When to approach novel prey cues? Social learning strategies in frog-eating bats

Animals can use different sources of information when making decisions. Foraging animals often have access to both self-acquired and socially acquired information about prey. The fringe-lipped bat, Trachops cirrhosus, hunts frogs by approaching the calls that frogs produce to attract mates. We examined how the reliability of self-acquired prey cues affects social learning of novel prey cues. We trained bats to associate an artificial acoustic cue (mobile phone ringtone) with food rewards. Bats were assigned to treatments in which the trained cue was either an unreliable indicator of reward (rewarded 50% of the presentations) or a reliable indicator (rewarded 100% of the presentations), and they were exposed to a conspecific tutor foraging on a reliable (rewarded 100%) novel cue or to the novel cue with no tutor. Bats whose trained cue was unreliable and who had a tutor were significantly more likely to preferentially approach the novel cue when compared with bats whose trained cue was reliable, and to bats that had no tutor. Reliability of self-acquired prey cues therefore affects social learning of novel prey cues by frog-eating bats. Examining when animals use social information to learn about novel prey is key to understanding the social transmission of foraging innovations.     

Classification of insects by echolocating greater horseshoe bats

Summary Echolocating greater horseshoe bats (Rhinolophus ferrumequinum) detect insects by concentrating on the characteristic amplitude- and frequency modulation pattern fluttering insects impose on the returning echoes. This study shows that horseshoe bats can also further analyse insect echoes and thus recognize and categorize the kind of insect they are echolocating.Four greater horseshoe bats were trained in a twoalternative forced-choice procedure to choose the echo of one particular insect species turning its side towards the bat (Fig. 1). The bats were able to discriminate with over 90% correct choices between the reward-positive echo and the echoes of other insect species all fluttering with exactly the same wingbeat rate (Fig. 4).When the angular orientation of the reward-positive insect was changed (Fig. 2), the bats still preferred these unknown echoes over echoes from other insect species (Fig. 5) without any further training. Because the untrained bats did not show any prey preference, this indicates that the bats were able to perform an aspect-anglein-dependent classification of insects.Finally we tested what parameters in the echo were responsible for species recognition. It turned out that the bats especially used the small echo-modulations in between glints as a source of information (Fig. 7). Neither the amplitudenor the frequencymodulation of the echoes alone was sufficient for recognition of the insect species (Fig. 8). Bats performed a pattern recognition task based on complex computations of several acoustic parameters, an ability which might be termed cognitive.Abbreviations AM amplitude modulation - CF constant frequency - FM frequency modulation - S+ positive stimulus - S- negative stimulus     

Experimental evidence for group hunting via eavesdropping in echolocating bats

Group foraging has been suggested as an important factor for the evolution of sociality. However, visual cues are predominantly used to gain information about group members'' foraging success in diurnally foraging animals such as birds, where group foraging has been studied most intensively. By contrast, nocturnal animals, such as bats, would have to rely on other cues or signals to coordinate foraging. We investigated the role of echolocation calls as inadvertently produced cues for social foraging in the insectivorous bat Noctilio albiventris. Females of this species live in small groups, forage over water bodies for swarming insects and have an extremely short daily activity period. We predicted and confirmed that (i) free-ranging bats are attracted by playbacks of echolocation calls produced during prey capture, and that (ii) bats of the same social unit forage together to benefit from passive information transfer via the change in group members'' echolocation calls upon finding prey. Network analysis of high-resolution automated radio telemetry confirmed that group members flew within the predicted maximum hearing distance 94±6 per cent of the time. Thus, echolocation calls also serve as intraspecific communication cues. Sociality appears to allow for more effective group foraging strategies via eavesdropping on acoustical cues of group members in nocturnal mammals.     

