Sounds emitted by plants under stress are airborne and informative.

Stressed plants show altered phenotypes, including changes in color, smell, and shape. Yet, airborne sounds emitted by stressed plants have not been investigated before. Here we show that stressed plants emit airborne sounds that can be recorded from a distance and classified. We recorded ultrasonic sounds emitted by tomato and tobacco plants inside an acoustic chamber, and in a greenhouse, while monitoring the plant's physiological parameters. We developed machine learning models that succeeded in identifying the condition of the plants, including dehydration level and injury, based solely on the emitted sounds. These informative sounds may also be detectable by other organisms. This work opens avenues for understanding plants and their interactions with the environment and may have significant impact on agriculture.

Relation of connectome topology to brain volume across 103 mammalian species.

The brain connectome is an embedded network of anatomically interconnected brain regions, and the study of its topological organization in mammals has become of paramount importance due to its role in scaffolding brain function and behavior. Unlike many other observable networks, brain connections incur material and energetic cost, and their length and density are volumetrically constrained by the skull. Thus, an open question is how differences in brain volume impact connectome topology. We address this issue using the MaMI database, a diverse set of mammalian connectomes reconstructed from 201 animals, covering 103 species and 12 taxonomy orders, whose brain size varies over more than 4 orders of magnitude. Our analyses focus on relationships between volume and modular organization. After having identified modules through a multiresolution approach, we observed how connectivity features relate to the modular structure and how these relations vary across brain volume. We found that as the brain volume increases, modules become more spatially compact and dense, comprising more costly connections. Furthermore, we investigated how spatial embedding shapes network communication, finding that as brain volume increases, nodes' distance progressively impacts communication efficiency. We identified modes of variation in network communication policies, as smaller and bigger brains show higher efficiency in routing- and diffusion-based signaling, respectively. Finally, bridging network modularity and communication, we found that in larger brains, modular structure imposes stronger constraints on network signaling. Altogether, our results show that brain volume is systematically related to mammalian connectome topology and that spatial embedding imposes tighter restrictions on larger brains.

Echolocating bats rely on an innate speed-of-sound reference.

Animals must encode fundamental physical relationships in their brains. A heron plunging its head underwater to skewer a fish must correct for light refraction, an archerfish shooting down an insect must "consider" gravity, and an echolocating bat that is attacking prey must account for the speed of sound in order to assess its distance. Do animals learn these relations or are they encoded innately and can they adjust them as adults are all open questions. We addressed this question by shifting the speed of sound and assessing the sensory behavior of a bat species that naturally experiences different speeds of sound. We found that both newborn pups and adults are unable to adjust to this shift, suggesting that the speed of sound is innately encoded in the bat brain. Moreover, our results suggest that bats encode the world in terms of time and do not translate time into distance. Our results shed light on the evolution of innate and flexible sensory perception.

Pregnancy-related sensory deficits might impair foraging in echolocating bats.

BACKGROUND: Reproduction entails substantial demands throughout its distinct stages. The mammalian gestation period imposes various energetic costs and movement deficits, but its effects on the sensory system are poorly understood. Bats rely heavily on active sensing, using echolocation to forage in complete darkness, or when lighting is uncertain. We examined the effects of pregnancy on bat echolocation. RESULTS: We show that pregnant Kuhl's pipistrelles (Pipistrellus kuhlii) altered their echolocation and flight behavior. Specifically, pregnant bats emitted longer echolocation signals at an ~ 15% lower rate, while flying more slowly and at a lower altitude compared to post-lactating females. A sensorimotor foraging model suggests that these changes could lead to an ~ 15% reduction in hunting performance during pregnancy. CONCLUSIONS: Sensory deficits related to pregnancy could impair foraging in echolocating bats. Our study demonstrates an additional cost of reproduction of possible relevance to other sensory modalities and organisms.

Fruit bats adjust their decision-making process according to environmental dynamics.

