not usually dependent on larval densities. Position and orientation of attendant females will be effective for them to detect intruders which approach their larvae by walking along the stem, while it can inhibit the females from detecting parasitoids which fly and land directly on the leaf close to the larvae. The results suggest a trade-off in the effectiveness of prey defensive behaviour against different enemy species: prey defensive behaviour specific to one type of the enemy may make the prey more vulnerable to the other.     

The neurobiology and behavior of the American water shrew (Sorex palustris)

American water shrews (Sorex palustris) are aggressive predators that dive into streams and ponds to find prey at night. They do not use eyesight for capturing fish or for discriminating shapes. Instead they make use of vibrissae to detect and attack water movements generated by active prey and to detect the form of stationary prey. Tactile investigations are supplemented with underwater sniffing. This remarkable behavior consists of exhalation of air bubbles that spread onto objects and are then re-inhaled. Recordings for ultrasound both above and below water provide no evidence for echolocation or sonar, and presentation of electric fields and anatomical investigations provide no evidence for electroreception. Counts of myelinated fibers show by far the largest volume of sensory information comes from the trigeminal nerve compared to optic and cochlear nerves. This is in turn reflected in the organization of the water shrew’s neocortex, which contains two large somatosensory areas and much smaller visual and auditory areas. The shrew’s small brain with few cortical areas may allow exceptional speed in processing sensory information and producing motor output. Water shrews can accurately attack the source of a water disturbance in only 50 ms, perhaps outpacing any other mammalian predator.     

Behavioral stochastic resonance: how the noise from a Daphnia swarm enhances individual prey capture by juvenile paddlefish.

Zooplankton emit weak electric fields into the surrounding water that originate from their own muscular activities associated with swimming and feeding. Juvenile paddlefish prey upon single zooplankton by detecting and tracking these weak electric signatures. The passive electric sense in this fish is provided by an elaborate array of electroreceptors, Ampullae of Lorenzini, spread over the surface of an elongated rostrum. We have previously shown that the fish use stochastic resonance to enhance prey capture near the detection threshold of their sensory system. However, stochastic resonance requires an external source of electrical noise in order to function. A swarm of plankton, for example Daphnia, can provide the required noise. We hypothesize that juvenile paddlefish can detect and attack single Daphnia as outliers in the vicinity of the swarm by using noise from the swarm itself. From the power spectral density of the noise plus the weak signal from a single Daphnia, we calculate the signal-to-noise ratio, Fisher information and discriminability at the surface of the paddlefish's rostrum. The results predict a specific attack pattern for the paddlefish that appears to be experimentally testable.     

Fear in animals: a meta-analysis and review of risk assessment

The amount of risk animals perceive in a given circumstance (i.e. their degree of 'fear') is a difficult motivational state to study. While many studies have used flight initiation distance as a proxy for fearfulness and examined the factors influencing the decision to flee, there is no general understanding of the relative importance of these factors. By identifying factors with large effect sizes, we can determine whether anti-predator strategies reduce fear, and we gain a unique perspective on the coevolution of predator and anti-predator behaviour. Based on an extensive review and formal meta-analysis, we found that predator traits that were associated with greater risk (speed, size, directness of approach), increased prey distance to refuge and experience with predators consistently amplified the perception of risk (in terms of flight initiation distance). While fish tolerated closer approach when in larger schools, other taxa had greater flight initiation distances when in larger groups. The presence of armoured and cryptic morphologies decreased perception of risk, but body temperature in lizards had no robust effect on flight initiation distance. We find that selection generally acts on prey to be sensitive to predator behaviour, as well as on prey to modify their behaviour and morphology.     

Three-dimensional analysis of object properties during active electrolocation in mormyrid weakly electric fishes (Gnathonemus petersii)

Weakly electric fishes are nocturnal and orientate in the absence of vision by using their electrical sense. This enables them not only to navigate but also to perceive and recognize objects in complete darkness. They create an electric field around their bodies by producing electric signals with specialized electric organs. Objects within this field alter the electric current at electroreceptor organs, which are distributed over almost the entire body surface. During active electrolocation, fishes detect, localize and analyse objects by monitoring their self-produced electric signals. We investigated the ability of the mormyrid Gnathonemus petersii to perceive objects three-dimensionally in space. Within a range of about 12 cm, G. petersii can perceive the distance of objects. Depth perception is independent of object size, shape and material. The mechanism for distance determination through electrolocation involves calculating the ratio between two parameters (maximal slope and maximal amplitude) of the electrical image which each object projects onto the fish's skin. During active electrolocation, electric fishes cannot only locate objects in space but in addition can determine the three-dimensional shape of an object. Up to certain limits, objects are spontaneously categorized according to their shapes, but not according to their sizes or the materials of which they are made.     

