Brandon L. Southall

Beaked Whales Respond to Simulated and Actual Navy Sonar

Beaked whales have mass stranded during some naval sonar exercises, but the cause is unknown. They are difficult to sight but can reliably be detected by listening for echolocation clicks produced during deep foraging dives. Listening for these clicks, we documented Blainvilles beaked whales, Mesoplodon densirostris, in a naval underwater range where sonars are in regular use near Andros Island, Bahamas. An array of bottom-mounted hydrophones can detect beaked whales when they click anywhere within the range. We used two complementary methods to investigate behavioral responses of beaked whales to sonar: an opportunistic approach that monitored whale responses to multi-day naval exercises involving tactical mid-frequency sonars, and an experimental approach using playbacks of simulated sonar and control sounds to whales tagged with a device that records sound, movement, and orientation. Here we show that in both exposure conditions beaked whales stopped echolocating during deep foraging dives and moved away. During actual sonar exercises, beaked whales were primarily detected near the periphery of the range, on average 16 km away from the sonar transmissions. Once the exercise stopped, beaked whales gradually filled in the center of the range over 2–3 days. A satellite tagged whale moved outside the range during an exercise, returning over 2–3 days post-exercise. The experimental approach used tags to measure acoustic exposure and behavioral reactions of beaked whales to one controlled exposure each of simulated military sonar, killer whale calls, and band-limited noise. The beaked whales reacted to these three sound playbacks at sound pressure levels below 142 dB re 1 µPa by stopping echolocation followed by unusually long and slow ascents from their foraging dives. The combined results indicate similar disruption of foraging behavior and avoidance by beaked whales in the two different contexts, at exposures well below those used by regulators to define disturbance.

A New Context‐Based Approach to Assess Marine Mammal Behavioral Responses to Anthropogenic Sounds

Acute effects of anthropogenic sounds on marine mammals, such as from military sonars, energy development, and offshore construction, have received considerable international attention from scientists, regulators, and industry. Moreover, there has been increasing recognition and concern about the potential chronic effects of human activities (e.g., shipping). It has been demonstrated that increases in human activity and background noise can alter habitats of marine animals and potentially mask communications for species that rely on sound to mate, feed, avoid predators, and navigate. Without exception, regulatory agencies required to assess and manage the effects of noise on marine mammals have addressed only the acute effects of noise on hearing and behavior. Furthermore, they have relied on a single exposure metric to assess acute effects: the absolute sound level received by the animal. There is compelling evidence that factors other than received sound level, including the activity state of animals exposed to different sounds, the nature and novelty of a sound, and spatial relations between sound source and receiving animals (i.e., the exposure context) strongly affect the probability of a behavioral response. A more comprehensive assessment method is needed that accounts for the fact that multiple contextual factors can affect how animals respond to both acute and chronic noise. We propose a three-part approach. The first includes measurement and evaluation of context-based behavioral responses of marine mammals exposed to various sounds. The second includes new assessment metrics that emphasize relative sound levels (i.e., ratio of signal to background noise and level above hearing threshold). The third considers the effects of chronic and acute noise exposure. All three aspects of sound exposure (context, relative sound level, and chronic noise) mediate behavioral response, and we suggest they be integrated into ecosystem-level management and the spatial planning of human offshore activities.

First direct measurements of behavioural responses by Cuvier's beaked whales to mid-frequency active sonar.

Most marine mammal strandings coincident with naval sonar exercises have involved Cuviers beaked whales (Ziphius cavirostris). We recorded animal movement and acoustic data on two tagged Ziphius and obtained the first direct measurements of behavioural responses of this species to mid-frequency active (MFA) sonar signals. Each recording included a 30-min playback (one 1.6-s simulated MFA sonar signal repeated every 25 s); one whale was also incidentally exposed to MFA sonar from distant naval exercises. Whales responded strongly to playbacks at low received levels (RLs; 89–127 dB re 1 µPa): after ceasing normal fluking and echolocation, they swam rapidly, silently away, extending both dive duration and subsequent non-foraging interval. Distant sonar exercises (78–106 dB re 1 µPa) did not elicit such responses, suggesting that context may moderate reactions. The observed responses to playback occurred at RLs well below current regulatory thresholds; equivalent responses to operational sonars could elevate stranding risk and reduce foraging efficiency.

Underwater temporary threshold shift induced by octave-band noise in three species of pinniped.

Pure-tone sound detection thresholds were obtained in water for one harbor seal (Phoca vitulina), two California sea lions (Zalophus californianus), and one northern elephant seal (Mirounga angustirostris) before and immediately following exposure to octave-band noise. Additional thresholds were obtained following a 24-h recovery period. Test frequencies ranged from 100 Hz to 2000 Hz and octave-band exposure levels were approximately 60-75 dB SL (sensation level at center frequency). Each subject was trained to dive into a noise field and remain stationed underwater during a noise-exposure period that lasted a total of 20-22 min. Following exposure, three of the subjects showed threshold shifts averaging 4.8 dB (Phoca), 4.9 dB (Zalophus), and 4.6 dB (Mirounga). Recovery to baseline threshold levels was observed in test sessions conducted within 24 h of noise exposure. Control sessions in which the subjects completed a simulated noise exposure produced shifts that were significantly smaller than those observed following noise exposure. These results indicate that noise of moderate intensity and duration is sufficient to induce TTS under water in these pinniped species.

