Latencies of click-evoked auditory responses in a harbor porpoise exceed the time interval between subsequent echolocation clicks.

Most auditory evoked potential (AEP) studies in echolocating toothed whales measure neural responses to outgoing clicks and returning echoes using short-latency auditory brainstem responses (ABRs) arising a few ms after acoustic stimuli. However, little is known about longer-latency cortical AEPs despite their relevance for understanding echo processing and auditory stream segregation. Here, we used a non-invasive AEP setup with low click repetition rates on a trained harbor porpoise to test the long-standing hypothesis that echo information from distant targets is completely processed before the next click is emitted. We reject this hypothesis by finding reliable click-related AEP peaks with latencies of 90 and 160 ms, which are longer than 99% of click intervals used by echolocating porpoises, demonstrating that some higher-order echo processing continues well after the next click emission even during slow clicking. We propose that some of the echo information, such as range to evasive prey, is used to guide vocal-motor responses within 50-100 ms, but that information used for discrimination and auditory scene analysis is processed more slowly, integrating information over many click-echo pairs. We conclude by showing theoretically that the identified long-latency AEPs may enable hearing sensitivity measurements at frequencies ten times lower than current ABR methods.

Comparison of the marine soundscape before and during the COVID-19 pandemic in dolphin habitat in Sarasota Bay, FL.

During the COVID-19 pandemic, changes in vessel activity and associated noise have been reported globally. Sarasota Bay is home to a large and increasing number of recreational vessels as well as a long-term resident community of bottlenose dolphins, Tursiops truncatus. Data were analyzed from two hydrophones to compare the soundscape during the COVID-19 pandemic to previous years (March-May 2020 and 2018/2019). Hourly metrics were calculated: vessel passes, 95th percentile sound levels [125 Hz and 16 kHz third octave bands (TOBs), and two broader bands: 88-1122 Hz and 1781-17 959 Hz], and dolphin whistle detection to understand changes in vessel activity and the effect on wildlife. Vessel activity increased during COVID-19 restrictions by almost 80% at one site and remained the same at the other site. Of the four sound level measures, only the 125 Hz TOB and 88-1122 Hz band increased with vessel activity at both sites, suggesting that these may be appropriate measures of noise from rapid pass-bys of small vessels in very shallow (<10 m) habitats. Dolphin whistle detection decreased during COVID-19 restrictions at one site but remained the same at the site that experienced increased vessel activity. The results suggest that pandemic effects on wildlife should not be viewed as homogeneous globally.

Modeling potential masking of echolocating sperm whales exposed to continuous 1-2 kHz naval sonar.

Modern active sonar systems can (almost) continuously transmit and receive sound, which can lead to more masking of important sounds for marine mammals than conventional pulsed sonar systems transmitting at a much lower duty cycle. This study investigated the potential of 1-2 kHz active sonar to mask echolocation-based foraging of sperm whales by modeling their echolocation detection process. Continuous masking for an echolocating sperm whale facing a sonar was predicted for sonar sound pressure levels of 160 dB re 1 µPa2, with intermittent masking at levels of 120 dB re 1 µPa2, but model predictions strongly depended on the animal orientation, harmonic content of the sonar, click source level, and target strength of the prey. The masking model predicted lower masking potential of buzz clicks compared to regular clicks, even though the energy source level is much lower. For buzz clicks, the lower source level is compensated for by the reduced two-way propagation loss to nearby prey during buzzes. These results help to predict what types of behavioral changes could indicate masking in the wild. Several key knowledge gaps related to masking potential of sonar in echolocating odontocetes were identified that require further investigation to assess the significance of masking.

Why whales are big but not bigger: Physiological drivers and ecological limits in the age of ocean giants.

