On-board recordings reveal no jamming avoidance in wild bats.

Animals often deal with situations in which vast sensory input is received simultaneously. They therefore must possess sophisticated mechanisms to select important input and ignore the rest. In bat echolocation, this problem is at its extreme. Echolocating bats emit sound signals and analyse the returning echoes to sense their environment. Bats from the same species use signals with similar frequencies. Nearby bats therefore face the difficulty of distinguishing their own echoes from the signals of other bats, a problem often referred to as jamming. Because bats commonly fly in large groups, jamming might simultaneously occur from numerous directions and at many frequencies. Jamming is a special case of the general phenomenon of sensory segregation. Another well-known example is the human problem of following conversation within a crowd. In both situations, a flood of auditory incoming signals must be parsed into important versus irrelevant information. Here, we present a novel method, fitting wild bats with a miniature microphone, which allows studying jamming from the bat's 'point of view'. Previous studies suggested that bats deal with jamming by shifting their echolocation frequency. On-board recordings suggest otherwise. Bats shifted their frequencies, but they did so because they were responding to the conspecifics as though they were nearby objects rather than avoiding being jammed by them. We show how bats could use alternative measures to deal with jamming instead of shifting their frequency. Despite its intuitive appeal, a spectral jamming avoidance response might not be the prime mechanism to avoid sensory interference from conspecifics.

Stability and responsiveness in a self-organized living architecture.

Robustness and adaptability are central to the functioning of biological systems, from gene networks to animal societies. Yet the mechanisms by which living organisms achieve both stability to perturbations and sensitivity to input are poorly understood. Here, we present an integrated study of a living architecture in which army ants interconnect their bodies to span gaps. We demonstrate that these self-assembled bridges are a highly effective means of maintaining traffic flow over unpredictable terrain. The individual-level rules responsible depend only on locally-estimated traffic intensity and the number of neighbours to which ants are attached within the structure. We employ a parameterized computational model to reveal that bridges are tuned to be maximally stable in the face of regular, periodic fluctuations in traffic. However analysis of the model also suggests that interactions among ants give rise to feedback processes that result in bridges being highly responsive to sudden interruptions in traffic. Subsequent field experiments confirm this prediction and thus the dual nature of stability and flexibility in living bridges. Our study demonstrates the importance of robust and adaptive modular architecture to efficient traffic organisation and reveals general principles regarding the regulation of form in biological self-assemblies.

High temporal resolution data reveal low bat and insect activity over managed meadows in central Europe.

Increasing agriculture and pesticide use have led to declines in insect populations and biodiversity worldwide. In addition to insect diversity, it is also important to consider insect abundance, due to the importance of insects as food for species at higher trophic levels such as bats. We monitored spatiotemporal variation in abundance of nocturnal flying insects over meadows, a common open landscape structure in central Europe, and correlated it with bat feeding activity. Our most important result was that insect abundance was almost always extremely low. This was true regardless of management intensity of the different meadows monitored. We also found no correlation of insect abundance or the presence of insect swarms with bat feeding activity. This suggests that insect abundance over meadows was too low and insect swarms too rare for bats to risk expending energy to search for them. Meadows appeared to be poor habitat for nocturnal flying insects, and of low value as a foraging habitat for bats. Our study highlights the importance of long-term monitoring of insect abundance, especially at high temporal scales to identify and protect foraging habitats. This will become increasingly important given the rapid decline of insects.

What determines the information update rate in echolocating bats.

The rate of sensory update is one of the most important parameters of any sensory system. The acquisition rate of most sensory systems is fixed and has been optimized by evolution to the needs of the animal. Echolocating bats have the ability to adjust their sensory update rate which is determined by the intervals between emissions - the inter-pulse intervals (IPI). The IPI is routinely adjusted, but the exact factors driving its regulation are unknown. We use on-board audio recordings to determine how four species of echolocating bats with different foraging strategies regulate their sensory update rate during commute flights. We reveal strong correlations between the IPI and various echolocation and movement parameters. Specifically, the update rate increases when the signals' peak-energy frequency and intensity increases while the update rate decreases when flight speed and altitude increases. We suggest that bats control their information update rate according to the behavioral mode they are engaged in, while always maintaining sensory continuity. Specifically, we suggest that bats apply two modes of attention during commute flights. Our data moreover suggests that bats emit echolocation signals at accurate intervals without the need for external feedback.

