Stealth echolocation in aerial hawking bats reflects a substrate gleaning ancestry.

Predator-prey co-evolution can escalate into an evolutionary arms race.1 Examples of insect countermeasures to bat echolocation are well-known,2 but presumptive direct counter strategies in bats to insect anti-bat tactics are rare. The emission of very low-intensity calls by the hawking Barbastella barbastellus to circumvent high-frequency moth hearing is the most convincing countermeasure known.2,3 However, we demonstrate that stealth echolocation did not evolve through a high-intensity aerial hawking ancestor becoming quiet as previously hypothesized2,3,4 but from a gleaning ancestor transitioning into an obligate aerial hawker. Our ancestral state reconstructions show that the Plecotini ancestor likely gleaned prey using low-intensity calls typical of gleaning bats and that this ability-and associated traits-was subsequently lost in the barbastelle lineage. Barbastelles did not, however, revert to the oral, high-intensity call emission that other hawking bats use but retained the low-intensity nasal emission of closely related gleaning plecotines despite an extremely limited echolocation range. We further show that barbastelles continue to emit low-intensity calls even under adverse noise conditions and do not broaden the echolocation beam during the terminal buzz, unlike other vespertilionids attacking airborne prey.5,6 Together, our results suggest that barbastelles' echolocation is subject to morphological constraints prohibiting higher call amplitudes and beam broadening in the terminal buzz. We suggest that an abundance of eared prey allowed the co-opting and maintenance of low-intensity, nasal echolocation in today's obligate hawking barbastelle and that this unique foraging behavior7 persists because barbastelles remain a rare, acoustically inconspicuous predator to eared moths. VIDEO ABSTRACT.

A synthesis of deimatic behaviour.

Deimatic behaviours, also referred to as startle behaviours, are used against predators and rivals. Although many are spectacular, their proximate and ultimate causes remain unclear. In this review we aim to synthesise what is known about deimatic behaviour and identify knowledge gaps. We propose a working hypothesis for deimatic behaviour, and discuss the available evidence for the evolution, ontogeny, causation, and survival value of deimatic behaviour using Tinbergen's Four Questions as a framework. Our overarching aim is to direct future research by suggesting ways to address the most pressing questions in this field.

The influence of bat ecology on viral diversity and reservoir status.

Repeated emergence of zoonotic viruses from bat reservoirs into human populations demands predictive approaches to preemptively identify virus-carrying bat species. Here, we use machine learning to examine drivers of viral diversity in bats, determine whether those drivers depend on viral genome type, and predict undetected viral carriers. Our results indicate that bat species with longer life spans, broad geographic distributions in the eastern hemisphere, and large group sizes carry more viruses overall. Life span was a stronger predictor of deoxyribonucleic acid viral diversity, while group size and family were more important for predicting ribonucleic acid viruses, potentially reflecting broad differences in infection duration. Importantly, our models predict 54 bat species as likely carriers of zoonotic viruses, despite not currently being considered reservoirs. Mapping these predictions as a proportion of local bat diversity, we identify global regions where efforts to reduce disease spillover into humans by identifying viral carriers may be most productive.

Sonar strobe groups and buzzes are produced before powered flight is achieved in the juvenile big brown bat, Eptesicus fuscus.

Laryngeally echolocating bats produce a rapid succession of echolocation calls just before landing. These landing buzzes exhibit an increase in call rate and a decrease in call peak frequency and duration relative to pre-buzz calls, and resemble the terminal buzz phase calls of an aerial hawking bat's echolocation attack sequence. Sonar strobe groups (SSGs) are clustered sequences of non-buzz calls whose pulse intervals (PIs) are fairly regular and shorter than the PIs both before and after the cluster, but longer than the PIs of buzz calls. Like buzzes, SSGs are thought to indicate increased auditory attention. We recorded the echolocation calls emitted by juvenile big brown bats (Eptesicus fuscus) over postnatal development from birth to 32 days old, when full flight has normally been achieved, and tested the following hypotheses: (i) buzz production precedes the onset of controlled, powered flight; (ii) the emission of SSGs precedes buzzes and coincides with the onset of fluttering behaviour; and (iii) the onset of flight is attained first by young bats with adult-like wing loadings. We found that E. fuscus pups emitted landing buzzes before they achieved powered flight and produced SSGs several days before emitting landing buzzes. Both observations indicate that the onset of adult-like echolocation behaviour occurs prior to adult-like flight behaviour. Pups that achieved flight first were typically those that also first achieved low, adult-like wing loadings. Our results demonstrate that echolocation and flight develop in parallel but may be temporally offset, such that the sensory system precedes the locomotory system during postnatal ontogeny.