The largest animals are marine filter feeders, but the underlying mechanism of their large size remains unexplained. We measured feeding performance and prey quality to demonstrate how whale gigantism is driven by the interplay of prey abundance and harvesting mechanisms that increase prey capture rates and energy intake. The foraging efficiency of toothed whales that feed on single prey is constrained by the abundance of large prey, whereas filter-feeding baleen whales seasonally exploit vast swarms of small prey at high efficiencies. Given temporally and spatially aggregated prey, filter feeding provides an evolutionary pathway to extremes in body size that are not available to lineages that must feed on one prey at a time. Maximum size in filter feeders is likely constrained by prey availability across space and time.

Discrimination of fast click-series produced by tagged Risso's dolphins (Grampus griseus) for echolocation or communication.

Early studies that categorized odontocete pulsed sounds had few means of discriminating signals used for biosonar-based foraging from those used for communication. This capability to identify the function of sounds is important for understanding and interpreting behavior; it is also essential for monitoring and mitigating potential disturbance from human activities. Archival tags were placed on free-ranging Grampus griseus to quantify and discriminate between pulsed sounds used for echolocation-based foraging and those used for communication. Two types of rapid click-series pulsed sounds, buzzes and burst pulses, were identified as produced by the tagged dolphins and classified using a Gaussian mixture model based on their duration, association with jerk (i.e. rapid change of acceleration) and temporal association with click trains. Buzzes followed regular echolocation clicks and coincided with a strong jerk signal from accelerometers on the tag. They consisted of series averaging 359±210 clicks (mean±s.d.) with an increasing repetition rate and relatively low amplitude. Burst pulses consisted of relatively short click series averaging 45±54 clicks with decreasing repetition rate and longer inter-click interval that were less likely to be associated with regular echolocation and the jerk signal. These results suggest that the longer, relatively lower amplitude, jerk-associated buzzes are used in this species to capture prey, mostly during the bottom phase of foraging dives, as seen in other odontocetes. In contrast, the shorter, isolated burst pulses that are generally emitted by the dolphins while at or near the surface are used outside of a direct, known foraging context.

First indications that northern bottlenose whales are sensitive to behavioural disturbance from anthropogenic noise.

Although northern bottlenose whales were the most heavily hunted beaked whale, we have little information about this species in its remote habitat of the North Atlantic Ocean. Underwater anthropogenic noise and disruption of their natural habitat may be major threats, given the sensitivity of other beaked whales to such noise disturbance. We attached dataloggers to 13 northern bottlenose whales and compared their natural sounds and movements to those of one individual exposed to escalating levels of 1-2 kHz upsweep naval sonar signals. At a received sound pressure level (SPL) of 98 dB re 1 µPa, the whale turned to approach the sound source, but at a received SPL of 107 dB re 1 µPa, the whale began moving in an unusually straight course and then made a near 180° turn away from the source, and performed the longest and deepest dive (94 min, 2339 m) recorded for this species. Animal movement parameters differed significantly from baseline for more than 7 h until the tag fell off 33-36 km away. No clicks were emitted during the response period, indicating cessation of normal echolocation-based foraging. A sharp decline in both acoustic and visual detections of conspecifics after exposure suggests other whales in the area responded similarly. Though more data are needed, our results indicate high sensitivity of this species to acoustic disturbance, with consequent risk from marine industrialization and naval activity.

Using accelerometers to determine the calling behavior of tagged baleen whales.

Low-frequency acoustic signals generated by baleen whales can propagate over vast distances, making the assignment of calls to specific individuals problematic. Here, we report the novel use of acoustic recording tags equipped with high-resolution accelerometers to detect vibrations from the surface of two tagged fin whales that directly match the timing of recorded acoustic signals. A tag deployed on a buoy in the vicinity of calling fin whales and a recording from a tag that had just fallen off a whale were able to detect calls acoustically but did not record corresponding accelerometer signals that were measured on calling individuals. Across the hundreds of calls measured on two tagged fin whales, the accelerometer response was generally anisotropic across all three axes, appeared to depend on tag placement and increased with the level of received sound. These data demonstrate that high-sample rate accelerometry can provide important insights into the acoustic behavior of baleen whales that communicate at low frequencies. This method helps identify vocalizing whales, which in turn enables the quantification of call rates, a fundamental component of models used to estimate baleen whale abundance and distribution from passive acoustic monitoring.

