Hunting bats adjust their echolocation to receive weak prey echoes for clutter reduction

This study was funded by the Carlsberg Semper Ardens grant to P.T.M. and by the Emmy Noether program of the Deutsche Forschungsgemeinschaft (DFG; German Research Foundation, grant no. 241711556) to H.R.G. All experiments were carried out under the following licenses: 721/12.06.2017, 180/07.08.2018, and 795/17.05.2019.How animals extract information from their surroundings to guide motor patterns is central to their survival. Here, we use echo-recording tags to show how wild hunting bats adjust their sensory strategies to their prey and natural environment. When searching, bats maximize the chances of detecting small prey by using large sensory volumes. During prey pursuit, they trade spatial for temporal information by reducing sensory volumes while increasing update rate and redundancy of their sensory scenes. These adjustments lead to very weak prey echoes that bats protect from interference by segregating prey sensory streams from the background using a combination of fast-acting sensory and motor strategies. Counterintuitively, these weak sensory scenes allow bats to be efficient hunters close to background clutter broadening the niches available to hunt for insects.Publisher PDFPeer reviewe

Open-source workflow approaches to passive acoustic monitoring of bats

The work was funded by grants to PTM from Carlsberg Semper Ardens Research Projects and the Independent Research Fund Denmark.The affordability, storage and power capacity of compact modern recording hardware have evolved passive acoustic monitoring (PAM) of animals and soundscapes into a non-invasive, cost-effective tool for research and ecological management particularly useful for bats and toothed whales that orient and forage using ultrasonic echolocation. The use of PAM at large scales hinges on effective automated detectors and species classifiers which, combined with distance sampling approaches, have enabled species abundance estimation of toothed whales. But standardized, user-friendly and open access automated detection and classification workflows are in demand for this key conservation metric to be realized for bats. We used the PAMGuard toolbox including its new deep learning classification module to test the performance of four open-source workflows for automated analyses of acoustic datasets from bats. Each workflow used a different initial detection algorithm followed by the same deep learning classification algorithm and was evaluated against the performance of an expert manual analyst. Workflow performance depended strongly on the signal-to-noise ratio and detection algorithm used: the full deep learning workflow had the best classification accuracy (≤67%) but was computationally too slow for practical large-scale bat PAM. Workflows using PAMGuard's detection module or triggers onboard an SM4BAT or AudioMoth accurately classified up to 47%, 59% and 34%, respectively, of calls to species. Not all workflows included noise sampling critical to estimating changes in detection probability over time, a vital parameter for abundance estimation. The workflow using PAMGuard's detection module was 40 times faster than the full deep learning workflow and missed as few calls (recall for both ~0.6), thus balancing computational speed and performance. We show that complete acoustic detection and classification workflows for bat PAM data can be efficiently automated using open-source software such as PAMGuard and exemplify how detection choices, whether pre- or post-deployment, hardware or software-driven, affect the performance of deep learning classification and the downstream ecological information that can be extracted from acoustic recordings. In particular, understanding and quantifying detection/classification accuracy and the probability of detection are key to avoid introducing biases that may ultimately affect the quality of data for ecological management.Publisher PDFPeer reviewe

Dolphin echolocation behaviour during active long-range target approaches

Financial support was provided by the US Office of Naval Research Code 32 (Mine Countermeasures, Acoustics Phenomenology & Modeling Group). M.L. and P.T.M. were funded by frame grants from the National Danish Research Council (Det Frie Forskningsråd) and by a Semper Ardens grant from the Carlsberg Foundation. M.L.’s travel expenses were covered by grants from Augustinus Fonden and DAS-Fonden (Danish Acoustical Society, Dansk Akustisk Selskab). F.H.J. was funded by an AIAS-COFUND fellowship from Aarhus Institute of Advanced Studies under the EU's Seventh Framework Programme (Agreement No. 609033).Echolocating toothed whales generally adjust click intensity and rate according to target range to ensure that echoes from targets of interest arrive before a subsequent click is produced, presumably facilitating range estimation from the delay between clicks and returning echoes. However, this click-echo-click paradigm for the dolphin biosonar is mostly based on experiments with stationary animals echolocating fixed targets at ranges below ∼120 m. Therefore, we trained two bottlenose dolphins instrumented with a sound recording tag to approach a target from ranges up to 400 m and either touch the target (subject TRO) or detect a target orientation change (subject SAY). We show that free-swimming dolphins dynamically increase interclick interval (ICI) out to target ranges of ∼100 m. TRO consistently kept ICIs above the two-way travel time (TWTT) for target ranges shorter than ∼100 m, whereas SAY switched between clicking at ICIs above and below the TWTT for target ranges down to ∼25 m. Source levels changed on average by 17log10(target range), but with considerable variation for individual slopes (4.1 standard deviations for by-trial random effects), demonstrating that dolphins do not adopt a fixed automatic gain control matched to target range. At target ranges exceeding ∼100 m, both dolphins frequently switched to click packet production in which interpacket intervals exceeded the TWTT, but ICIs were shorter than the TWTT. We conclude that the click-echo-click paradigm is not a fixed echolocation strategy in dolphins, and we demonstrate the first use of click packets for free-swimming dolphins when solving an echolocation task.Publisher PDFPeer reviewe