Foraging ecology and audition in echolocating bats

The types of echolocation signal and the auditory capacities of echolocating bats are adapted to specific acoustical constraints of the foraging areas. Bats hunting insects above the canopy use low frequencies for echolocation; this is an adaptation to prey detection over long distances. Bats foraging close to and within foliage avoid masking of insect echoes by specializing on 'fluttering target' detection. 'Gleaning' bats are adapted to the auditory detection of very faint noises generated by ground-dwelling prey, and are capable of analysing fine changes in the echo spectrum, which may indicate a stationary prey changing its posture on a substrate. This review of recent research demonstrates that, in bats, foraging ecology and audition are intricately interrelated and interdependent.     

Dietary composition and echolocation call design of three sympatric insectivorous bat species from China

Studying the diet of echolocating, insectivorous bats can provide important insights into their foraging behaviors and ecological constraints they are facing. By examining an extensive data set covering a period of 2 years, the present study identifies the dietary composition of three sympatric insectivorous bat species in rural areas of Beijing municipality. Each species clearly has different preferences for particular food items. Greater horseshoe bats, Rhinolophus ferrumequinum, preferred to catch nocturnal, actively flying insects, mostly moths (Lepidoptera), and to a lesser percentage flies (Diptera), beetles (Coleoptera), and flying ants and termites (Hymenoptera). Other nocturnal insects which do not exhibit any perceptible wing movements, such as true bugs (Homoptera), or strictly diurnal insects that hardly ever fly in the dark, such as grasshoppers (Orthoptera) and dragon- and damselflies (Odonata), were never found in droppings of horseshoe bats. Large mouse-eared bats, Myotis chinensis, preferentially glean relatively large terrestrial prey of the order Coleoptera (mostly carabid beetles) and Orthoptera, whereas greater tube-nosed bats, Murina leucogaster, consume predominantly smaller, diurnal Coleoptera (mostly soldier beetles, Cantharidae, and ladybugs, Coccinellidae). Our findings also indicate previously not described, significant spectro-temporal differences in the echolocation signals of M. chinensis and M. leucogaster. The results suggest that in our study area the dramatic differences in the dietary composition of these three bat species are mainly based upon differences in their foraging behaviors, including differences in their echolocation signal structure. The dietary data provide important background information for conservational efforts, such as habitat protection.     

Use of sewage treatment works as foraging sites by insectivorous bats

Sewage treatment works (STWs) with percolating filter beds are known to provide profitable foraging areas for insectivorous birds because of their association with high macroinvertebrate densities. Fly larvae developing on filter beds at STWs may similarly provide a valuable resource for foraging bats. Over the last two decades, however, there has been a decline in filter beds towards a system of 'activated sludge'. Insects and bat activity were surveyed at 30 sites in Scotland using these two different types of sewage treatment in order to assess the possible implications of these changes for foraging bats. Bat activity (number of passes) recorded from broad-band bat detectors was quantified at three points within each site. The biomass of aerial insects, sampled over the same period as the detector surveys, was measured using a suction trap. The biomass of insects and activity of Pipistrellus spp. were significantly higher at filter beds than at activated sludge sites. In addition, although foraging activity of Pipistrellus spp. at filter beds was comparable to that of adjacent 'good' foraging habitat, foraging at activated sludge sites was considerably lower. This study indicates the high potential value of an anthropogenic process to foraging bats, particularly in a landscape where their insect prey has undergone a marked decline, and suggests that the current preference for activated sludge systems is likely to reduce the value of treatment works as foraging sites for bats.     

