The active space of sperm whale codas: inter-click information for intra-unit communication.

Sperm whales (Physeter macrocephalus) are social mega-predators who form stable matrilineal units that often associate within a larger vocal clan. Clan membership is defined by sharing a repertoire of coda types consisting of specific temporal spacings of multi-pulsed clicks. It has been hypothesized that codas communicate membership across socially segregated sympatric clans, but others propose that codas are primarily used for behavioral coordination and social cohesion within a closely spaced social unit. Here, we test these hypotheses by combining measures of ambient noise levels and coda click source levels with models of sound propagation to estimate the active space of coda communication. Coda clicks were localized off the island of Dominica with a four- or five-element 80 m vertical hydrophone array, allowing us to calculate the median RMS source levels of 1598 clicks from 444 codas to be 161 dB re. 1 µPa (IQR 153-167), placing codas among the most powerful communication sounds in toothed whales. However, together with measured ambient noise levels, these source levels lead to a median active space of coda communication of ∼4 km, reflecting the maximum footprint of a single foraging sperm whale unit. We conclude that while sperm whale codas may contain information about clan affiliation, their moderate active space shows that codas are not used for long range acoustic communication between units and clans, but likely serve to mediate social cohesion and behavioral transitions in intra-unit communication.

Large sensory volumes enable Southern elephant seals to exploit sparse deep-sea prey.

The ability of echolocating toothed whales to detect and classify prey at long ranges enables efficient searching and stalking of sparse prey in these time-limited dives. However, nonecholocating deep-diving seals such as elephant seals appear to have much less sensory advantage over their prey. Both elephant seals and their prey rely on visual and hydrodynamic cues that may be detectable only at short ranges in the deep ocean, leading us to hypothesize that elephant seals must adopt a less efficient reactive mode of hunting that requires high prey densities. To test that hypothesis, we deployed high-resolution sonar and movement tags on 25 females to record simultaneous predator and prey behavior during foraging interactions. We demonstrate that elephant seals have a sensory advantage over their prey that allows them to potentially detect prey 5 to 10 s before striking. The corresponding prey detection ranges of 7 to 17 m enable stealthy approaches and prey-specific capture tactics. In comparison, prey react at a median range of 0.7 m, close to the neck extension range of striking elephant seals. Estimated search swathes of 150 to 900 m2 explain how elephant seals can locate up to 2,000 prey while swimming more than 100 km per day. This efficient search capability allows elephant seals to subsist on prey densities that are consonant with the deep scattering layer resources estimated by hydroacoustic surveys but which are two orders of magnitude lower than the prey densities needed by a reactive hunter.

Cheap gulp foraging of a giga-predator enables efficient exploitation of sparse prey.

The giant rorqual whales are believed to have a massive food turnover driven by a high-intake lunge feeding style aptly described as the world's largest biomechanical action. This high-drag feeding behavior is thought to limit dive times and constrain rorquals to target only the densest prey patches, making them vulnerable to disturbance and habitat change. Using biologging tags to estimate energy expenditure as a function of feeding rates on 23 humpback whales, we show that lunge feeding is energetically cheap. Such inexpensive foraging means that rorquals are flexible in the quality of prey patches they exploit and therefore more resilient to environmental fluctuations and disturbance. As a consequence, the food turnover and hence the ecological role of these marine giants have likely been overestimated.

Echolocating bats prefer a high risk-high gain foraging strategy to increase prey profitability.

Predators that target multiple prey types are predicted to switch foraging modes according to prey profitability to increase energy returns in dynamic environments. Here, we use bat-borne tags and DNA metabarcoding of feces to test the hypothesis that greater mouse-eared bats make immediate foraging decisions based on prey profitability and changes in the environment. We show that these bats use two foraging strategies with similar average nightly captures of 25 small, aerial insects and 29 large, ground-dwelling insects per bat, but with much higher capture success in the air (76%) vs ground (30%). However, owing to the 3-20 times larger ground prey, 85% of the nightly food acquisition comes from ground prey despite the 2.5 times higher failure rates. We find that most bats use the same foraging strategy on a given night suggesting that bats adapt their hunting behavior to weather and ground conditions. We conclude that these bats use high risk-high gain gleaning of ground prey as a primary foraging tactic, but switch to aerial hunting when environmental changes reduce the profitability of ground prey, showing that prey switching matched to environmental dynamics plays a key role in covering the energy intake even in specialized predators.