High thresholds for avoidance of sonar by free-ranging long-finned pilot whales (Globicephala melas).

The potential effects of exposing marine mammals to military sonar is a current concern. Dose-response relationships are useful for predicting potential environmental impacts of specific operations. To reveal behavioral response thresholds of exposure to sonar, we conducted 18 exposure/control approaches to 6 long-finned pilot whales. Source level and proximity of sonar transmitting one of two frequency bands (1-2 kHz and 6-7 kHz) were increased during exposure sessions. The 2-dimensional movement tracks were analyzed using a changepoint method to identify the avoidance response thresholds which were used to estimate dose-response relationships. No support for an effect of sonar frequency or previous exposures on the probability of response was found. Estimated response thresholds at which 50% of population show avoidance (SPLmax=170 dB re 1 µPa, SELcum=173 dB re 1 µPa(2) s) were higher than previously found for other cetaceans. The US Navy currently uses a generic dose-response relationship to predict the responses of cetaceans to naval active sonar, which has been found to underestimate behavioural impacts on killer whales and beaked whales. The navy curve appears to match more closely our results with long-finned pilot whales, though it might underestimate the probability of avoidance for pilot-whales at long distances from sonar sources.

Changes in dive behavior during naval sonar exposure in killer whales, long-finned pilot whales, and sperm whales.

Anthropogenic underwater sound in the environment might potentially affect the behavior of marine mammals enough to have an impact on their reproduction and survival. Diving behavior of four killer whales (Orcinus orca), seven long-finned pilot whales (Globicephala melas), and four sperm whales (Physeter macrocephalus) was studied during controlled exposures to naval sonar [low frequency active sonar (LFAS): 1-2 kHz and mid frequency active sonar (MFAS): 6-7 kHz] during three field seasons (2006-2009). Diving behavior was monitored before, during and after sonar exposure using an archival tag placed on the animal with suction cups. The tag recorded the animal's vertical movement, and additional data on horizontal movement and vocalizations were used to determine behavioral modes. Killer whales that were conducting deep dives at sonar onset changed abruptly to shallow diving (ShD) during LFAS, while killer whales conducting deep dives at the onset of MFAS did not alter dive mode. When in ShD mode at sonar onset, killer whales did not change their diving behavior. Pilot and sperm whales performed normal deep dives (NDD) during MFAS exposure. During LFAS exposures, long-finned pilot whales mostly performed fewer deep dives and some sperm whales performed shallower and shorter dives. Acoustic recording data presented previously indicates that deep diving (DD) is associated with feeding. Therefore, the observed changes in dive behavior of the three species could potentially reduce the foraging efficiency of the affected animals.

Estimated Tissue and Blood N(2) Levels and Risk of Decompression Sickness in Deep-, Intermediate-, and Shallow-Diving Toothed Whales during Exposure to Naval Sonar.

Naval sonar has been accused of causing whale stranding by a mechanism which increases formation of tissue N(2) gas bubbles. Increased tissue and blood N(2) levels, and thereby increased risk of decompression sickness (DCS), is thought to result from changes in behavior or physiological responses during diving. Previous theoretical studies have used hypothetical sonar-induced changes in both behavior and physiology to model blood and tissue N(2) tension [Formula: see text], but this is the first attempt to estimate the changes during actual behavioral responses to sonar. We used an existing mathematical model to estimate blood and tissue N(2) tension [Formula: see text] from dive data recorded from sperm, killer, long-finned pilot, Blainville's beaked, and Cuvier's beaked whales before and during exposure to Low- (1-2 kHz) and Mid- (2-7 kHz) frequency active sonar. Our objectives were: (1) to determine if differences in dive behavior affects risk of bubble formation, and if (2) behavioral- or (3) physiological responses to sonar are plausible risk factors. Our results suggest that all species have natural high N(2) levels, with deep diving generally resulting in higher end-dive [Formula: see text] as compared with shallow diving. Sonar exposure caused some changes in dive behavior in both killer whales, pilot whales and beaked whales, but this did not lead to any increased risk of DCS. However, in three of eight exposure session with sperm whales, the animal changed to shallower diving, and in all these cases this seem to result in an increased risk of DCS, although risk was still within the normal risk range of this species. When a hypothetical removal of the normal dive response (bradycardia and peripheral vasoconstriction), was added to the behavioral response during model simulations, this led to an increased variance in the estimated end-dive N(2) levels, but no consistent change of risk. In conclusion, we cannot rule out the possibility that a combination of behavioral and physiological responses to sonar have the potential to alter the blood and tissue end-dive N(2) tension to levels which could cause DCS and formation of in vivo bubbles, but the actually observed behavioral responses of cetaceans to sonar in our study, do not imply any significantly increased risk of DCS.

