Danuta Maria Wisniewska

Single source sound production and dynamic beam formation in echolocating harbour porpoises (Phocoena phocoena)

SUMMARY Echolocating toothed whales produce high-powered clicks by pneumatic actuation of phonic lips in their nasal complexes. All non-physeteroid toothed whales have two pairs of phonic lips allowing many of these species to produce both whistles and clicks at the same time. That has led to the hypothesis that toothed whales can increase the power outputs and bandwidths of clicks, and enable fast clicking and beam steering by acutely timed actuation of both phonic lip pairs simultaneously. Here we test that hypothesis by applying suction cup hydrophones on the sound-producing nasal complexes of three echolocating porpoises (Phocoena phocoena) with symmetrical pairs of phonic lips. Using time of arrival differences on three hydrophones, we show that all recorded clicks from these three porpoises are produced by the right pair of phonic lips with no evidence of simultaneous or independent actuation of the left pair. It is demonstrated that porpoises, despite actuation of only one sound source, can change their output and sound beam probably through conformation changes in the sound-producing soft tissues and nasal sacs, and that the coupling of the phonic lips and the melon acts as a waveguide for sound energy between 100 and 160 kHz to generate a forward-directed sound beam for echolocation.

What a jerk: prey engulfment revealed by high-rate, super-cranial accelerometry on a harbour seal (Phoca vitulina)

A key component in understanding the ecological role of marine mammal predators is to identify how and where they capture prey in time and space. Satellite and archival tags on pinnipeds generally only provide diving and position information, and foraging is often inferred to take place in particular shaped dives or when the animal remains in an area for an extended interval. However, fast movements of the head and jaws may provide reliable feeding cues that can be detected by small low-power accelerometers mounted on the head. To test this notion, a harbour seal (Phoca vitulina) was trained to wear an OpenTag (sampling at 200 or 333 Hz with ±2 or ±16 g clipping) on its head while catching fish prey in front of four underwater digital high-speed video cameras. We show that both raptorial and suction feeding generate jerk (i.e. differential of acceleration) signatures with maximum peak values exceeding 1000 m s−3. We conclude that reliable prey capture cues can be derived from fast-sampling, head-mounted accelerometer tags, thus holding a promising potential for long-term studies of foraging ecology and field energetics of aquatic predators in their natural environments.

Acoustic gaze adjustments during active target selection in echolocating porpoises

SUMMARY Visually dominant animals use gaze adjustments to organize perceptual inputs for cognitive processing. Thereby they manage the massive sensory load from complex and noisy scenes. Echolocation, as an active sensory system, may provide more opportunities to control such information flow by adjusting the properties of the sound source. However, most studies of toothed whale echolocation have involved stationed animals in static auditory scenes for which dynamic information control is unnecessary. To mimic conditions in the wild, we designed an experiment with captive, free-swimming harbor porpoises tasked with discriminating between two hydrophone-equipped targets and closing in on the selected target; this allowed us to gain insight into how porpoises adjust their acoustic gaze in a multi-target dynamic scene. By means of synchronized cameras, an acoustic tag and on-target hydrophone recordings we demonstrate that porpoises employ both beam direction control and range-dependent changes in output levels and pulse intervals to accommodate their changing spatial relationship with objects of immediate interest. We further show that, when switching attention to another target, porpoises can set their depth of gaze accurately for the new target location. In combination, these observations imply that porpoises exert precise vocal-motor control that is tied to spatial perception akin to visual accommodation. Finally, we demonstrate that at short target ranges porpoises narrow their depth of gaze dramatically by adjusting their output so as to focus on a single target. This suggests that echolocating porpoises switch from a deliberative mode of sensorimotor operation to a reactive mode when they are close to a target.

Nasal sound production in echolocating delphinids (Tursiops truncatus and Pseudorca crassidens) is dynamic, but unilateral: clicking on the right side and whistling on the left side

SUMMARY Toothed whales produce sound in their nasal complex by pneumatic actuation of phonic lip pairs within the blowhole. It has been hypothesized that dual actuation of the phonic lip pairs can generate two pulses that merge to form a single echolocation click with a higher source level, broader bandwidth and larger potential for beam steering than if produced by a single pair of phonic lips. Here, we test that hypothesis by measuring the sound production of five echolocating delphinids using hydrophones around the animals and imbedded in on-animal suction cups. We show that the studied animals click with their right pair of phonic lips and whistle with their left pair. We demonstrate that, with just a single pair of phonic lips, they can change the click energy levels over five orders of magnitude, change the click centroid frequencies over more than two octaves, and modulate the sound radiation from the melon for beam steering. We conclude that all of the click dynamics ascribed to dual actuation of two phonic lip pairs can be achieved with actuation of just the right pair of phonic lips, and we propose that the large dynamic range of source outputs is achieved by highly controlled modulation of the pneumatic driving pressure, the tension of the phonic lip labia and the conformation of the fatty melon and associated air sacs.

