Release from bats: genetic distance and sensoribehavioural regression in the Pacific field cricket, Teleogryllus oceanicus

The auditory thresholds of the AN2 interneuron and the behavioural thresholds of the anti-bat flight-steering responses that this cell evokes are less sensitive in female Pacific field crickets that live where bats have never existed (Moorea) compared with individuals subjected to intense levels of bat predation (Australia). In contrast, the sensitivity of the auditory interneuron, ON1 which participates in the processing of both social signals and bat calls, and the thresholds for flight orientation to a model of the calling song of male crickets show few differences between the two populations. Genetic analyses confirm that the two populations are significantly distinct, and we conclude that the absence of bats has caused partial regression in the nervous control of a defensive behaviour in this insect. This study represents the first examination of natural evolutionary regression in the neural basis of a behaviour along a selection gradient within a single species.     

Tympanal mechanics and neural responses in the ears of a noctuid moth

Ears evolved in many groups of moths to detect the echolocation calls of predatory bats. Although the neurophysiology of bat detection has been intensively studied in moths for decades, the relationship between sound-induced movement of the noctuid tympanic membrane and action potentials in the auditory sensory cells (A1 and A2) has received little attention. Using laser Doppler vibrometry, we measured the velocity and displacement of the tympanum in response to pure tone pulses for moths that were intact or prepared for neural recording. When recording from the auditory nerve, the displacement of the tympanum at the neural threshold remained constant across frequencies, whereas velocity varied with frequency. This suggests that the key biophysical parameter for triggering action potentials in the sensory cells of noctuid moths is tympanum displacement, not velocity. The validity of studies on the neurophysiology of moth hearing rests on the assumption that the dissection and recording procedures do not affect the biomechanics of the ear. There were no consistent differences in tympanal velocity or displacement when moths were intact or prepared for neural recordings for sound levels close to neural threshold, indicating that this and other neurophysiological studies provide good estimates of what intact moths hear at threshold.     

Phonotaxis during walking and flight: are differences in selectivity due to predation pressure?

Female selectivity was tested in Tettigonia viridissima during two different phonotaxis situations; compensated walking and tethered flight. For two of the three temporal parameters that are important for call recognition in T. viridissima, selectivity was similar in the two situations. Selectivity for the third parameter (minimum interval duration between the double pulses) was much higher during walking than during flight: walking females responded only to stimuli with intervals of 28 ms or longer, while call models with intervals of 18 ms were attractive during flight. One interneuron (TN-1) is probably involved in filtering the minimum interval duration. As this neuron is also the most likely candidate for transmitting bat calls during flight, it is suggested that the selectivity differences between walking and flying might be due to the need for detecting predator signals during flight, when TN-1 would be occupied listening for bats. With TN-1 unavailable for song processing during flight, temporal selectivity for the minimum interval duration should be reduced, as was found here.     

Sound strategy: acoustic aposematism in the bat–tiger moth arms race

The night sky is the venue for an ancient arms race. Insectivorous bats with their ultrasonic sonar exert an enormous selective pressure on nocturnal insects. In response insects have evolved the ability to hear bat cries, to evade their hunting maneuvers, and some, the tiger moths (Arctiidae), to utter an ultrasonic reply. We here determine what it is that tiger moths say to bats. We chose four species of arctiid moths, Cycnia tenera, Euchaetes egle, Utetheisa ornatrix, and Apantesis nais, that naturally differ in their levels of unpalatability and their ability to produce sound. Moths were tethered and offered to free-flying naïve big brown bats, Eptesicus fuscus. The ability of the bats to capture each species was compared to their ability to capture noctuid, geometrid, and wax moth controls over a learning period of 7 days. We repeated the experiment using the single arctiid species E. egle that through diet manipulation and simple surgery could be rendered palatable or unpalatable and sound producing or mute. We again compared the capture rates of these categories of E. egle to control moths. Using both novel learning approaches we have found that the bats only respond to the sounds of arctiids when they are paired with defensive chemistry. The sounds are in essence a warning to the bats that the moth is unpalatable—an aposematic signal.Electronic Supplementary Material  Supplementary material is available for this article at     

