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.

Calibrated microphone array recordings reveal that a gleaning bat emits low-intensity echolocation calls even in open-space habitat.

Echolocating bats use ultrasound for orientation and prey capture in darkness. Ultrasound is strongly attenuated in air. Consequently, aerial-hawking bats generally emit very intense echolocation calls to maximize detection range. However, call levels vary more than tenfold (>20 dB) between species and are tightly linked to the foraging strategy. The brown long-eared bat (Plecotus auritus) is a primarily gleaning, low-amplitude species that may occasionally hawk airborne prey. We used state-of-the-art calibrated acoustic 3D-localization and automated call analysis to measure P. auritus' source levels. Plecotus auritus emits echolocation calls of low amplitude (92 dB rmsSPL re. 20 µPa at 10 cm) even while flying in open-space. While P. auritus thus probably benefits from delayed evasive manoeuvres of eared insects, we propose that low-amplitude echolocation did not evolve as an adaptive countermeasure, but is limited by morphological constraints.

Urbanisation generates multiple trait syndromes for terrestrial animal taxa worldwide.

Cities can host significant biological diversity. Yet, urbanisation leads to the loss of habitats, species, and functional groups. Understanding how multiple taxa respond to urbanisation globally is essential to promote and conserve biodiversity in cities. Using a dataset encompassing six terrestrial faunal taxa (amphibians, bats, bees, birds, carabid beetles and reptiles) across 379 cities on 6 continents, we show that urbanisation produces taxon-specific changes in trait composition, with traits related to reproductive strategy showing the strongest response. Our findings suggest that urbanisation results in four trait syndromes (mobile generalists, site specialists, central place foragers, and mobile specialists), with resources associated with reproduction and diet likely driving patterns in traits associated with mobility and body size. Functional diversity measures showed varied responses, leading to shifts in trait space likely driven by critical resource distribution and abundance, and taxon-specific trait syndromes. Maximising opportunities to support taxa with different urban trait syndromes should be pivotal in conservation and management programmes within and among cities. This will reduce the likelihood of biotic homogenisation and helps ensure that urban environments have the capacity to respond to future challenges. These actions are critical to reframe the role of cities in global biodiversity loss.

Evaluating the potential of urban areas for bat conservation with citizen science data.

Global change, including urbanisation, threatens many of the >1400 bat species. Nevertheless, certain areas within highly urbanised cities may be suitable to harbour bat populations. Thus, managing urban habitats could contribute to bat conservation. Here, we wanted to establish evidence-based recommendations on how to improve urban spaces for the protection of bats. In a team effort with >200 citizen scientists, we recorded bat vocalisations up to six times over the course of 2 years at each of 600 predefined sites in the Berlin metropolitan area. For each species we identified the preferred and non-preferred landscape features. Our results show that artificial light at night (ALAN) had a negative impact on all species. For soprano pipistrelles and mouse-eared bats ALAN had the largest effect sizes among all environmental predictors. Canopy cover and open water were especially important for bat species that forage along vegetation edges and for trawling bats, respectively. Occurrence probability of species foraging in open space decreased with increasing distance to water bodies. On a larger scale, impervious surfaces tended to have positive effects on some species that are specialised on foraging along edge structures. Our study constitutes an important contribution to the growing body of literature showing that despite the many negative impacts of urbanisation on wildlife, urban environments can harbour bat populations if certain conditions are met, such as access to vegetation and water bodies and low levels of ALAN. Our findings are of high relevance for urban planners and conservationists, as they allow inferences on how to manage urban spaces in a bat-friendly way. We recommend limiting ALAN to the minimum necessary and maintaining and creating uninterrupted vegetated corridors between areas with high levels of canopy cover and water bodies, in which ALAN should be entirely avoided.

Task-dependent vocal adjustments to optimize biosonar-based information acquisition.