Insight into the mechanisms of neuronal processing from electric fish

Weakly electric fish use their electric fields to locate objects and communicate with each other. Their electric discharges vary with species, gender, and social status. This variation is mediated by steroid and peptide hormones that influence ion currents through changes in gene expression or phosphorylation state. Understanding how electric fish decode the perturbations of their electric fields that result from interactions with the discharges of other fish or prey is illuminating general mechanisms of neuronal processing. Their central sensory circuits are specialized to process amplitude modulated signals, to detect microsecond variations in spike timing, and are dynamically reconfigured depending on the stimulus parameters.     

A new pressure sensory mechanism for prey detection in birds: the use of principles of seabed dynamics?

We demonstrate a novel mechanism for prey detection in birds. Red knots (Calidris canutus), sandpipers that occur worldwide in coastal intertidal areas, are able to detect their favourite hard-shelled prey even when buried in sand beyond the reach of their bills. In operant conditioning experiments designed to find out whether the birds could tell buckets containing only wet sand from buckets containing hard objects in wet sand, we show that they detect the presence not only of deeply buried live bivalves but also of stones. The latter finding virtually excludes, under experimental conditions, prey-detection mechanisms based on vision, acoustics, smell, taste, vibrational signals emitted by prey, temperature gradients and electromagnetic fields. A failure to discriminate between food and non-food trays with dry sand indicates that pore water is involved. Based on the presence of large arrays of Herbst corpuscles (sensory organs that can measure the acceleration due to changes in pressure), the specifics of foraging technique and the characteristics of sediments on which red knots feed, we deduce that the sensory mechanism involves the perception of pressure gradients that are formed when bills probe in soft sediments in which inanimate objects block pore water flow. To our knowledge, this mechanism has not been described before. It is argued that repeated probing in soft, wet sediments allows red knots to induce a residual pressure build-up of sufficient strength to detect the pressure disturbance caused by a nearby object. The cyclic process of shaking loosely packed sand grains followed by gravitational settling into a closer packing, leads, owing to insufficient drainage of the sediment, to a locally increased pressure disturbance that is ''pumped up'' at each shake.     

Hydrodynamic image formation by the peripheral lateral line system of the Lake Michigan mottled sculpin, Cottus bairdi

Lake Michigan mottled sculpin (Cottus bairdi) have a lateral-line-mediated prey-capture behaviour that consists of an initial orientation towards the prey, a sequence of approach movements, and a final strike at the prey. This unconditioned behaviour can be elicited from blinded sculpin in the laboratory by both real and artificial (vibrating sphere) prey. In order to visualize what Lake Michigan mottled sculpin might perceive through their lateral line when approaching prey, we have combined anatomical, neurophysiological, behavioural and computational modelling techniques to produce three-dimensional maps of how excitation patterns along the lateral line sensory surface change as sculpin approach a vibrating sphere. Changes in the excitation patterns and the information they contain about source location are consistent with behavioural performance, including the approach pathways taken by sculpin to the sphere, the maximum distances at which approaches can be elicited, distances from which strikes are launched, and strike success. Information content is generally higher for laterally located sources than for frontally located sources and this may explain exceptional performance (e.g. successful strikes from unusually long distances) in response to lateral sources and poor performance (e.g. unsuccessful strikes) to frontal sources.     

Spatial co-occurrence networks predict the feeding histories of polyphagous arthropod predators at field scales

