Understanding vessel noise across a network of marine protected areas.

Protected areas are typically managed as a network of sites exposed to varying anthropogenic conditions. Managing these networks benefits from monitoring of conditions across sites to help prioritize coordinated efforts. Monitoring marine vessel activity and related underwater radiated noise impacts across a network of protected areas, like the U.S. National Marine Sanctuary system, helps managers ensure the quality of habitats used by a wide range of marine species. Here, we use underwater acoustic detections of vessels to quantify different characteristics of vessel noise at 25 locations within eight marine sanctuaries including the Hawaiian Archipelago and the U.S. east and west coasts. Vessel noise metrics, including temporal presence and sound levels, were paired with Automatic Identification System (AIS) vessel tracking data to derive a suite of robust vessel noise indicators for use across the network of marine protected areas. Network-wide comparisons revealed a spectrum of vessel noise conditions that closely matched AIS vessel traffic composition. Shifts in vessel noise were correlated with the decrease in vessel activity early in the COVID-19 pandemic, and vessel speed reduction management initiatives. Improving our understanding of vessel noise conditions in these protected areas can help direct opportunities for reducing vessel noise, such as establishing and maintaining noise-free periods, enhancing port efficiency, engaging with regional and international vessel quieting initiatives, and leveraging co-benefits of management actions for reducing ocean noise.

Behavioural responses of fin whales to military mid-frequency active sonar.

The effect of active sonars on marine mammal behaviour is a topic of considerable interest and scientific investigation. Some whales, including the largest species (blue whales, Balaenoptera musculus), can be impacted by mid-frequency (1-10 kHz) military sonars. Here we apply complementary experimental methods to provide the first experimentally controlled measurements of behavioural responses to military sonar and similar stimuli for a related endangered species, fin whales (Balaenoptera physalus). Analytical methods include: (i) principal component analysis paired with generalized additive mixed models; (ii) hidden Markov models; and (iii) structured expert elicitation using response severity metrics. These approaches provide complementary perspectives on the nature of potential changes within and across individuals. Behavioural changes were detected in five of 15 whales during controlled exposure experiments using mid-frequency active sonar or pseudorandom noise of similar frequency, duration and source and received level. No changes were detected during six control (no noise) sequences. Overall responses were more limited in occurrence, severity and duration than in blue whales and were less dependent upon contextual aspects of exposure and more contingent upon exposure received level. Quantifying the factors influencing marine mammal responses to sonar is critical in assessing and mitigating future impacts.

Call repertoire and inferred ecotype presence of killer whales (Orcinus orca) recorded in the southeastern Chukchi Sea.

Killer whales occur in the Arctic but few data exist regarding the ecotypes present. The calling behavior differs among ecotypes, which can be distinguished based on pulsed call type, call rate, and bandwidth. In this study, a passive acoustic recorder was deployed 75 km off Point Hope, Alaska, in the southeastern Chukchi Sea to identify which ecotypes were present. A total of 1323 killer whale pulsed calls were detected on 38 of 276 days during the summers (June-August) of 2013-2015. The majority of calls (n = 804, 61%) were recorded in 2013 with the most calls recorded in July (76% of total calls). The calls were manually grouped into six categories: multipart, downsweep, upsweep, modulated, single modulation, and flat. Most detections were flat (n = 485, 37%) or multipart calls (n = 479, 36%), which contained both high and low frequency components. Call comparisons with those reported in the published literature showed similarities with other transient populations in fundamental frequency contour point distribution and median frequency. This study provides the first comprehensive catalog of transient killer whale calls in this region as well as reports on previously undescribed calls.

Animal-Borne Metrics Enable Acoustic Detection of Blue Whale Migration.

