Continuous sound from a marine vibrator causes behavioural responses of free-ranging, spawning Atlantic cod (Gadus morhua).

Marine vibrators are a new technology being developed for seismic surveys. These devices can transmit continuous instead of impulsive sound and operate over a narrower frequency band and at lower peak pressure than airguns, which is assumed to reduce their environmental impacts. We exposed spawning Atlantic cod (Gadus morhua) to sound produced by a prototype, but full-scale, marine vibrator, and monitored behavioural responses of tagged cod using acoustic telemetry. Fish were exposed to 10 × 3 h continuous sound treatments over a 4-day period using a randomised-block design. Sound exposure levels were comparable to airgun exposure experiments conducted previously with the same set-up ranging from ∼115 to 145 dB re 1 µPa2s during exposure. Telemetry data were used to assess 1) whether marine vibrator exposure displaced cod from the spawning ground, through estimation of residence and survival probabilities, and 2) fine-scale behavioural responses within the test site, namely swimming depth, activity levels, displacement, and home ranges. Forty-two spawning cod were tagged prior to the exposure, with 22 present during the exposure. All 22 tags were equipped with pressure sensors and ten of these additionally with accelerometers. While no premature departure from the spawning site was observed, cod reacted to the exposure by decreasing their activity levels (by up to 50%, SE = 7%) and increasing their swimming depth (by up to 2.5 m, SE = 1.0 m) within the test site during the exposure period. These behavioural responses varied by sex and time of day. Cod reactions to a marine vibrator may be more pronounced than reactions to airguns, possibly because continuous sound is more disturbing to fish than intermittent sound at the same exposure levels. However, given sample size limitations of the present study, further studies with continuous sound are necessary to fully understand its impact and biological significance.

Behavioral responses to predatory sounds predict sensitivity of cetaceans to anthropogenic noise within a soundscape of fear.

SignificanceAcoustic signals travel efficiently in the marine environment, allowing soniferous predators and prey to eavesdrop on each other. Our results with four cetacean species indicate that they use acoustic information to assess predation risk and have evolved mechanisms to reduce predation risk by ceasing foraging. Species that more readily gave up foraging in response to predatory sounds of killer whales also decreased foraging more during 1- to 4-kHz sonar exposures, indicating that species exhibiting costly antipredator responses also have stronger behavioral reactions to anthropogenic noise. This advance in our understanding of the drivers of disturbance helps us to predict what species and habitats are likely to be most severely impacted by underwater noise pollution in oceans undergoing increasing anthropogenic activities.

When the noise goes on: received sound energy predicts sperm whale responses to both intermittent and continuous navy sonar.

Anthropogenic noise sources range from intermittent to continuous, with seismic and navy sonar technology moving towards near-continuous transmissions. Continuous active sonar (CAS) may be used at a lower amplitude than traditional pulsed active sonar (PAS), but potentially with greater cumulative sound energy. We conducted at-sea experiments to contrast the effects of navy PAS versus CAS on sperm whale behaviour using animal-attached sound- and movement-recording tags (n=16 individuals) in Norway. Changes in foraging effort and proxies for foraging success and cost during sonar and control exposures were assessed while accounting for baseline variation [individual effects, time of day, bathymetry and blackfish (pilot/killer whale) presence] in generalized additive mixed models (GAMMs). We found no reduction in time spent foraging during exposures to medium-level PAS (MPAS) transmitted at the same peak amplitude as CAS. In contrast, we found similar reductions in foraging during CAS (d.f.=1, F=8.0, P=0.005) and higher amplitude PAS (d.f.=1, F=20.8, P<0.001) when received at similar energy levels integrated over signal duration. These results provide clear support for sound energy over amplitude as the response driver. We discuss the importance of exposure context and the need to measure cumulative sound energy to account for intermittent versus more continuous sources in noise impact assessments.

Northern bottlenose whales in a pristine environment respond strongly to close and distant navy sonar signals.

