SMART-BARN: Scalable multimodal arena for real-time tracking behavior of animals in large numbers.

The SMART-BARN (scalable multimodal arena for real-time tracking behavior of animals in large numbers) achieves fast, robust acquisition of movement, behavior, communication, and interactions of animals in groups, within a large (14.7 meters by 6.6 meters by 3.8 meters), three-dimensional environment using multiple information channels. Behavior is measured from a wide range of taxa (insects, birds, mammals, etc.) and body size (from moths to humans) simultaneously. This system integrates multiple, concurrent measurement techniques including submillimeter precision and high-speed (300 hertz) motion capture, acoustic recording and localization, automated behavioral recognition (computer vision), and remote computer-controlled interactive units (e.g., automated feeders and animal-borne devices). The data streams are available in real time allowing highly controlled and behavior-dependent closed-loop experiments, while producing comprehensive datasets for offline analysis. The diverse capabilities of SMART-BARN are demonstrated through three challenging avian case studies, while highlighting its broad applicability to the fine-scale analysis of collective animal behavior across species.

Combining acoustic tracking and LiDAR to study bat flight behaviour in three-dimensional space.

BACKGROUND: Habitat structure strongly influences niche differentiation, facilitates predator avoidance, and drives species-specific foraging strategies of bats. Vegetation structure is also a strong driver of echolocation call characteristics. The fine-scale assessment of how bats utilise such structures in their natural habitat is instrumental in understanding how habitat composition shapes flight- and acoustic behaviour. However, it is notoriously difficult to study their species-habitat relationship in situ. METHODS: Here, we describe a methodology combining Light Detection and Ranging (LiDAR) to characterise three-dimensional vegetation structure and acoustic tracking to map bat behaviour. This makes it possible to study fine-scale use of habitat by bats, which is essential to understand spatial niche segregation in bats. Bats were acoustically tracked with microphone arrays and bat calls were classified to bat guild using automated identification. We did this in multiple LiDAR scanned vegetation plots in forest edge habitat. The datasets were spatially aligned to calculate the distance between bats' positions and vegetation structures. RESULTS: Our results are a proof of concept of combining LiDAR with acoustic tracking. Although it entails challenges with combining mass-volumes of fine-scale bat movements and vegetation information, we show the feasibility and potential of combining those two methods through two case studies. The first one shows stereotyped flight patterns of pipistrelles around tree trunks, while the second one presents the distance that bats keep to the vegetation in the presence of artificial light. CONCLUSION: By combining bat guild specific spatial behaviour with precise information on vegetation structure, the bat guild specific response to habitat characteristics can be studied in great detail. This opens up the possibility to address yet unanswered questions on bat behaviour, such as niche segregation or response to abiotic factors in interaction with natural vegetation. This combination of techniques can also pave the way for other applications linking movement patterns of other vocalizing animals and 3D space reconstruction.

A multi-species evaluation of digital wildlife monitoring using the Sigfox IoT network.

Bio-telemetry from small tags attached to animals is one of the principal methods for studying the ecology and behaviour of wildlife. The field has constantly evolved over the last 80 years as technological improvement enabled a diversity of sensors to be integrated into the tags (e.g., GPS, accelerometers, etc.). However, retrieving data from tags on free-ranging animals remains a challenge since satellite and GSM networks are relatively expensive and or power hungry. Recently a new class of low-power communication networks have been developed and deployed worldwide to connect the internet of things (IoT). Here, we evaluated one of these, the Sigfox IoT network, for the potential as a real-time multi-sensor data retrieval and tag commanding system for studying fauna across a diversity of species and ecosystems. We tracked 312 individuals across 30 species (from 25 g bats to 3 t elephants) with seven different device concepts, resulting in more than 177,742 successful transmissions. We found a maximum line of sight communication distance of 280 km (on a flying cape vulture [Gyps coprotheres]), which sets a new documented record for animal-borne digital data transmission using terrestrial infrastructure. The average transmission success rate amounted to 68.3% (SD 22.1) on flying species and 54.1% (SD 27.4) on terrestrial species. In addition to GPS data, we also collected and transmitted data products from accelerometers, barometers, and thermometers. Further, we assessed the performance of Sigfox Atlas Native, a low-power method for positional estimates based on radio signal strengths and found a median accuracy of 12.89 km (MAD 5.17) on animals. We found that robust real-time communication (median message delay of 1.49 s), the extremely small size of the tags (starting at 1.28 g without GPS), and the low power demands (as low as 5.8 µAh per transmitted byte) unlock new possibilities for ecological data collection and global animal observation.