Deadly diving? Physiological and behavioural management of decompression stress in diving mammals.

Decompression sickness (DCS; 'the bends') is a disease associated with gas uptake at pressure. The basic pathology and cause are relatively well known to human divers. Breath-hold diving marine mammals were thought to be relatively immune to DCS owing to multiple anatomical, physiological and behavioural adaptations that reduce nitrogen gas (N(2)) loading during dives. However, recent observations have shown that gas bubbles may form and tissue injury may occur in marine mammals under certain circumstances. Gas kinetic models based on measured time-depth profiles further suggest the potential occurrence of high blood and tissue N(2) tensions. We review evidence for gas-bubble incidence in marine mammal tissues and discuss the theory behind gas loading and bubble formation. We suggest that diving mammals vary their physiological responses according to multiple stressors, and that the perspective on marine mammal diving physiology should change from simply minimizing N(2) loading to management of the N(2) load. This suggests several avenues for further study, ranging from the effects of gas bubbles at molecular, cellular and organ function levels, to comparative studies relating the presence/absence of gas bubbles to diving behaviour. Technological advances in imaging and remote instrumentation are likely to advance this field in coming years.

Short- and long-term changes in right whale calling behavior: the potential effects of noise on acoustic communication.

The impact of anthropogenic noise on marine mammals has been an area of increasing concern over the past two decades. Most low-frequency anthropogenic noise in the ocean comes from commercial shipping which has contributed to an increase in ocean background noise over the past 150 years. The long-term impacts of these changes on marine mammals are not well understood. This paper describes both short- and long-term behavioral changes in calls produced by the endangered North Atlantic right whale (Eubalaena glacialis) and South Atlantic right whale (Eubalaena australis) in the presence of increased low-frequency noise. Right whales produce calls with a higher average fundamental frequency and they call at a lower rate in high noise conditions, possibly in response to masking from low-frequency noise. The long-term changes have occurred within the known lifespan of individual whales, indicating that a behavioral change, rather than selective pressure, has resulted in the observed differences. This study provides evidence of a behavioral change in sound production of right whales that is correlated with increased noise levels and indicates that right whales may shift call frequency to compensate for increased band-limited background noise.

Foraging Blainville's beaked whales (Mesoplodon densirostris) produce distinct click types matched to different phases of echolocation.

Blainville's beaked whales (Mesoplodon densirostris Blainville) echolocate for prey during deep foraging dives. Here we use acoustic tags to demonstrate that these whales, in contrast to other toothed whales studied, produce two distinct types of click sounds during different phases in biosonar-based foraging. Search clicks are emitted during foraging dives with inter-click intervals typically between 0.2 and 0.4 s. They have the distinctive form of an FM upsweep (modulation rate of about 110 kHz ms(-1)) with a -10 dB bandwidth from 26 to 51 kHz and a pulse length of 270 micros, somewhat similar to chirp signals in bats and Cuvier's beaked whales (Ziphius cavirostris Cuvier), but quite different from clicks of other toothed whales studied. In comparison, the buzz clicks, produced in short bursts during the final stage of prey capture, are short (105 micros) transients with no FM structure and a -10 dB bandwidth from 25 to 80 kHz or higher. Buzz clicks have properties similar to clicks reported from large delphinids and hold the potential for higher temporal resolution than the FM clicks. It is suggested that the two click types are adapted to the separate problems of target detection and classification versus capture of low target strength prey in a cluttered acoustic environment.