Diet and prey selection in the trawling long-fingered bat

The diet of the long-fingered bat Myotis capaccinii is poorly known, and there is no previously recorded information on this species' prey preferences. To investigate these subjects, we captured 51 individuals at a nursery cave in the Iberian Peninsula, from pre-breeding to post-lactation seasons. Each bat's diet composition was assessed by faecal content analysis and its foraging places (rivers, pools and channels) identified by radio-telemetry. To estimate prey availability, we sampled arthropods in the individual bats' identified foraging places and also emulated the bats' hunting technique. The bats' diet comprised of arthropods, dominated by small insects with aquatic larvae and flying adult phases. The most consumed taxon was Nematocera (mainly Chironomidae), including adults and pupae, which were also found to be the most abundant prey over water. Other frequently consumed prey were brachycerans, lepidopterans, arachnids, trichopterans and neuropterans. Diet proportions were compared with prey availability to infer a rank of preferences. The preferred prey were lepidopterans and arachnids, both having a terrestrial life cycle and a bigger size than any other taxa consumed. Without discarding the possible underestimation of prey's aerial availability, the observed preference pattern seems to be a consequence of selection for size more than for specific taxa. Apparently M. capaccinii efficiently exploit water-related prey according to availability when the bats hunt low over the water's surface, and are also able to take more profitable prey found higher in the air.     

Multimodal cues improve prey localization under complex environmental conditions

Predators often eavesdrop on sexual displays of their prey. These displays can provide multimodal cues that aid predators, but the benefits in attending to them should depend on the environmental sensory conditions under which they forage. We assessed whether bats hunting for frogs use multimodal cues to locate their prey and whether their use varies with ambient conditions. We used a robotic set-up mimicking the sexual display of a male túngara frog (Physalaemus pustulosus) to test prey assessment by fringe-lipped bats (Trachops cirrhosus). These predatory bats primarily use sound of the frog''s call to find their prey, but the bats also use echolocation cues returning from the frog''s dynamically moving vocal sac. In the first experiment, we show that multimodal cues affect attack behaviour: bats made narrower flank attack angles on multimodal trials compared with unimodal trials during which they could only rely on the sound of the frog. In the second experiment, we explored the bat''s use of prey cues in an acoustically more complex environment. Túngara frogs often form mixed-species choruses with other frogs, including the hourglass frog (Dendropsophus ebraccatus). Using a multi-speaker set-up, we tested bat approaches and attacks on the robofrog under three different levels of acoustic complexity: no calling D. ebraccatus males, two calling D. ebraccatus males and five D. ebraccatus males. We found that bats are more directional in their approach to the robofrog when more D. ebraccatus males were calling. Thus, bats seemed to benefit more from multimodal cues when confronted with increased levels of acoustic complexity in their foraging environments. Our data have important consequences for our understanding of the evolution of multimodal sexual displays as they reveal how environmental conditions can alter the natural selection pressures acting on them.     

Echolocation behavior of rufous horseshoe bats hunting for insects in the flycatcher-style

Summary The echolocation behavior ofRhinolophus rouxi when waiting for insects on a perch and when pursuing them in short hunting flights is described. It reveals that flycatcher-style hunting is one foraging strategy utilized by this species. It also suggests that bats use fluttering target information to classify their prey.     

Optic flow informs distance but not profitability for honeybees

How do flying insects monitor foraging efficiency? Honeybees (Apis mellifera) use optic flow information as an odometer to estimate distance travelled, but here we tested whether optic flow informs estimation of foraging costs also. Bees were trained to feeders in flight tunnels such that bees experienced the greatest optic flow en route to the feeder closest to the hive. Analyses of dance communication showed that, as expected, bees indicated the close feeder as being further, but they also indicated this feeder as the more profitable, and preferentially visited this feeder when given a choice. We show that honeybee estimates of foraging cost are not reliant on optic flow information. Rather, bees can assess distance and profitability independently and signal these aspects as separate elements of their dances. The optic flow signal is sensitive to the nature of the environment travelled by the bee, and is therefore not a good index of flight energetic costs, but it provides a good indication of distance travelled for purpose of navigation and communication, as long as the dancer and recruit travel similar routes. This study suggests an adaptive dual processing system in honeybees for communicating and navigating distance flown and for evaluating its energetic costs.     