Micro-sized open-source and low-cost GPS loggers below 1 g minimise the impact on animals while collecting thousands of fixes.

GPS-enabled loggers have been proven as valuable tools for monitoring and understanding animal movement, behaviour and ecology. While the importance of recording accurate location estimates is well established, deployment on many, especially small species, has been limited by logger mass and cost. We developed an open-source and low-cost 0.65 g GPS logger with a simple smartphone-compatible user interface, that can record more than 10,000 GPS fixes on a single 30 mAh battery charge (resulting mass including battery: 1.3 g). This low-budget 'TickTag' (currently 32 USD) allows scientists to scale-up studies while becoming a 'wearable' for larger animals and simultaneously enabling high-definition studies on small animals. Tests on two different species (domestic dog, Canis lupus familiaris and greater mouse-eared bats, Myotis myotis) showed that our combination of optimised hardware design and software-based recording strategies increases the number of achievable GPS fixes per g device mass compared to existing micro-sized solutions. We propose that due to the open-source access, as well as low cost and mass, the TickTag fills a technological gap in wildlife ecology and will open up new possibilities for wildlife research and conservation.

Acoustic differentiation and classification of wild belugas and narwhals using echolocation clicks.

Belugas (Delphinapterus leucas) and narwhals (Monodon monoceros) are highly social Arctic toothed whales with large vocal repertoires and similar acoustic profiles. Passive Acoustic Monitoring (PAM) that uses multiple hydrophones over large spatiotemporal scales has been a primary method to study their populations, particularly in response to rapid climate change and increasing underwater noise. This study marks the first acoustic comparison between wild belugas and narwhals from the same location and reveals that they can be acoustically differentiated and classified solely by echolocation clicks. Acoustic recordings were made in the pack ice of Baffin Bay, West Greenland, during 2013. Multivariate analyses and Random Forests classification models were applied to eighty-one single-species acoustic events comprised of numerous echolocation clicks. Results demonstrate a significant difference between species' acoustic parameters where beluga echolocation was distinguished by higher frequency content, evidenced by higher peak frequencies, center frequencies, and frequency minimums and maximums. Spectral peaks, troughs, and center frequencies for beluga clicks were generally > 60 kHz and narwhal clicks < 60 kHz with overlap between 40-60 kHz. Classification model predictive performance was strong with an overall correct classification rate of 97.5% for the best model. The most important predictors for species assignment were defined by peaks and notches in frequency spectra. Our results provide strong support for the use of echolocation in PAM efforts to differentiate belugas and narwhals acoustically.

Vertical sonar beam width and scanning behavior of wild belugas (Delphinapterus leucas) in West Greenland.

Echolocation signals of wild beluga whales (Delphinapterus leucas) were recorded in 2013 using a vertical, linear 16-hydrophone array at two locations in the pack ice of Baffin Bay, West Greenland. Individual whales were localized for 4:42 minutes of 1:04 hours of recordings. Clicks centered on the recording equipment (i.e. on-axis clicks) were isolated to calculate sonar parameters. We report the first sonar beam estimate of in situ recordings of wild belugas with an average -3 dB asymmetrical vertical beam width of 5.4°, showing a wider ventral beam. This narrow beam width is consistent with estimates from captive belugas; however, our results indicate that beluga sonar beams may not be symmetrical and may differ in wild and captive contexts. The mean apparent source level for on-axis clicks was 212 dB pp re 1 µPa and whales were shown to vertically scan the array from 120 meters distance. Our findings support the hypothesis that highly directional sonar beams and high source levels are an evolutionary adaptation for Arctic odontocetes to reduce unwanted surface echoes from sea ice (i.e., acoustic clutter) and effectively navigate through leads in the pack ice (e.g., find breathing holes). These results provide the first baseline beluga sonar metrics from free-ranging animals using a hydrophone array and are important for acoustic programs throughout the Arctic, particularly for acoustic classification between belugas and narwhals (Monodon monoceros).

