Males miss and females forgo: Auditory masking from vessel noise impairs foraging efficiency and success in killer whales.

Understanding how the environment mediates an organism's ability to meet basic survival requirements is a fundamental goal of ecology. Vessel noise is a global threat to marine ecosystems and is increasing in intensity and spatiotemporal extent due to growth in shipping coupled with physical changes to ocean soundscapes from ocean warming and acidification. Odontocetes rely on biosonar to forage, yet determining the consequences of vessel noise on foraging has been limited by the challenges of observing underwater foraging outcomes and measuring noise levels received by individuals. To address these challenges, we leveraged a unique acoustic and movement dataset from 25 animal-borne biologging tags temporarily attached to individuals from two populations of fish-eating killer whales (Orcinus orca) in highly transited coastal waters to (1) test for the effects of vessel noise on foraging behaviors-searching (slow-click echolocation), pursuit (buzzes), and capture and (2) investigate the mechanism of interference. For every 1 dB increase in maximum noise level, there was a 4% increase in the odds of searching for prey by both sexes, a 58% decrease in the odds of pursuit by females and a 12.5% decrease in the odds of prey capture by both sexes. Moreover, all but one deep (≥75 m) foraging attempt with noise ≥110 dB re 1 µPa (15-45 kHz band; n = 6 dives by n = 4 whales) resulted in failed prey capture. These responses are consistent with an auditory masking mechanism. Our findings demonstrate the effects of vessel noise across multiple phases of odontocete foraging, underscoring the importance of managing anthropogenic inputs into soundscapes to achieve conservation objectives for acoustically sensitive species. While the timescales for recovering depleted prey species may span decades, these findings suggest that complementary actions to reduce ocean noise in the short term offer a critical pathway for recovering odontocete foraging opportunities.

Auditory masking of tonal and conspecific signals by continuous active sonar, amplitude modulated noise, and Gaussian noise in killer whales (Orcinus orca).

Continuous active sonar is thought to mitigate severe acoustic impacts due to its lower sound pressure level compared to pulsed active sonar typically used by world navies. However, due to its almost continuous duty cycle, continuous active sonar could have a higher potential for auditory masking. Here, we evaluate the auditory masking potential of several noise types including a recording of continuous active sonar, amplitude modulated noise, and Gaussian noise, on signal detection in two killer whales. Signals were either a 1.5 kHz pure tone or a recording of a broadband burst-pulse killer whale call. For the 1.5 kHz tone, all noise types resulted in statistically significant masking, however, there was a release from masking of approximately 13 dB for the amplitude-modulated noise. When the killer whale call was the signal, the whales employed an off-frequency listening strategy where the whales were able to detect frequency components of the signal that did not directly overlap with the noise. However, this strategy was less useful for the continuous active sonar noise due to its broadband harmonic structure. Continuous active sonar has spectral features that considerably overlap with those of killer whale calls, making this type of noise an effective auditory masker.

Kinematic signatures of prey capture from archival tags reveal sex differences in killer whale foraging activity.

Studies of odontocete foraging ecology have been limited by the challenges of observing prey capture events and outcomes underwater. We sought to determine whether subsurface movement behavior recorded from archival tags could accurately identify foraging events by fish-eating killer whales. We used multisensor bio-logging tags attached by suction cups to Southern Resident killer whales (Orcinus orca) to: (1) identify a stereotyped movement signature that co-occurred with visually confirmed prey capture dives; (2) construct a prey capture dive detector and validate it against acoustically confirmed prey capture dives; and (3) demonstrate the utility of the detector by testing hypotheses about foraging ecology. Predation events were significantly predicted by peaks in the rate of change of acceleration ('jerk peak'), roll angle and heading variance. Detection of prey capture dives by movement signatures enabled substantially more dives to be included in subsequent analyses compared with previous surface or acoustic detection methods. Males made significantly more prey capture dives than females and more dives to the depth of their preferred prey, Chinook salmon. Additionally, only half of the tag deployments on females (5 out of 10) included a prey capture dive, whereas all tag deployments on males exhibited at least one prey capture dive (12 out of 12). This dual approach of kinematic detection of prey capture coupled with hypothesis testing can be applied across odontocetes and other marine predators to investigate the impacts of social, environmental and anthropogenic factors on foraging ecology.