One of the main functions of behavioral plasticity lies in the ability to contend with dynamic environments. Indeed, while numerous studies have shown that animals adapt their behavior to the environment, how they adapt their latent learning and decision strategies to changes in the environment is less understood. Here, we used a controlled experiment to examine the bats' ability to adjust their decision strategy according to the environmental dynamics. Twenty-five Egyptian fruit bats were placed individually in either a stable or a volatile environment for four consecutive nights. In the stable environment, two feeders offered food, each with a different reward probability (0.2 vs. 0.8) that remained fixed over two nights and were then switched, while in the volatile environment, the positions of the more and the less rewarding feeders were changed every hour. We then fit two alternative commonly used models namely, reinforcement learning and win-stay-lose-shift strategies to the bats' behavior. We found that while the bats adapted their decision-making strategy to the environmental dynamics, they seemed to be limited in their responses based on natural priors. Namely, when the environment had changed slowly, at a rate that is natural for these bats, they seemed to rely on reinforcement learning and their performance was nearly optimal, but when the experimental environment changed much faster than in the natural environment, the bats stopped learning and switched to a random decision-making strategy. Together, these findings exemplify both the bats' decision-making plasticity as well as its natural limitations.

A bio-mimetic miniature drone for real-time audio based short-range tracking.

One of the most difficult sensorimotor behaviors exhibited by flying animals is the ability to track another flying animal based on its sound emissions. From insects to mammals, animals display this ability in order to localize and track conspecifics, mate or prey. The pursuing individual must overcome multiple non-trivial challenges including the detection of the sounds emitted by the target, matching the input received by its (mostly) two sensors, localizing the direction of the sound target in real time and then pursuing it. All this has to be done rapidly as the target is constantly moving. In this project, we set to mimic this ability using a physical bio-mimetic autonomous drone. We equipped a miniature commercial drone with our in-house 2D sound localization electronic circuit which uses two microphones (mimicking biological ears) to localize sound signals in real-time and steer the drone in the horizontal plane accordingly. We focus on bat signals because bats are known to eavesdrop on conspecifics and follow them, but our approach could be generalized to other biological signals and other man-made signals. Using two different experiments, we show that our fully autonomous aviator can track the position of a moving sound emitting target and pursue it in real-time. Building an actual robotic-agent, forced us to deal with real-life difficulties which also challenge animals. We thus discuss the similarities and differences between our and the biological approach.

Echolocating bats detect but misperceive a multidimensional incongruent acoustic stimulus.

Coherent perception relies on integrating multiple dimensions of a sensory modality, for example, color and shape in vision. We reveal how different acoustic dimensions, specifically echo intensity and sonar aperture (or width), are important for correct perception by echolocating bats. We flew bats down a corridor blocked by objects with different intensity-aperture combinations. To our surprise, bats crashed straight into large (aperture) walls with weak echo intensity as if they did not exist. The echolocation behavior of the bats indicated that they did detect the wall, suggesting that crashing was not a result of limited sensory sensitivity, but of a perceptual deficit. We systematically manipulated intensity and aperture by changing the materials and width of different reflectors, and we conclude that a coherent echo-based percept is created only when these two acoustic dimensions have certain relations which are typical for objects in nature (e.g., large and intense or small and weak reflectors). Nevertheless, we show that these preferred relations are not innate. We show that young pups are not constrained to these relations and that new intensity-aperture associations can also be learned by adult bats.

Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome.

Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that the presence of an environmental reservoir increases the risk of host declines and threat of extinction, the influence of reservoir dynamics on transmission and population impacts remains poorly described. Here we show that the extent of the environmental reservoir explains broad patterns of host infection and the severity of disease impacts of a virulent pathogen. We examined reservoir and host infection dynamics and the resulting impacts of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome, in 39 species of bats at 101 sites across the globe. Lower levels of pathogen in the environment consistently corresponded to delayed infection of hosts, fewer and less severe infections, and reduced population impacts. In contrast, an extensive and persistent environmental reservoir led to early and widespread infections and severe population declines. These results suggest that continental differences in the persistence or decay of P. destructans in the environment altered infection patterns in bats and influenced whether host populations were stable or experienced severe declines from this disease. Quantifying the impact of the environmental reservoir on disease dynamics can provide specific targets for reducing pathogen levels in the environment to prevent or control future epidemics.

Echolocating bats rapidly adjust their mouth gape to control spatial acquisition when scanning a target.