Molecular diet analysis finds an insectivorous desert bat community dominated by resource sharing despite diverse echolocation and foraging strategies.

Interspecific differences in traits can alter the relative niche use of species within the same environment. Bats provide an excellent model to study niche use because they use a wide variety of behavioral, acoustic, and morphological traits that may lead to multi-species, functional groups. Predatory bats have been classified by their foraging location (edge, clutter, open space), ability to use aerial hawking or substrate gleaning and echolocation call design and flexibility, all of which may dictate their prey use. For example, high frequency, broadband calls do not travel far but offer high object resolution while high intensity, low frequency calls travel further but provide lower resolution. Because these behaviors can be flexible, four behavioral categories have been proposed: (a) gleaning, (b) behaviorally flexible (gleaning and hawking), (c) clutter-tolerant hawking, and (d) open space hawking. Many recent studies of diet in bats use molecular tools to identify prey but mainly focus on one or two species in isolation; few studies provide evidence for substantial differences in prey use despite the many behavioral, acoustic, and morphological differences. Here, we analyze the diet of 17 sympatric species in the Chihuahuan desert and test the hypothesis that peak echolocation frequency and behavioral categories are linked to differences in diet. We find no significant correlation between dietary richness and echolocation peak frequency though it spanned close to 100 kHz across species. Our data, however, suggest that bats which use both gleaning and hawking strategies have the broadest diets and are most differentiated from clutter-tolerant aerial hawking species.

Phylogeny matters: revisiting 'a comparison of bats and rodents as reservoirs of zoonotic viruses'.

Diseases emerging from wildlife have been the source of many major human outbreaks. Predicting key sources of these outbreaks requires an understanding of the factors that explain pathogen diversity in reservoir species. Comparative methods are powerful tools for understanding variation in pathogen diversity and rely on correcting for phylogenetic relatedness among reservoir species. We reanalysed a previously published dataset, examining the relative effects of species' traits on patterns of viral diversity in bats and rodents. We expanded on prior work by using more highly resolved phylogenies for bats and rodents and incorporating a phylogenetically controlled principal components analysis. For rodents, sympatry and torpor use were important predictors of viral richness and, as previously reported, phylogeny had minimal impact in models. For bats, in contrast to prior work, we find that phylogeny does have an effect in models. Patterns of viral diversity in bats were related to geographical distribution (i.e. latitude and range size) and life history (i.e. lifespan, body size and birthing frequency). However, the effects of these predictors were marginal relative to citation count, emphasizing that the ability to accurately assess reservoir status largely depends on sampling effort and highlighting the need for additional data in future comparative studies.

A method for rapid testing of social learning in vampire bats.

Designing experiments on social learning using an untested behaviour or species requires baseline knowledge of how the animals will perform. We conducted a pilot study of a procedure for rapidly testing social learning in the highly social common vampire bat (Desmodus rotundus) using a simple maze. To create demonstrators, we allowed captive bats to learn to exit a three-dimensional maze, which reunited them with their colony as a reward. We then filmed naive bats in the same maze, comparing their ability to exit the maze before, during and after the addition of a trained demonstrator. The presence of a demonstrator increased the exit rates of naive bats, presumably by attracting the attention of the naive bats to the maze exit. Four of the five naive bats that exited in the presence of a demonstrator retained the ability to exit without the demonstrator. No naive bat exited during trials without a potential demonstrator present. This experimental procedure appears to be a promising approach for efficient tests of social learning in vampire bats because maze difficulty can be manipulated to adjust learning rates and each trial requires only 15 min.

Younger vampire bats (Desmodus rotundus) are more likely than adults to explore novel objects.

