Echolocating bats use a nearly time-optimal strategy to intercept prey

Acquisition of food in many animal species depends on the pursuit and capture of moving prey. Among modern humans, the pursuit and interception of moving targets plays a central role in a variety of sports, such as tennis, football, Frisbee, and baseball. Studies of target pursuit in animals, ranging from dragonflies to fish and dogs to humans, have suggested that they all use a constant bearing (CB) strategy to pursue prey or other moving targets. CB is best known as the interception strategy employed by baseball outfielders to catch ballistic fly balls. CB is a time-optimal solution to catch targets moving along a straight line, or in a predictable fashion--such as a ballistic baseball, or a piece of food sinking in water. Many animals, however, have to capture prey that may make evasive and unpredictable maneuvers. Is CB an optimum solution to pursuing erratically moving targets? Do animals faced with such erratic prey also use CB? In this paper, we address these questions by studying prey capture in an insectivorous echolocating bat. Echolocating bats rely on sonar to pursue and capture flying insects. The bat's prey may emerge from foliage for a brief time, fly in erratic three-dimensional paths before returning to cover. Bats typically take less than one second to detect, localize and capture such insects. We used high speed stereo infra-red videography to study the three dimensional flight paths of the big brown bat, Eptesicus fuscus, as it chased erratically moving insects in a dark laboratory flight room. We quantified the bat's complex pursuit trajectories using a simple delay differential equation. Our analysis of the pursuit trajectories suggests that bats use a constant absolute target direction strategy during pursuit. We show mathematically that, unlike CB, this approach minimizes the time it takes for a pursuer to intercept an unpredictably moving target. Interestingly, the bat's behavior is similar to the interception strategy implemented in some guided missiles. We suggest that the time-optimal strategy adopted by the bat is in response to the evolutionary pressures of having to capture erratic and fast moving insects.     

Discrimination of signals simulating movement of a sound source by dogs after ablation of the auditory cortex

The ability to perceive a moving sound image at dichotic stimulation was studied by means of avoidance technique for decorticated (AI, AII, Ep) dogs. The bilateral ablation disturbed the temporal cue discrimination of the direction of movement. But the animals retained the ability to localize the moving signal using delta I-cue.     

Spatial facilitation by a high-performance dragonfly target-detecting neuron

Many animals visualize and track small moving targets at long distances-be they prey, approaching predators or conspecifics. Insects are an excellent model system for investigating the neural mechanisms that have evolved for this challenging task. Specialized small target motion detector (STMD) neurons in the optic lobes of the insect brain respond strongly even when the target size is below the resolution limit of the eye. Many STMDs also respond robustly to small targets against complex stationary or moving backgrounds. We hypothesized that this requires a complex mechanism to avoid breakthrough responses by background features, and yet to adequately amplify the weak signal of tiny targets. We compared responses of dragonfly STMD neurons to small targets that begin moving within the receptive field with responses to targets that approach the same location along longer trajectories. We find that responses along longer trajectories are strongly facilitated by a mechanism that builds up slowly over several hundred milliseconds. This allows the neurons to give sustained responses to continuous target motion, thus providing a possible explanation for their extraordinary sensitivity.     

Acoustical communication and the mating system of the Australian whistling moth Hecatesia exultans (Noctuidae: Agaristinae)

Males of the Australian whistling moth Hecatesia exultans produce ultrasonic acoustical signals while perched on low vegetation. Some males call more or less continuously for several hours during midday with individuals occupying the same general calling area for up to several weeks. The nearest neighbour of calling males is typically 15 to 25m distant, at the outer edge of the estimated range at which neighbours can detect each other's ultrasonic signals. Calling male intruders occasionally enter an occupied territory, resulting in aerial clashes with nearly continuous signalling by both combatants. Males respond to playback of taped signals by flying toward the speaker and sometimes by calling while perched on or near the speaker. Females sometimes visit calling males, with copulation following very soon after the female alights on vegetation near the male's perch. Males increase the rate of sound production by about 11% when presented with moving pinned specimens or paper models of conspecifics. These observations and experiments indicate that males use ultrasound as long-distance communication signals designed to attract sexually receptive females and to establish territorial residency in competition with other males.     