Bats are the only mammals capable of powered flight and therefore need a high calorie intake to survive. They hunt at night using the echoes made by their own calls to navigate and locate prey. Bats can use different tactics to hunt for food: hawking involves catching prey on the wing and requires fast aerial manoeuvring and more intense echolocation calls, while gleaning involves listening for movements of ground and water dwelling prey as the bat hovers. Some bat species specialise as hawkers or gleaners but maintain the ability to hunt with both methods. With the ever-growing impact of human activities on their habitats, it is important to understand how adaptable bats feeding habits are to changes in their environment. To find out more, Stidsholt et al. studied greater mouse-eared bats, which primarily feed by gleaning. To understand how this species chooses feeding strategies they fitted bats with tiny backpacks that could record the animal's location and foraging behaviour. They could also monitor prey sizes by recording the sounds of the bats chewing. Stidsholt et al. found that, although these bats tried to catch prey on the ground more often than in the air, they were actually more successful as airborne hunters. Despite this, gleaning was still a more profitable strategy for them, because the body mass of ground prey is higher than for airborne prey. Gleaning gave the bats a higher calorie intake, even though their capture rate was lower. Although feeding habits differed slightly between individual bats on a given night of monitoring, there were much larger changes in behaviour between different feeding nights. This shows that, although this species of bat prefers gleaning, they will switch strategies to hawking as their environment changes, for example if there is more airborne prey, or if rainfall makes it hard to hear movements on the ground. Bats tended to get enough calories for their needs but did not catch more prey than they needed to survive. Stidsholt et al. concluded that greater mouse-eared bats change their feeding strategy based on prey availability and size, as well as the bat's environment. Their study provides an important insight into how bats fit into the ecosystem and how adaptable bats might be to changes in their habitat.

Vessel noise exposures of harbour seals from the Wadden Sea.

The North Sea faces intense ship traffic owing to increasing human activities at sea. As harbour seals (Phoca vitulina) are abundant top predators in the North Sea, it is hypothesised that they experience repeated, high-amplitude vessel exposures. Here, we test this hypothesis by quantifying vessel noise exposures from deployments of long-term sound and movement tags (DTAGs) on nine harbour seals from the Wadden Sea. An automated tool was developed to detect intervals of elevated noise in the sound recordings. An assessment by multiple raters was performed to classify the source as either vessels or other sounds. A total of 133 vessel passes were identified with received levels > 97 dB re 1µPa RMS in the 2 kHz decidecade band and with ambient noise > 6 dB below this detection threshold. Tagged seals spent most of their time within Marine Protected Areas (89 ± 13%, mean ± SD) and were exposed to high-amplitude vessel passes 4.3 ± 1.6 times per day. Only 32% of vessel passes were plausibly associated with an AIS-registered vessel. We conclude that seals in industrialized waters are exposed repeatedly to vessel noise, even in areas designated as protected, and that exposures are poorly predicted by AIS data.

Toothed whales use distinct vocal registers for echolocation and communication.

Echolocating toothed whales (odontocetes) capture fast-moving prey in dark marine environments, which critically depends on their ability to generate powerful, ultrasonic clicks. How their supposedly air-driven sound source can produce biosonar clicks at depths of >1000 meters, while also producing rich vocal repertoires to mediate complex social communication, remains unknown. We show that odontocetes possess a sound production system based on air driven through nasal passages that is functionally analogous to laryngeal and syringeal sound production. Tissue vibration in different registers produces distinct echolocation and communication signals across all major odontocete clades, and thus provides a physiological basis for classifying their vocal repertoires. The vocal fry register is used by species from porpoises to sperm whales for generating powerful, highly air-efficient echolocation clicks.

3D visualization processes for recreating and studying organismal form.