Impact assessments for sonar operations typically use received sound levels to predict behavioural disturbance in marine mammals. However, there are indications that cetaceans may learn to associate exposures from distant sound sources with lower perceived risk. To investigate the roles of source distance and received level in an area without frequent sonar activity, we conducted multi-scale controlled exposure experiments ( n = 3) with 12 northern bottlenose whales near Jan Mayen, Norway. Animals were tagged with high-resolution archival tags ( n = 1 per experiment) or medium-resolution satellite tags ( n = 9 in total) and subsequently exposed to sonar. We also deployed bottom-moored recorders to acoustically monitor for whales in the exposed area. Tagged whales initiated avoidance of the sound source over a wide range of distances (0.8-28 km), with responses characteristic of beaked whales. Both onset and intensity of response were better predicted by received sound pressure level (SPL) than by source distance. Avoidance threshold SPLs estimated for each whale ranged from 117-126 dB re 1 µPa, comparable to those of other tagged beaked whales. In this pristine underwater acoustic environment, we found no indication that the source distances tested in our experiments modulated the behavioural effects of sonar, as has been suggested for locations where whales are frequently exposed to sonar.

Lack of behavioural responses of humpback whales (Megaptera novaeangliae) indicate limited effectiveness of sonar mitigation.

Exposure to underwater sound can cause permanent hearing loss and other physiological effects in marine animals. To reduce this risk, naval sonars are sometimes gradually increased in intensity at the start of transmission ('ramp-up'). Here, we conducted experiments in which tagged humpback whales were approached with a ship to test whether a sonar operation preceded by ramp-up reduced three risk indicators - maximum sound pressure level (SPLmax), cumulative sound exposure level (SELcum) and minimum source-whale range (Rmin) - compared with a sonar operation not preceded by ramp-up. Whales were subject to one no-sonar control session and either two successive ramp-up sessions (RampUp1, RampUp2) or a ramp-up session (RampUp1) and a full-power session (FullPower). Full-power sessions were conducted only twice; for other whales we used acoustic modelling that assumed transmission of the full-power sequence during their no-sonar control. Averaged over all whales, risk indicators in RampUp1 (n=11) differed significantly from those in FullPower (n=12) by -3.0 dB (SPLmax), -2.0 dB (SELcum) and +168 m (Rmin), but not significantly from those in RampUp2 (n=9). Only five whales in RampUp1, four whales in RampUp2 and none in FullPower or control sessions avoided the sound source. For RampUp1, we found statistically significant differences in risk indicators between whales that avoided the sonar and whales that did not: -4.7 dB (SPLmax), -3.4 dB (SELcum) and +291 m (Rmin). In contrast, for RampUp2, these differences were smaller and not significant. This study suggests that sonar ramp-up has a positive but limited mitigative effect for humpback whales overall, but that ramp-up can reduce the risk of harm more effectively in situations when animals are more responsive and likely to avoid the sonar, e.g. owing to novelty of the stimulus, when they are in the path of an approaching sonar ship.

Avoidance responses of minke whales to 1-4kHz naval sonar.

Minke whales are difficult to study and little information exists regarding their responses to anthropogenic sound. This study pools data from behavioural response studies off California and Norway. Data are derived from four tagged animals, of which one from each location was exposed to naval sonar signals. Statistical analyses were conducted using Mahalanobis distance to compare overall changes in parameters summarising dive behaviour, avoidance behaviour, and potential energetic costs of disturbance. Our quantitative analysis showed that both animals initiated avoidance behaviour, but responses were not associated with unusual dive behaviour. In one exposed animal the avoidance of the sonar source included a 5-fold increase in horizontal speed away from the source, implying a significant increase in metabolic rate. Despite the different environmental settings and exposure contexts, clear changes in behaviour were observed providing the first insights into the nature of responses to human noise for this wide-ranging species.

Disturbance-specific social responses in long-finned pilot whales, Globicephala melas.