The behavioral responses of a nocturnal burrowing marsupial (Lasiorhinus latifrons) to drone flight

The use of drones in wildlife research and management is increasing. Recent evidence has demonstrated the impact of drones on animal behavior, but the response of nocturnal animals to drone flight remains unknown. Utilizing a lightweight commercial drone, the behavioral response of southern hairy‐nosed wombats (Lasiorhinus latifrons) to drone flights was observed at Kooloola Station, Swan Reach, South Australia. All wombats flown over during both day and night flights responded behaviorally to the presence of drones. The response differed based on time of day. The most common night‐time behavior elicited by drone flight was retreat, compared to stationary alertness behavior observed for daytime drone flights. The behavioral response of the wombats increased as flight altitude decreased. The marked difference of behavior between day and night indicates that this has implications for studies using drones. The behavior observed during flights was altered due to the presence of the drone, and therefore, shrewd study design is important (i.e., acclimation period to drone flight). Considering the sensory adaptations of the target species and how this may impact its behavioral response when flying at night is essential.     

The Songbird as a Percussionist: Syntactic Rules for Non-Vocal Sound and Song Production in Java Sparrows

Music and dance are two remarkable human characteristics that are closely related. Communication through integrated vocal and motional signals is also common in the courtship displays of birds. The contribution of songbird studies to our understanding of vocal learning has already shed some light on the cognitive underpinnings of musical ability. Moreover, recent pioneering research has begun to show how animals can synchronize their behaviors with external stimuli, like metronome beats. However, few studies have applied such perspectives to unraveling how animals can integrate multimodal communicative signals that have natural functions. Additionally, studies have rarely asked how well these behaviors are learned. With this in mind, here we cast a spotlight on an unusual animal behavior: non-vocal sound production associated with singing in the Java sparrow (Lonchura oryzivora), a songbird. We show that male Java sparrows coordinate their bill-click sounds with the syntax of their song-note sequences, similar to percussionists. Analysis showed that they produced clicks frequently toward the beginning of songs and before/after specific song notes. We also show that bill-clicking patterns are similar between social fathers and their sons, suggesting that these behaviors might be learned from models or linked to learning-based vocalizations. Individuals untutored by conspecifics also exhibited stereotypical bill-clicking patterns in relation to song-note sequence, indicating that while the production of bill clicking itself is intrinsic, its syncopation appears to develop with songs. This paints an intriguing picture in which non-vocal sounds are integrated with vocal courtship signals in a songbird, a model that we expect will contribute to the further understanding of multimodal communication.     

Neurogenesis or neuronal specification: phosphorylation strikes again!

One way to localize sounds is to measure differences in sound intensity at the two ears. This comparison is made in the lateral superior olive, where signals from both ears converge. Magnusson et al. in this issue of Neuron show that dendritic GABA release can regulate this comparison, which may allow animals localizing sounds to adapt to listening conditions.     

The language of lizards: interpreting the function of visual displays of the Indian rock lizard, Psammophilus dorsalis (Agamidae)

The first step in understanding any communication system is to document signal diversity relative to the context of signalling (e.g. sex of the signaller and audience). Observation of 30 free-ranging rock lizards (Psammophilus dorsalis) on rock outcrops in southern India over a period of 18 months revealed that these lizards produce a complex array of ritualized signals involving push-ups (head-bobbing), dorsal flattening, extension of the legs or gular region, and tail-raising. Push-ups were performed by both sexes, usually after moving from one location to another. Push-ups were rarely accompanied by other postural modifications, and seem to function as non-directed signals. Dorsal flattening was elicited by birds flying overhead, and seems to make the lizard less conspicuous to predators. There was, nonetheless, a strong sex difference in the frequency of this behaviour, because the habitats used by males (open rocks) exposed them to more birds. Males displayed to females by extending their gular folds and arching their backs; other animals (e.g. squirrels, monkeys) also elicited the latter posture from both sexes. Leg extension was observed for both males and females, but in different contexts—males in response to conspecifics, females in response to other animals. Females raised their tails in response to encountering a male. Thus, these lizards have a complex repertoire of postures for predator evasion, for interaction with other species and with conspecifics, and for communicating sex-specific social information about gender (tail-raise) or dominance status (gular extension, leg extension).     