Sensory collectives in natural systems.

Groups of animals inhabit vastly different sensory worlds, or umwelten, which shape fundamental aspects of their behaviour. Yet the sensory ecology of species is rarely incorporated into the emerging field of collective behaviour, which studies the movements, population-level behaviours, and emergent properties of animal groups. Here, we review the contributions of sensory ecology and collective behaviour to understanding how animals move and interact within the context of their social and physical environments. Our goal is to advance and bridge these two areas of inquiry and highlight the potential for their creative integration. To achieve this goal, we organise our review around the following themes: (1) identifying the promise of integrating collective behaviour and sensory ecology; (2) defining and exploring the concept of a 'sensory collective'; (3) considering the potential for sensory collectives to shape the evolution of sensory systems; (4) exploring examples from diverse taxa to illustrate neural circuits involved in sensing and collective behaviour; and (5) suggesting the need for creative conceptual and methodological advances to quantify 'sensescapes'. In the final section, (6) applications to biological conservation, we argue that these topics are timely, given the ongoing anthropogenic changes to sensory stimuli (e.g. via light, sound, and chemical pollution) which are anticipated to impact animal collectives and group-level behaviour and, in turn, ecosystem composition and function. Our synthesis seeks to provide a forward-looking perspective on how sensory ecologists and collective behaviourists can both learn from and inspire one another to advance our understanding of animal behaviour, ecology, adaptation, and evolution.

DNA methylation predicts age and provides insight into exceptional longevity of bats.

Exceptionally long-lived species, including many bats, rarely show overt signs of aging, making it difficult to determine why species differ in lifespan. Here, we use DNA methylation (DNAm) profiles from 712 known-age bats, representing 26 species, to identify epigenetic changes associated with age and longevity. We demonstrate that DNAm accurately predicts chronological age. Across species, longevity is negatively associated with the rate of DNAm change at age-associated sites. Furthermore, analysis of several bat genomes reveals that hypermethylated age- and longevity-associated sites are disproportionately located in promoter regions of key transcription factors (TF) and enriched for histone and chromatin features associated with transcriptional regulation. Predicted TF binding site motifs and enrichment analyses indicate that age-related methylation change is influenced by developmental processes, while longevity-related DNAm change is associated with innate immunity or tumorigenesis genes, suggesting that bat longevity results from augmented immune response and cancer suppression.

Acoustic evaluation of behavioral states predicted from GPS tracking: a case study of a marine fishing bat.

BACKGROUND: Multiple methods have been developed to infer behavioral states from animal movement data, but rarely has their accuracy been assessed from independent evidence, especially for location data sampled with high temporal resolution. Here we evaluate the performance of behavioral segmentation methods using acoustic recordings that monitor prey capture attempts. METHODS: We recorded GPS locations and ultrasonic audio during the foraging trips of 11 Mexican fish-eating bats, Myotis vivesi, using miniature bio-loggers. We then applied five different segmentation algorithms (k-means clustering, expectation-maximization and binary clustering, first-passage time, hidden Markov models, and correlated velocity change point analysis) to infer two behavioral states, foraging and commuting, from the GPS data. To evaluate the inference, we independently identified characteristic patterns of biosonar calls ("feeding buzzes") that occur during foraging in the audio recordings. We then compared segmentation methods on how well they correctly identified the two behaviors and if their estimates of foraging movement parameters matched those for locations with buzzes. RESULTS: While the five methods differed in the median percentage of buzzes occurring during predicted foraging events, or true positive rate (44-75%), a two-state hidden Markov model had the highest median balanced accuracy (67%). Hidden Markov models and first-passage time predicted foraging flight speeds and turn angles similar to those measured at locations with feeding buzzes and did not differ in the number or duration of predicted foraging events. CONCLUSION: The hidden Markov model method performed best at identifying fish-eating bat foraging segments; however, first-passage time was not significantly different and gave similar parameter estimates. This is the first attempt to evaluate segmentation methodologies in echolocating bats and provides an evaluation framework that can be used on other species.