Echolocation click parameters and biosonar behaviour of the dwarf sperm whale (Kogia sima)

PhD and fieldwork funding were provided by the Danmarks Grundforskningsfond (27125 to P.T.M.), the Oticon Fonden (18-0340 to C.E.M.) the Dansk Akustisk Selskab (to C.E.M.), the South Africa National Research Foundation (research career advancement fellowship to S.E.) and the Claude Leon Foundation (postdoctoral fellowship to T.G.).Dwarf sperm whales (Kogia sima) are small toothed whales that produce narrow-band high-frequency (NBHF) echolocation clicks. Such NBHF clicks, subject to high levels of acoustic absorption, are usually produced by small, shallow-diving odontocetes, such as porpoises, in keeping with their short-range echolocation and fast click rates. Here, we sought to address the problem of how the little-studied and deep-diving Kogia can hunt with NBHF clicks in the deep sea. Specifically, we tested the hypotheses that Kogia produce NBHF clicks with longer inter-click intervals (ICIs), higher directionality and higher source levels (SLs) compared with other NBHF species. We did this by deploying an autonomous deep-water vertical hydrophone array in the Bahamas, where no other NBHF species are present, and by taking opportunistic recordings of a close-range Kogia sima in a South African harbour. Parameters from on-axis clicks (n=46) in the deep revealed very narrow-band clicks (root mean squared bandwidth, BWRMS, of 3±1 kHz), with SLs of up to 197 dB re. 1 µPa peak-to-peak (μPapp) at 1 m, and a half-power beamwidth of 8.8 deg. Their ICIs (mode of 245 ms) were much longer than those of porpoises (<100 ms), suggesting an inspection range that is longer than detection ranges of single prey, perhaps to facilitate auditory streaming of a complex echo scene. On-axis clicks in the shallow harbour (n=870) had ICIs and SLs in keeping with source parameters of other NBHF cetaceans. Thus, in the deep, dwarf sperm whales use a directional, but short-range echolocation system with moderate SLs, suggesting a reliable mesopelagic prey habitat.Publisher PDFPeer reviewe

Implications of porpoise echolocation and dive behaviour on passive acoustic monitoring

Funding: The post-doctoral position for J.D.J.M. was funded by a FNU – Danish Natural Science Research Council grant to P.T.M. This study was also funded by the German Federal Agency for Nature Conservation via the grants “Effects of underwater noise on marine vertebrates” (Cluster 7, Z1.2-53302/2010/14) and “Under Water Noise Effects—UWE” (Project No. FKZ 3515822000). The contribution by T.A.M. was funded under the ACCURATE project (U.S. Navy Living Marine Resources Program, Contract No. N3943019C2176) and CEAUL (funded by FCT—Fundação para a Ciência e a Tecnologia, Portugal, through Project No. UIDB/00006/2020).Harbour porpoises are visually inconspicuous but highly soniferous echolocating marine predators that are regularly studied using passive acoustic monitoring (PAM). PAM can provide quality data on animal abundance, human impact, habitat use, and behaviour. The probability of detecting porpoise clicks within a given area ( P ̂ ) is a key metric when interpreting PAM data. Estimates of P ̂ can be used to determine the number of clicks per porpoise encounter that may have been missed on a PAM device, which, in turn, allows for the calculation of abundance and ideally non-biased comparison of acoustic data between habitats and time periods. However, P ̂ is influenced by several factors, including the behaviour of the vocalising animal. Here, the common implicit assumption that changes in animal behaviour have a negligible effect on P ̂ between different monitoring stations or across time is tested. Using a simulation-based approach informed by acoustic biologging data from 22 tagged harbour porpoises, it is demonstrated that porpoise behavioural states can have significant (up to 3× difference) effects on P ̂ . Consequently, the behavioural state of the animals must be considered in analysis of animal abundance to avoid substantial over- or underestimation of the true abundance, habitat use, or effects of human disturbance.Publisher PDFPeer reviewe

Ultra-high foraging rates of harbor porpoises make them vulnerable to anthropogenic disturbance