BACKGROUND: As well known to any photographer, controlling the "field of view" offers an extremely powerful mechanism by which to adjust target acquisition. Only a few natural sensory systems can actively control their field of view (e.g., dolphins, whales, and bats). Bats are known for their active sensing abilities and modify their echolocation signals by actively controlling their spectral and temporal characteristics. Less is known about bats' ability to actively modify their bio-sonar field of view. RESULTS: We show that Pipistrellus kuhlii bats rapidly narrow their sensory field of view (i.e., their bio-sonar beam) when scanning a target. On-target vertical sonar beams were twofold narrower than off-target beams. Continuous measurements of the mouth gape of free-flying bats revealed that they control their bio-sonar beam by a ~3.6 mm widening of their mouth gape: namely, bats open their mouth to narrow the beam and vice versa. CONCLUSIONS: Bats actively and rapidly control their echolocation vertical beam width by modifying their mouth gape. We hypothesize that narrowing their vertical beam narrows the zone of ensonification when estimating the elevation of a target. In other words, bats open their mouth to improve sensory localization.

TrackUSF, a novel tool for automated ultrasonic vocalization analysis, reveals modified calls in a rat model of autism.

BACKGROUND: Various mammalian species emit ultrasonic vocalizations (USVs), which reflect their emotional state and mediate social interactions. USVs are usually analyzed by manual or semi-automated methodologies that categorize discrete USVs according to their structure in the frequency-time domains. This laborious analysis hinders the effective use of USVs as a readout for high-throughput analysis of behavioral changes in animals. RESULTS: Here we present a novel automated open-source tool that utilizes a different approach towards USV analysis, termed TrackUSF. To validate TrackUSF, we analyzed calls from different animal species, namely mice, rats, and bats, recorded in various settings and compared the results with a manual analysis by a trained observer. We found that TrackUSF detected the majority of USVs, with less than 1% of false-positive detections. We then employed TrackUSF to analyze social vocalizations in Shank3-deficient rats, a rat model of autism, and revealed that these vocalizations exhibit a spectrum of deviations from appetitive calls towards aversive calls. CONCLUSIONS: TrackUSF is a simple and easy-to-use system that may be used for a high-throughput comparison of ultrasonic vocalizations between groups of animals of any kind in any setting, with no prior assumptions.

Inner Hemispheric and Interhemispheric Connectivity Balance in the Human Brain.

The connectome of the brain has a great impact on the function of the brain as the structure of the connectome affects the speed and efficiency of information transfer. As a highly energy-consuming organ, an efficient network structure is essential. A previous study has shown consistent overall brain connectivity across a large variety of species. This connectivity conservation was explained by a balance between interhemispheric and intrahemispheric connections; that is, spices with highly connected hemispheres appear to have weaker interhemisphere connections. This study examines this connectivity trade-off in the human brain using diffusion-based tractography and network analysis in the Human Connectome Project (970 subjects, 527 female). We explore the biological origins of this phenomenon, heritability, and the effect on cognitive measures.The proportion of commissural fibers in the brain had a negative correlation to hemispheric efficiency, pointing to a trade-off between inner hemispheric and interhemispheric connectivity. Network hubs including anterior and middle cingulate cortex, superior frontal areas, medial occipital areas, the parahippocampal gyrus, post- and precentral gyri, and the precuneus had the strongest contribution to this phenomenon. Other results show a high heritability as well as a strong connection to crystalized intelligence. This work presents cohort-based network analysis research, spanning a large variety of samples and exploring the overall architecture of the human connectome. Our results show a connectivity conservation phenomenon at the base of the overall brain network architecture. This network structure may explain much of the functional, behavioral, and cognitive variability among different brains.SIGNIFICANCE STATEMENT The network structure of the brain is at the basis of every brain function as it dictates the characteristics of information transfer. Understanding the patterns and mechanisms that guide the connectome structure is crucial to understanding the brain itself. Here we unravel the mechanism at the base of the connectivity conservation phenomenon by exploring the interaction between hemispheric and commissural connectivity in a large-scale cohort-based connectivity study. We describe the trade-off between the two components and examine the origins of the trade-off and observe the effect on cognitive abilities and behavior.

Adaptive learning and recall of motor-sensory sequences in adult echolocating bats.