Animals need to acquire adequate and sufficient information to guide movements, yet information acquisition and processing are costly. Animals thus face a trade-off between gathering too little and too much information and, accordingly, actively adapt sensory input through motor control. Echolocating animals provide a unique opportunity to study the dynamics of adaptive sensing in naturally behaving animals, as every change in the outgoing echolocation signal directly affects information acquisition and the perception of the dynamic acoustic scene. Here, we investigated the flexibility with which bats dynamically adapt information acquisition depending on a task. We recorded the echolocation signals of wild-caught Western barbastelle bats (Barbastella barbastellus) while they were flying through an opening, drinking on the wing, landing on a wall and capturing prey. We show that the echolocation signal sequences during target approach differed in a task-dependent manner; bats started the target approach earlier and increased the information update rate more when the task became increasingly difficult, and bats also adjusted the dynamics of call duration shortening and peak frequency shifts accordingly. These task-specific differences existed from the onset of object approach, implying that bats plan their sensory-motor programme for object approach exclusively based on information received from search call echoes. We provide insight into how echolocating animals deal with the constraints they face when sequentially sampling the world through sound by adjusting acoustic information flow from slow to extremely fast in a highly dynamic manner. Our results further highlight the paramount importance of high behavioural flexibility for acquiring information.

Insectivorous bats integrate social information about species identity, conspecific activity and prey abundance to estimate cost-benefit ratio of interactions.

Animals can use inadvertent social information to improve fitness-relevant decisions, for instance about where to forage or with whom to interact. Since bats emit high-amplitude species-specific echolocation calls when flying, they provide a constant flow of inadvertent social information to others who can decode that acoustic information. Of particular interest is the rate of feeding buzzes-characteristic call sequences preceding any prey capture-which correlates with insect abundance. Previous studies investigating eavesdropping in bats yielded very different and in part contradictory results likely because they commonly focused on single species only, differed substantially in playback buzz rate and did usually not account for (baseline) conspecific activity. Our goal was to overcome these limitations and systematically test which inadvertent social information bats integrate when eavesdropping on others and how this integration affects space use and both intra- and interspecific interactions, respectively. We used a community-wide approach and investigated the effects of a broad range of playback feeding buzz rates and conspecific activity on eavesdropping responses in 24 bat species combinations in the wild. For the first time, we reveal that finely graded and density-dependent eavesdropping responses are not limited to particular foraging styles or call types, but instead are ubiquitous among insectivorous bats. All bats integrated social information about calling species identity, prey abundance and conspecific activity to estimate the cost-benefit ratio of prospective interactions, yet in a species-specific manner. The effect of buzz rate was multifaceted, as bats responded differently to different buzz rates, and responses were additionally modulated by heterospecific recognition. Conspecific activity, in contrast, had a negative effect on the eavesdropping responses of all bats. These findings can explain the inconsistent results of previous studies and advance our understanding of the complex nature of conspecific and heterospecific interactions within bat communities. A comprehensive understanding of how bats incorporate social information into their decision-making will help researchers to explain species distribution patterns and eventually to unravel mechanisms of species coexistence.

'No cost of echolocation for flying bats' revisited.

Echolocation is energetically costly for resting bats, but previous experiments suggested echolocation to come at no costs for flying bats. Yet, previous studies did not investigate the relationship between echolocation, flight speed, aerial manoeuvres and metabolism. We re-evaluated the 'no-cost' hypothesis, by quantifying the echolocation pulse rate, the number of aerial manoeuvres (landings and U-turns), and the costs of transport in the 5-g insectivorous bat Rhogeessa io (Vespertilionidae). On average, bats (n = 15) travelled at 1.76 ± 0.36 m s⁻¹ and performed 11.2 ± 6.1 U-turns and 2.8 ± 2.9 ground landings when flying in an octagonal flight cage. Bats made more U-turns with decreasing wing loading (body weight divided by wing area). At flight, bats emitted 19.7 ± 2.7 echolocation pulses s⁻¹ (range 15.3-25.8 pulses s⁻¹), and metabolic rate averaged 2.84 ± 0.95 ml CO2 min⁻¹, which was more than 16 times higher than at rest. Bats did not echolocate while not engaged in flight. Costs of transport were not related to the rate of echolocation pulse emission or the number of U-turns, but increased with increasing number of landings; probably as a consequence of slower travel speed when staying briefly on ground. Metabolic power of flight was lower than predicted for R. io under the assumption that energetic costs of echolocation call production is additive to the aerodynamic costs of flight. Results of our experiment are consistent with the notion that echolocation does not add large energetic costs to the aerodynamic power requirements of flight in bats.

