Scientists have long sought to identify and quantify the sensory inputs that define changes in behaviour of wild animals. This quest is severely hampered by the fact that most animals use a large array of different sensory systems to inform behavioural transitions, making it very difficult to identify pertinent sensory cues available to the study animal in ecologically relevant settings. “It is the ultimate dream of any sensory physiologist to be able to tap into the sensory stream of wild animals. The miniature tags developed here will exactly enable such eavesdropping on the echo streams returning to the ears of echolocating bats, and thereby allow us to understand on what sensory basis animals make decisions.” Professor Peter Teglberg Madsen, Aarhus University Echolocating bats are ideal model organisms for addressing this problem, because their hunting and navigation behaviour rely almost exclusively on hearing echoes generated from loud self-generated calls. With this Semper Ardens project, I seek to exploit that fact by developing a 2.6 gram data logger that, when mounted on free-flying bats, can record both the emitted, powerful calls and the weak echoes returning to the bats ears, allowing us for the first time to tap into the sensory stream of small mammals in the wild. Thus, we can now record the exact information that is available to the dominant sensory system of a hunting animal in the wild and tie the information to the details of how the animal is changing its behaviour to information flow. Echolocation: Active Sensing for Dynamic Perception Animals perceive their environment by comparing information provided by their senses with innate and learned models of structure in time and space. The decoding of such sensory information in the brain demands the simultaneous handling of an immense barrage of inputs from multiple sources and senses to form the animal’s perceived version of the environment, the so-called umwelt. Most senses operate passively, integrating information in the form of energy from the surroundings that impinges on the sensory organ. However, a few senses, such as echolocation, gather information through an active process where the animal itself delivers the energy that it subsequently detects in the form of echoes. Echolocating animals use powerful, directional calls coupled with acute auditory processing to acquire echo information with remarkable spatial and temporal resolution allowing them to find and capture prey in dark environments, which would otherwise be inaccessible (figure 1). Echolocation has evolved independently in two major groups of mammals, bats in air and toothed whales in water. Common for them is that they hunt under conditions of poor lighting by emission of very powerful, ultrasonic pulses and subsequent auditory analysis of weak echoes from prey items returning milliseconds later. This seemingly exotic sense is actually the main sensory modality in one in four mammalian species (1100 species of bats and 70 species of toothed whales) for navigation and prey finding. Underpinning the success of this sensory modality is a tightly-coupled suite of biomechanical and neural processing systems that forms a tight feedback loop between sensory inputs and motor outputs. Echolocating animals receive information only when they emit sound, which means that they control the information flow by the rate, type and direction of the sounds they produce, as well as by adjusting the sensitivity of their hearing as a function of time after call emission. These parameters directly influence the temporal resolution and spatial extent of their sensory volume, enabling dynamic control of attention in response to environmental complexity and behavioural objectives. Accordingly, the way that echolocating bats manipulate their perception of the surrounding environment is to a large extend revealed by the sonar pulses they emit. Echolocating bats are therefore ideal experimental models for studying sensory and cognitive adaptations that confer advantages in handling a dynamic sensory scene in time and space to inform behavioural changes of wild animals. Figure 1: Three combined still photos of a bat catching a tethered meal worm from a string in the lab. Bats can eat up to 15% of their own body weight in insects during nocturnal foraging bouts in complete darkness. Photo by Lasse Jakobsen, University of Southern Denmark. Bat Echolocation Studied Beyond Classic Laboratory Settings Since the discovery of echolocation in bats (figure 1) more than 70 years ago, a large number of studies on hearing, sound production, acoustic behaviour, and sound radiation have formed a coherent synthesis of how bats navigate and catch prey with sound in complete darkness. This deep understanding has been enabled by dedicated laboratory experiments where echolocating bats have been tasked with intercepting meal worms suspended in an-echoic rooms and increasingly also via recordings of bats foraging by echolocation in the field. “This project is truly an interdisciplinary and collaborative project drawing on the combined strengths of biologists and engineers to break into a new scientific frontier.” Professor Peter Teglberg Madsen, Aarhus University These studies have revealed a set of remarkable acoustic gaze changes which have been interpreted as indicating structural phases in the process of finding and intercepting prey on the wing: a search phase of long, powerful calls at low rates, an approach phase where the call levels, durations