Sounds associated with foraging and prey capture in individual fish-eating killer whales, Orcinus orca.

Foraging behavior in odontocetes is fundamentally tied to the use of sound. Resident-type killer whales use echolocation to locate and capture elusive salmonid prey. In this investigation, acoustic recording tags were suction cup-attached to endangered Southern Resident killer whales to describe their acoustic behavior during different phases of foraging that, along with detections of prey handling sounds (e.g., crunches) and observed predation events, allow confirmation of prey capture. Echolocation click trains were categorized based on the inter-click interval (ICI) according to hypothesized foraging function. Whales produced slow click trains (ICI >100 ms) at shallowest depths but over the largest change of depth, fast click trains (10 ms < ICI ≤100 ms) at intermediate depths, and buzz trains (ICI ≤10 ms) at deepest depths over the smallest depth change. These results align with hypotheses regarding biosonar use to search, pursue and capture prey. Males exhibited a higher probability of producing slow click trains, buzzes and prey handling sounds, indicating higher levels of prey searching and capture to support the energy requirement of their larger body size. These findings identify relevant acoustic indicators of subsurface foraging behaviors of killer whales, enabling investigations of human impacts on sound use and foraging.

Vocal performance affects metabolic rate in dolphins: implications for animals communicating in noisy environments.

Many animals produce louder, longer or more repetitious vocalizations to compensate for increases in environmental noise. Biological costs of increased vocal effort in response to noise, including energetic costs, remain empirically undefined in many taxa, particularly in marine mammals that rely on sound for fundamental biological functions in increasingly noisy habitats. For this investigation, we tested the hypothesis that an increase in vocal effort would result in an energetic cost to the signaler by experimentally measuring oxygen consumption during rest and a 2 min vocal period in dolphins that were trained to vary vocal loudness across trials. Vocal effort was quantified as the total acoustic energy of sounds produced. Metabolic rates during the vocal period were, on average, 1.2 and 1.5 times resting metabolic rate (RMR) in dolphin A and B, respectively. As vocal effort increased, we found that there was a significant increase in metabolic rate over RMR during the 2 min following sound production in both dolphins, and in total oxygen consumption (metabolic cost of sound production plus recovery costs) in the dolphin that showed a wider range of vocal effort across trials. Increases in vocal effort, as a consequence of increases in vocal amplitude, repetition rate and/or duration, are consistent with behavioral responses to noise in free-ranging animals. Here, we empirically demonstrate for the first time in a marine mammal, that these vocal modifications can have an energetic impact at the individual level and, importantly, these data provide a mechanistic foundation for evaluating biological consequences of vocal modification in noise-polluted habitats.

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.

The metabolic cost of communicative sound production in bottlenose dolphins (Tursiops truncatus).

Bottlenose dolphins (Tursiops truncatus) produce various communicative sounds that are important for social behavior, maintaining group cohesion and coordinating foraging. For example, whistle production increases during disturbances, such as separations of mother-calf pairs and vessel approaches. It is clear that acoustic communication is important to the survival of these marine mammals, yet the metabolic cost of producing whistles and other socials sounds and the energetic consequences of modifying these sounds in response to both natural and anthropogenic disturbance are unknown. We used flow-through respirometry to determine whether the metabolic cost of sound production could be quantified in two captive dolphins producing social sounds (whistles and squawks). On average, we found that metabolic rates measured during 2 min periods of sound production were 1.2 times resting values. Up to 7 min were required for metabolism to return to resting values following vocal periods. The total metabolic cost (over resting values) of the 2 min vocal period plus the required recovery period (163.3 to 2995.9 ml O2 or 3279.6 to 60,166.7 J) varied by individual as well as by mean duration of sounds produced within the vocal period. Observed variation in received cumulative sound energy levels of vocalizations was not related to total metabolic costs. Furthermore, our empirical findings did not agree with previous theoretical estimates of the metabolic cost of whistles. This study provides the first empirical data on the metabolic cost of sound production in dolphins, which can be used to estimate metabolic costs of vocal responses to environmental perturbations in wild dolphins.