Ultrasonic courtship song in the Asian corn borer moth, Ostrinia furnacalis

Although sex pheromone communication in the genus Ostrinia (Lepidoptera: Crambidae) has been studied intensively, acoustic communication in this genus has not been explored. In this study, we report that male-produced ultrasound serves as a courtship song in the Asian corn borer moth, O. furnacalis. Upon landing close to a pheromone-releasing female, a male showed a series of courtship behaviors involving emission of ultrasound. The sounds were produced when the wings were vibrated quickly in an upright position. The male song was composed of chirps, i.e., groups of pulses (duration of a chirp = 58.9 ms, 8.8 pulses/chirp), with a broadband frequency of 25–100 kHz. In flight tunnel experiments, deaf and hearing females showed a significant difference in the incidence of three behavioral responses to courting males, i.e., immediate acceptance, acceptance after walking, and rejection. Deaf females showed more ‘rejection’ and less ‘acceptance after walking’ than hearing females, indicating that the detection of male-produced ultrasound plays an important role in the acceptance of a male. The findings are discussed in the context of exploitation of receiver bias and mate choice.     

Frequent summer nuptial flights of ants provide a primary food source for bats

In many ant species, nuptial flight tends to be short in time and assumed to be synchronous across a large area. Here, we report that, in the upper Jordan Valley, northern Israel, massive nuptial flights of Carpenter ants (Camponotus sp.) occur frequently throughout the summer, and their alates form up to 90% of the diet of the greater mouse-tailed bat (Rhinopoma microphyllum) during this period. This fat and protein-rich diet enables female bats to lactate during summer, and the large amount of fat that both sexes accumulate may serve as an energy source for their following winter hibernation and posthibernation mating in early spring (March–April). We suggest that the annual movement of these bats to the Mediterranean region of Israel may have evolved in order to enable them to exploit the extremely nutritious forms of ant alates when the bats’ energetic demands are highest.     

Behavioural correlates of urbanisation in the Cape ground squirrel Xerus inauris

Urbanisation critically threatens biodiversity because of habitat destruction and novel selection pressures. Some animals can respond to these challenges by modifying their behaviour, particularly anti-predator behaviour, allowing them to persist in heavily transformed urban areas. We investigated whether the anti-predator behaviour of the Cape ground squirrel Xerus inauris differed in three localities that differed in their level of urbanisation. According to the habituation hypothesis, we predicted that ground squirrels in urban areas would: (a) be less vigilant and forage more; (b) trade-off flight/vigilance in favour of foraging; and (c) have shorter flight initiation distances (FID) when approached by a human observer. Observations were made in winter and summer at each locality. As expected, ground squirrels in urbanised areas were less vigilant and had shorter FIDs but did not trade-off between foraging and vigilance. In contrast, a population in a non-urbanised locality showed greater levels of vigilance, FID and traded-off vigilance and foraging. A population in a peri-urban locality showed mixed responses. Our results indicate that Cape ground squirrels reduce their anti-predator behaviour in urban areas and demonstrate a flexible behavioural response to urbanisation.     

Hot-blooded singers: endothermy facilitates crepuscular signaling in African platypleurine cicadas (Hemiptera: Cicadidae:<Emphasis Type="Italic"> Platypleura</Emphasis> spp.)

The cicada genus Platypleura has a wide distribution across Africa and southern Asia. We describe endothermic thermoregulation in four South African species that show crepuscular signaling behavior. This is the first evidence of thermoregulation in platypleurine cicadas. Field measurements of body temperature ( T _b) show that these animals regulate T _b through endogenous heat production. Maximum T _b measured was 22.1°C above ambient temperature during calling activity at dusk. The mean T _b during dusk activity did not differ from the mean T _b during diurnal activity. A unique behavior for cicadas, a temperature-dependent telescoping pulsation of the abdomen, was observed in the laboratory during endogenous warm-up. This behavior is part of a unique method of heat generation in endothermic cicadas. Males generally call from trunks and branches within the canopy and appear to use endothermy even when the sun is available to elevate T _b. Endothermy may provide the cicadas with the advantage of decreasing predation and acoustic competition by permitting calling from perches that most complement their cryptic coloration patterns and that ectotherms cannot use due to thermal constraints. In addition, endothermy may permit calling activity during crepuscular hours when atmospheric conditions are optimal for acoustic communication and predation risks are minimal.     

