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.     

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”.     

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.     

Keeping the blood flowing—plasminogen activator genes and feeding behavior in vampire bats

The blood feeding vampire bats emerged from New World leaf-nosed bats that fed on fruit and insects. Plasminogen activator, a serine protease that regulates blood coagulation, is known to be expressed in the saliva of Desmodus rotundus (common vampire bat) and is thought to be a key enzyme for the emergence of blood feeding in vampire bats. To better understand the evolution of this biological function, we studied the plasminogen activator (PA) genes from all vampire bat species in light of their feeding transition to bird and subsequently mammalian blood. We include the rare species Diphylla ecaudata and Diaemus youngi, where plasminogen activator had not previously been studied and demonstrate that PA gene duplication observed in Desmodus is not essential to the vampire phenotype, but relates to the emergence of predominant mammalian blood feeding in this species. Plasminogen activator has evolved through gene duplication, domain loss, and sequence evolution leading to change in fibrin-specificity and susceptibility to plasminogen activator inhibitor-1. Before undertaking this study, only the four plasminogen activator isoforms from Desmodus were known. The evolution of vampire bat plasminogen activators can now be linked phylogenetically to the transition in feeding behavior among vampire bat species from bird to mammalian blood. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Torpor and activity in a free-ranging tropical bat: implications for the distribution and conservation of mammals?

Bats are most diverse in the tropics, but there are no quantitative data on torpor use for energy conservation by any tropical bat in the wild. We examined the thermal biology, activity patterns and torpor use of two tree-roosting long-eared bats (Nyctophilus geoffroyi, 7.8?g) in tropical northern Australia in winter using temperature telemetry. Bats commenced activity about 20?min after sunset, ended activity about 2.5?h before sunrise and entered torpor everyday in the early morning even when minimum ambient temperatures (T _a) were as high as 23°C. On average, bats remained torpid for almost 5?h, mean minimum skin temperature (T _skin) measured was 22.8?±?0.1°C and daily T _skin minima were correlated with T _a. Our study shows that even in the tropics, torpor is frequently employed by bats, suggesting that worldwide most bat species are heterothermic and use torpor for energy conservation. We propose that the ability of employing torpor and the resulting highly plastic energy requirements may partially explain why these small insectivorous bats can inhabit almost the entire Australian continent despite vastly different climatic and likely trophic conditions. Reduced energy requirements also may permit survival in degraded or modified habitats, reduce the need for foraging and reduce exposure to predators. Thus, the ability to employ torpor may be one important reason for why most Australian bats and other heterothermic mammals have not gone extinct whereas many obligatory homeothermic mammals that cannot employ torpor and have high energy and foraging requirements have suffered high rates of extinctions.     

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.     

Ignoring the irrelevant: auditory tolerance of audible but innocuous sounds in the bat-detecting ears of moths

Noctuid moths listen for the echolocation calls of hunting bats and respond to these predator cues with evasive flight. The African bollworm moth, Helicoverpa armigera, feeds at flowers near intensely singing cicadas, Platypleura capensis, yet does not avoid them. We determined that the moth can hear the cicada by observing that both of its auditory receptors (A1 and A2 cells) respond to the cicada's song. The firing response of the A1 cell rapidly adapts to the song and develops spike periods in less than a second that are in excess of those reported to elicit avoidance flight to bats in earlier studies. The possibility also exists that for at least part of the day, sensory input in the form of olfaction or vision overrides the moth's auditory responses. While auditory tolerance appears to allow H. armigera to exploit a food resource in close proximity to acoustic interference, it may render their hearing defence ineffective and make them vulnerable to predation by bats during the evening when cicadas continue to sing. Our study describes the first field observation of an eared insect ignoring audible but innocuous sounds.     

Bechstein’s bats maintain individual social links despite a complete reorganisation of their colony structure

Several social mammals, including elephants and some primates, whales and bats, live in multilevel societies that form temporary subgroups. Despite these fission–fusion dynamics, group members often maintain long-term bonds. However, it is unclear whether such individual links and the resulting stable social subunits continue to exist after a complete reorganisation of a society, e.g. following a population crash. Here, we employed a weighted network analysis on 7,109 individual roosting records collected over 4 years in a wild Bechstein’s bat colony. We show that, in response to a strong population decline, the colony’s two stable social subunits fused into a non-modular social network. Nevertheless, in the first year after the crash, long-term bonds were still detectable, suggesting that the bats remembered previous individual relationships. Our findings are important for understanding the flexibility of animal societies in the face of dramatic changes and for the conservation of social mammals with declining populations.

     

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.     

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.     