Divergent foraging strategies between populations of sympatric matrilineal killer whales.

In cooperative species, human-induced rapid environmental change may threaten cost-benefit tradeoffs of group behavioral strategies that evolved in past environments. Capacity for behavioral flexibility can increase population viability in novel environments. Whether the partitioning of individual responsibilities within social groups is fixed or flexible across populations is poorly understood, despite its relevance for predicting responses to global change at the population and species levels and designing successful conservation programs. We leveraged bio-logging data from two populations of fish-eating killer whales (Orcinus orca) to quantify patterns of fine-scale foraging movements and their relationships with demography. We reveal striking interpopulation differences in patterns of individual foraging behavior. Females from the endangered Southern Resident (SRKW) population captured less prey and spent less time pursuing prey than SRKW males or Northern Resident (NRKW) females, whereas NRKW females captured more prey than NRKW males. The presence of a calf (≤3 years) reduced the number of prey captured by adult females from both populations, but disproportionately so for SRKW. SRKW adult males with a living mother captured more prey than those whose mother had died, whereas the opposite was true for NRKW adult males. Across populations, males foraged in deeper areas than females, and SRKW captured prey deeper than NRKW. These population-level differences in patterns of individual foraging behavior challenge the existing paradigm that females are the disproportionate foragers in gregarious resident killer whales, and demonstrate considerable variation in the foraging strategies across populations of an apex marine predator experiencing different environmental stressors.

Temporal summation of airborne tones in a California sea lion (Zalophus californianus).

The trade-off between sound level and duration on hearing sensitivity (temporal summation) was investigated in a California sea lion (Zalophus californianus) using airborne pure-tone stimuli. Thresholds were behaviorally measured using the method of constant stimuli at 2.5, 5, and 10 kHz for nine signal durations ranging from 25 to 500 ms. In general, thresholds decreased as duration increased up to 300 ms, beyond which thresholds did not significantly improve. When these data were fitted separately to two versions of an exponential model, the estimated time constants (92-167 ms) were generally consistent between the two fits. However, the model with more free parameters generated fits with consistently higher R(2) values, while avoiding potential arbitrary decisions about which data to include. The time constants derived for the California sea lion were generally consistent with those reported for other mammals, including other pinnipeds. The current study did not show a clear correlation between time constant and test frequency. The results should be considered when conducting audiometric work, assessing communications ranges, and evaluating potential noise impacts of airborne tonal signals on California sea lions.

Do male northern elephant seals recognize individuals or merely relative dominance rank?

Vocal recognition was tested in a socially dynamic context where many individuals interact: the female defense polygyny practiced by male northern elephant seals. The goal was to tease apart whether animals recognize other individuals or instead use a simple rule-based category (i.e., relative dominance rank). A total of 67 playback experiments conducted with 18 males at Año Nuevo State Reserve, California, tested three aspects of recognition: (1) recognition of relative rank; (2) whether such recognition was continuous or categorical; and (3) recognition of familiarity. Results indicate that males recognize familiar individuals although responses are primarily based on relative dominance rank.

Effects of noise levels and call types on the source levels of killer whale calls.