Verhalten und Neurobiologie von stimmbegabten Insekten

Crickets, tettigoniids (bush crickets or long-horned grasshoppers) and acridids (short-horned grasshoppers) are well-suited animals to study acoustically mediated behavior and to search for the underlying sensory, nervous, and effector mechanisms. Several behavioral tactics are described which improve reproductive success, serve to avoid predators such as bats, or have been developed for defence against parasitic insects. Phonotactic orientation of female crickets toward the calling male was chosen, since for this behavior the underlying sensory and nervous mechanisms have been intensively studied. Song recognition was found to be based on one critical parameter of the song, thesyllable period, and the females show abandpass behavior for which a correlate exists inlocal brain neurons. Sound orientation is based on apressure gradient mechanism in each ear, and it needs abinaural intensity comparison within the central nervous system. With intracellular recordings from auditory interneurons during phonotactic orientation and their manipulation, a cellular correlate could be found which obeys the rule “turn to the side most strongly stimulated”.     

Coherent array of branched filamentary scales along the wing margin of a small moth

In butterflies and moths, the wing margins are fringed with specialized scales that are typically longer than common scales. In the hindwings of some small moths, the posterior margins are fringed with particularly long filamentary scales. Despite the small size of these moth wings, these scales are much longer than those of large moths and butterflies. In the current study, photography of the tethered flight of a small moth, Phthorimaea operculella, revealed a wide array composed of a large number of long filamentary scales. This array did not become disheveled in flight, maintaining a coherent sheet-like structure during wingbeat. Examination of the morphology of individual scales revealed that each filamentary scale consists of a proximal stalk and distal branches. Moreover, not only long scales but also shorter scales of various lengths were found to coexist in each small section of the wing margin. Scale branches were ubiquitously and densely distributed within the scale array to form a mesh-like architecture similar to a nonwoven fabric. We propose that possible mechanical interactions among branched filamentary scales, mediated by these branches, may contribute to maintaining a coherent sheet-like structure of the scale array during wingbeat.     

Free-flight phonotaxis in a parasitoid fly: behavioural thresholds, relative attraction and susceptibility to noise

 The phonotactic capacity of tachinid flies to acoustically detect and localize a sound source simulating their cricket host was investigated in a large flight room. Acoustic measurements were performed to estimate the actual stimulus delivered to the flies, revealing highly heterogeneous sound fields. When presented with a simulated cricket song in red or infrared light conditions, the flies readily flew to the sound source and landed on it. Behavioural phonotactic thresholds were established as a function of carrier frequency and were found to coincide well with the frequency of the host's natural song (4.5–5.2 kHz). Experiments revealed that the same range of frequencies is preferentially attractive to the free-flying flies, and that the reliability of signal detection in the presence of noise is best at behaviourally relevant frequencies. Received: 23 February 2000 / Accepted in revised form: 6 June 2000     

Vision complements echolocation in an aerial-hawking bat

The northern bat Eptesicus nilssonii normally hunts flying insects in the air using frequency-modulated echolocation calls. It is also known to detect and catch visually conspicuous prey (white moths) hovering low among grass stalks. To overcome the problem with acoustic clutter from the grass, which interferes with target echo detection, the bats make use of visual cues in addition to those of echolocation. We therefore investigated the minimum size of prey that the bats could distinguish by using vision, by presenting the bats with different sized dead and spread moths. We found that vision increased the chance of detection only when the moths had a wingspan of at least 5 cm. Smaller targets were detected using echolocation alone. The mean detection range was 3.5 m, suggesting that the bats need a visual acuity of 49 of arc to detect the prey. This is consistent with results of optomotor response tests and counts of retinal ganglion cells in closely related species. Our results suggest that the visual acuity of Eptesicus bats may not be adequate for prey detection under normal conditions, but that the bats can use vision when the prey is unusually large and conspicuous. The northern bats display a flexibility in prey detection techniques not previously recognised among aerial-hawking bats and they are able to use their full visual capacity in the field.     