The precedence effect in the horizontal and vertical planes in experiments with a moving lagging signal

The precedence effect in the localization of a moving lagging sound source was studied in experiments on humans under the free field conditions in the presence of a stationary (lead) sound source. Broad-band noise (5–18 kHz) bursts 1 s in duration presented in the horizontal and vertical planes were used as signals. The lead-lag delays ranged from 1 to 40 ms. The results showed that, if the signals were presented in the horizontal plane, the probability of correct localization of the moving lagging signal was decreased for delays shorter than 25 ms; if the signals were presented in the vertical plane, it was decreased for delays shorter than 40 ms. If the delays were shorter than 8–10 ms, the subjects could not localize the moving lagging signal at all. In this interval of delays, the subjects could localize only the lead signal. The mean echo threshold for signals presented in the horizontal plane was smaller than for signals presented in the vertical plane (7.3 and 10.1 ms, respectively). However, comparison of these values across the sample of subject did not show significant differences [F(1, 5) = 5.52, p = 0.07]. The results of the study suggest that the precedence effect causes a tendency towards a stronger suppression of a moving lagging signal in the vertical plane than in the horizontal plane.     

Visual control of cursorial prey pursuit by tiger beetles (Cicindelidae)

Target detection poses problems for moving animals, such as tiger beetles, that track targets visually. The pursuer's movements degrade target image contrast and induce reafferent image movement that confounds continuous detection of prey. In nature, beetles pursue prey discontinuously with several iterations of stop-and-go running. The beetle's dynamics were analyzed by filming pursuits of prey or experimenter-controlled dummies. Durations of stops are inversely related to prey visual angular velocity; as the prey image moves between neighboring ommatidial fields, the beetle relocalizes it and renews running. During subsequent runs, translation and rotation depend upon prey visual angular velocity and position, respectively, seen during the previous stop. The beetle runs, then stops, while prey continues moving. After two to three iterations of stop-and-go the beetle catches its prey, suggesting open-loop control of running. Computational model simulations produce good qualitative spatio-temporal fit with actual pursuits. However, when pursuing prey dummies, beetles track continuously and quickly follow changes in target position, suggesting closed-loop control using a position-sensitive servo mechanism. Differences between these types of pursuit control system are discussed with respect to limitations in signal detection, particularly spatio-temporal contrast, that may force beetles to use an open-loop system. Accepted: 7 April 1997     

Forecast ability of the auditory system during perception of gradually or abruptly moving short sound images

The ability to localize endpoints of sound image trajectories was studied in comparison with stationary sound image positions. Sound images moved either gradually or abruptly to the left or right from the head midline. Different types of sound image movement were simulated by manipulating the interaural time delay. Subjects were asked to estimate the position of the virtual sound source, using the graphic tablet. It was revealed that the perceived endpoints of the moving sound image trajectories, like stationary stimulus positions, depended on the interaural time delay. The perceived endpoints of the moving sound images simulated by stimuli with the final interaural time delay lower than 200 micros were displaced further from the head midline as compared to stationary stimuli of the same interaural time delays. This forward displacement of the perceived position of the moving target can be considered as "representational momentum" and can be explained by mental extrapolation of the dynamic information, which is necessary for successive sensorimotor coordination. For interaural time delays above 400 micros, final positions of gradually and abruptly moving sound sources were closer to the head midline than corresponding stationary sound image position. When comparing the results of both duration conditions, it was shown that in case of longer stimuli the endpoints of gradually moving sound images were lateralized further from the head midline for interaural time delays above 400 micros.     

The erroneous courtship hypothesis: do insects really engage in aerial wars of attrition?