Accurate parameter estimates relevant to the vocal behavior of marine mammals are needed to assess potential effects of anthropogenic sound exposure including how masking noise reduces the active space of sounds used for communication. Information about how these animals modify their vocal behavior in response to noise exposure is also needed for such assessment. Prior studies have reported variations in the source levels of killer whale sounds, and a more recent study reported that killer whales compensate for vessel masking noise by increasing their call amplitude. The objectives of the current study were to investigate the source levels of a variety of call types in southern resident killer whales while also considering background noise level as a likely factor related to call source level variability. The source levels of 763 discrete calls along with corresponding background noise were measured over three summer field seasons in the waters surrounding the San Juan Islands, WA. Both noise level and call type were significant factors on call source levels (1-40 kHz band, range of 135.0-175.7 dB(rms) re 1 [micro sign]Pa at 1 m). These factors should be considered in models that predict how anthropogenic masking noise reduces vocal communication space in marine mammals.

Vessels and their sounds reduce prey capture effort by endangered killer whales (Orcinus orca).

Vessel traffic is prevalent throughout marine environments. However, we often have a limited understanding of vessel impacts on marine wildlife, particularly cetaceans, due to challenges of studying fully-aquatic species. To investigate vessel and acoustic effects on cetacean foraging behavior, we attached suction-cup sound and movement tags to endangered Southern Resident killer whales in their summer habitat while collecting geo-referenced proximate vessel data. We identified prey capture dives using whale kinematic signatures and found that the probability of capturing prey increased as salmon abundance increased, but decreased as vessel speed increased. When vessels emitted navigational sonar, whales made longer dives to capture prey and descended more slowly when they initiated these dives. Finally, whales descended more quickly when noise levels were higher and vessel approaches were closer. These findings advance a growing understanding of vessel and sound impacts on marine wildlife and inform efforts to manage vessel impacts on endangered populations.

Speaking up: Killer whales (Orcinus orca) increase their call amplitude in response to vessel noise.

This study investigated the effects of anthropogenic sound exposure on the vocal behavior of free-ranging killer whales. Endangered Southern Resident killer whales inhabit areas including the urban coastal waters of Puget Sound near Seattle, WA, where anthropogenic sounds are ubiquitous, particularly those from motorized vessels. A calibrated recording system was used to measure killer whale call source levels and background noise levels (1-40 kHz). Results show that whales increased their call amplitude by 1 dB for every 1 dB increase in background noise levels. Furthermore, nearby vessel counts were positively correlated with these observed background noise levels.

Hidden Markov models reveal temporal patterns and sex differences in killer whale behavior.

Behavioral data can be important for effective management of endangered marine predators, but can be challenging to obtain. We utilized suction cup-attached biologging tags equipped with stereo hydrophones, triaxial accelerometers, triaxial magnetometers, pressure and temperature sensors, to characterize the subsurface behavior of an endangered population of killer whales (Orcinus orca). Tags recorded depth, acoustic and movement behavior on fish-eating killer whales in the Salish Sea between 2010-2014. We tested the hypotheses that (a) distinct behavioral states can be characterized by integrating movement and acoustic variables, (b) subsurface foraging occurs in bouts, with distinct periods of searching and capture temporally separated from travel, and (c) the probabilities of transitioning between behavioral states differ by sex. Using Hidden Markov modeling of two acoustic and four movement variables, we identified five temporally distinct behavioral states. Persistence in the same state on a subsequent dive had the greatest likelihood, with the exception of deep prey pursuit, indicating that behavior was clustered in time. Additionally, females spent more time at the surface than males, and engaged in less foraging behavior. These results reveal significant complexity and sex differences in subsurface foraging behavior, and underscore the importance of incorporating behavior into the design of conservation strategies.

Comparative physiology of vocal musculature in two odontocetes, the bottlenose dolphin (Tursiops truncatus) and the harbor porpoise (Phocoena phocoena).

