Petter Helgevold Kvadsheim

The Severity of behavioral changes observed during experimental exposures of killer (Orcinus orca), long-finned Pilot (Globicephala melas), and sperm (Physeter macrocephalus) whales to naval sonar

This study describes behavioral changes of wild cetaceans observed during controlled exposures of naval sonar. In 2006 through 2009, 14 experiments were conducted with killer (n = 4), long-finned pilot (n = 6), and sperm (n = 4) whales. A total of 14 6-7 kHz upsweep, 13 1-2 kHz upsweep, and five 1-2 kHz downsweep sonar exposures, as well as seven Silent vessel control exposure sessions and eight playbacks of killer whale sounds were conducted. Sonar signals were transmitted by a towable source that approached each tagged subject from a starting distance of 6 to 8 km with a ramp up of source levels (from 152 to 158 to a maximum of 198 to 214 dB re: 1 μPa m). This procedure resulted in a gradual escalation of the sonar received level at the whale, measured by towed hydrophones and by tags that record movement and sound (Dtags). Observers tracked the position of each tagged animal and recorded group-level surface behavior. Two expert panels independently scored the severity of diverse behavioral changes observed during each sonar and control exposure, using the 0 to 9 point severity scale of Southall et al. (2007), and then reached consensus with a third-party moderator. The most severe responses scored (i.e., most likely to affect vital rates) included a temporary separation of a calf from its group, cessation of feeding or resting, and avoidance movements that continued after the sonar stopped transmitting. Higher severity scores were more common during sonar exposure than during Silent control sessions. Scored responses started at lower sound pressure levels (SPLs) for killer whales and were more severe during sonar exposures to killer and sperm whales than to long-finned pilot whales. Exposure sessions with the higher source level of 1 to 2 kHz sonar had more changes and a trend for higher maximum severity than 6 to 7 kHz sessions, but the order of the sessions had no effect. This approach is helpful to standardize the description of behavioral changes that occurred during our experiments and to identify and describe the severity of potential responses of free-ranging cetaceans to sonar.

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.

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.

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 animals 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.

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.

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.

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.

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, Blainvilles beaked and Cuviers 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.

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.

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.