Integrating remote sensing methods during controlled exposure experiments to quantify group responses of dolphins to navy sonar.

Human noise can be harmful to sound-centric marine mammals. Significant research has focused on characterizing behavioral responses of protected cetacean species to navy mid-frequency active sonar (MFAS). Controlled exposure experiments (CEE) using animal-borne tags have proved valuable, but smaller dolphins are not amenable to tagging and groups of interacting individuals are more relevant behavioral units for these social species. To fill key data gaps on group responses of social delphinids that are exposed to navy MFAS in large numbers, we describe novel approaches for the coordinated collection and integrated analysis of multiple remotely-sensed datasets during CEEs. This involves real-time coordination of a sonar source, shore-based group tracking, aerial photogrammetry to measure fine-scale movements and passive acoustics to quantify vocal activity. Using an example CEE involving long-beaked common dolphins (Delphinus delphis bairdii), we demonstrate how resultant quantitative metrics can be used to estimate behavioral changes and noise exposure-response relationships.

Prey-mediated behavioral responses of feeding blue whales in controlled sound exposure experiments.

Behavioral response studies provide significant insights into the nature, magnitude, and consequences of changes in animal behavior in response to some external stimulus. Controlled exposure experiments (CEEs) to study behavioral response have faced challenges in quantifying the importance of and interaction among individual variability, exposure conditions, and environmental covariates. To investigate these complex parameters relative to blue whale behavior and how it may change as a function of certain sounds, we deployed multi-sensor acoustic tags and conducted CEEs using simulated mid-frequency active sonar (MFAS) and pseudo-random noise (PRN) stimuli, while collecting synoptic, quantitative prey measures. In contrast to previous approaches that lacked such prey data, our integrated approach explained substantially more variance in blue whale dive behavioral responses to mid-frequency sounds (r2 = 0.725 vs. 0.14 previously). Results demonstrate that deep-feeding whales respond more clearly and strongly to CEEs than those in other behavioral states, but this was only evident with the increased explanatory power provided by incorporating prey density and distribution as contextual covariates. Including contextual variables increases the ability to characterize behavioral variability and empirically strengthens previous findings that deep-feeding blue whales respond significantly to mid-frequency sound exposure. However, our results are only based on a single behavioral state with a limited sample size, and this analytical framework should be applied broadly across behavioral states. The increased capability to describe and account for individual response variability by including environmental variables, such as prey, that drive foraging behavior underscores the importance of integrating these and other relevant contextual parameters in experimental designs. Our results suggest the need to measure and account for the ecological dynamics of predator-prey interactions when studying the effects of anthropogenic disturbance in feeding animals.

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.

Acoustic and foraging behavior of a Baird's beaked whale, Berardius bairdii, exposed to simulated sonar.

Beaked whales are hypothesized to be particularly sensitive to anthropogenic noise, based on previous strandings and limited experimental and observational data. However, few species have been studied in detail. We describe the underwater behavior of a Baird's beaked whale (Berardius bairdii) from the first deployment of a multi-sensor acoustic tag on this species. The animal exhibited shallow (23 ± 15 m max depth), intermediate (324 ± 49 m), and deep (1138 ± 243 m) dives. Echolocation clicks were produced with a mean inter-click interval of approximately 300 ms and peak frequency of 25 kHz. Two deep dives included presumed foraging behavior, with echolocation pulsed sounds (presumed prey capture attempts) associated with increased maneuvering, and sustained inverted swimming during the bottom phase of the dive. A controlled exposure to simulated mid-frequency active sonar (3.5-4 kHz) was conducted 4 hours after tag deployment, and within 3 minutes of exposure onset, the tagged whale increased swim speed and body movement, and continued to show unusual dive behavior for each of its next three dives, one of each type. These are the first data on the acoustic foraging behavior in this largest beaked whale species, and the first experimental demonstration of a response to simulated sonar.

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.

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.

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.

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.

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.