Males of various flying insects perform conspicuous aerial interactions around their mating stations. The broadly accepted interpretation of their aerial interaction is a war of attrition, where two contestants perform costly displays, and the one that reaches its cost threshold earlier gives up. The implicit but important requirement in this model is that some forces that match the intensity of display of the two contestants are necessary, and failure to enforce matching allows foul contestants that delay or stop their display to avoid paying contest costs. In addition, wars of attrition require flying insects to distinguish the sex of flying conspecifics because their aerial interactions begin when intruders fly into the territory. We investigated past research on the behaviour of odonates and butterflies aiming to clarify whether the two prerequisites of wars of attrition are fulfilled: (1) contestants can inflict substantial costs on nondisplaying opponents and (2) contestants can discriminate the sex of flying conspecifics. In odonates, we found an abundance of evidence suggesting that contests involve physical attack and that the ability of sexual discrimination is sufficient. Therefore, wars of attrition may occur in territorial odonates. In butterflies, however, we could not find any evidence that the two prerequisites are filled. The aerial interactions of butterflies are better interpreted as courtship between sexually active males (the erroneous courtship hypothesis). Based on these results, we discuss future directions of research on the aerial contests of flying insects.     

Precedence effect at horizontal and vertical plane and moving lagging signal

The precedence effect refers to the fact that humans are able to localize sound sources in reverberant environments. In this study, sound localization was studied with dual sound source: stationary (lead) and moving (lag) for two planes: horizontal and vertical. Duration of lead and lag signals was 1s. Lead-lag delays ranged from 1-40 ms. Testing was conducted in free field, with broadband noise busts (5-18 kHz). The listeners indicated the perceived location of the lag signal. Results suggest that at delays above to 25 ms in horizontal plane and 40 ms in vertical plane subjects localized correctly the moving signal. At short delays (up to 8-10 ms), regardless of the instructions, all subjects pointed to the trajectory near the lead. The echo threshold varied dramatically across listeners. Mean echo thresholds were 7.3 ms in horizontal plane and 10.1 ms in vertical plane. Statistically significant differences were not observed for two planes [F(1, 5) = 5.52; p = 0.07].     

Moving in a moving medium: new perspectives on flight

One of the defining features of the aerial environment is its variability; air is almost never still. This has profound consequences for flying animals, affecting their flight stability, speed selection, energy expenditure and choice of flight path. All these factors have important implications for the ecology of flying animals, and the ecosystems they interact with, as well as providing bio-inspiration for the development of unmanned aerial vehicles. In this introduction, we touch on the factors that drive the variability in airflows, the scales of variability and the degree to which given airflows may be predictable. We then summarize how papers in this volume advance our understanding of the sensory, biomechanical, physiological and behavioural responses of animals to air flows. Overall, this provides insight into how flying animals can be so successful in this most fickle of environments.This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’.     

Estimating position and velocity of a submerged moving object by the clawed frog Xenopus and by fish—A cybernetic approach

The lateral-line system is a unique facility of aquatic animals to locate predator, prey, or conspecifics. We present a detailed model of how the clawed frog Xenopus, or fish, can localize submerged moving objects in three dimensions by using their lateral-line system. In so doing we develop two models of a slightly different nature. First, we exploit the characteristic properties of the velocity field, such as zeros and maxima or minima, that a moving object generates at the lateral-line organs and that are directly accessible neuronally, in the context of a simplified geometry. In addition, we show that the associated neuronal model is robust with respect to noise. Though we focus on the superficial neuromasts of Xenopus the same arguments apply mutatis mutandis to the canal lateral-line system of fish. Second, we present a full-blown three-dimensional reconstruction of the source on the basis of a maximum likelihood argument.     

Through the eye, slowly: delays and localization errors in the visual system

Reviews on the visual system generally praise its amazing performance. Here we deal with its biggest weakness: sluggishness. Inherent delays lead to mislocalization when things move or, more generally, when things change. Errors in time translate into spatial errors when we pursue a moving object, when we try to localize a target that appears just before a gaze shift, or when we compare the position of a flashed target with the instantaneous position of a continuously moving one (or one that appears to be moving even though no change occurs in the retinal image). Studying such diverse errors might rekindle our thinking about how the brain copes with real-time changes in the world.     