Highly Directional Sonar Beam of Narwhals (Monodon monoceros) Measured with a Vertical 16 Hydrophone Array.

Recordings of narwhal (Monodon monoceros) echolocation signals were made using a linear 16 hydrophone array in the pack ice of Baffin Bay, West Greenland in 2013 at eleven sites. An average -3 dB beam width of 5.0° makes the narwhal click the most directional biosonar signal reported for any species to date. The beam shows a dorsal-ventral asymmetry with a narrower beam above the beam axis. This may be an evolutionary advantage for toothed whales to reduce echoes from the water surface or sea ice surface. Source level measurements show narwhal click intensities of up to 222 dB pp re 1 µPa, with a mean apparent source level of 215 dB pp re 1 µPa. During ascents and descents the narwhals perform scanning in the vertical plane with their sonar beam. This study provides valuable information for reference sonar parameters of narwhals and for the use of acoustic monitoring in the Arctic.

How Nectar-Feeding Bats Localize their Food: Echolocation Behavior of Leptonycteris yerbabuenae Approaching Cactus Flowers.

Nectar-feeding bats show morphological, physiological, and behavioral adaptations for feeding on nectar. How they find and localize flowers is still poorly understood. While scent cues alone allow no precise localization of a floral target, the spatial properties of flower echoes are very precise and could play a major role, particularly at close range. The aim of this study is to understand the role of echolocation for classification and localization of flowers. We compared the approach behavior of Leptonycteris yerbabuenae to flowers of a columnar cactus, Pachycereus pringlei, to that to an acrylic hollow hemisphere that is acoustically conspicuous to bats, but has different acoustic properties and, contrary to the cactus flower, present no scent. For recording the flight and echolocation behaviour we used two infrared video cameras under stroboscopic illumination synchronized with ultrasound recordings. During search flights all individuals identified both targets as a possible food source and initiated an approach flight; however, they visited only the cactus flower. In experiments with the acrylic hemisphere bats aborted the approach at ca. 40-50 cm. In the last instant before the flower visit the bats emitted a long terminal group of 10-20 calls. This is the first report of this behaviour for a nectar-feeding bat. Our findings suggest that L. yerbabuenae use echolocation for classification and localization of cactus flowers and that the echo-acoustic characteristics of the flower guide the bats directly to the flower opening.

No evidence for spectral jamming avoidance in echolocation behavior of foraging pipistrelle bats.

Frequency shifts in signals of bats flying near conspecifics have been interpreted as a spectral jamming avoidance response (JAR). However, several prerequisites supporting a JAR hypothesis have not been controlled for in previous studies. We recorded flight and echolocation behavior of foraging Pipistrellus pipistrellus while flying alone and with a conspecific and tested whether frequency changes were due to a spectral JAR with an increased frequency difference, or whether changes could be explained by other reactions. P. pipistrellus reacted to conspecifics with a reduction of sound duration and often also pulse interval, accompanied by an increase in terminal frequency. This reaction is typical of behavioral situations where targets of interest have captured the bat's attention and initiated a more detailed exploration. All observed frequency changes were predicted by the attention reaction alone, and do not support the JAR hypothesis of increased frequency separation. Reaction distances of 1-11 m suggest that the attention response may be elicited either by detection of the conspecific by short range active echolocation or by long range passive acoustic detection of echolocation calls.