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. DOI: http://dx.doi.org/10.7554/eLife.05651.001

Buzzing during biosonar-based interception of prey in the delphinids Tursiops truncatus and Pseudorca crassidens

Echolocating bats and toothed whales probe their environment with ultrasonic sound pulses, using returning echoes to navigate and find prey in a process that appears to have resulted from a remarkable convergence of the two taxa. Here, we report the first detailed quantification of echolocation behaviour during prey capture in the most studied delphinid species, a false killer whale and a bottlenose dolphin. Using acoustic DTAGs, we demonstrate that just prior to prey interception these delphinids change their acoustic gaze dramatically by reducing inter-click intervals and output >10-fold in a high repetition rate, low output buzz. Buzz click rates of 250–500 Hz for large but agile animals suggest that sampling rates during capture are scaled with the whales manoeuvrability. These observations support the growing notion that fast sonar sampling accompanied by a low output level is critical for high rate feedback to inform motor patterns during prey interception in all echolocating toothed whales.

High rates of vessel noise disrupt foraging in wild harbour porpoises (Phocoena phocoena)

Shipping is the dominant marine anthropogenic noise source in the worlds oceans, yet we know little about vessel encounter rates, exposure levels and behavioural reactions for cetaceans in the wild, many of which rely on sound for foraging, communication and social interactions. Here, we used animal-borne acoustic tags to measure vessel noise exposure and foraging efforts in seven harbour porpoises in highly trafficked coastal waters. Tagged porpoises encountered vessel noise 17–89% of the time and occasional high-noise levels coincided with vigorous fluking, bottom diving, interrupted foraging and even cessation of echolocation, leading to significantly fewer prey capture attempts at received levels greater than 96 dB re 1 µPa (16 kHz third-octave). If such exposures occur frequently, porpoises, which have high metabolic requirements, may be unable to compensate energetically with negative long-term fitness consequences. That shipping noise disrupts foraging in the high-frequency-hearing porpoise raises concerns that other toothed whale species may also be affected.

Sperm whale codas may encode individuality as well as clan identity

Sperm whales produce codas for communication that can be grouped into different types according to their temporal patterns. Codas have led researchers to propose that sperm whales belong to distinct cultural clans, but it is presently unclear if they also convey individual information. Coda clicks comprise a series of pulses and the delay between pulses is a function of organ size, and therefore body size, and so is one potential source of individual information. Another potential individual-specific parameter could be the inter-click intervals within codas. To test whether these parameters provide reliable individual cues, stereo-hydrophone acoustic tags (Dtags) were attached to five sperm whales of the Azores, recording a total of 802 codas. A discriminant function analysis was used to distinguish 288 5 Regular codas from four of the sperm whales and 183 3 Regular codas from two sperm whales. The results suggest that codas have consistent individual features in their inter-click intervals and inter-pulse intervals which may contribute to individual identification. Additionally, two whales produced different coda types in distinct foraging dive phases. Codas may therefore be used by sperm whales to convey information of identity as well as activity within a social group to a larger extent than previously assumed.

Response to ‘Biosonar sources in odontocetes: considering structure and function’

If we knew how all 73 species produce sound, it would be a conclusion and not a hypothesis: a hypothesis is a fundamental part of experimental biology where a general mechanism is proposed from a limited data set at hand, and then subsequently tested through falsification attempts in future

Click communication in wild harbour porpoises ( Phocoena phocoena )

Social delphinids employ a vocal repertoire of clicks for echolocation and whistles for communication. Conversely, the less social and acoustically cryptic harbour porpoises (Phocoena phocoena) only produce narrow-band high-frequency (NBHF) clicks with properties that appear poorly suited for communication. Nevertheless, these small odontocetes likely mediate social interactions, such as mate choice and mother-calf contact, with sound. Here, we deployed six tags (DTAG3) on wild porpoises in Danish waters for a total of 96 hours to investigate if the patterns and use of stereotyped NBHF click trains are consistent with a communication function. We show that wild porpoises produce frequent (up to 27