The study of biological form is a vital goal of evolutionary biology and functional morphology. We review an emerging set of methods that allow scientists to create and study accurate 3D models of living organisms and animate those models for biomechanical and fluid dynamic analyses. The methods for creating such models include 3D photogrammetry, laser and CT scanning, and 3D software. New multi-camera devices can be used to create accurate 3D models of living animals in the wild and captivity. New websites and virtual reality/augmented reality devices now enable the visualization and sharing of these data. We provide examples of these approaches for animals ranging from large whales to lizards and show applications for several areas: Natural history collections; body condition/scaling, bioinspired robotics, computational fluids dynamics (CFD), machine learning, and education. We provide two datasets to demonstrate the efficacy of CFD and machine learning approaches and conclude with a prospectus.

Key questions in marine mammal bioenergetics.

Bioenergetic approaches are increasingly used to understand how marine mammal populations could be affected by a changing and disturbed aquatic environment. There remain considerable gaps in our knowledge of marine mammal bioenergetics, which hinder the application of bioenergetic studies to inform policy decisions. We conducted a priority-setting exercise to identify high-priority unanswered questions in marine mammal bioenergetics, with an emphasis on questions relevant to conservation and management. Electronic communication and a virtual workshop were used to solicit and collate potential research questions from the marine mammal bioenergetic community. From a final list of 39 questions, 11 were identified as 'key' questions because they received votes from at least 50% of survey participants. Key questions included those related to energy intake (prey landscapes, exposure to human activities) and expenditure (field metabolic rate, exposure to human activities, lactation, time-activity budgets), energy allocation priorities, metrics of body condition and relationships with survival and reproductive success and extrapolation of data from one species to another. Existing tools to address key questions include labelled water, animal-borne sensors, mark-resight data from long-term research programs, environmental DNA and unmanned vehicles. Further validation of existing approaches and development of new methodologies are needed to comprehensively address some key questions, particularly for cetaceans. The identification of these key questions can provide a guiding framework to set research priorities, which ultimately may yield more accurate information to inform policies and better conserve marine mammal populations.

Thresholds for noise induced hearing loss in harbor porpoises and phocid seals.

Intense sound sources, such as pile driving, airguns, and military sonars, have the potential to inflict hearing loss in marine mammals and are, therefore, regulated in many countries. The most recent criteria for noise induced hearing loss are based on empirical data collected until 2015 and recommend frequency-weighted and species group-specific thresholds to predict the onset of temporary threshold shift (TTS). Here, evidence made available after 2015 in light of the current criteria for two functional hearing groups is reviewed. For impulsive sounds (from pile driving and air guns), there is strong support for the current threshold for very high frequency cetaceans, including harbor porpoises (Phocoena phocoena). Less strong support also exists for the threshold for phocid seals in water, including harbor seals (Phoca vitulina). For non-impulsive sounds, there is good correspondence between exposure functions and empirical thresholds below 10 kHz for porpoises (applicable to assessment and regulation of military sonars) and between 3 and 16 kHz for seals. Above 10 kHz for porpoises and outside of the range 3-16 kHz for seals, there are substantial differences (up to 35 dB) between the predicted thresholds for TTS and empirical results. These discrepancies call for further studies.

Sowerby's beaked whale biosonar and movement strategy indicate deep-sea foraging niche differentiation in mesoplodont whales.

Closely related species are expected to diverge in foraging strategy, reflecting the evolutionary drive to optimize foraging performance. The most speciose cetacean genus, Mesoplodon, comprises beaked whales with little diversity in external morphology or diet, and overlapping distributions. Moreover, the few studied species of beaked whales (Ziphiidae) show very similar foraging styles with slow, energy-conserving movement during long, deep foraging dives. This raises the question of what factors drive their speciation. Using data from animal-attached tags and aerial imagery, we tested the hypothesis that two similar-sized mesoplodonts, Sowerby's (Mesoplodon bidens) and Blainville's (Mesoplodon densirostris) beaked whales, exploit a similar low-energy niche. We show that, compared with the low-energy strategist Blainville's beaked whale, Sowerby's beaked whale lives in the fast lane. While targeting a similar mesopelagic/bathypelagic foraging zone, they consistently swim and hunt faster, perform shorter deep dives, and echolocate at a faster rate with higher frequency clicks. Further, extensive near-surface travel between deep dives challenges the interpretation of beaked whale shallow inter-foraging dives as a management strategy for decompression sickness. The distinctively higher frequency echolocation clicks do not hold apparent foraging benefits. Instead, we argue that a high-speed foraging style influences dive duration and echolocation behaviour, enabling access to a distinct prey population. Our results demonstrate that beaked whales exploit a broader diversity of deep-sea foraging and energetic niches than hitherto suspected. The marked deviation of Sowerby's beaked whales from the typical ziphiid foraging strategy has potential implications for their response to anthropogenic sounds, which appears to be strongly behaviourally driven in other ziphiids.