and call intervals are reduced with decreasing range to the target, and then finally a capture phase that involves a further reduction in inter-call intervals and outputs by two orders of magnitude in the last few seconds of prey capture enabling high resolution tracking of moving prey items. This acoustic behaviour is very similar to the terminal buzz of echolocating toothed whales, leading me and professor Annemarie Surlykke at SDU to recently propose a remarkable functional convergence of echolocation in bats and toothed whales despite the dramatically different environments in which these echolocation systems evolved. One in four species of mammals are bats: More than 1000 species of echolocating bats have adapted to feed on a large range of food items from frogs, fish, and insects to fruit across a broad suite of ecological niches all over the world. 2.6 gram Miniature Acoustic and Accelerometer Tags to Study Bat Echolocation However, comparisons of echolocation behaviour in ecologically relevant settings across these taxa suffer from a major problem: the size (<100 grams) and flight speed (3-5 m/sec) of bats combined with the rapid attenuation of their ultrasonic calls in air have meant that they can only be studied in highly controlled, and therefore, artificial lab settings or during 2-3 sec snapshots when the bats pass by recording arrays in the field. Using echolocation only, bats can detect and capture an insect in complete darkness at 3-10 metres distance, differentiate between materials and textures of objects and find their way home if released many kilometres from their roosts. Therefore, I am with this ambitious Semper Ardens-project striving for the first time to address: 1) how often bats encounter and capture food by echolocation during a long, dark night, 2) how they use acoustic gaze changes to manage the barrage of echoic information from complex, highly dynamic acoustic scenes in the wild comprising both prey and non-prey targets, 3) how they dynamically track insect prey targets that have evolved to detect and avoid predation. In the last few years we have been able to address similar questions in echolocating toothed whales using cutting edge, multi-sensor tags that, when placed with suction cups on animals in the wild, record both the outgoing clicks and returning echoes in concert with changes in motor patterns as logged with inertial sensors in the tags. Up until very recently, such advanced, archival tags have been much too big (>200 grams) to use on echolocating bats. However, supported with a Semper Ardens Research Grant from the Carlsberg Foundation, I have now toegether with Dr. mark Johnson from St. Andrews university in Scotland, developed a fully operational 2.6 gram acoustic tag for bats (figure 2). Figure 2: The smallest ultrasound recording tag in the world: Weighing in at only 2.6 grams, the bat tag features a sensitive microphone covering a frequency range from 1 to 100 kHz, a preamplifier, three accelerometers, a battery, and a memory card. This enables high fidelity recordings of the emitted calls and the echoes returning from the environment, concomitant with the movements of the bat. Photo by Laura Stidsholt, Aarhus University. Using porpoises as stepping stones for testing increasingly smaller tags over the last year, we have recently, via an extreme miniaturisation of the electronics and sensors, made the first very successful experiments on free flying, echolocating bats in close collaboration with international colleagues (figure 3). The miniature tag record the wing beats, mouth movements and outgoing sonar pulses of bats. But most importantly, they record the echoic scene returning to the bats’ ears, allowing us full access to the sensory stream that informs behavioural transitions in the flying bat during approach, search, and capture of aerial prey (figure 3). Therefore, we now have a unique, world first solution to the problem of how to study the echolocation of bats catching prey on the wing during entire foraging bouts in the wild. This is a ground breaking opportunity to study how one in four mammalian species forage with ultrasound that in a broader perspective will revolutionise how we can study the sensory physiology and behaviour of small animals in the wild. The long term and high end support of the Semper Ardens Research Grant is thus critically enabling my group to be at the very forefront of echolocation research and in studying sensory physiology of wild animals. There are already plans to branch out this technology to other small vocalizing animals, such as song birds, and to use these miniature recording devices to understand the effects natural and man-made soundscapes on a large suite of organisms. In a broader perspective, this research effort can help conserve bat species, of which many are critically endangered and no one understands why, and hopefully inform the development of artificial echolocation systems to aid navigation and improve the daily lives of visually impaired humans. Figure 3: Tag recording from a bat flying towards a target. A) shows how the differentiated accelerometer outputs providing information about each wing beat, while B) shows the concomitantly recorded calls from the flying bat. C) shows a spectrogram of the first call in B) along with a suite of different echoes returning at delays and hence ranges out to 5 metres, allowing us to display and quantify the self-generated auditory scene of the bat. Figure by Laura Stidsholt, Aarhus University.