How anthropogenic noise affects foraging

The influence of human activity on the biosphere is increasing. While direct damage (e.g. habitat destruction) is relatively well understood, many activities affect wildlife in less apparent ways. Here, we investigate how anthropogenic noise impairs foraging, which has direct consequences for animal survival and reproductive success. Noise can disturb foraging via several mechanisms that may operate simultaneously, and thus, their effects could not be disentangled hitherto. We developed a diagnostic framework that can be applied to identify the potential mechanisms of disturbance in any species capable of detecting the noise. We tested this framework using Daubenton's bats, which find prey by echolocation. We found that traffic noise reduced foraging efficiency in most bats. Unexpectedly, this effect was present even if the playback noise did not overlap in frequency with the prey echoes. Neither overlapping noise nor nonoverlapping noise influenced the search effort required for a successful prey capture. Hence, noise did not mask prey echoes or reduce the attention of bats. Instead, noise acted as an aversive stimulus that caused avoidance response, thereby reducing foraging efficiency. We conclude that conservation policies may seriously underestimate numbers of species affected and the multilevel effects on animal fitness, if the mechanisms of disturbance are not considered.     

Innate plasticity of a predatory behavior: nonlearned context dependence of avian flush-displays

If a foraging adaptation comprises a signal for sensory exploitationof prey, does the behavior and its use develop through learning,like many foraging behaviors or does it depend on nonlearnedstereotypical motor actions, like many signals for sensory exploitation?We asked whether the visually conspicuous motor pattern of bodypivoting with spread tail and wings used by the painted redstart(Myioborus pictus) to flush insect prey is a nonlearned phenotypictrait. The motion pattern and the increase in these displaysunder branches (context dependence based on physical propertiesof the habitat) help the wild birds in foraging because preythat rest on substrates is visually stimulated, flushed intothe air, and consequently chased in aerial pursuits. In unrewardedconditions in the aviary, both the foraging-experienced adultsand the foraging-naive hand-raised fledglings increased thefrequency of flush-displays at locations with substrates abovebirds, recreating the pattern of foraging observed in adultsin their natural habitats. The results imply that parent–offspringcultural transmission or learning during foraging is not requiredfor the development of both the display motion pattern and theadaptive context-dependent increase in display frequency. Sucha nonlearned context dependence based on physical propertiesof the habitat is remarkable considering that avian foragingcontext-dependent plasticity is often based on learning. Wehypothesize that this innate character of the signals may bea result of evolution to exploit universal properties of visuallytriggered escape behaviors of various insects that are predictablyflushed from their resting sites in the habitat.     

Flight performance, echolocation and foraging behaviour in noctule bats Nyctalus noctula

The noctule Nyctulus noctula (Schreber, 1774) is a relatively large (c. 25 g) insectivorous bat which catches insects on the wing (by aerial hawking). Emergence at a maternity roost was earliest relative to sunset when females were lactating, and bats may then have risked predation by flying at higher light levels during a period of high energy demand. Flight performance was quantified by using stereophotogrammetry. At feeding sites bats flew at 6.0 ± 2.1 m/s. This was faster than predicted minimum power speed (V _mp), and either between V _mp and maximum range speed (V _mr), or close to their predicted V _mr, depending on which aerodynamic model of flight power requirements was used. The echolocation behaviour of noctules is flexible. Long duration, low frequency calls (c. 20 kHz) with little frequency modulation were emitted while cruising, but at foraging sites the calls became more frequency-modulated. As the noctule is traditionally thought of as using low frequency echolocation, it was expected to receive weak echoes from small targets and therefore to specialize in eating large insect prey. Although the bats ate mainly beetles, large numbers of small dipterans were also eaten. The noctule is probably able to detect such small items because, when foraging, its calls become broadband and sweep from high frequencies. Higher harmonics are also present, and these may assist in the detection of small prey. In noctules, as in many bats, there appears to be a 1:1 link between wingbeat and call production during the search phase of foraging.     