Cryptic mammalian species: a new species of whiskered bat (Myotis alcathoe n. sp.) in Europe

The analysis of morphological, behavioural and genetic characters of whiskered bats revealed a new European bat species within the family Vespertilionidae. We describe the morphology, karyology, genetic similarity, ecology and distribution of Myotis alcathoe n. sp. It closely resembles Myotis mystacinus, Myotis brandtii and Myotis ikonnikovi in morphology, but all four species show clear genetic differences in two mitochondrial genes (ND1 and 12S rRNA). Myotis alcathoe n. sp. is the smallest species among the European whiskered bats and uses the highest-frequency echolocation calls of all the European Myotis species. It prefers to hunt in small valleys with deciduous trees and flowing water, which is an endangered habitat. Records from Greece and Hungary indicate a distribution range in south-eastern Europe.     

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     

Echolocation calls of Poey’s flower bat (<Emphasis Type="Italic">Phyllonycteris poeyi</Emphasis>) unlike those of other phyllostomids

Unlike any other foraging phyllostomid bat studied to date, Poey’s flower bats (Phyllonycteris poeyi-Phyllostomidae) emit relatively long (up to 7.2 ms), intense, single-harmonic echolocation calls. These calls are readily detectable at distances of at least 15 m. Furthermore, the echolocation calls contain only the first harmonic, which is usually filtered out in the vocal tract of phyllostomids. The foraging echolocation calls of P. poeyi are more like search-phase echolocation calls of sympatric aerial-feeding bats (Molossidae, Vespertilionidae, Mormoopidae). Intense, long, narrowband, single-harmonic echolocation calls focus acoustic energy maximizing range and favoring detection, which may be particularly important for cruising bats, like P. poeyi, when flying in the open. Flying in enclosed spaces, P. poeyi emit short, low-intensity, frequency-modulated, multiharmonic echolocation calls typical of other phyllostomids. This is the first report of a phyllostomid species emitting long, intense, single-harmonic echolocation calls with most energy in the first harmonic.     

Neural basis of singing in crickets: central pattern generation in abdominal ganglia

The neural mechanisms underlying cricket singing behavior have been the focus of several studies, but the central pattern generator (CPG) for singing has not been localized conclusively. To test if the abdominal ganglia contribute to the singing motor pattern and to analyze if parts of the singing CPG are located in these ganglia, we systematically truncated the abdominal nerve cord of fictively singing crickets while recording the singing motor pattern from a front-wing nerve. Severing the connectives anywhere between terminal ganglion and abdominal ganglion A3 did not preclude singing, although the motor pattern became more variable and failure-prone as more ganglia were disconnected. Singing terminated immediately and permanently after transecting the connectives between the metathoracic ganglion complex and the first unfused abdominal ganglion A3. The contribution of abdominal ganglia for singing pattern generation was confirmed by intracellular interneuron recordings and current injections. During fictive singing, an ascending interneuron with its soma and dendrite in A3 depolarized rhythmically. It spiked 10 ms before the wing-opener activity and hyperpolarized in phase with the wing-closer activity. Depolarizing current injection elicited rhythmic membrane potential oscillations and spike bursts that elicited additional syllables and reliably reset the ongoing chirp rhythm. Our results disclose that the abdominal ganglion A3 is directly involved in generating the singing motor pattern, whereas the more posterior ganglia seem to provide only stabilizing feedback to the CPG circuit. Localizing the singing CPG in the anterior abdominal neuromeres now allows analyzing its circuitry at the level of identified interneurons in subsequent studies.     

Hot bats: extreme thermal tolerance in a desert heat wave

Climate change is predicted to increase temperature extremes and thus thermal stress on organisms. Animals living in hot deserts are already exposed to high ambient temperatures (T _a) making them especially vulnerable to further warming. However, little is known about the effect of extreme heat events on small desert mammals, especially tree-roosting microbats that are not strongly protected from environmental temperature fluctuations. During a heat wave with record T _as at Sturt National Park, we quantified the thermal physiology and behaviour of a single free-ranging little broad-nosed (Scotorepens greyii, henceforth Scotorepens) and two inland freetail bats (Mormopterus species 3, henceforth Mormopterus) using temperature telemetry over 3 days. On 11 and 13 January, maximum T _a was ～45.0 °C, and all monitored bats were thermoconforming. On 12 January 2013, when T _a exceeded 48.0 °C, Scotorepens abandoned its poorly insulated roost during the daytime, whereas both Mormopterus remained in their better insulated roosts and were mostly thermoconforming. Maximum skin temperatures (T _skin) ranged from 44.0 to 44.3 °C in Scotorepens and from 40.0 to 45.8 °C in Mormopterus, and these are the highest T _skin values reported for any free-ranging bat. Our study provides the first evidence of extensive heat tolerance in free-ranging desert microbats. It shows that these bats can tolerate the most extreme T _skin range known for mammals (3.3 to 45.8 °C) and delay regulation of T _skin by thermoconforming over a wide temperature range and thus decrease the risks of dehydration and consequently death.     