Social interactions among animals can influence their response to disturbance. We investigated responses of long-finned pilot whales to killer whale sound playbacks and two anthropogenic sources of disturbance: tagging effort and naval sonar exposure. The acoustic scene and diving behaviour of tagged individuals were recorded along with the social behaviour of their groups. All three disturbance types resulted in larger group sizes, increasing social cohesion during disturbance. However, the nature and magnitude of other responses differed between disturbance types. Tagging effort resulted in a clear increase in synchrony and a tendency to reduce surface logging and to become silent (21% of cases), whereas pilot whales increased surface resting during sonar exposure. Killer whale sounds elicited increased calling rates and the aggregation of multiple groups, which approached the sound source together. This behaviour appears to represent a mobbing response, a likely adaptive social defence against predators or competitors. All observed response-tactics would reduce risk of loss of group coordination, suggesting that, in social pilot whales, this could drive behavioural responses to disturbance. However, the behavioural means used to achieve social coordination depends upon other considerations, which are disturbance-specific.

Controlled Sonar Exposure Experiments on Cetaceans in Norwegian Waters: Overview of the 3S-Project.

In mitigating the risk of sonar operations, the behavioral response of cetaceans is one of the major knowledge gaps that needs to be addressed. The 3S-Project has conducted a number of controlled exposure experiments with a realistic sonar source in Norwegian waters from 2006 to 2013. In total, the following six target species have been studied: killer, long-finned pilot, sperm, humpback, minke, and northern bottlenose whales. A total of 38 controlled sonar exposures have been conducted on these species. Responses from controlled and repeated exposure runs have been recorded using acoustic and visual observations as well as with electronic tags on the target animal. So far, the first dose-response curves as well as an overview of the scored severity of responses have been revealed. In this paper, an overview is presented of the approach for the study, including the results so far as well as the current status of the ongoing analysis.

Assessing the Effectiveness of Ramp-Up During Sonar Operations Using Exposure Models.

Ramp-up procedures are used to mitigate the impact of sound on marine mammals. Sound exposure models combined with observations of marine mammals responding to sound can be used to assess the effectiveness of ramp-up procedures. We found that ramp-up procedures before full-level sonar operations can reduce the risk of hearing threshold shifts with marine mammals, but their effectiveness depends strongly on the responsiveness of the animals. In this paper, we investigated the effect of sonar parameters (source level, pulse-repetition time, ship speed) on sound exposure by using a simple analytical model and highlight the mechanisms that limit the effectiveness of ramp-up procedures.

How effectively do horizontal and vertical response strategies of long-finned pilot whales reduce sound exposure from naval sonar?

The behaviour of a marine mammal near a noise source can modulate the sound exposure it receives. We demonstrate that two long-finned pilot whales both surfaced in synchrony with consecutive arrivals of multiple sonar pulses. We then assess the effect of surfacing and other behavioural response strategies on the received cumulative sound exposure levels and maximum sound pressure levels (SPLs) by modelling realistic spatiotemporal interactions of a pilot whale with an approaching source. Under the propagation conditions of our model, some response strategies observed in the wild were effective in reducing received levels (e.g. movement perpendicular to the source's line of approach), but others were not (e.g. switching from deep to shallow diving; synchronous surfacing after maximum SPLs). Our study exemplifies how simulations of source-whale interactions guided by detailed observational data can improve our understanding about motivations behind behaviour responses observed in the wild (e.g., reducing sound exposure, prey movement).

Dose-response relationships for the onset of avoidance of sonar by free-ranging killer whales.

Eight experimentally controlled exposures to 1-2 kHz or 6-7 kHz sonar signals were conducted with four killer whale groups. The source level and proximity of the source were increased during each exposure in order to reveal response thresholds. Detailed inspection of movements during each exposure session revealed sustained changes in speed and travel direction judged to be avoidance responses during six of eight sessions. Following methods developed for Phase-I clinical trials in human medicine, response thresholds ranging from 94 to 164 dB re 1 µPa received sound pressure level (SPL) were fitted to Bayesian dose-response functions. Thresholds did not consistently differ by sonar frequency or whether a group had previously been exposed, with a mean SPL response threshold of 142 ± 15 dB (mean ± s.d.). High levels of between- and within-individual variability were identified, indicating that thresholds depended upon other undefined contextual variables. The dose-response functions indicate that some killer whales started to avoid sonar at received SPL below thresholds assumed by the U.S. Navy. The predicted extent of habitat over which avoidance reactions occur depends upon whether whales responded to proximity or received SPL of the sonar or both, but was large enough to raise concerns about biological consequences to the whales.