Cardiac responses to acoustic playback experiments in the captive bottlenose dolphin (Tursiops truncatus).

Acoustic recordings were used to investigate the cardiac responses of a captive dolphin (Tursiops truncatus) to sound playback stimuli. A suction-cup hydrophone placed on the ventral midline of the dolphin produced a continuous heartbeat signal while the dolphin was submerged. Heartbeats were timed by applying a matched-filter to the phonocardiogram. Significant heart rate accelerations were observed in response to playback stimuli involving conspecific vocalizations compared with baseline rates or tank noise playbacks. This method documents that objective psychophysiological measures can be obtained for physically unrestrained cetaceans. In addition, the results are the 1st to show cardiac responses to acoustic stimuli from a cetacean at depth. Preliminary evidence suggests that the cardiac response patterns of dolphins are consistent with the physiological defense and startle responses in terrestrial mammals and birds.

Buoyant balaenids: the ups and downs of buoyancy in right whales.

A variety of marine mammal species have been shown to conserve energy by using negative buoyancy to power prolonged descent glides during dives. A new non-invasive tag attached to North Atlantic right whales recorded swim stroke from changes in pitch angle derived from a three-axis accelerometer. These results show that right whales are positively buoyant near the surface, a finding that has significant implications for both energetics and management. Some of the most powerful fluke strokes observed in tagged right whales occur as they counteract this buoyancy as they start a dive. By contrast, right whales use positive buoyancy to power glides during ascent. Right whales appear to use their positive buoyancy for more efficient swimming and diving. However, this buoyancy may pose added risks of vessel collision. Such collisions are the primary source of anthropogenic mortality for North Atlantic right whales, whose population is critically endangered and declining. Buoyancy may impede diving responses to oncoming vessels and right whales may have a reduced ability to manoeuvre during free ascents. These risk factors can inform efforts to avoid collisions.

Animal behavior. Dolphins whistle a signature tune.

Dolphins are remarkably intelligent creatures renowned for their ability to imitate manmade sounds and for producing individual signature whistles that enable them to recognize each other. Now, in his Perspective, Tyack discusses new findings showing that vocal imitation is important for communication among bottlenose dolphins in the wild (Janik). Apparently, bottlenose dolphins, when they are separated in the wild, address each other by matching each other's whistles.

Synthesis and modification of the whistles of the bottlenose dolphin, Tursiops truncatus.

A signal-processing algorithm was developed to analyze harmonic frequency-modulated sounds, to modify the parameters of the analyzed signal, and to synthesize a new analytically specified signal that resembles the original signal in specified features. This algorithm was used with dolphin whistles, a frequency-modulated harmonic signal that has typically been described in terms of its contour, or pattern of modulation of the fundamental frequency. In order to test whether other features may also be salient to dolphins, the whistle analysis calculates the energies at the harmonics as well as the fundamental frequency of the whistle. The modification part of the algorithm can set all of these energies to a constant, can shift the whistle frequency, and can expand or compress the time base or the frequency of the whistle. The synthesis part of the algorithm then synthesizes a waveform based upon the energies and frequencies of the fundamental and first two harmonics. These synthetic whistles will be useful for evaluating what acoustic features dolphins use in discriminating different whistles.

Social evolution in toothed whales.

Two contrasting results emerge from comparisons of the social systems of several odontocetes with terrestrial mammals. Researchers have identified remarkable convergence in prominent features of the social systems of odontocetes such as the sperm whale and bottlenose dolphin with a few well-known terrestrial mammals such as the elephant and chimpanzee. In contrast, studies on killer whales and Baird's beaked whale reveal novel social solutions to aquatic living. The combination of convergent and novel features in odontocete social systems promise a more general understanding of the ecological determinants of social systems in both terrestrial and aquatic habitats, as well as the relationship between relative brain size and social evolution.