Why pinnipeds don’t echolocate

Odontocete cetaceans have evolved a highly advanced system of active biosonar. It has been hypothesized that other groups of marine animals, such as the pinnipeds, possess analogous sound production, reception, and processing mechanisms that allow for underwater orientation using active echolocation. Despite sporadic investigation over the past 30 years, the accumulated evidence in favor of the pinniped echolocation hypothesis is unconvincing. We argue that an advanced echolocation system is unlikely to have evolved in pinnipeds primarily because of constraints imposed by the obligate amphibious functioning of the pinniped auditory system. As a result of these constraints, pinnipeds have not developed highly acute, aquatic, high frequency sound production or reception systems required for underwater echolocation. Instead, it appears that pinnipeds have evolved enhanced visual, tactile, and passive listening skills. The evolutionary refinement of alternative sensory systems allows pinnipeds to effectively forage, navigate, and avoid predators under water despite the lack of active biosonar capabilities.

Masking in three pinnipeds: Underwater, low-frequency critical ratios

Behavioral techniques were used to determine underwater masked hearing thresholds for a northern elephant seal (Mirounga angustirostris), a harbor seal (Phoca vitulina), and a California sea lion (Zalophus californianus). Octave-band white noise maskers were centered at five test frequencies ranging from 200 to 2500 Hz; a slightly wider noise band was used for testing at 100 Hz. Critical ratios were calculated at one masking noise level for each test frequency. Above 200 Hz, critical ratios increased with frequency. This pattern is similar to that observed in most animals tested, and indicates that these pinnipeds lack specializations for detecting low-frequency tonal sounds in noise. However, the individual pinnipeds in this study, particularly the northern elephant seal, detected signals at relatively low signal-to-noise ratios. These results provide a means of estimating zones of auditory masking for pinnipeds exposed to anthropogenic noise sources.

Underwater temporary threshold shift in pinnipeds : Effects of noise level and duration

Behavioral psychophysical techniques were used to evaluate the residual effects of underwater noise on the hearing sensitivity of three pinnipeds: a California sea lion (Zalophus californianus), a harbor seal (Phoca vitulina), and a northern elephant seal (Mirounga angustirostris). Temporary threshold shift (TTS), defined as the difference between auditory thresholds obtained before and after noise exposure, was assessed. The subjects were exposed to octave-band noise centered at 2500 Hz at two sound pressure levels: 80 and 95 dB SL (re: auditory threshold at 2500 Hz). Noise exposure durations were 22, 25, and 50 min. Threshold shifts were assessed at 2500 and 3530 Hz. Mean threshold shifts ranged from 2.9-12.2 dB. Full recovery of auditory sensitivity occurred within 24 h of noise exposure. Control sequences, comprising sham noise exposures, did not result in significant mean threshold shifts for any subject. Threshold shift magnitudes increased with increasing noise sound exposure level (SEL) for two of the three subjects. The results underscore the importance of including sound exposure metrics (incorporating sound pressure level and exposure duration) in order to fully assess the effects of noise on marine mammal hearing.

A New Framework for Assessing the Effects of Anthropogenic Sound on Marine Mammals in a Rapidly Changing Arctic

The recent loss of Arctic sea ice provides humans unprecedented access to the region. Marine mammals rely on sound as a primary sensory modality, and the noise associated with increasing human activities offshore can interfere with vital life functions. Many coastal communities rely on marine mammals for food and cultural identity, and subsistence hunters have expressed strong concerns that underwater sound from human activities negatively affects both the animals and hunting success. Federal regulations require scientists and oil and gas operators to acquire incidental harassment authorizations for activities that may disturb marine mammals. Currently, authorization requests are focused on the impacts of sound from activities considered in isolation of one another, and this precludes any possibility of a meaningful analysis of the cumulative impacts from multiple sources. We propose a new assessment framework that is based on the acoustic habitats that constitute the aggregate sound field from multiple sources, compiled at spatial and temporal scales consistent with the ecology of Arctic marine mammals.

Marine mammal noise exposure criteria: Initial scientific recommendations.

An expert panel reviewed the expanding literature on marine mammal (cetacean and pinniped) auditory and behavioral responses to sound exposure to develop comprehensive, scientifically based noise exposure criteria [Aquatic Mammals 33(4)]. They used precautionary extrapolation procedures to predict exposure levels above which adverse effects (both physical and behavioral) could be expected. Due to the paucity of data on long‐term exposures, criteria were developed for single exposure events only. Marine mammals were broken into functional hearing groups. Exposure types were lumped into three broad classes (single pulses, multiple pulses, and nonpulses). Levels estimated to induce permanent noise‐induced hearing loss were determined for each of 15 sound type/animal group combinations. For example, injury criteria for pinnipeds in water exposed to multiple pulses were 186 dB re 1 μPa2 ‐s (weighted SEL) and 218 dBpk re 1 μPa (unweighted peak SPL). Discrete behavioral disturbance thresholds could only be deter...

Comparative assessment of amphibious hearing in pinnipeds

Auditory sensitivity in pinnipeds is influenced by the need to balance efficient sound detection in two vastly different physical environments. Previous comparisons between aerial and underwater hearing capabilities have considered media-dependent differences relative to auditory anatomy, acoustic communication, ecology, and amphibious life history. New data for several species, including recently published audiograms and previously unreported measurements obtained in quiet conditions, necessitate a re-evaluation of amphibious hearing in pinnipeds. Several findings related to underwater hearing are consistent with earlier assessments, including an expanded frequency range of best hearing in true seals that spans at least six octaves. The most notable new results indicate markedly better aerial sensitivity in two seals (Phoca vitulina and Mirounga angustirostris) and one sea lion (Zalophus californianus), likely attributable to improved ambient noise control in test enclosures. An updated comparative analysis alters conventional views and demonstrates that these amphibious pinnipeds have not necessarily sacrificed aerial hearing capabilities in favor of enhanced underwater sound reception. Despite possessing underwater hearing that is nearly as sensitive as fully aquatic cetaceans and sirenians, many seals and sea lions have retained acute aerial hearing capabilities rivaling those of terrestrial carnivores.