Learn it now,sing it later? Field and laboratory studies on song repertoire acquisition and song use in nightingales

In many bird species, song changes with age. The mechanisms that account for such changes are only partially understood. Common nightingales Luscinia megarhynchos change the size and composition of their repertoire between their first and second breeding season. To inquire into mechanisms involved in such changes, we compared the singing of 1-year-old and older free-living nightingales. Older males have more song types in common than have 1-year olds. Certain song types frequently sung by older birds did not (or only rarely) occur in the repertoire of yearlings (‘mature’ song types). We conducted learning experiments with hand-reared nightingales to address reasons for the lack of mature song types. The acquisition success of mature songs was as good as that of control songs (commonly sung by both age groups). However, the analysis of song type use revealed that all yearlings sang common song types more often than mature types. This indicates that the absence of certain song types in the repertoires of free-living yearlings cannot be accounted for by learning and/or motor constraints during song learning. Moreover, our results suggest that in communication networks, animals may restrict the actual use of their signal repertoire to a certain subset depending on the context.     

Effect of field margins on moths depends on species mobility: Field-based evidence for landscape-scale conservation

Agri-environment schemes (AES) are widely used policy instruments intended to combat widespread biodiversity declines across agricultural landscapes. Here, using a light trapping and mark-release-recapture study at a field-scale on nine common and widespread larger moth species, we investigate the effect of wide field margins (a popular current scheme option) and the presence of hedgerow trees (a potential scheme option in England) on moth abundance. Of these, we show that wide field margins positively affected abundances, although species did not all respond in the same way. We demonstrate that this variation can be attributed to species-specific mobility characteristics. Those species for which the effect of wide margins was strongest covered shorter distances, and were more frequently recaptured at their site of first capture. This demonstrates that the standard, field-scale uptake of AES may be effective only for less mobile species. We discuss that a landscape-scale approach, in contrast, could deliver significant biodiversity gains, as our results indicate that such an approach (perhaps delivered through targeting farmers to join AES) would be effective for the majority of wider countryside species, irrespective of their mobility level.     

Codling moth males do not discriminate between pheromone and a pheromone/antagonist blend during upwind flight

Discrimination between conspecific and heterospecific signals is a key element in the evolution of pheromone-mediated communication in insects. Pheromone antagonists prevent heterospecific attraction. They are typically pheromone synergists in other species and enable specific communication in closely related species, using partly the same chemicals. In codling moth, Cydia pomonella, as in other moths, upwind flights to a pheromone/antagonist blend were slower and more convoluted than to pheromone. However, this deteriorated flight behaviour did not account for the strong decrease in male attraction. The pheromone/antagonist blend blocked instead the onset of upwind flight. This was corroborated by placing a separate source of pheromone close by, which restored male attraction. Males flying upwind did not discriminate between pheromone and the adjacent pheromone/antagonist blend, and landed on either source. This indicates differences in the neural regulation for initiating and maintaining a behavioural response to pheromone.     

Acoustic mirror effect increases prey detection distance in trawling bats

Many different and phylogenetically distant species of bats forage for insects above water bodies and take insects from and close to the surface; the so-called trawling behaviour. Detection of surface-based prey by echolocation is facilitated by acoustically smooth backgrounds such as water surfaces that reflect sound impinging at an acute angle away from the bat and thereby render a prey object acoustically conspicuous. Previous measurements had shown that the echo amplitude of a target on a smooth surface is higher than that of the same target in mid-air, due to an acoustic mirror effect. In behavioural experiments with three pond bats (Myotis dasycneme), we tested the hypothesis that the maximum distances at which bats can detect prey are larger for prey on smooth surfaces than for the same prey in an airborne situation. We determined the moment of prey detection from a change in echolocation behaviour and measured the detection distance in 3D space from IR-video recordings using stereo-photogrammetry. The bats showed the predicted increase in detection distance for prey on smooth surfaces. The acoustic mirror effect therefore increases search efficiency and contributes to the acoustic advantages encountered by echolocating bats when foraging at low heights above smooth water surfaces. These acoustic advantages may have favoured the repeated evolution of trawling behaviour.     

Acoustic orientation via sequential comparison in an ultrasonic moth

Orientation of female lesser wax moths (Achroia grisella) to male calling song was tested on a locomotion-compensator device that withheld all inter-aural acoustic differences from the insect. Under these circumstances, females remained longer in the vicinity of the sound source if they experienced a variable sound level that increased when approaching the source rather than a level that remained constant at all times. Analyses of orientation paths revealed that greater retention near the source was achieved by enhanced turning when the perceived sound level remained unchanged or decreased but retaining the previous heading when the level increased. These findings suggest that acoustic orientation can be supplemented by mechanisms based on sequential, as opposed to instantaneous, comparison of auditory input. Such mechanisms may be valuable when binaural hearing is impaired or asymmetric or in environments where acoustic differences at the two ears are unreliable indications of direction to the sound source.     