The effects of age on neophobia and exploration are best described in birds and primates, and broader comparisons require reports from other taxa. Here we present data showing age-dependent exploration in a long-lived social species, the common vampire bat (Desmodus rotundus). A previous study found that vampire bats regurgitated food to partners trapped in a cage. Interestingly, while only a few adult bats visited the trapped bat, in every trial all or most of the eight young males in the colony would visit the trapped bat without feeding it. To test whether this behavioral difference resulted from age class differences in exploration, we compared responses of the bats to a trapped conspecific versus an inanimate novel object. Some adults and young showed interest in trapped conspecifics, but only the young males explored the novel objects. Additional novel object tests in a second captive colony showed that higher rates of novel object exploration were shown by young of both sexes. Our results corroborate past findings from other mammals and birds that age predicts exploration. If age-dependent exploration is indeed adaptive, then the role of age as a predictor of exploration tendency should depend on species-specific life history traits. Finally, because younger vampire bats also appear to have higher exposure to pathogens such as rabies virus, there may be implications for pathogen transmission if younger and more exploratory vampire bats are more likely to feed on novel hosts.

Bats without borders: Predators learn novel prey cues from other predatory species.

Learning from others allows individuals to adapt rapidly to environmental change. Although conspecifics tend to be reliable models, heterospecifics with similar resource requirements may be suitable surrogates when conspecifics are few or unfamiliar with recent changes in resource availability. We tested whether Trachops cirrhosus, a gleaning bat that localizes prey using their mating calls, can learn about novel prey from conspecifics and the sympatric bat Lophostoma silvicolum. Specifically, we compared the rate for naïve T. cirrhosus to learn an unfamiliar tone from either a trained conspecific or heterospecific alone through trial and error or through social facilitation. T. cirrhosus learned this novel cue from L. silvicolum as quickly as from conspecifics. This is the first demonstration of social learning of a novel acoustic cue in bats and suggests that heterospecific learning may occur in nature. We propose that auditory-based social learning may help bats learn about unfamiliar prey and facilitate their adaptive radiation.

Auditory opportunity and visual constraint enabled the evolution of echolocation in bats.

Substantial evidence now supports the hypothesis that the common ancestor of bats was nocturnal and capable of both powered flight and laryngeal echolocation. This scenario entails a parallel sensory and biomechanical transition from a nonvolant, vision-reliant mammal to one capable of sonar and flight. Here we consider anatomical constraints and opportunities that led to a sonar rather than vision-based solution. We show that bats' common ancestor had eyes too small to allow for successful aerial hawking of flying insects at night, but an auditory brain design sufficient to afford echolocation. Further, we find that among extant predatory bats (all of which use laryngeal echolocation), those with putatively less sophisticated biosonar have relatively larger eyes than do more sophisticated echolocators. We contend that signs of ancient trade-offs between vision and echolocation persist today, and that non-echolocating, phytophagous pteropodid bats may retain some of the necessary foundations for biosonar.

Fungus Causing White-Nose Syndrome in Bats Accumulates Genetic Variability in North America with No Sign of Recombination.

Emerging fungal diseases of wildlife are on the rise worldwide, and the white-nose syndrome (WNS) epidemic in North American bats is a catastrophic example. The causal agent of WNS is a single clone of the fungus Pseudogymnoascus destructans. Early evolutionary change in this clonal population has major implications for disease ecology and conservation. Accumulation of variation in the fungus through mutation, and shuffling of variation through recombination, could affect the virulence and transmissibility of the fungus and the durability of what appears to be resistance arising in some bat populations. Our genome-wide analysis shows that the clonal population of P. destructans has expanded in size from a single genotype, has begun to accumulate variation through mutation, and presents no evidence as yet of genetic exchange among individuals. IMPORTANCE Since its discovery in 2006, the emerging infectious disease known as white-nose syndrome has killed millions of bats in North America, making it one of the most devastating wildlife epidemics in recorded history. We demonstrate that there has been as yet only spontaneous mutation across the North American population of P. destructans, and we find no indication of recombination. Thus, selective forces, which might otherwise impact pathogenic virulence, have so far had essentially no genetic variation on which to act. Our study confirmed the time of origin for the first and, thus far, only introduction of P. destructans to North America. This system provides an unprecedented opportunity to follow the evolution of a host-pathogen interaction unfolding in real time.