How man-made interference might cause gas bubble emboli in deep diving whales.

Recent cetacean mass strandings in close temporal and spatial association with sonar activity has raised the concern that anthropogenic sound may harm breath-hold diving marine mammals. Necropsy results of the stranded whales have shown evidence of bubbles in the tissues, similar to those in human divers suffering from decompression sickness (DCS). It has been proposed that changes in behavior or physiological responses during diving could increase tissue and blood N2 levels, thereby increasing DCS risk. 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 were used to estimate the changes in blood and tissue N2 tension (PN2 ). Our objectives were to determine if differences in (1) dive behavior or (2) physiological responses to sonar are plausible risk factors for bubble formation. The theoretical estimates indicate that all species may experience high N2 levels. However, unexpectedly, deep diving generally result in higher end-dive PN2 as compared with shallow diving. In this focused review we focus on three possible explanations: (1) We revisit an old hypothesis that CO2, because of its much higher diffusivity, forms bubble precursors that continue to grow in N2 supersaturated tissues. Such a mechanism would be less dependent on the alveolar collapse depth but affected by elevated levels of CO2 following a burst of activity during sonar exposure. (2) During deep dives, a greater duration of time might be spent at depths where gas exchange continues as compared with shallow dives. The resulting elevated levels of N2 in deep diving whales might also make them more susceptible to anthropogenic disturbances. (3) Extended duration of dives even at depths beyond where the alveoli collapse could result in slow continuous accumulation of N2 in the adipose tissues that eventually becomes a liability.

Modeling effectiveness of gradual increases in source level to mitigate effects of sonar on marine mammals.

Ramp-up or soft-start procedures (i.e., gradual increase in the source level) are used to mitigate the effect of sonar sound on marine mammals, although no one to date has tested whether ramp-up procedures are effective at reducing the effect of sound on marine mammals. We investigated the effectiveness of ramp-up procedures in reducing the area within which changes in hearing thresholds can occur. We modeled the level of sound killer whales (Orcinus orca) were exposed to from a generic sonar operation preceded by different ramp-up schemes. In our model, ramp-up procedures reduced the risk of killer whales receiving sounds of sufficient intensity to affect their hearing. The effectiveness of the ramp-up procedure depended strongly on the assumed response threshold and differed with ramp-up duration, although extending the duration of the ramp up beyond 5 min did not add much to its predicted mitigating effect. The main factors that limited effectiveness of ramp up in a typical antisubmarine warfare scenario were high source level, rapid moving sonar source, and long silences between consecutive sonar transmissions. Our exposure modeling approach can be used to evaluate and optimize mitigation procedures.

Responses of male sperm whales (Physeter macrocephalus) to killer whale sounds: implications for anti-predator strategies.

Interactions between individuals of different cetacean species are often observed in the wild. Killer whales (Orcinus orca) can be potential predators of many other cetaceans, and the interception of their vocalizations by unintended cetacean receivers may trigger anti-predator behavior that could mediate predator-prey interactions. We explored the anti-predator behaviour of five typically-solitary male sperm whales (Physeter macrocephalus) in the Norwegian Sea by playing sounds of mammal-feeding killer whales and monitoring behavioural responses using multi-sensor tags. Our results suggest that, rather than taking advantage of their large aerobic capacities to dive away from the perceived predator, sperm whales responded to killer whale playbacks by interrupting their foraging or resting dives and returning to the surface, changing their vocal production, and initiating a surprising degree of social behaviour in these mostly solitary animals. Thus, the interception of predator vocalizations by male sperm whales disrupted functional behaviours and mediated previously unrecognized anti-predator responses.

Behavior of captive herring exposed to naval sonar transmissions (1.0-1.6 kHz) throughout a yearly cycle.