BACKGROUND: Learning to adapt to changes in the environment is highly beneficial. This is especially true for echolocating bats that forage in diverse environments, moving between open spaces to highly complex ones. Bats are known for their ability to rapidly adjust their sensing according to auditory information gathered from the environment within milliseconds but can they also benefit from longer adaptive processes? In this study, we examined adult bats' ability to slowly adapt their sensing strategy to a new type of environment they have never experienced for such long durations, and to then maintain this learned echolocation strategy over time. RESULTS: We show that over a period of weeks, Pipistrellus kuhlii bats gradually adapt their pre-takeoff echolocation sequence when moved to a constantly cluttered environment. After adopting this improved strategy, the bats retained an ability to instantaneously use it when placed back in a similarly cluttered environment, even after spending many months in a significantly less cluttered environment. CONCLUSIONS: We demonstrate long-term adaptive flexibility in sensory acquisition in adult animals. Our study also gives further insight into the importance of sensory planning in the initiation of a precise sensorimotor behavior such as approaching for landing.

Fruit bats adjust their foraging strategies to urban environments to diversify their diet.

BACKGROUND: Urbanization is one of the most influential processes on our globe, putting a great number of species under threat. Some species learn to cope with urbanization, and a few even benefit from it, but we are only starting to understand how they do so. In this study, we GPS tracked Egyptian fruit bats from urban and rural populations to compare their movement and foraging in urban and rural environments. Because fruit trees are distributed differently in these two environments, with a higher diversity in urban environments, we hypothesized that foraging strategies will differ too. RESULTS: When foraging in urban environments, bats were much more exploratory than when foraging in rural environments, visiting more sites per hour and switching foraging sites more often on consecutive nights. By doing so, bats foraging in settlements diversified their diet in comparison to rural bats, as was also evident from their choice to often switch fruit species. Interestingly, the location of the roost did not dictate the foraging grounds, and we found that many bats choose to roost in the countryside but nightly commute to and forage in urban environments. CONCLUSIONS: Bats are unique among small mammals in their ability to move far rapidly. Our study is an excellent example of how animals adjust to environmental changes, and it shows how such mobile mammals might exploit the new urban fragmented environment that is taking over our landscape.

Urban bat pups take after their mothers and are bolder and faster learners than rural pups.

BACKGROUND: Urbanization is rapidly changing our planet and animals that live in urban environments must quickly adjust their behavior. One of the most prevalent behavioral characteristics of urban dwelling animals is an increased level of risk-taking. Here, we aimed to reveal how urban fruitbats become risk-takers, and how they differ behaviorally from rural bats, studying both genetic and non-genetic factors that might play a role in the process. We assessed the personality of newborn pups from both rural and urban colonies before they acquired experience outdoors, examining risk-taking, exploration, and learning rates. RESULTS: Urban pups exhibited significantly higher risk-taking levels, they were faster learners, but less exploratory than their rural counterparts. A cross-fostering experiment revealed that pups were more similar to their adoptive mothers, thus suggesting a non-genetic mechanism and pointing towards a maternal effect. We moreover found that lactating urban mothers have higher cortisol levels in their milk, which could potentially explain the transmission of some personality traits from mother to pup. CONCLUSIONS: Young bats seem to acquire environment suitable traits via post-birth non-genetic maternal effects. We offer a potential mechanism for how urban pups can acquire urban-suitable behavioral traits through hormonal transfer from their mothers.

Hearing, echolocation, and beam steering from day 0 in tongue-clicking bats.

Little is known about the ontogeny of lingual echolocation. We examined the echolocation development of Rousettus aegyptiacus, the Egyptian fruit bat, which uses rapid tongue movements to produce hyper-short clicks and steer the beam's direction. We recorded from day 0 to day 35 postbirth and assessed hearing and beam-steering abilities. On day 0, R. aegyptiacus pups emit isolation calls and hyper-short clicks in response to acoustic stimuli, demonstrating hearing. Auditory brainstem response recordings show that pups are sensitive to pure tones of the main hearing range of adult Rousettus and to brief clicks. Newborn pups produced clicks in the adult paired pattern and were able to use their tongues to steer the sonar beam. As they aged, pups produced click pairs faster, converging with adult intervals by age of first flights (7-8 weeks). In contrast with laryngeal bats, Rousettus echolocation frequency and duration are stable through to day 35, but shift by the time pups begin to fly, possibly owing to tongue-diet maturation effects. Furthermore, frequency and duration shift in the opposite direction of mammalian laryngeal vocalizations. Rousettus lingual echolocation thus appears to be a highly functional sensory system from birth and follows a different ontogeny from that of laryngeal bats.