Feeding rate and attack specialization: the roles of predator experience and energetic tradeoffs

Synopsis Individual mosquitofish, Gambusia affinis, can adopt a broad range of attack selectivities. In part, this variation can be explained by the past experiences of a fish. Individuals selected the more profitable Ceriodaphnia dubia (Cladocera) over less profitable cyclopoid copepods to a greater degree after being exposed to both prey types than did individuals experienced with only one of the prey types. Feeding rate (biomass ingested per unit time) declined with increased attack specialization on the profitable prey (Ceriodaphnia) when such prey were scarce, a result in agreement with assumptions of optimal diet theory. When profitable prey were abundant feeding rate was a bimodal function of the intensity of specialization on profitable prey; fish that specialized on cyclopoid copepods (the less profitable prey type) fed at higher rates than did generalists. This may be the result of antagonistic learning that precluded feeding efficiently on more than one type of prey at a time. The data are consistent with the hypothesis that rejection of unsuitable prey involves a time cost. The two preceeding aspects of foraging behavior, which are absent from most optimal diet models, could lead to failure in predicting the attack specialization of some predators, An additional aspect of the results was the generally weak relationship between feeding efficiency and specialization behavior. This suggests that feeding rate may not have been as tightly linked to the specialization behavior a predator adopts as is assumed by current foraging theory.     

Echolocation range and wingbeat period match in aerial-hawking bats

Aerial-hawking bats searching the sky for prey face the problem that flight and echolocation exert independent and possibly conflicting influences on call intervals. These bats can only exploit their full echolocation range unambiguously if they emit their next call when all echoes from the preceding call would have arrived. However, not every call interval is equally available. The need to reduce the high energetic costs of echolocation forces aerial-hawking bats to couple call emission to their wingbeat. We compared the wingbeat periods of 11 aerial-hawking bat species with the delays of the last-expected echoes. Acoustic flight-path tracking was employed to measure the source levels (SLs) of echolocation calls in the field. SLs were very high, extending the known range to 133 dB peak equivalent sound pressure level. We calculated the maximum detection distances for insects, larger flying objects and background targets. Wingbeat periods were derived from call intervals. Small and medium-sized bats in fact matched their maximum detection range for insects and larger flying targets to their wingbeat period. The tendency to skip calls correlated with the species' detection range for background targets. We argue that a species' call frequency is at such a pitch that the resulting detection range matches their wingbeat period.     

On-board telemetry of emitted sounds from free-flying bats: compensation for velocity and distance stabilizes echo frequency and amplitude

To understand complex sensory-motor behavior related to object perception by echolocating bats, precise measurements are needed for echoes that bats actually listen to during flight. Recordings of echolocation broadcasts were made from flying bats with a miniature light-weight microphone and radio transmitter (Telemike) set at the position of the bat's ears and carried during flights to a landing point on a wall. Telemike recordings confirm that flying horseshoe bats (Rhinolophus ferrumequinum nippon) adjust the frequency of their sonar broadcasts to compensate for echo Doppler shifts. Returning constant frequency echoes were maintained at the bat's reference frequency +/-83 Hz during flight, indicating that the bats compensated for frequency changes with an accuracy equivalent to that at rest. The flying bats simultaneously compensate for increases in echo amplitude as target range becomes shorter. Flying bats thus receive echoes with both stabilized frequencies and stabilized amplitudes. Although it is widely understood that Doppler-shift frequency compensation facilitates detection of fluttering insects, approaches to a landing do not involve fluttering objects. Combined frequency and amplitude compensation may instead be for optimization of successive frequency modulated echoes for target range estimation to control approach and landing.     

食虫蝙蝠与昆虫之间的相互作用和协同进化关系

食虫蝙蝠与昆虫之间是捕食和被捕食的关系,夜行性昆虫是食虫蝙蝠主要的食物来源。在漫长的协同进化中,蝙蝠施加的捕食压力导致夜行性昆虫一系列特征的进化,其中一部分昆虫进化出能听到蝙蝠的超声波信号并采取逃跑行为或者能通过其它方式躲避蝙蝠,同时昆虫的适应性特征同样影响着蝙蝠的回声定位和捕食策略。本文从蝙蝠捕食昆虫的种类、昆虫对蝙蝠捕食的反应和食虫性蝙蝠对昆虫防卫的适应对策等三个方面对食虫蝙蝠与昆虫之间的相互关系进行了概述。     

Do cattle egrets gain information from conspecifics when foraging?