Oilbirds produce echolocation signals beyond their best hearing range and adjust signal design to natural light conditions.

Oilbirds are active at night, foraging for fruits using keen olfaction and extremely light-sensitive eyes, and echolocate as they leave and return to their cavernous roosts. We recorded the echolocation behaviour of wild oilbirds using a multi-microphone array as they entered and exited their roosts under different natural light conditions. During echolocation, the birds produced click bursts (CBs) lasting less than 10 ms and consisting of a variable number (2-8) of clicks at 2-3 ms intervals. The CBs have a bandwidth of 7-23 kHz at -6 dB from signal peak frequency. We report on two unique characteristics of this avian echolocation system. First, oilbirds reduce both the energy and number of clicks in their CBs under conditions of clear, moonlit skies, compared with dark, moonless nights. Second, we document a frequency mismatch between the reported best frequency of oilbird hearing (approx. 2 kHz) and the bandwidth of their echolocation CBs. This unusual signal-to-sensory system mismatch probably reflects avian constraints on high-frequency hearing but may still allow oilbirds fine-scale, close-range detail resolution at the upper extreme (approx. 10 kHz) of their presumed hearing range. Alternatively, oilbirds, by an as-yet unknown mechanism, are able to hear frequencies higher than currently appreciated.

Body Size Predicts Echolocation Call Peak Frequency Better than Gape Height in Vespertilionid Bats.

In most vocalizing vertebrates, lighter animals tend to produce acoustic signals of higher frequency than heavier animals. Two hypotheses propose to explain this negative relationship in vespertilionid bats: (i) mass-signal frequency allometry and (ii) emitter-limited (maximum gape) signal directionality. The first hypothesis, that lighter bats with smaller larynges are constrained to calls with higher frequencies, is supported at the species level. The second hypothesis proposes that in open space, small bats use higher frequencies to achieve narrow sonar beams, as beam directionality increases with both emitter size (maximum gape) and signal frequency. This hypothesis is supported within a comparative context but remains untested beyond a few species. We analyzed gape, body mass, and echolocation data under a phylogenetic comparative framework to test these hypotheses, and considered forearm length as both a proxy for wing design and an alternative measure of bat size. Controlling for mass, we found no support for the directionality hypothesis. Body mass and relative forearm length were negatively related to open space echolocation call peak frequency, reflecting species-specific size differences, but also the influence of wing design and preferred foraging habitat on size-independent species-specific differences in echolocation call design.

Evolutionary escalation: the bat-moth arms race.

Echolocation in bats and high-frequency hearing in their insect prey make bats and insects an ideal system for studying the sensory ecology and neuroethology of predator-prey interactions. Here, we review the evolutionary history of bats and eared insects, focusing on the insect order Lepidoptera, and consider the evidence for antipredator adaptations and predator counter-adaptations. Ears evolved in a remarkable number of body locations across insects, with the original selection pressure for ears differing between groups. Although cause and effect are difficult to determine, correlations between hearing and life history strategies in moths provide evidence for how these two variables influence each other. We consider life history variables such as size, sex, circadian and seasonal activity patterns, geographic range and the composition of sympatric bat communities. We also review hypotheses on the neural basis for anti-predator behaviours (such as evasive flight and sound production) in moths. It is assumed that these prey adaptations would select for counter-adaptations in predatory bats. We suggest two levels of support for classifying bat traits as counter-adaptations: traits that allow bats to eat more eared prey than expected based on their availability in the environment provide a low level of support for counter-adaptations, whereas traits that have no other plausible explanation for their origination and maintenance than capturing defended prey constitute a high level of support. Specific predator counter-adaptations include calling at frequencies outside the sensitivity range of most eared prey, changing the pattern and frequency of echolocation calls during prey pursuit, and quiet, or 'stealth', echolocation.

Sonar sound groups and increased terminal buzz duration reflect task complexity in hunting bats.