Comparing Distribution of Harbour Porpoises (Phocoena phocoena) Derived from Satellite Telemetry and Passive Acoustic Monitoring.

Cetacean monitoring is essential in determining the status of a population. Different monitoring methods should reflect the real trends in abundance and patterns in distribution, and results should therefore ideally be independent of the selected method. Here, we compare two independent methods of describing harbour porpoise (Phocoena phocoena) relative distribution pattern in the western Baltic Sea. Satellite locations from 13 tagged harbour porpoises were used to build a Maximum Entropy (MaxEnt) model of suitable habitats. The data set was subsampled to one location every second day, which were sufficient to make reliable models over the summer (Jun-Aug) and autumn (Sep-Nov) seasons. The modelled results were compared to harbour porpoise acoustic activity obtained from 36 static acoustic monitoring stations (C-PODs) covering the same area. The C-POD data was expressed as the percentage of porpoise positive days/hours (the number of days/hours per day with porpoise detections) by season. The MaxEnt model and C-POD data showed a significant linear relationship with a strong decline in porpoise occurrence from west to east. This study shows that two very different methods provide comparable information on relative distribution patterns of harbour porpoises even in a low density area.

Bidirectional Echolocation in the Bat Barbastella barbastellus: Different Signals of Low Source Level Are Emitted Upward through the Nose and Downward through the Mouth.

The Barbastelle bat (Barbastella barbastellus) preys almost exclusively on tympanate moths. While foraging, this species alternates between two different signal types. We investigated whether these signals differ in emission direction or source level (SL) as assumed from earlier single microphone recordings. We used two different settings of a 16-microphone array to determine SL and sonar beam direction at various locations in the field. Both types of search signals had low SLs (81 and 82 dB SPL rms re 1 m) as compared to other aerial-hawking bats. These two signal types were emitted in different directions; type 1 signals were directed downward and type 2 signals upward. The angle between beam directions was approximately 70°. Barbastelle bats are able to emit signals through both the mouth and the nostrils. As mouth and nostrils are roughly perpendicular to each other, we conclude that type 1 signals are emitted through the mouth while type 2 signals and approach signals are emitted through the nose. We hypothesize that the "stealth" echolocation system of B. barbastellus is bifunctional. The more upward directed nose signals may be mainly used for search and localization of prey. Their low SL prevents an early detection by eared moths but comes at the expense of a strongly reduced detection range for the environment below the bat. The more downward directed mouth signals may have evolved to compensate for this disadvantage and may be mainly used for spatial orientation. We suggest that the possibly bifunctional echolocation system of B. barbastellus has been adapted to the selective foraging of eared moths and is an excellent example of a sophisticated sensory arms race between predator and prey.

Range-dependent flexibility in the acoustic field of view of echolocating porpoises (Phocoena phocoena).

Toothed whales use sonar to detect, locate, and track prey. They adjust emitted sound intensity, auditory sensitivity and click rate to target range, and terminate prey pursuits with high-repetition-rate, low-intensity buzzes. However, their narrow acoustic field of view (FOV) is considered stable throughout target approach, which could facilitate prey escape at close-range. Here, we show that, like some bats, harbour porpoises can broaden their biosonar beam during the terminal phase of attack but, unlike bats, maintain the ability to change beamwidth within this phase. Based on video, MRI, and acoustic-tag recordings, we propose this flexibility is modulated by the melon and implemented to accommodate dynamic spatial relationships with prey and acoustic complexity of surroundings. Despite independent evolution and different means of sound generation and transmission, whales and bats adaptively change their FOV, suggesting that beamwidth flexibility has been an important driver in the evolution of echolocation for prey tracking.

Scanning behavior in echolocating common pipistrelle bats (Pipistrellus pipistrellus).