Fat and fed: frequent use of summer torpor in a subtropical bat

A widely held view is that torpor is avoided by mammals whenever possible because of potential costs associated with reduced body temperatures and slowed metabolic processes. We examined this hypothesis by quantifying use of torpor in relation to body condition of free-ranging northern long-eared bats (Nyctophilus bifax, approximately 10 g), a species known to hibernate, from a subtropical region during the austral summer when insects were abundant. Temperature-telemetry revealed that bats used torpor on 85% of observation days and on 38% of all nights. Torpor bouts ranged from 0.7 to 21.2 h, but the relationship between duration of torpor bouts and ambient temperature was not significant. However, skin temperature of torpid bats was positively correlated with ambient temperature. Against predictions, individuals with a high body condition index (i.e., good fat/energy reserves) expressed longer and deeper torpor bouts and also employed torpor more often during the activity phase at night than those with low body condition index. We provide the first evidence that use of torpor in a free-ranging subtropical mammal is positively related with high body condition index. This suggests that employment of torpor is maximised and foraging minimised not because of food shortages or low energy stores but likely to avoid predation when bats are not required to feed.     

High bat (Chiroptera) diversity in the Early Eocene of India

The geographic origin of bats is still unknown, and fossils of earliest bats are rare and poorly diversified, with, maybe, the exception of Europe. The earliest bats are recorded from the Early Eocene of North America, Europe, North Africa and Australia where they seem to appear suddenly and simultaneously. Until now, the oldest record in Asia was from the Middle Eocene. In this paper, we report the discovery of the oldest bat fauna of Asia dating from the Early Eocene of the Cambay Formation at Vastan Lignite Mine in Western India. The fossil taxa are described on the basis of well-preserved fragments of dentaries and lower teeth. The fauna is highly diversified and is represented by seven species belonging to seven genera and at least four families. Two genera and five species are new. Three species exhibit very primitive dental characters, whereas four others indicate more advanced states. Unexpectedly, this fauna presents strong affinities with the European faunas from the French Paris Basin and the German Messel locality. This could result from the limited fossil record of bats in Asia, but could also suggest new palaeobiogeographic scenarios involving the relative position of India during the Early Eocene.     

The evolutionary origin of auditory receptors in Tettigonioidea: the complex tibial organ of Schizodactylidae

Audition in insects is of polyphyletic origin. Tympanal ears derived from proprioceptive or vibratory receptor organs, but many questions of the evolution of insect auditory systems are still open. Despite the rather typical bauplan of the insect body, e.g., with a fixed number of segments, tympanal ears evolved at very different places, but only ensiferans have ears at the foreleg tibia, located in the tibial organ. The homology and monophyly of ensiferan ears is controversial, and no precursor organ was unambiguously identified for auditory receptors. The latter can only be identified by comparative study of recent atympanate taxa. These atympanate taxa are poorly investigated. In this paper, we report the neuroanatomy of the tibial organ of Comicus calcaris (Irish 1986), an atympanate Schizodactylid (splay-footed cricket). This representative of a Gondwana relict group has a tripartite sensory organ, homologous to tettigoniid ears. A comparison with morphology-based cladistic phylogeny indicates that the tripartite neuronal organization present in the majority of Tettigonioidea presumably preceded evolution of a hearing sense in the Tettigonioidea. Furthermore, the absence of a tripartite organ in Grylloidea argues against a monophyletic origin and homology of the cricket and katydid ears. The tracheal attachment of sensory neurons typical for ears of Tettigonioidea is present in C. calcaris and may have facilitated cooption for auditory function. The functional auditory organ was presumably formed in evolution by successive non-neural modifications of trachea and tympana. This first investigation of the neuroanatomy of Schizodactylidae suggests a non-auditory chordotonal organ as the precursor for auditory receptors of related tympanate taxa and adds evidence for the phylogenetic position of the group.