More difficult tasks are generally regarded as such because they demand greater attention. Echolocators provide rare insight into this relationship because biosonar signals can be monitored. Here we show that bats produce longer terminal buzzes and more sonar sound groups during their approach to prey under presumably more difficult conditions. Specifically, we found Daubenton's bats, Myotis daubentonii, produced longer buzzes when aerial-hawking versus water-trawling prey, but that bats taking revolving air- and water-borne prey produced more sonar sound groups than did the bats when taking stationary prey. Buzz duration and sonar sound groups have been suggested to be independent means by which bats attend to would-be targets and other objects of interest. We suggest that for attacking bats both should be considered as indicators of task difficulty and that the buzz is, essentially, an extended sonar sound group.

Echolocation in the bat, Rhinolophus capensis: the influence of clutter, conspecifics and prey on call design and intensity.

Echolocating bats are exposed not only to the echoes of their own calls, but often the signals of conspecifics and other bats. For species emitting short, frequency modulated signals e.g. vespertilionoids, adjustments in both the frequency and time domain have been observed in such situations. However, bats using long duration, constant frequency calls may confront special challenges, since these bats should be less able to avoid temporal and frequency overlap. Here we investigated echolocation call design in the highduty cycle bat, Rhinolophus capensis, as bats flew with either a conspecific or heterospecific in a large outdoor flight-room. We compared these recordings to those made of bats flying alone in the same flight-room, and in a smaller flight room, alone, and hunting tethered moths. We found no differences in duty cycle or peak frequency of the calls of R. capensis across conditions. However, in the presence of a conspecific or the vespertilionoid, Miniopterus natalensis, R. capensis produced longer frequency-modulated downward sweeps at the terminus of their calls with lower minimum frequencies than when flying alone. In the presence of the larger high-duty cycle bat, R. clivosus, R. capensis produced shorter calls than when flying alone or with a conspecific. These changes are similar to those of vespertilionoids when flying from open to more cluttered environments. They are not similar to those differences observed in vespertilionoids when flying with other bats. Also unlike vespertilinoids, R. capensis used calls 15 dB less intense in conspecific pairs than when alone.

Range-dependent flexibility in the acoustic field of view of echolocating porpoises (Phocoena phocoena).

Toothed whales use sonar to detect, locate, and track prey. They adjust emitted sound intensity, auditory sensitivity and click rate to target range, and terminate prey pursuits with high-repetition-rate, low-intensity buzzes. However, their narrow acoustic field of view (FOV) is considered stable throughout target approach, which could facilitate prey escape at close-range. Here, we show that, like some bats, harbour porpoises can broaden their biosonar beam during the terminal phase of attack but, unlike bats, maintain the ability to change beamwidth within this phase. Based on video, MRI, and acoustic-tag recordings, we propose this flexibility is modulated by the melon and implemented to accommodate dynamic spatial relationships with prey and acoustic complexity of surroundings. Despite independent evolution and different means of sound generation and transmission, whales and bats adaptively change their FOV, suggesting that beamwidth flexibility has been an important driver in the evolution of echolocation for prey tracking.

Clutter and conspecifics: a comparison of their influence on echolocation and flight behaviour in Daubenton's bat, Myotis daubentonii.

We compared the influence of conspecifics and clutter on echolocation and flight speed in the bat Myotis daubentonii. In a large room, actual pairs of bats exhibited greater disparity in peak frequency (PF), minimum frequency (F MIN) and call period compared to virtual pairs of bats, each flying alone. Greater inter-individual disparity in PF and F MIN may reduce acoustic interference and/or increase signal self-recognition in the presence of conspecifics. Bats flying alone in a smaller flight room, to simulate a more cluttered habitat as compared to the large flight room, produced calls of shorter duration and call period, lower intensity, and flew at lower speeds. In cluttered space, shorter call duration should reduce masking, while shorter call period equals more updates to the bat's auditory scene. Lower intensity likely reflects reduced range detection requirements, reduced speed the demands of flying in clutter. Our results show that some changes (e.g. PF separation) are associated with conspecifics, others with closed habitat (e.g. reduced call intensity). However, we demonstrate that call duration, period, and flight speed appear similarly influenced by conspecifics and clutter. We suggest that some changes reduce conspecific interference and/or improve self-recognition, while others demonstrate that bats experience each other like clutter.

Sensory biology: echolocation from click to call, mouth to wing.

Echolocators use echoes of sounds they produce, clicks or calls, to detect objects. Usually, these signals originate from the head. New work reveals that three species of bats use their wings to generate echolocation signals.