High heart rates in hunting harbour porpoises.

The impressive breath-hold capabilities of marine mammals are facilitated by both enhanced O2 stores and reductions in the rate of O2 consumption via peripheral vasoconstriction and bradycardia, called the dive response. Many studies have focused on the extreme role of the dive response in maximizing dive duration in marine mammals, but few have addressed how these adjustments may compromise the capability to hunt, digest and thermoregulate during routine dives. Here, we use DTAGs, which record heart rate together with foraging and movement behaviour, to investigate how O2 management is balanced between the need to dive and forage in five wild harbour porpoises that hunt thousands of small prey daily during continuous shallow diving. Dive heart rates were moderate (median minimum 47-69 bpm) and relatively stable across dive types, dive duration (0.5-3.3 min) and activity. A moderate dive response, allowing for some perfusion of peripheral tissues, may be essential for fuelling the high field metabolic rates required to maintain body temperature and support digestion during diving in these small, continuously feeding cetaceans. Thus, despite having the capacity to prolong dives via a strong dive response, for these shallow-diving cetaceans, it appears to be more efficient to maintain circulation while diving: extreme heart rate gymnastics are for deep dives and emergencies, not everyday use.

Echolocating toothed whales use ultra-fast echo-kinetic responses to track evasive prey.

Visual predators rely on fast-acting optokinetic responses to track and capture agile prey. Most toothed whales, however, rely on echolocation for hunting and have converged on biosonar clicking rates reaching 500/s during prey pursuits. If echoes are processed on a click-by-click basis, as assumed, neural responses 100× faster than those in vision are required to keep pace with this information flow. Using high-resolution biologging of wild predator-prey interactions, we show that toothed whales adjust clicking rates to track prey movement within 50-200 ms of prey escape responses. Hypothesising that these stereotyped biosonar adjustments are elicited by sudden prey accelerations, we measured echo-kinetic responses from trained harbour porpoises to a moving target and found similar latencies. High biosonar sampling rates are, therefore, not supported by extreme speeds of neural processing and muscular responses. Instead, the neurokinetic response times in echolocation are similar to those of tracking responses in vision, suggesting a common neural underpinning.

In the animal world, split-second decisions determine whether a predator eats, or its prey survives. There is a strong evolutionary advantage to fast reacting brains and bodies. For example, the eye muscles of hunting cheetahs must lock on to a gazelle and keep track of it, no matter how quickly or unpredictably it moves. In fact, in monkeys and primates, these muscles can react to sudden movements in as little as 50 milliseconds ­ faster than the blink of an eye. But what about animals that do not rely on vision to hunt? To find food at night or in the deep ocean, whales and porpoises make short ultrasonic sounds, or 'clicks', and then listen for returning echoes. As they close in on a prey, they need to click faster to get quicker updates on its location. What is unclear is how fast they react to the echoes. Just before a kill, a harbour porpoise can click over 500 times a second: if they wait for the echo from one click before making the next one, they would need responses 100 times faster than human eyes. Exploring this topic is difficult, as it requires tracking predator and prey at the same time. Vance et al. took up the challenge by building sound and movement recorders that attach to whales with suction cups. These were used on two different hunters: deep-diving beaked whales and shallow-hunting harbour porpoises. Both species adapted their click rate depending on how far they were from their prey, but their response times were similar to visual responses in monkeys and humans. This means that whales and porpoises do not act on each echo before clicking again: instead, they respond to groups of tens of clicks at a time. This suggests that their brains may be wired in much the same way as the ones of visual animals. In the ocean, increased human activity creates a dangerous noise pollution that disrupts the delicate hunting mechanism of whales and porpoises. Better understanding how these animals find their food may therefore help conservation efforts.

Inflight head stabilization associated with wingbeat cycle and sonar emissions in the lingual echolocating Egyptian fruit bat, Rousettus aegyptiacus.