Echolocating bats construct an auditory world sequentially by analyzing successive pulse-echo pairs. Many other mammals rely upon a visual world, acquired by sequential foveal fixations connected by visual gaze saccades. We investigated the scanning behavior of bats and compared it to visual scanning. We assumed that each pulse-echo pair evaluation corresponds to a foveal fixation and that sonar beam movements between pulses can be seen as acoustic gaze saccades. We used a two-dimensional 16 microphone array to determine the sonar beam direction of succeeding pulses and to characterize the three dimensional scanning behavior in the common pipistrelle bat (Pipistrellus pipistrellus) flying in the field. We also used variations of signal amplitude of single microphone recordings as indicator for scanning behavior in open space. We analyzed 33 flight sequences containing more than 700 echolocation calls to determine bat positions, source levels, and beam aiming. When searching for prey and orienting in space, bats moved their sonar beam in all directions, often alternately back and forth. They also produced sequences with irregular or no scanning movements. When approaching the array, the scanning movements were much smaller and the beam was moved over the array in small steps. Differences in the scanning pattern at various recording sites indicated that the scanning behavior depended on the echolocation task that was being performed. The scanning angles varied over a wide range and were often larger than the maximum angle measurable by our array. We found that echolocating bats use a "saccade and fixate" strategy similar to vision. Through the use of scanning movements, bats are capable of finding and exploring targets in a wide search cone centered along flight direction.

Asymmetry and dynamics of a narrow sonar beam in an echolocating harbor porpoise.

A key component in the operation of a biosonar system is the radiation of sound energy from the sound producing head structures of toothed whales and microbats. The current view involves a fixed transmission aperture by which the beam width can only change via changes in the frequency of radiated clicks. To test that for a porpoise, echolocation clicks were recorded with high angular resolution using a 16 hydrophone array. The beam is narrower than previously reported (DI = 24 dB) and slightly dorso-ventrally compressed (horizontal -3 dB beam width: 13°, vertical -3 dB beam width: 11°). The narrow beam indicates that all smaller toothed whales investigated so far have surprisingly similar beam widths across taxa and habitats. Obtaining high directionality may thus be at least in part an evolutionary factor that led to high centroid frequencies in a group of smaller toothed whales emitting narrow band high frequency clicks. Despite the production of stereotyped narrow band high frequency clicks, changes in the directionality by a few degrees were observed, showing that porpoises can obtain changes in sound radiation.

Source level reduction and sonar beam aiming in landing big brown bats (Eptesicus fuscus).

Reduction of echolocation call source levels in bats has previously been studied using set-ups with one microphone. By using a 16 microphone array, sound pressure level (SPL) variations, possibly caused by the scanning movements of the bat, can be excluded and the sonar beam aiming can be studied. During the last two meters of approach flights to a landing platform in a large flight room, five big brown bats aimed sonar beams at the landing site and reduced the source level on average by 7 dB per halving of distance. Considerable variation was found among the five individuals in the amount of source level reduction ranging from 4 to 9 dB per halving of distance. These results are discussed with respect to automatic gain control and intensity compensation and the combination of the two effects. It is argued that the two effects together do not lead to a stable echo level at the cochlea. This excludes a tightly coupled closed loop feed back control system as an explanation for the observed reduction of signal SPL in landing big brown bats.

Source levels of echolocation signals vary in correlation with wingbeat cycle in landing big brown bats (Eptesicus fuscus).

Recordings of the echolocation signals of landing big brown bats with a two-dimensional 16-microphone array revealed that the source level reduction of 7 dB per halving of distance is superimposed by a variation of up to 12 dB within single call groups emitted during the approach. This variation correlates with the wingbeat cycle. The timing of call emission correlates with call group size. First pulses of groups containing many calls are emitted earlier than first calls in groups with fewer calls or single calls. This suggests that the emission of pulse groups follows a fixed motor pattern where the information gained from the preceding pulse group determines how many calls will be emitted in the next group. Single calls and call groups are centred at the middle of the upstroke. Expiration is indicated by call emission. The pause between groups is centred at the middle of the downstroke and indicates inspiration. The hypothesis that the source level variation could be caused by changes in the subglottic pressure due to the contraction of the major flight muscles is discussed.