In agricultural systems, polyphagous beetles and spiders are abundant components of the beneficial arthropod community. Although data on the dietary ranges of these groups is increasing, remarkably little is understood regarding how individuals interact with their prey at small spatial scales. We demonstrate the utility of a spatially-explicit network model that integrates predator behaviour using predator-prey co-occurrences. Three co-occurrence matrices, one each for June, July and August, were generated using Vortis suction sample data collected from an 80 point grid imposed on a field of winter wheat. Heuristic predator-prey linkages, based on positive spatial co-occurrence, were imposed on these three matrices to create networks. It was found that primary consumers were highly aggregated and showed a strong tendency to co-occur. This contrasted with patterns of predator–predator or predator–prey co-occurrences that either aggregated to their prey or were weak and more scattered. These patterns could not be explained by either competition for resources or body size differences. Procrustean methods indicated that the networks were temporally dynamic, consistently achieving rates of turnover >60%. A negative relationship was found between decreasing predator–prey co-occurrence in the network and the number of prey positives in the guts of those predators. For large polyphagous beetles, the closer they were to their prey at the field scale, the more likely they were to have eaten them. This simple underlying relationship suggests that spatial co-occurrence networks can be used to predict feeding behaviour and could make a valuable contribution to food web structuring.     

Passive electroreception in aquatic mammals

Passive electroreception is a sensory modality in many aquatic vertebrates, predominantly fishes. Using passive electroreception, the animal can detect and analyze electric fields in its environment. Most electric fields in the environment are of biogenic origin, often produced by prey items. These electric fields can be relatively strong and can be a highly valuable source of information for a predator, as underlined by the fact that electroreception has evolved multiple times independently. The only mammals that possess electroreception are the platypus (Ornithorhynchus anatinus) and the echidnas (Tachyglossidae) from the monotreme order, and, recently discovered, the Guiana dolphin (Sotalia guianensis) from the cetacean order. Here we review the morphology, function and origin of the electroreceptors in the two aquatic species, the platypus and the Guiana dolphin. The morphology shows certain similarities, also similar to ampullary electroreceptors in fishes, that provide cues for the search for electroreceptors in more vertebrate and invertebrate species. The function of these organs appears to be very similar. Both species search for prey animals in low-visibility conditions or while digging in the substrate, and sensory thresholds are within one order of magnitude. The electroreceptors in both species are innervated by the trigeminal nerve. The origin of the accessory structures, however, is completely different; electroreceptors in the platypus have developed from skin glands, in the Guiana dolphin, from the vibrissal system.     

Phylogenetic and ecological factors influencing the number and distribution of electroreceptors in elasmobranchs

Electroreception is found throughout the animal kingdom from invertebrates to mammals and has been shown to play an important role in prey detection, facilitating social behaviours, the detection of predators and orientation to the earth's magnetic field for navigation. Electroreceptors in elasmobranchs, the ampullae of Lorenzini, detect minute electric fields and independently process these stimuli, thereby providing spatial information to the central nervous system on the location of a source, often potential prey. The ampullae of Lorenzini are individually connected to a single somatic pore on the surface of the skin, with the spatial separation of each pore directly influencing how electrical stimuli are detected and processed. Pore abundance varies across taxonomic groups resulting in unique species-specific differences. The intricate distribution patterns created by the specific positioning of somatic pores on the head are, however, consistent within families, resulting in patterns that are identifiable at higher taxonomic levels. As elasmobranchs evolved, the electrosensory system became more complex and highly specialized, which is evident by a general trend of increasing pore abundance over time. The elasmobranch electrosensory system has evolved to operate efficiently under the environmental conditions of the particular habitat in which a species lives. For example, reduced pore abundance is evident in oceanic pelagic elasmobranchs, for whom visual cues are thought to be of great importance. Pore abundance and spatial distribution may be influenced by multiple factors including head morphology, phylogeny, feeding behaviour and habitat.     

Response of juvenile scalloped hammerhead sharks to electric stimuli

Sharks can use their electrosensory system to detect electric fields in their environment. Measurements of their electrosensitivity are often derived by calculating the voltage gradient from a model of the charge distribution for an ideal dipole. This study measures the charge distribution around a dipole in seawater and confirms the close correspondence with the model. From this, it is possible to predict how the sharks will respond to dipolar electric fields comprised of differing parameters. We tested these predictions by exposing sharks to different sized dipoles and levels of applied current that simulated the bioelectric fields of their natural prey items. The sharks initiated responses from a significantly greater distance with larger dipole sizes and also from a significantly greater distance with increasing levels of electric current. This study is the first to provide empirical evidence supporting a popular theoretical model and test predictions about how sharks will respond to a variety of different electric stimuli.     