This study was partly funded by the German Federal Agency for Nature Conservation (BfN) under the contract Z1.2-5330/2010/14 and the BfN-Cluster 7 “Effects of underwater noise on marine vertebrates.” D.M.W. and P.T.M. were also supported by the Danish National Research Foundation (FNU) and the Carlsberg Foundation, and M.J. was also supported by the Marine Alliance for Science and Technology Scotland (MASTS) and by a Marie Curie-Sklodowska award.The question of how individuals acquire and allocate resources to maximize fitness is central in evolutionary ecology. Basic information on prey selection, search effort, and capture rates are critical for understanding a predator’s role in its ecosystem and for predicting its response to natural and anthropogenic disturbance. Yet, for most marine species, foraging interactions cannot be observed directly. The high costs of thermoregulation in water require that small marine mammals have elevated energy intakes compared to similar-sized terrestrial mammals [1]. The combination of high food requirements and their position at the apex of most marine food webs may make small marine mammals particularly vulnerable to changes within the ecosystem [2–4], but the lack of detailed information about their foraging behavior often precludes an informed conservation effort. Here, we use high-resolution movement and prey echo recording tags on five wild harbor porpoises to examine foraging interactions in one of the most metabolically challenged cetacean species. We report that porpoises forage nearly continuously day and night, attempting to capture up to 550 small (3–10 cm) fish prey per hour with a remarkable prey capture success rate of >90%. Porpoises therefore target fish that are smaller than those of commercial interest, but must forage almost continually to meet their metabolic demands with such small prey, leaving little margin for compensation. Thus, for these “aquatic shrews,” even a moderate level of anthropogenic disturbance in the busy shallow waters they share with humans may have severe fitness consequences at individual and population levels.PostprintPeer reviewe

Long-term sound and movement recording tags to study natural behavior and reaction to ship noise of seals

This study was funded by the German Federal Agency of Nature Conservation under the project “Effects of underwater noise on marine vertebrates” (Cluster 7, Z1.2‐53302/2010/14) and “Under Water Noise Effects – UWE” (Project numbers FKZ 3515822000). MJ was supported for development of the tags by a Marie Sklodowska‐Curie career integration grant and by the Marine Alliance for Science and Technology Scotland. PTM and DMW were partly supported by a large frame grant from the Danish National Research Council. DMW was also supported by an Office of Naval Research grant to Jeremy Goldbogen at Stanford University.1.  The impact of anthropogenic noise on marine fauna is of increasing conservation concern with vessel noise being one of the major contributors. Animals that rely on shallow coastal habitats may be especially vulnerable to this form of pollution. 2.  Very limited information is available on how much noise from ship traffic individual animals experience, and how they may react to it due to a lack of suitable methods. To address this, we developed long-duration audio and 3D-movement tags (DTAGs) and deployed them on three harbor seals and two gray seals in the North Sea during 2015-2016. 3. These tags recorded sound, accelerometry, magnetometry, and pressure continuously for up to 21 days. GPS positions were also sampled for one seal continuously throughout the recording period. A separate tag, combining a camera and an accelerometer logger, was deployed on two harbor seals to visualize specific behaviors that helped interpret accelerometer signals in the DTAG data. 4.  Combining data from depth, accelerometer, and audio sensors, we found that animals spent 6.6%-42.3% of the time hauled out (either on land or partly submerged), and 5.3%-12.4% of their at-sea time resting at the sea bottom, while the remaining time was used for traveling, resting at surface, and foraging. Animals were exposed to audible vessel noise 2.2%-20.5% of their time when in water, and we demonstrate that interruption of functional behaviors (e.g., resting) in some cases coincides with high-level vessel noise. Two-thirds of the ship noise events were traceable by the AIS vessel tracking system, while one-third comprised vessels without AIS. 5.  This preliminary study demonstrates how concomitant long-term continuous broadband on-animal sound and movement recordings may be an important tool in future quantification of disturbance effects of anthropogenic activities at sea and assessment of long-term population impacts on pinnipeds.Publisher PDFPeer reviewe

A 2.6-gram sound and movement tag for studying the acoustic scene and kinematics of echolocating bats

This study was supported by the Carlsberg Foundation via a Semper Ardens grant, ONR, N00014-17-1- 2736; AFOSR FA9550-14-1-0398, and NSF NCS-FO:1734744 and a Human Frontiers Science Program Long-Term Fellowship to AS. These experiments were approved by The Danish Council for Experiments on Animals under permit number: 2016-15-0201-00989 and by the Johns Hopkins University Animal Care and Use Committee under protocol number BA17A107. We thank Uwe Firzlaff and Lutz Wiegrebe for their help.1. To study sensorimotor behaviour in wild animals, it is necessary to synchronously record the sensory inputs available to the animal, and its movements. To do this, we have developed a biologging device that can record the primary sensory information and the associated movements during foraging and navigating in echolocating bats. 2. This 2.6 -gram tag records the sonar calls and echoes from an ultrasonic microphone, while simultaneously sampling fine-scale movement in three dimensions from wideband accelerometers and magnetometers. In this study, we tested the tag on an European noctula (Nyctalus noctula) during target approaches and on four big brown bats (Eptesicus fuscus) during prey interception in a flight room. 3. We show that the tag records both the outgoing calls and echoes returning from objects at biologically relevant distances. Inertial sensor data enables the detection of behavioural events such as flying, turning, and resting. In addition, individual wing-beats can be tracked and synchronized to the bat's sound emissions to study the coordination of different motor events. 4. By recording the primary acoustic flow of bats concomitant with associated behaviours on a very fine time-scale, this type of biologging method will foster a deeper understanding of how sensory inputs guide feeding behaviours in the wild.PostprintPeer reviewe