Sensory processing of environmental stimuli is challenged by head movements that perturb sensorimotor coordinate frames directing behaviors. In the case of visually guided behaviors, visual gaze stabilization results from the integrated activity of the vestibuloocular reflex and motor efference copy originating within circuits driving locomotor behavior. In the present investigation, it was hypothesized that head stabilization is broadly implemented in echolocating bats during sustained flight, and is temporally associated with emitted sonar signals which would optimize acoustic gaze. Predictions from these hypotheses were evaluated by measuring head and body kinematics with motion sensors attached to the head and body of free-flying Egyptian fruit bats. These devices were integrated with ultrasonic microphones to record sonar emissions and elucidate the temporal association with periods of head stabilization. Head accelerations in the Earth-vertical axis were asymmetric with respect to wing downstroke and upstroke relative to body accelerations. This indicated that inflight head and body accelerations were uncoupled, outcomes consistent with the mechanisms that limit vertical head acceleration during wing downstroke. Furthermore, sonar emissions during stable flight occurred most often during wing downstroke and head stabilization, supporting the conclusion that head stabilization behavior optimized sonar gaze and environmental interrogation via echolocation.

Wild bats briefly decouple sound production from wingbeats to increase sensory flow during prey captures.

Active sensing animals such as echolocating bats produce the energy with which they probe their environment. The intense echolocation calls of bats are energetically expensive, but their cost can be reduced by synchronizing the exhalations needed to vocalize to wingbeats. Here, we use sound-and-movement recording tags to investigate how wild bats balance efficient sound production with information needs during foraging and navigation. We show that wild bats prioritize energy efficiency over sensory flow when periodic snapshots of the acoustic scene are sufficient during travel and search. Rapid calls during tracking and interception of close prey are decoupled from the wingbeat but are weaker and comprise <2% of all calls during a night of hunting. The limited use of fast sonar sampling provides bats with high information update rates during critical hunting moments but adds little to their overall costs of sound production despite the inefficiency of decoupling calls from wingbeats.

Directional biosonar beams allow echolocating harbour porpoises to actively discriminate and intercept closely spaced targets.

Echolocating toothed whales face the problem that high sound speeds in water mean that echoes from closely spaced targets will arrive at time delays within their reported auditory integration time of some 264 µs. Here, we test the hypothesis that echolocating harbour porpoises cannot resolve and discriminate targets within a clutter interference zone given by their integration time. To do this, we trained two harbour porpoises (Phocoena phocoena) to actively approach and choose between two spherical targets at four varying inter-target distances (13.5, 27, 56 and 108 cm) in a two-alternative forced-choice task. The free-swimming, blindfolded porpoises were tagged with a sound and movement tag (DTAG4) to record their echoic scene and acoustic outputs. The known ranges between targets and the porpoise, combined with the sound levels received on target-mounted hydrophones revealed how the porpoises controlled their acoustic gaze. When targets were close together, the discrimination task was more difficult because of smaller echo time delays and lower echo level ratios between the targets. Under these conditions, buzzes were longer and started from farther away, source levels were reduced at short ranges, and the porpoises clicked faster, scanned across the targets more, and delayed making their discrimination decision until closer to the target. We conclude that harbour porpoises can resolve and discriminate closely spaced targets, suggesting a clutter rejection zone much shorter than their auditory integration time, and that such clutter rejection is greatly aided by spatial filtering with their directional biosonar beam.

Heart rate and startle responses in diving, captive harbour porpoises (Phocoena phocoena) exposed to transient noise and sonar.

Anthropogenic noise can alter marine mammal behaviour and physiology, but little is known about cetacean cardiovascular responses to exposures, despite evidence that acoustic stressors, such as naval sonars, may lead to decompression sickness. Here, we measured heart rate and movements of two trained harbour porpoises during controlled exposure to 6-9 kHz sonar-like sweeps and 40 kHz peak-frequency noise pulses, designed to evoke acoustic startle responses. The porpoises initially responded to the sonar sweep with intensified bradycardia despite unaltered behaviour/movement, but habituated rapidly to the stimuli. In contrast, 40 kHz noise pulses consistently evoked rapid muscle flinches (indicative of startles), but no behavioural or heart rate changes. We conclude that the autonomous startle response appears decoupled from, or overridden by, cardiac regulation in diving porpoises, whereas certain novel stimuli may motivate oxygen-conserving cardiovascular measures. Such responses to sound exposure may contribute to gas mismanagement for deeper-diving cetaceans.