Resource Ephemerality Drives Social Foraging in Bats.

Observations of animals feeding in aggregations are often interpreted as events of social foraging, but it can be difficult to determine whether the animals arrived at the foraging sites after collective search [1-4] or whether they found the sites by following a leader [5, 6] or even independently, aggregating as an artifact of food availability [7, 8]. Distinguishing between these explanations is important, because functionally, they might have very different consequences. In the first case, the animals could benefit from the presence of conspecifics, whereas in the second and third, they often suffer from increased competition [3, 9-13]. Using novel miniature sensors, we recorded GPS tracks and audio of five species of bats, monitoring their movement and interactions with conspecifics, which could be inferred from the audio recordings. We examined the hypothesis that food distribution plays a key role in determining social foraging patterns [14-16]. Specifically, this hypothesis predicts that searching for an ephemeral resource (whose distribution in time or space is hard to predict) is more likely to favor social foraging [10, 13-15] than searching for a predictable resource. The movement and social interactions differed between bats foraging on ephemeral versus predictable resources. Ephemeral species changed foraging sites and showed large temporal variation nightly. They aggregated with conspecifics as was supported by playback experiments and computer simulations. In contrast, predictable species were never observed near conspecifics and showed high spatial fidelity to the same foraging sites over multiple nights. Our results suggest that resource (un)predictability influences the costs and benefits of social foraging.

Moving in the Anthropocene: Global reductions in terrestrial mammalian movements.

Animal movement is fundamental for ecosystem functioning and species survival, yet the effects of the anthropogenic footprint on animal movements have not been estimated across species. Using a unique GPS-tracking database of 803 individuals across 57 species, we found that movements of mammals in areas with a comparatively high human footprint were on average one-half to one-third the extent of their movements in areas with a low human footprint. We attribute this reduction to behavioral changes of individual animals and to the exclusion of species with long-range movements from areas with higher human impact. Global loss of vagility alters a key ecological trait of animals that affects not only population persistence but also ecosystem processes such as predator-prey interactions, nutrient cycling, and disease transmission.

Bats aggregate to improve prey search but might be impaired when their density becomes too high.

Social foraging is a very common yet extremely complex behavior. Numerous studies attempted to model it with little supporting evidence. Studying it in the wild is difficult because it requires monitoring the animal's movement, its foraging success, and its interactions with conspecifics. We present a novel system that enables full night ultrasonic recording of freely foraging bats, in addition to GPS tracking. As they rely on echolocation, audio recordings of bats allow tapping into their sensory acquisition of the world. Rapid changes in echolocation allowed us to reveal the bats' dynamic reactions in response to prey or conspecifics­two key behaviors that are extremely difficult to assess in most animals. We found that bats actively aggregate and forage as a group. However, we also found that when the group became too dense, bats were forced to devote sensory attention to conspecifics that frequently entered their biosonar "field of view," impairing the bats' prey detection performance. Why then did bats fly in such high densities? By emitting echolocation calls, bats constantly provide public information about their detection of prey. Bats could therefore benefit from intentionally flying at a distance that enables eavesdropping on conspecifics. Group foraging, therefore, probably allowed bats to effectively operate as an array of sensors, increasing their searching efficiency. We suggest that two opposing forces are at play in determining the efficient foraging density: on the one hand, higher densities improve prey detection, but on the other hand, they increase conspecific interference.