Atlantic herring, Clupea harengus, is a hearing specialist, and several studies have demonstrated strong responses to man-made noise, for example, from an approaching vessel. To avoid negative impacts from naval sonar operations, a set of studies of reaction patters of herring to low-frequency (1.0-1.5 kHz) naval sonar signals has been undertaken. This paper presents herring reactions to sonar signals and other stimuli when kept in captivity under detailed acoustic and video monitoring. Throughout the experiment, spanning three seasons of a year, the fish did not react significantly to sonar signals from a passing frigate, at received root-mean-square sound-pressure level (SPL) up to 168 dB re 1 µPa. In contrast, the fish did exhibit a significant diving reaction when exposed to other sounds, with a much lower SPL, e.g., from a two-stroke engine. This shows that the experimental setup is sensitive to herring reactions when occurring. The lack of herring reaction to sonar signals is consistent with earlier in situ behavioral studies. The complexity of the behavioral reactions in captivity underline the need for better understanding of the causal relationship between stimuli and reaction patterns of fish.

Pilot whales attracted to killer whale sounds: acoustically-mediated interspecific interactions in cetaceans.

In cetaceans' communities, interactions between individuals of different species are often observed in the wild. Yet, due to methodological and technical challenges very little is known about the mediation of these interactions and their effect on cetaceans' behavior. Killer whales (Orcinus orca) are a highly vocal species and can be both food competitors and potential predators of many other cetaceans. Thus, the interception of their vocalizations by unintended cetacean receivers may be particularly important in mediating interspecific interactions. To address this hypothesis, we conducted playbacks of killer whale vocalizations recorded during herring-feeding activity to free-ranging long-finned pilot whales (Globicephala melas). Using a multi-sensor tag, we were able to track the whales and to monitor changes of their movements and social behavior in response to the playbacks. We demonstrated that the playback of killer whale sounds to pilot whales induced a clear increase in group size and a strong attraction of the animals towards the sound source. These findings provide the first experimental evidence that the interception of heterospecific vocalizations can mediate interactions between different cetacean species in previously unrecognized ways.

Behavioral responses of herring (Clupea harengus) to 1-2 and 6-7 kHz sonar signals and killer whale feeding sounds.

Military antisubmarine sonars produce intense sounds within the hearing range of most clupeid fish. The behavioral reactions of overwintering herring (Clupea harengus) to sonar signals of two different frequency ranges (1-2 and 6-7 kHz), and to playback of killer whale feeding sounds, were tested in controlled exposure experiments in Vestfjorden, Norway, November 2006. The behavior of free ranging herring was monitored by two upward-looking echosounders. A vessel towing an operational naval sonar source approached and passed over one of them in a block design setup. No significant escape reactions, either vertically or horizontally, were detected in response to sonar transmissions. Killer whale feeding sounds induced vertical and horizontal movements of herring. The results indicate that neither transmission of 1-2 kHz nor 6-7 kHz have significant negative influence on herring on the received sound pressure level tested (127-197 and 139-209 dB(rms) re 1 microPa, respectively). Military sonars of such frequencies and source levels may thus be operated in areas of overwintering herring without substantially affecting herring behavior or herring fishery. The avoidance during playback of killer whale sounds demonstrates the nature of an avoidance reaction and the ability of the experimental design to reveal it.

Inhibition of shivering in hypothermic seals during diving.

The mammalian response to hypothermia is increased metabolic heat production, usually by way of muscular activity, such as shivering. Seals, however, have been reported to respond to diving with hypothermia, which in other mammals under other circumstances would have elicited vigorous shivering. In the diving situation, shivering could be counterproductive, because it obviously would increase oxygen consumption and therefore reduce diving capacity. We have measured the electromyographic (EMG) activity of three different muscles and the rectal and brain temperature of hooded seals (Cystophora cristata) while they were exposed to low ambient temperatures in a climatic chamber and while they performed a series of experimental dives in cold water. In air, the seals had a normal mammalian shivering response to cold. Muscles were recruited in a sequential manner until body temperature stopped dropping. Shivering was initiated when rectal temperature fell below 35.3 +/- 0.6 degrees C (n = 6). In the hypothermic diving seal, however, the EMG activity in all of the muscles that had been shivering vigorously before submergence was much reduced, or stopped altogether, whereas it increased again upon emergence but was again reduced if diving was repeated. We conclude that shivering is inhibited during diving to allow a decrease in body temperature whereby oxygen consumption is decreased and diving capacity is extended.