Acoustically eavesdropping bat predators take longer to capture katydid prey signalling in aggregation.

Prey that are signalling in aggregation become more conspicuous with increasing numbers and tend to attract more predators. Such grouping may, however, benefit prey by lowering the risk of being captured because of the predator's difficulty in targeting individuals. Previous studies have investigated anti-predatory benefits of prey aggregation using visual predators, but it is unclear whether such benefits are gained in an auditory context. We investigated whether katydids of the genus Mecopoda gain protection from their acoustically eavesdropping bat predator Megaderma spasma when calling in aggregation. In a choice experiment, bats approached calls of prey aggregations more often than those of prey calling alone, indicating that prey calling in aggregation are at higher risk. In prey capture tasks, however, the average time taken and the number of flight passes made by bats before capturing a katydid were significantly higher for prey calling in aggregation than when calling alone, indicating that prey face lower predation risk when calling in aggregation. Another common anti-predatory strategy, calling from within vegetation, increased the time taken by bats to capture katydids calling alone but did not increase the time taken to capture prey calling from aggregations. The increased time taken to capture prey calling in aggregation compared with solitary calling prey offers an escape opportunity, thus providing prey that signal acoustically in aggregations with anti-predatory benefits. For bats, greater detectability of calling prey aggregations is offset by lower foraging efficiency, and this trade-off may shape predator foraging strategies in natural environments.

Echolocating bats can adjust sensory acquisition based on internal cues.

BACKGROUND: Sensory systems acquire both external and internal information to guide behavior. Adjustments based on external input are much better documented and understood than internal-based sensory adaptations. When external input is not available, idiothetic-internal-cues become crucial for guiding behavior. Here, we take advantage of the rapid sensory adjustments exhibited by bats in order to study how animals rely on internal cues in the absence of external input. Constant frequency echolocating bats are renowned for their Doppler shift compensation response used to adjust their emission frequency in order to optimize sensing. Previous studies documented the importance of external echoes for this response. RESULTS: We show that the Doppler compensation system works even without external feedback. Bats experiencing accelerations in an echo-free environment exhibited an intact compensation response. Moreover, using on-board GPS tags on free-flying bats in the wild, we demonstrate that the ability to perform Doppler shift compensation response based on internal cues might be essential in real-life when echo feedback is not available. CONCLUSIONS: We thus show an ecological need for using internal cues as well as an ability to do so. Our results illustrate the robustness of one particular sensory behavior; however, we suggest this ability to rely on different streams of information (i.e., internal or external) is probably relevant for many sensory behaviors.

Ear-Bot: Locust Ear-on-a-Chip Bio-Hybrid Platform.

During hundreds of millions of years of evolution, insects have evolved some of the most efficient and robust sensing organs, often far more sensitive than their man-made equivalents. In this study, we demonstrate a hybrid bio-technological approach, integrating a locust tympanic ear with a robotic platform. Using an Ear-on-a-Chip method, we manage to create a long-lasting miniature sensory device that operates as part of a bio-hybrid robot. The neural signals recorded from the ear in response to sound pulses, are processed and used to control the robot's motion. This work is a proof of concept, demonstrating the use of biological ears for robotic sensing and control.

Plants' ability to sense and respond to airborne sound is likely to be adaptive: reply to comment by Pyke et al.

Ecol. Lett. 22, 2019, 1483 demonstrated, for the first time, a rapid response of a plant to the airborne sounds of pollinators. Pyke et al. argue that this response is unlikely to be adaptive. Here we clarify some misunderstandings, and demonstrate the potential adaptive value using theoretical modelling and field observations.

Increased sugar concentration in response to a wide range of pollinator sounds can be adaptive for the plant: answer to Raguso et al.

In Veits et al., we showed that flowers respond to a range of pollinator sounds by increased nectar sugar concentration. Here we clarify that (1) our argument is relevant to most pollinators, and not limited to bees (2) specifically, bees do access Oenothera Drumondii nectar in this area.