Insectivorous bats form mobile sensory networks to optimize prey localization: The case of the common noctule bat

ECOLOGY Insectivorous bats form mobile sensory networks to optimize prey localization: The case of the common noctule bat

Animals that depend on ephemeral, patchily distributed prey often use public information to locate resource patches. The use of public information can lead to the aggregation of foragers at prey patches, a mechanism known as local enhancement. However, when ephemeral resources are distributed over large areas, foragers may also need to increase search efficiency, and thus apply social strategies when sampling the landscape. While sensory networks of visually oriented animals have already been confirmed, we lack an understanding of how acoustic eavesdropping adds to the formation of sensory networks. Here we radio-tracked a total of eighty-one aerial-hawking bats at very high spatiotemporal resolution during five sessions over three years, recording up to nineteen individuals simultaneously. Analyses of interactive flight behavior provide conclusive evidence that bats form temporary mobile sensory networks by adjusting their movements to neighboring conspecifics while probing the airspace for prey. Complementary agent-based simulations confirmed that the observed movement patterns can lead to the formation of mobile sensory networks, and that bats located prey faster when networking than when relying only on local enhancement or searching solitarily. However, the benefit of networking diminished with decreasing group size. The combination of empirical analyses and simulations elucidates how animal groups use acoustic information to efficiently locate unpredictable and ephemeral food patches. Our results highlight that declining local populations of social foragers may thus suffer from Allee effects that increase the risk of collapses under global change scenarios, like insect decline and habitat degradation.

Significance

For predators that depend on ephemeral prey patches, like aerial-hawking insectivores, searching for prey is akin to finding the proverbial needle in a haystack. Global change and resulting insect decline and habitat degradation make finding prey even more challenging. Simultaneous high-throughput radio-tracking of common noctule bats suggests that social strategies may be the key to mastering this challenge. When searching for insects, bats adjusted their movements to their neighbors consistent with the formation of mobile sensory networks. A simulation model confirmed that the observed behavior leads to increased search efficiency when prey is patchily distributed. However, the model also revealed that mobile sensory networks become unstable when the group becomes too small, indicating synergistic negative effects of local population declines.

Animals can use social information inadvertently provided by con- and heterospecifics to locate food resources. The use of social information, delivered via the location and performance of other foragers, becomes particularly beneficial when the occurrence of food varies unpredictably in space and time. The most prominent mechanism for social information transfer among foragers is termed "local enhancement": foraging individuals spot and approach nearby feeding con- or heterospecifics, and consequently aggregate at food patches. However, local enhancement may be an insufficient mechanism for animals that must search for food across large areas, can detect feeding con- or heterospecifics only at relatively short distances, or feed on rapidly depleting or spatiotemporally ephemeral resources. For predatory fish, and recently also for vultures and insectivorous bats, it has been suggested that individuals can overcome the limitations of individual prey detection by forming foraging "arrays" or "chains." We term these assemblages "mobile sensory networks," based on a similar term used in robotics and control systems, to emphasize the key elements of this social foraging mechanism.

In contrast to local enhancement, members of a mobile sensory network do not only use information from others that already found prey, but constantly exchange information while searching for food. Food-searching individuals move while actively sensing both their environment and the behavior of their neighbors, allowing each forager to gather sensory information across a much larger area than it alone could scan. Mobile sensory networks are more efficient in gathering information than groups of solitary foragers, but require frequent coordination of movements among individuals. Cohesion of moving groups can be maintained by simple movement rules that lead to the alignment of neighboring individuals. Theoretical studies have explored the idea of mobile sensory networks maximizing the efficiency of foragers that depend on ephemeral and patchily distributed food resources. Empirical studies suggest the existence of mobile sensory network formation in bats, yet this is based only on observations that foraging individuals were attracted to the broadcast of specific echolocation calls from successfully foraging conspecifics, so-called feeding buzzes,

or by the fact that foraging individuals encountered conspecifics more often than expected. Indeed, feeding buzzes indicate that bats are actively attacking prey, and therefore convey information on prey availability that can induce local enhancement in food searching bats. Yet, these previous studies cannot explain the formation of mobile sensory networks as they missed the dynamic nature of the interactions of bats during food search. Direct evidence of interactive movement responses of free-ranging animals that lead to the formation of mobile sensory networks during prey search is still lacking. Observing the formation of mobile sensory networks in natural systems requires simultaneous monitoring of many individuals at high resolution, a feat that has been challenging to achieve in empirical studies thus far. Recent technological advances in tracking systems, which provide high-throughput data collection, now make it possible to shed light on the fine-scale patterns emerging from interactive movements in the wild.

Here, we used a fully automated radio tracking system based on trilateration, to simultaneously record the movements of dozens of common noctule bats at higher spatiotemporal resolutions than so far achieved for aerial insectivores. Aerial-hawking insectivorous bats are particularly suited for studying social aspects of foraging ecology since they face the dilemma of finding ephemeral patches of insects while being severely constrained in the distance at which they can detect prey. Distances at which echolocating bats may detect large insects or insect patches are usually below ten to fifteen meters, due to the rapid attenuation of ultrasound in air. In contrast, the distance at which bats can eavesdrop on echolocating conspecifics is more than ten-fold larger, reaching up to one hundred sixty meters under optimal conditions. This notable difference between prey detection distance and conspecific detection distance may promote the evolution of group-foraging strategies. For bats, group foraging via eavesdropping on the foraging calls of hunting conspecifics leading to local enhancement is indeed well documented, but the formation of mobile sensory networks during prey search still lacks solid evidence from dynamic movement interactions of bats. Assuming that aerial-insectivorous bats depending on ephemeral prey apply a mobile sensory network search strategy as proposed by Egert-Berg et al. and Cvikel et al., we hypothesize that food-searching common noctule bats adjust their movements to food-searching neighbors, and that such behavior will lead to the formation of mobile sensory networks that increase the efficiency of prey search. Specifically, we predict that bats align at the maximum eavesdropping distance of approximately one hundred sixty meters by flying in parallel, and that they decrease or increase distance to conspecifics when farther apart from or closer to conspecifics, respectively. We further present an agent-based simulation model and predict that modeled bats form chains of interconnected individuals. We also predict that, under realistic conditions of colony size and prey distribution, bats that apply a mobile sensory network search strategy will find food patches faster than bats searching for food solitarily.

Here, we combined empirical tracking data and simulations to explain the formation of mobile sensory networks in bats hunting insects in open airspace and to investigate the benefits and constraints of mobile sensory networking. We recorded the movements of eighty-one common noctule bats during three hundred fifty-nine foraging flights at one-eighth Hertz resolution in five recording sessions (three spring sessions and two summer sessions over three consecutive years). We defined flights as movements of a bat in a particular night, with data recordings for at least fifteen minutes and no pauses longer than five minutes between data-points. We analyzed the fine-scale movements of individuals in relation to tagged conspecifics and identified mechanisms by which they form and maintain mobile sensory networks. We subsequently built a theoretical model that was based on the empirically identified movement patterns to confirm the emergence of mobile sensory network in bats. Using the simulation, we predicted how benefits and stability of mobile sensory networks depend on group size and prey distribution.