Summary We examined whether individual cattle egrets (Bubulcus ibis) base their decisions of where to forage, and how long to stay in a patch, on the behavior of other flock members. Cattle egrets commonly forage in flocks associated with cattle and capture prey at higher rates when they do not share a cow with another egret. Foraging egrets provide cues of the location of prey and their success in capturing prey. Therefore, there is the possibility of information transfer between egrets in a flock. We predicted that egrets should only move to occupied patches when the resident was capturing enough prey that it is profitable for the invader to share the patch or take over the patch. However, egrets did not seem to decide where to forage based on neighbors' rates of energy intake, but rather on the presence or absence of conspecifics in a patch. We also predicted that an egret should remain in a patch until its rate of energy intake dropped to or below the average rate for other egrets within the flock. However, egrets that were foraging more efficiently than the average rate for the flock switched patches sooner than less efficient foragers. Egrets did not appear to increase foraging success by gaining information on patch quality from neighbors.     

Echolocation constraints of Daubenton's Bat foraging over water

1. Daubenton's Bats ( Myotis daubentonii ) foraging over a stream concentrated their activity over calm surfaces, avoiding an adjacent area with small ripples (< 3 cm high). Aerial insects were most abundant over the ripples, so insect distribution could not explain why the bats avoided this area.
2. The bats flew low over water and always ( N = 22) directed the head forwards, presumably emitting the echolocation beam parallel to the surface, thus minimizing clutter. At an angle of incidence of 30° there was significantly more clutter from the rippled water.
3. The ripples produced ultrasonic noises in the form of transient pulses at an average rate of 6·2 per second. In the present case, such pulses were common enough potentially to interfere with target detection by the bats. Transient noises and echo clutter from moving ripples may be the principal reason why bats generally avoid foraging low over turbulent water.
4. The target strength of a potential insect prey at the water surface and the source levels of the bats' searching signals were measured to use in estimating the echo level at the bat when it detects the prey. The echo level at detection (+ 38 dB sound pressure level) was about the same as the clutter level extrapolated to the detection distance. This suggests that Daubenton's Bat operates at very low signal-to-noise ratios when foraging for insects near the water surface.     

Habitat-specific sensory-exploitative signals in birds: propensity of dipteran prey to cause evolution of plumage variation in flush-pursuit insectivores

Sensory exploitation occurs when signals trigger behavioral reactions that diminish the receiver's fitness. Research in this area focuses on the match between the signal's form and the receiver's sensitivity, but the effect of habitat on interspecific sensory exploitation is rarely addressed. Myioborus redstarts use conspicuous wing and tail displays of contrasting black-and-white plumage patches to flush dipteran insects, which are then pursued and captured in flight. Previous studies have shown that by increasing the distance at which insects perform an escape response, conspicuous visual displays improve the birds' foraging performance. We tested the hypothesis that selection for a visual signal that maximizes prey escape distance under local habitat conditions can lead to the evolution of geographic variation in plumage pattern among Myioborus redstarts. Using models of foraging birds, we recorded the escape responses of Dipterous insects to a range of plumage patterns and background tones (from light to dark) to determine whether the plumage pattern that maximizes prey flushing is dependent upon that habitat (background) against which birds are viewed by their prey. Our results indicate that the effectiveness of a particular plumage pattern in flushing dipteran prey depends strongly on the background against which that plumage pattern is displayed, and darker habitat (background) conditions generally favor plumages with more extensive patches of white in the tail. However, the addition of white wing patches that imitate the plumage of the painted redstart (Myioborus pictus) generally increases insect escape responses but reduces the effect that tail pattern variation and background tone have on escape behavior. These experiments support the hypothesis that habitat-specific natural selection to enhance sensory exploitation of prey escape responses could produce geographic variation in plumage patterns of flush-pursuers.