Deep-diving beaked whales dive together but forage apart.

Echolocating animals that forage in social groups can potentially benefit from eavesdropping on other group members, cooperative foraging or social defence, but may also face problems of acoustic interference and intra-group competition for prey. Here, we investigate these potential trade-offs of sociality for extreme deep-diving Blainville's and Cuvier's beaked whales. These species perform highly synchronous group dives as a presumed predator-avoidance behaviour, but the benefits and costs of this on foraging have not been investigated. We show that group members could hear their companions for a median of at least 91% of the vocal foraging phase of their dives. This enables whales to coordinate their mean travel direction despite differing individual headings as they pursue prey on a minute-by-minute basis. While beaked whales coordinate their echolocation-based foraging periods tightly, individual click and buzz rates are both independent of the number of whales in the group. Thus, their foraging performance is not affected by intra-group competition or interference from group members, and they do not seem to capitalize directly on eavesdropping on the echoes produced by the echolocation clicks of their companions. We conclude that the close diving and vocal synchronization of beaked whale groups that quantitatively reduces predation risk has little impact on foraging performance.

Toothed whale auditory brainstem responses measured with a non-invasive, on-animal tag.

Empirical measurements of odontocete hearing are limited to captive individuals, constituting a fraction of species across the suborder. Data from more species could be available if such measurements were collected from unrestrained animals in the wild. This study investigated whether electrophysiological hearing data could be recorded from a trained harbor porpoise (Phocoena phocoena) using a non-invasive, animal-attached tag. The results demonstrate that auditory brainstem responses to external and self-generated stimuli can be measured from a stationary odontocete using an animal-attached recorder. With additional development, tag-based electrophysiological platforms may facilitate the collection of hearing data from freely swimming odontocetes in the wild.

How loud is the underwater noise from operating offshore wind turbines?

Offshore wind turbines are increasingly abundant sources of underwater low frequency noise. This increase raises concern for the cumulative contribution of wind farms to the underwater soundscape and possible impact on marine ecosystems. Here, available measurements of underwater noise from different wind turbines during operation are reviewed to show that source levels are at least 10-20 dB lower than ship noise in the same frequency range. The most important factor explaining the measured sound pressure levels from wind turbines is distance to the turbines with smaller effects of wind speed and turbine size. A simple multi-turbine model demonstrates that cumulative noise levels could be elevated up to a few kilometres from a wind farm under very low ambient noise conditions. In contrast, the noise is well below ambient levels unless it is very close to the individual turbines in locations with high ambient noise from shipping or high wind speeds. The rapid increase in the number and size of offshore wind farms means that the cumulative contribution from the many turbines may be considerable and should be included in assessments for maritime spatial planning purposes as well and environmental impact assessments of individual projects.

High resolution three-dimensional beam radiation pattern of harbour porpoise clicks with implications for passive acoustic monitoring.

The source properties and radiation patterns of animal vocalisations define, along with propagation and noise conditions, the active space in which these vocalisations can be detected by conspecifics, predators, prey, and by passive acoustic monitoring (PAM). This study reports the 4π (360° horizontal and vertical) beam profile of a free-swimming, trained harbour porpoise measured using a 27-element hydrophone array. The forward echolocation beam is highly directional, as predicted by a piston model, and is consistent with previous measurements. However, at off-axis angles greater than ±30°, the beam attenuates more rapidly than the piston model and no side lobes are present. A diffuse back beam is also present with levels about -30 dB relative to the source level. In PAM, up to 50% of detections can be from portions of the beam profile with distorted click spectra, although this drops substantially for higher detection thresholds. Simulations of the probability of acoustically detecting a harbour porpoise show that a traditional piston model can underestimate the probability of detection compared to the actual three-dimensional radiation pattern documented here. This highlights the importance of empirical 4π measurements of beam profiles of toothed whales, both to improve understanding of toothed whale biology and to inform PAM.