Detecting predator–prey relationships in the sea

Understanding the strength and diversity of predator‐prey interactions among species is essential to understand ecosystem consequences of population‐level variation. Directly quantifying the predatory behaviour of wild fishes at large spatial scales (>100 m) in the open sea is fraught with difficulties. To date the only empirical approach has been to search for correlations in the abundance of predators and their putative prey. As an example we use this approach to search for predators of the keystone crown‐of‐thorns starfish. We show that this approach is unlikely to detect predator–prey linkages because the theoretical relationship is non‐linear, resulting in multiple possible prey responses for single given predator abundance. Instead we suggest some indication of the strength and ecosystem importance of a predator–prey relationship can be gained by using the abundance of both predators and their putative prey to parameterize functional response models.     

Individual‐based models of cod movement and population dynamics

Understanding the strength and diversity of predator‐prey interactions among species is essential to understand ecosystem consequences of population‐level variation. Directly quantifying the predatory behaviour of wild fishes at large spatial scales (>100 m) in the open sea is fraught with difficulties. To date the only empirical approach has been to search for correlations in the abundance of predators and their putative prey. As an example we use this approach to search for predators of the keystone crown‐of‐thorns starfish. We show that this approach is unlikely to detect predator–prey linkages because the theoretical relationship is non‐linear, resulting in multiple possible prey responses for single given predator abundance. Instead we suggest some indication of the strength and ecosystem importance of a predator–prey relationship can be gained by using the abundance of both predators and their putative prey to parameterize functional response models.     

The visual fields of Common Guillemots Uria aalge and Atlantic Puffins Fratercula arctica: foraging,vigilance and collision vulnerability

Significant differences in avian visual fields are found between closely related species that differ in their foraging technique. We report marked differences in the visual fields of two auk species. In air, Common Guillemots Uria aalge have relatively narrow binocular fields typical of those found in non‐passerine predatory birds. Atlantic Puffins Fratercula arctica have much broader binocular fields similar to those that have hitherto been recorded in passerines and in a penguin. In water, visual fields narrow considerably and binocularity in the direction of the bill is probably abolished in both auk species. Although perceptual challenges associated with foraging are similar in both species during the breeding season, when they are piscivorous, Puffins (but not Guillemots) face more exacting perceptual challenges when foraging at other times, when they take a high proportion of small invertebrate prey. Capturing this prey probably requires more accurate, visually guided bill placement and we argue that this is met by the Puffin's broader binocular field, which is retained upon immersion; its upward orientation may enable prey to be seen in silhouette. These visual field configurations have potentially important consequences that render these birds vulnerable to collision with human artefacts underwater, but not in air. They also have consequences for vigilance behaviour.     

Detection and processing of electromagnetic and near-field acoustic signals in elasmobranch fishes

The acoustic near field of quietly moving underwater objects and the bio-electric field of aquatic animals exhibit great similarity, as both are predominantly governed by Laplace's equation. The acoustic and electrical sensory modalities thus may, in directing fishes to their prey, employ analogous processing algorithms, suggesting a common evolutionary design, founded on the salient physical features shared by the respective stimulus fields. Sharks and rays are capable of orientating to the earth's magnetic field and, hence, have a magnetic sense. The electromagnetic theory of orientation offers strong arguments for the animals using the electric fields induced by ocean currents and by their own motions in the earth's magnetic field. In the animal's frame of reference, in which the sense organs are at rest, the classical concept of motional electricity must be interpreted in relativistic terms. In the ampullae of Lorenzini, weak electric fields cause the ciliated apical receptor-cell membranes to produce graded, negative receptor currents opposite in direction to the fields applied. The observed currents form part of a positive-feedback mechanism, supporting the generation of receptor potentials much larger than the input signal. Acting across the basal cell membranes, the receptor potentials control the process of synaptic transmission.     

Temporal analysis of moving DC electric fields in aquatic media

Many aquatic vertebrates can sense the weak electric fields generated by other animals and may also sense geoelectric or electromagnetic phenomena for use in orientation. All these sources generate stationary (dc) fields. In addition, fields from animals are modulated by respiration and other body movements. Since electroreceptors are insensitive to a pure dc field, it has been suggested that the ac modulation carries most of the relevant information for electrosensory animals. However, in a natural situation pure dc fields are rare since any relative movement between source and receiver will transform a dc field into a time varying signal. In this paper, we will describe the properties of such signals and how they are filtered at the first stage of electrosensory information processing in the brain. We will show that the signal perceived by an animal traversing a dc electric field contains all the information necessary to reconstruct the distance to the source and that the signal conditioning algorithms are perfectly adapted to preserve such information.