Dose response severity functions for acoustic disturbance in cetaceans using recurrent event survival analysis

This work was financially supported by the U. S. Office of Naval Research grant N00014‐12‐1‐0204, under the project “Multi‐study Ocean acoustics Human effects Analysis” (MOCHA). . L. Tyack received funding from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) and their support is gratefully acknowledged. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions. The case study data were provided by the 3S project, which was funded by the U.S. Office of Naval Research, the Norwegian Ministry of Defense, the Netherlands Ministry of Defense, and WWF Norway.Behavioral response studies (BRSs) aim to enhance our understanding of the behavior changes made by animals in response to specific exposure levels of different stimuli, often presented in an increasing dosage. Here, we focus on BRSs that aim to understand behavioral responses of free-ranging whales and dolphins to manmade acoustic signals (although the methods are applicable more generally). One desired outcome of these studies is dose-response functions relevant to different species, signals and contexts. We adapted and applied recurrent event survival analysis (Cox proportional hazard models) to data from the 3S BRS project, where multiple behavioral responses of different severities had been observed per experimental exposure and per individual based upon expert scoring. We included species, signal type, exposure number and behavioral state prior to exposure as potential covariates. The best model included all main effect terms, with the exception of exposure number, as well as two interaction terms. The interactions between signal and behavioral state, and between species and behavioral state highlighted that the sensitivity of animals to different signal types (a 6–7 kHz upsweep sonar signal [MFAS] or a 1–2 kHz upsweep sonar signal [LFAS]) depended on their behavioral state (feeding or nonfeeding), and this differed across species. Of the three species included in this analysis (sperm whale [Physeter macrocephalus], killer whale [Orcinus orca] and long-finned pilot whale [Globicephala melas]), killer whales were consistently the most likely to exhibit behavioral responses to naval sonar exposure. We conclude that recurrent event survival analysis provides an effective framework for fitting dose-response severity functions to data from behavioral response studies. It can provide outputs that can help government and industry to evaluate the potential impacts of anthropogenic sound production in the ocean.Publisher PDFPeer reviewe

Diving behavior and fine-scale kinematics of free-ranging Risso’s dolphins foraging in shallow and deep-water habitats

Funding: SOCAL-BRS project, Chief of Naval Operations Environmental Readiness Division, the US Navy's Living Marine Resources Program, and the Office of Naval Research Marine Mammal Program; ONR grant N00014-15-1-255 and the MASTS pooling initiative (Marine Alliance for Science and Technology for Scotland supported by the Scottish Funding Council, grant reference HR09011, and contributing institutions) (PLT).Air-breathing marine predators must balance the conflicting demands of oxygen conservation during breath-hold and the cost of diving and locomotion to capture prey. However, it remains poorly understood how predators modulate foraging performance when feeding at different depths and in response to changes in prey distribution and type. Here, we used high-resolution multi-sensor tags attached to Risso’s dolphins (Grampus griseus) and concurrent prey surveys to quantify their foraging performance over a range of depths and prey types. Dolphins (N=33) foraged in shallow and deep habitats [seabed depths less or more than 560m, respectively] and within the deep habitat, in vertically stratified prey features occurring at several aggregation levels. Generalized linear mixed-effects models indicated that dive kinematics were driven by foraging depth rather than habitat. Bottom-phase duration and number of buzzes (attempts to capture prey) per dive increased with depth. In deep dives, dolphins were gliding for >50% of descent and adopted higher pitch angles both during descent and ascents, which was likely to reduce energetic cost of longer transits. This lower cost of transit was counteracted by the record of highest vertical swim speeds, rolling maneuvers and stroke rates at depth, together with a 4-fold increase in the inter-buzz interval, suggesting higher costs of pursuing and handling prey compared to shallow-water feeding. In spite of the increased capture effort at depth, dolphins managed to keep their estimated overall metabolic rate comparable across dive types. This indicates that adjustments in swimming modes may enable energy balance in deeper dives. If we think of the surface as a central place where divers return to breathe, our data match predictions that central place foragers should increase the number and likely quality of prey items at greater distances. These dolphins forage efficiently from near-shore benthic communities to depth-stratified scattering layers, enabling them to maximize their fitness.Publisher PDFPeer reviewe

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

Research was supported by the US Navy Chief of Naval Operations, Environmental Readiness Program, the Office of Naval Research, the Naval Postgraduate School, and the National Research Council.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.Publisher PDFPeer reviewe

Marine Mammal Behavioral Response Studies in Southern California: Advances in Technology and Experimental Methods