Communally breeding bats use physiological and behavioural adjustments to optimise daily energy expenditure

Small endotherms must change roosting and thermoregulatory behaviour in response to changes in ambient conditions if they are to achieve positive energy balance. In social species, for example many bats, energy expenditure is influenced by environmental conditions, such as ambient temperature, and also by social thermoregulation. Direct measurements of daily fluctuations in metabolic rates in response to ambient and behavioural variables in the field have not been technologically feasible until recently. During different reproductive periods, we investigated the relationships between ambient temperature, group size and energy expenditure in wild maternity colonies of Bechstein’s bats (Myotis bechsteinii). Bats used behavioural and physiological adjustments to regulate energy expenditure. Whether bats maintained normothermia or used torpor, the number of bats in the roosts as well changed with reproductive status and ambient temperature. During pregnancy and lactation, bats remained mostly normothermic and daily group sizes were relatively large, presumably to participate in the energetic benefits of social thermoregulation. In contrast, smaller groups were formed on days when bats used torpor, which occurred mostly during the post-lactation period. Thus, we were able to demonstrate on wild animals under natural conditions the significance of behavioural and physiological flexibility for optimal thermoregulatory behaviour in small endotherms.     

Selective aggressiveness in European free-tailed bats (Tadarida teniotis): influence of familiarity,age and sex

Bats are highly social mammals that often form large groups and represent good models to test the role played by individual status in shaping social relationships. Social cohesion relies on the ability of group and individual recognition, which is mediated by a range of sensorial cues. In this study, we selected the European free-tailed bat Tadarida teniotis as a model species to test the effects of familiarity, sex and age on aggressiveness and mutual tolerance. We hypothesize that T. teniotis is able to recognize group members and exhibit selective aggressiveness, and thus we predict fewer aggressive events and more amicable encounters between colony mates than between strangers. As female bats are generally more sociable and perform prolonged parental care to juveniles even after weaning, we hypothesize that sex and age of bats have significant influences on aggressive behaviours and thus predict that females will perform more amicable behaviours than males and that adults of both sexes will be less aggressive towards juveniles. Our results confirm that T. teniotis is able to discriminate between familiar and stranger individuals, showing higher rates of aggressive behaviours towards the latter. Females are more prone to exhibit amicable behaviours, particularly during same-sex interactions, while males show higher level of aggressiveness. Juveniles are subjected to fewer aggressive behaviours by adults of both sexes. Familiarity appears crucial for T. teniotis in determining the degree of aggressiveness during social interactions but the rate of aggressive events is also influenced by intrinsic individual factors such as sex and age.     

The oldest African bat from the early Eocene of El Kohol (Algeria)

The Afro-Arabian Paleogene fossil record of Chiroptera is very poor. In North Africa and Arabia, this record is limited, thus far, to a few localities mainly in Tunisia (Chambi, late early Eocene), Egypt (Fayum, late Eocene to early Oligocene), and Sultanate of Oman (Taqah, early Oligocene). It consists primarily of isolated teeth or mandible fragments. Interestingly, these African fossil bats document two modern groups (Vespertilionoidea and Rhinolophoidea) from the early Eocene, while the bat fossil record of the same epoch of North America, Eurasia, and Australia principally includes members of the ??Eochiroptera.?? This paraphyletic group contains all primitive microbats excluding modern families. In Algeria, the region of Brezina, southeast of the Atlas Mountains, is famous for the early Eocene El Kohol Formation, which has yielded one of the earliest mammalian faunas of the African landmass. Recent fieldwork in the same area has led to the discovery of a new vertebrate locality, including isolated teeth of Chiroptera. These fossils represent the oldest occurrence of Chiroptera in Africa, thus extending back the record of the group to the middle early Eocene (Ypresian) on that continent. The material consists of an upper molar and two fragments of lower molars. The dental character association matches that of ??Eochiroptera.?? As such, although very fragmentary, the material testifies to the first occurrence of ??Eochiroptera?? in Algeria, and by extension in Africa. This discovery demonstrates that this basal group of Chiroptera had a worldwide distribution during the early Paleogene.     

Evasive response to ultrasound by the crepuscular butterfly<Emphasis Type="Italic"> Manataria maculata</Emphasis>

The crepuscular nymphalid butterfly Manataria maculata was studied in Monteverde cloud forest, Costa Rica, during the dry season reproductive diapause. M. maculata has ears in the form of Vogel's organs located near the base of the forewings. Its behaviour in response to bursts of ultrasonic pulses (26 kHz, 110 dB SPL at 1 m) was condition-dependent. At dusk and dawn the sound consistently elicited evasive responses, similar to those of moths, in flying individuals. In contrast day-roosting individuals always remained motionless although they were alert to other stimuli. The daily movements between day- and night-roosts coincided in time and light intensity with the activity of insectivorous bats. This is the first reported case of ultrasonic hearing connected to evasive flights in a true butterfly (Papilionoidea). It strongly supports the idea that echolocating bats were involved in the evolution of hearing in butterflies.     

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.