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.

Breathing Patterns Indicate Cost of Exercise During Diving and Response to Experimental Sound Exposures in Long-Finned Pilot Whales.

Air-breathing marine predators that target sub-surface prey have to balance the energetic benefit of foraging against the time, energetic and physiological costs of diving. Here we use on-animal data loggers to assess whether such trade-offs can be revealed by the breathing rates (BR) and timing of breaths in long-finned pilot whales (Globicephela melas). We used the period immediately following foraging dives in particular, for which respiratory behavior can be expected to be optimized for gas exchange. Breath times and fluke strokes were detected using onboard sensors (pressure, 3-axis acceleration) attached to animals using suction cups. The number and timing of breaths were quantified in non-linear mixed models that incorporated serial correlation and individual as a random effect. We found that pilot whales increased their BR in the 5-10 min period prior to, and immediately following, dives that exceeded 31 m depth. While pre-dive BRs did not vary with dive duration, the initial post-dive BR was linearly correlated with duration of >2 min dives, with BR then declining exponentially. Apparent net diving costs were 1.7 (SE 0.2) breaths per min of diving (post-dive number of breaths, above pre-dive breathing rate unrelated to dive recovery). Every fluke stroke was estimated to cost 0.086 breaths, which amounted to 80-90% average contribution of locomotion to the net diving costs. After accounting for fluke stroke rate, individuals in the small body size class took a greater number of breaths per diving minute. Individuals reduced their breathing rate (from the rate expected by diving behavior) by 13-16% during playbacks of killer whale sounds and their first exposure to 1-2 kHz naval sonar, indicating similar responses to interspecific competitor/predator and anthropogenic sounds. Although we cannot rule out individuals increasing their per-breath O2 uptake to match metabolic demand, our results suggest that behavioral responses to experimental sound exposures were not associated with increased metabolic rates in a stress response, but metabolic rates instead appear to decrease. Our results support the hypothesis that maximal performance leads to predictable (optimized) breathing patterns, which combined with further physiological measurements could improve proxies of field metabolic rates and per-stroke energy costs from animal-borne behavior data.

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.

Sperm whales reduce foraging effort during exposure to 1-2 kHz sonar and killer whale sounds.

The time and energetic costs of behavioral responses to incidental and experimental sonar exposures, as well as control stimuli, were quantified using hidden state analysis of time series of acoustic and movement data recorded by tags (DTAG) attached to 12 sperm whales (Physeter macrocephalus) using suction cups. Behavioral state transition modeling showed that tagged whales switched to a non-foraging, non-resting state during both experimental transmissions of low-frequency active sonar from an approaching vessel (LFAS; 1-2 kHz, source level 214 dB re 1 µPa m, four tag records) and playbacks of potential predator (killer whale, Orcinus orca) sounds broadcast at naturally occurring sound levels as a positive control from a drifting boat (five tag records). Time spent in foraging states and the probability of prey capture attempts were reduced during these two types of exposures with little change in overall locomotion activity, suggesting an effect on energy intake with no immediate compensation. Whales switched to the active non-foraging state over received sound pressure levels of 131-165 dB re 1 µPa during LFAS exposure. In contrast, no changes in foraging behavior were detected in response to experimental negative controls (no-sonar ship approach or noise control playback) or to experimental medium-frequency active sonar exposures (MFAS; 6-7 kHz, source level 199 re 1 µPa m, received sound pressure level [SPL] = 73-158 dB re 1 µPa). Similarly, there was no reduction in foraging effort for three whales exposed to incidental, unidentified 4.7-5.1 kHz sonar signals received at lower levels (SPL = 89-133 dB re 1 µPa). These results demonstrate that similar to predation risk, exposure to sonar can affect functional behaviors, and indicate that increased perception of risk with higher source level or lower frequency may modulate how sperm whales respond to anthropogenic sound.

Potential Population Consequences of Active Sonar Disturbance in Atlantic Herring: Estimating the Maximum Risk.

Effects of noise on fish populations may be predicted by the population consequence of acoustic disturbance (PCAD) model. We have predicted the potential risk of population disturbance when the highest sound exposure level (SEL) at which adult herring do not respond to naval sonar (SEL(0)) is exceeded. When the population density is low (feeding), the risk is low even at high sonar source levels and long-duration exercises (>24 h). With densely packed populations (overwintering), a sonar exercise might expose the entire population to levels >SEL(0) within a 24-h exercise period. However, the disturbance will be short and the response threshold used here is highly conservative. It is therefore unlikely that naval sonar will significantly impact the herring population.

Protection of Marine Mammals.

Within the European Defense Agency (EDA), the Protection of Marine Mammals (PoMM) project, a comprehensive common marine mammal database essential for risk mitigation tools, was established. The database, built on an extensive dataset collection with the focus on areas of operational interest for European navies, consists of annual and seasonal distribution and density maps, random and systematic sightings, an encyclopedia providing knowledge on the characteristics of 126 marine mammal species, data on marine mammal protection areas, and audio information including numerous examples of various vocalizations. Special investigations on marine mammal acoustics were carried out to improve the detection and classification capabilities.

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.