Behavioral response studies (BRS) are increasingly being conducted to better understand basic behavioral patterns in marine animals and how underwater sounds, including from human sources, can affect them. These studies are being enabled and enhanced by advances in both acoustic sensing and transmission technologies. In the design of a 5-year project in southern California ("SOCAL-BRS"), the development of a compact, hand-deployable, ship-powered, 15-element vertical line array sound source enabled a fundamental change in overall project configuration from earlier efforts. The reduced size and power requirements of the sound source, which achieved relatively high output levels and directivity characteristics specified in the experimental design, enabled the use of substantially smaller research vessels. This size reduction favored a decentralization of field effort, with greater emphasis on mobile small boat operations capable of covering large areas to locate and tag marine mammals. These changes in configuration directly contributed to significant increases in tagging focal animals and conducting sound exposure experiments. During field experiments, received sound levels on tagged animals of several different species were within specified target ranges, demonstrating the efficacy of these new solutions to challenging field research problems.</p

Marine Mammal Behavioral Response Studies in Southern California: Advances in Technology and Experimental Methods

Behavioral response studies (BRS) are increasingly being conducted to better understand basic behavioral patterns in marine animals and how underwater sounds, including from human sources, can affect them. These studies are being enabled and enhanced by advances in both acoustic sensing and transmission technologies. In the design of a 5-year project in southern California ("SOCAL-BRS"), the development of a compact, hand-deployable, ship-powered, 15-element vertical line array sound source enabled a fundamental change in overall project configuration from earlier efforts. The reduced size and power requirements of the sound source, which achieved relatively high output levels and directivity characteristics specified in the experimental design, enabled the use of substantially smaller research vessels. This size reduction favored a decentralization of field effort, with greater emphasis on mobile small boat operations capable of covering large areas to locate and tag marine mammals. These changes in configuration directly contributed to significant increases in tagging focal animals and conducting sound exposure experiments. During field experiments, received sound levels on tagged animals of several different species were within specified target ranges, demonstrating the efficacy of these new solutions to challenging field research problems.</p

Delphinid whistle production and call matching during playback of simulated military sonar.

In 2007 and 2008, controlled exposure experiments were performed in the Bahamas to study behavioral responses to simulated mid-frequency active sonar (MFA) by three groups of odontocetes: false killer whales, Pseudorca crassidens; short-finned pilot whales, Globicephala macrorhynchus; and melon-headed whales, Peponocephala electra. An individual in each group was tagged with a Dtag to record acoustic and movement data. During exposures, some individuals produced whistles that seemed similar to the experimental MFA stimulus. Statistical tests were thus applied to investigate whistle-MFA similarity and the relationship between whistle production rate and MFA reception time. For the false killer whale group, overall whistle rate and production rate of the most MFA-like whistles decreased with time since last MFA reception. Despite quite low whistle rates overall by the melon-headed whales, statistical results indicated minor transient silencing after each signal reception. There were no apparent relationships between pilot whale whistle rates and MFA sounds within the exposure period. This variability of responses suggests that changes in whistle production in response to acoustic stimuli depend not only on species and sound source, but also on the social, behavioral, or environmental contexts of exposure

Delphinid whistle production and call matching during playback of simulated military sonar.

In 2007 and 2008, controlled exposure experiments were performed in the Bahamas to study behavioral responses to simulated mid-frequency active sonar (MFA) by three groups of odontocetes: false killer whales, Pseudorca crassidens; short-finned pilot whales, Globicephala macrorhynchus; and melon-headed whales, Peponocephala electra. An individual in each group was tagged with a Dtag to record acoustic and movement data. During exposures, some individuals produced whistles that seemed similar to the experimental MFA stimulus. Statistical tests were thus applied to investigate whistle-MFA similarity and the relationship between whistle production rate and MFA reception time. For the false killer whale group, overall whistle rate and production rate of the most MFA-like whistles decreased with time since last MFA reception. Despite quite low whistle rates overall by the melon-headed whales, statistical results indicated minor transient silencing after each signal reception. There were no apparent relationships between pilot whale whistle rates and MFA sounds within the exposure period. This variability of responses suggests that changes in whistle production in response to acoustic stimuli depend not only on species and sound source, but also on the social, behavioral, or environmental contexts of exposure

Blue whales respond to simulated mid-frequency military sonar

Mid-frequency military (1–10 kHz) sonars have been associated with lethal mass strandings of deep-diving toothed whales, but the effects on endangered baleen whale species are virtually unknown. Here, we used controlled exposure experiments with simulated military sonar and other mid-frequency sounds to measure behavioural responses of tagged blue whales (Balaenoptera musculus) in feeding areas within the Southern California Bight. Despite using source levels orders of magnitude below some operational military systems, our results demonstrate that mid-frequency sound can significantly affect blue whale behaviour, especially during deep feeding modes. When a response occurred, behavioural changes varied widely from cessation of deep feeding to increased swimming speed and directed travel away from the sound source. The variability of these behavioural responses was largely influenced by a complex interaction of behavioural state, the type of mid-frequency sound and received sound level. Sonar-induced disruption of feeding and displacement from high-quality prey patches could have significant and previously undocumented impacts on baleen whale foraging ecology, individual fitness and population health.Publisher PDFPeer reviewe

Acoustic and foraging behavior of a Baird’s beaked whale, <em>Berardius bairdii</em>, 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.</p