Wind-sensitive interneurones in the spider CNS (Cupiennius salei ): directional information processing of sensory inputs from trichobothria on the walking legs

Spiders can use air particle movements to localize moving prey. We studied the responses of 32 wind-sensitive interneurones in the hunting spider Cupiennius salei to prey stimuli. Stimulation with a tethered flying fly or with artificial air pulses activated plurisegmental interneurones that responded to changes in air movement velocity and were thus well suited to represent the highly fluctuating air stream typical of prey stimuli. In most interneurones (n = 18) the responses to the stimulation of different legs were not significantly different from each other. Different interneurones had different response characteristics and their latencies largely overlapped suggesting that there is parallel processing of the signals by populations of interneurones with different response characteristics. In two interneurones the number of spikes and the spiking pattern elicited by stimulation of each of the eight legs markedly differed depending on the leg stimulated. These neurones may play an important role in directional information processing. Stimulation of the adjacent legs from front to back or from back to front revealed two interneurones sensitive to the direction of successive stimulation of the legs. These neurones may be able to detect the motion of an air movement source in a preferred direction and thus act as nearfield motion detectors to localize a moving prey item. Accepted: 28 September 1996     

Learned or innate production of acoustic signals in fishes: a test using a cyprinid

No information on the inheritance of the ability to produce sounds exists for fishes. In birds, which usually provide extensive post-hatching parental care, acoustic signals are learned in some species but are innate in others. Almost no fishes provide extensive post-hatching parental care and, consequently, the offspring have little opportunity to hear and learn sounds produced by the parents (usually the male in fishes); they may, however, be exposed to acoustic signals of conspecifics in the same habitat. We used a cyprinid, Codoma ornata, to test whether sound production is learned from the parents or whether it is innate. Fertilized eggs of this species were raised in isolation from adults. Upon maturity, these fish were tested for sound production in aggressive and reproductive contexts. Fish which had no contact with adults, and therefore no opportunity to hear the acoustic signals of their species, produced sounds that were similar to those produced by their parents, and they produced these in the same contexts. Significant differences were observed in dominant frequency for one context, with the smaller F₁ fish having signals of higher frequency than parental fish. Since no opportunity for learning existed, this provided evidence that the ability to produce sounds is innate in this minnow species.     

Calling under pressure: short-finned pilot whales make social calls during deep foraging dives

Toothed whales rely on sound to echolocate prey and communicate with conspecifics, but little is known about how extreme pressure affects pneumatic sound production in deep-diving species with a limited air supply. The short-finned pilot whale (Globicephala macrorhynchus) is a highly social species among the deep-diving toothed whales, in which individuals socialize at the surface but leave their social group in pursuit of prey at depths of up to 1000 m. To investigate if these animals communicate acoustically at depth and test whether hydrostatic pressure affects communication signals, acoustic DTAGs logging sound, depth and orientation were attached to 12 pilot whales. Tagged whales produced tonal calls during deep foraging dives at depths of up to 800 m. Mean call output and duration decreased with depth despite the increased distance to conspecifics at the surface. This shows that the energy content of calls is lower at depths where lungs are collapsed and where the air volume available for sound generation is limited by ambient pressure. Frequency content was unaffected, providing a possible cue for group or species identification of diving whales. Social calls may be important to maintain social ties for foraging animals, but may be impacted adversely by vessel noise.     

Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans

The ability to optically excite or silence specific cells using optogenetics has become a powerful tool to interrogate the nervous system. Optogenetic experiments in small organisms have mostly been performed using whole-field illumination and genetic targeting, but these strategies do not always provide adequate cellular specificity. Targeted illumination can be a valuable alternative but it has only been shown in motionless animals without the ability to observe behavior output. We present a real-time, multimodal illumination technology that allows both tracking and recording the behavior of freely moving C. elegans while stimulating specific cells that express channelrhodopsin-2 or MAC. We used this system to optically manipulate nodes in the C. elegans touch circuit and study the roles of sensory and command neurons and the ultimate behavioral output. This technology enhances our ability to control, alter, observe and investigate how neurons, muscles and circuits ultimately produce behavior in animals using optogenetics.