Ecological correlates of cortisol levels in two bat species with contrasting feeding habits.

The immediate release of adrenal glucocorticoids can be crucial for an animal's survival when facing a stressor, but constantly elevated or exceptionally high glucocorticoid levels are usually detrimental for health. Although baseline and maximal secretion of glucocorticoids are regulated within narrow ranges within species, plasma glucocorticoid levels vary largely across vertebrates. We asked what ecological factors affect baseline plasma cortisol levels (CortI) and maximum levels (CortMax) following a physiological challenge through administration of adrenocorticotropic hormone (ACTH). Specifically, we studied whether seasonal fluctuations in food abundance correlate with the capacity of cortisol increases in two phyllostomid bat species with contrasting feeding habits: the sanguinivorous vampire bat (Desmodus rotundus) and the frugivorous short-tailed fruit bat (Carollia perspicillata). Both species coexist in habitats with various levels of seasonality (dry and rainforest). On a seasonal basis, resource abundance is more stable for vampire than for fruit bats, but previous studies suggested that daily foraging success may vary more for vampire than for fruit bats. CortI and CortMax varied seasonally in C. perspicillata from dry and rainforests, with the exception of CortMax in rainforest bats. Although we expected food availability to be stable year-round for vampire bats, we found CortI and CortMax of vampires to be higher during the rainy season than during the dry season. Also, we found CortMax to be higher in vampires from the rainforest than in those from the dry forest. CortMax of vampires were among the highest measured for a free-ranging mammal; a pattern that could be related to the species' vulnerability to starvation. We conclude that food availability modulates cortisol levels in free-ranging species that face seasonally fluctuating resources; in species, however, that benefit from food which is constantly abundant, other factors than food may become more important in modulating cortisol levels.

Rain increases the energy cost of bat flight.

Similar to insects, birds and pterosaurs, bats have evolved powered flight. But in contrast to other flying taxa, only bats are furry. Here, we asked whether flight is impaired when bat pelage and wing membranes get wet. We studied the metabolism of short flights in Carollia sowelli, a bat that is exposed to heavy and frequent rainfall in neotropical rainforests. We expected bats to encounter higher thermoregulatory costs, or to suffer from lowered aerodynamic properties when pelage and wing membranes catch moisture. Therefore, we predicted that wet bats face higher flight costs than dry ones. We quantified the flight metabolism in three treatments: dry bats, wet bats and no rain, wet bats and rain. Dry bats showed metabolic rates predicted by allometry. However, flight metabolism increased twofold when bats were wet, or when they were additionally exposed to rain. We conclude that bats may not avoid rain only because of sensory constraints imposed by raindrops on echolocation, but also because of energetic constraints.

Trapped in the darkness of the night: thermal and energetic constraints of daylight flight in bats.

Bats are one of the most successful mammalian groups, even though their foraging activities are restricted to the hours of twilight and night-time. Some studies suggested that bats became nocturnal because of overheating when flying in daylight. This is because--in contrast to feathered wings of birds--dark and naked wing membranes of bats efficiently absorb short-wave solar radiation. We hypothesized that bats face elevated flight costs during daylight flights, since we expected them to alter wing-beat kinematics to reduce heat load by solar radiation. To test this assumption, we measured metabolic rate and body temperature during short flights in the tropical short-tailed fruit bat Carollia perspicillata at night and during the day. Core body temperature of flying bats differed by no more than 2°C between night and daytime flights, whereas mass-specific CO(2) production rates were higher by 15 per cent during daytime. We conclude that increased flight costs only render diurnal bat flights profitable when the relative energy gain during daytime is high and risk of predation is low. Ancestral bats possibly have evolved dark-skinned wing membranes to reduce nocturnal predation, but a low degree of reflectance of wing membranes made them also prone to overheating and elevated energy costs during daylight flights. In consequence, bats may have become trapped in the darkness of the night once dark-skinned wing membranes had evolved.