The mechanism by which odontocetes produce sound is unique among mammals. To gain insight into the physiological properties that support sound production in toothed whales, we examined myoglobin content ([Mb]), non-bicarbonate buffering capacity (ß), fiber-type profiles, and myosin heavy chain expression of vocal musculature in two odontocetes: the bottlenose dolphin (Tursiops truncatus; n = 4) and the harbor porpoise (Phocoena phocoena; n = 5). Both species use the same anatomical structures to produce sound, but differ markedly in their vocal repertoires. Tursiops produce both broadband clicks and tonal whistles, while Phocoena only produce higher frequency clicks. Specific muscles examined in this study included: (1) the nasal musculature around the phonic lips on the right (RNM) and left (LNM) sides of the head, (2) the palatopharyngeal sphincter (PPS), which surrounds the larynx and aids in pressurizing cranial air spaces, and (3) the genioglossus complex (GGC), a group of muscles positioned ventrally within the head. Overall, vocal muscles had significantly lower [Mb] and ß than locomotor muscles from the same species. The PPS was predominately composed of small diameter slow-twitch fibers. Fiber-type and myosin heavy chain analyses revealed that the GGC was comprised largely of fast-twitch fibers (Tursiops: 88.6%, Phocoena: 79.7%) and had the highest ß of all vocal muscles. Notably, there was a significant difference in [Mb] between the RNM and LNM in Tursiops, but not Phocoena. Our results reveal shared physiological characteristics of individual vocal muscles across species that enhance our understanding of key functional roles, as well as species-specific differences which appear to reflect differences in vocal capacities.

Onset, growth, and recovery of in-air temporary threshold shift in a California sea lion (Zalophus californianus).

A California sea lion (Zalophus californianus) was tested in a behavioral procedure to assess noise-induced temporary threshold shift (TTS) in air. Octave band fatiguing noise was varied in both duration (1.5-50 min) and level (94-133 dB re 20 muPa) to generate a variety of equal sound exposure level conditions. Hearing thresholds were measured at the center frequency of the noise (2500 Hz) before, immediately after, and 24 h following exposure. Threshold shifts generated from 192 exposures ranged up to 30 dB. Estimates of TTS onset [159 dB re (20 muPa)(2) s] and growth (2.5 dB of TTS per dB of noise increase) were determined using an exponential function. Recovery for threshold shifts greater than 20 dB followed an 8.8 dB per log(min) linear function. Repeated testing indicated possible permanent threshold shift at the test frequency, but a later audiogram revealed no shift at this frequency or higher. Sea lions appear to be equally susceptible to noise in air and in water, provided that the noise exposure levels are referenced to absolute sound detection thresholds in both media. These data provide a framework within which to consider effects arising from more intense and/or sustained exposures.

The Relationship between Vessel Traffic and Noise Levels Received by Killer Whales (Orcinus orca).

Whale watching has become increasingly popular as an ecotourism activity around the globe and is beneficial for environmental education and local economies. Southern Resident killer whales (Orcinus orca) comprise an endangered population that is frequently observed by a large whale watching fleet in the inland waters of Washington state and British Columbia. One of the factors identified as a risk to recovery for the population is the effect of vessels and associated noise. An examination of the effects of vessels and associated noise on whale behavior utilized novel equipment to address limitations of previous studies. Digital acoustic recording tags (DTAGs) measured the noise levels the tagged whales received while laser positioning systems allowed collection of geo-referenced data for tagged whales and all vessels within 1000 m of the tagged whale. The objective of the current study was to compare vessel data and DTAG recordings to relate vessel traffic to the ambient noise received by tagged whales. Two analyses were conducted, one including all recording intervals, and one that excluded intervals when only the research vessel was present. For all data, significant predictors of noise levels were length (inverse relationship), number of propellers, and vessel speed, but only 15% of the variation in noise was explained by this model. When research-vessel-only intervals were excluded, vessel speed was the only significant predictor of noise levels, and explained 42% of the variation. Simple linear regressions (ignoring covariates) found that average vessel speed and number of propellers were the only significant correlates with noise levels. We conclude that vessel speed is the most important predictor of noise levels received by whales in this study. Thus, measures that reduce vessel speed in the vicinity of killer whales would reduce noise exposure in this population.