Linking individual and population scales is fundamental to many concepts in ecology [1], including migration [2, 3]. This behavior is a critical [4] yet increasingly threatened [5] part of the life history of diverse organisms. Research on migratory behavior is constrained by observational scale [2], limiting ecological understanding and precise management of migratory populations in expansive, inaccessible marine ecosystems [6]. This knowledge gap is magnified for dispersed oceanic predators such as endangered blue whales (Balaenoptera musculus). As capital breeders, blue whales migrate vast distances annually between foraging and breeding grounds, and their population fitness depends on synchrony of migration with phenology of prey populations [7, 8]. Despite previous studies of individual-level blue whale vocal behavior via bio-logging [9, 10] and population-level acoustic presence via passive acoustic monitoring [11], detection of the life history transition from foraging to migration remains challenging. Here, we integrate direct high-resolution measures of individual behavior and continuous broad-scale acoustic monitoring of regional song production (Figure 1A) to identify an acoustic signature of the transition from foraging to migration in the Northeast Pacific population. We find that foraging blue whales sing primarily at night, whereas migratory whales sing primarily during the day. The ability to acoustically detect population-level transitions in behavior provides a tool to more comprehensively study the life history, fitness, and plasticity of population behavior in a dispersed, capital breeding population. Real-time detection of this behavioral signal can also inform dynamic management efforts [12] to mitigate anthropogenic threats to this endangered population [13, 14]).

Variations in received levels on a sound and movement tag on a singing humpback whale: Implications for caller identification.

Bio-logging devices are advancing the understanding of marine animal behavior, but linking sound production and behavior of individual baleen whales is still unreliable. Tag placement potentially within the near field of the sound source creates uncertainty about how tagged animal sounds will register on recorders. This study used data from a tagged singing humpback whale to evaluate this question of how sound levels present on a tag when calls are produced by a tagged animal. Root-mean-square (rms) received levels (RLs) of song units ranged from 112 to 164 dB re 1 µPa rms, with some, but not all, of the lower frequency units registering on the tag's 800 Hz accelerometer sensor. Fifty-nine percent of recorded units measured lower acoustic RLs than previously reported source levels for humpback song, but signal-to-noise ratios (SNRs) were 30-45 dB during periods of the dive with low noise. This research highlights that tag RL does not alone predict caller identity, argues for higher SNR thresholds if using SNR to inform decisions about the source of a call, and provides a baseline for future research identifying diagnostic properties of tagged animal calls in cetacean bioacoustic tag datasets.

From a calf's perspective: humpback whale nursing behavior on two US feeding grounds.

Nursing influences growth rate and overall health of mammals; however, the behavior is difficult to study in wild cetaceans because it occurs below the surface and can thus be misidentified from surface observations. Nursing has been observed in humpback whales on the breeding and calving grounds, but the behavior remains unstudied on the feeding grounds. We instrumented three dependent calves (four total deployments) with combined video and 3D-accelerometer data loggers (CATS) on two United States feeding grounds to document nursing events. Two associated mothers were also tagged to determine if behavior diagnostic of nursing was evident in the mother's movement. Animal-borne video was manually analyzed and the average duration of successful nursing events was 23 s (±7 sd, n = 11). Nursing occurred at depths between 4.1-64.4 m (along the seafloor) and in close temporal proximity to foraging events by the mothers, but could not be predicted solely by relative positions of mother and calf. When combining all calf deployments, successful nursing was documented eleven times; totaling only 0.3% of 21.0 hours of video. During nursing events, calves had higher overall dynamic body acceleration (ODBA) and increased fluke-stroke rate (FSR) compared to non-nursing segments (Mixed effect models, ODBA: F1,107 = 13.57756, p = 0.0004, FSR: F1,107 = 32.31018, p < 0.0001). In contrast, mothers had lower ODBA and reduced FSR during nursing events compared to non-nursing segments. These data provide the first characterization of accelerometer data of humpback whale nursing confirmed by animal-borne video tags and the first analysis of nursing events on feeding grounds. This is an important step in understanding the energetic consequences of lactation while foraging.

Energetic and physical limitations on the breaching performance of large whales.

The considerable power needed for large whales to leap out of the water may represent the single most expensive burst maneuver found in nature. However, the mechanics and energetic costs associated with the breaching behaviors of large whales remain poorly understood. In this study we deployed whale-borne tags to measure the kinematics of breaching to test the hypothesis that these spectacular aerial displays are metabolically expensive. We found that breaching whales use variable underwater trajectories, and that high-emergence breaches are faster and require more energy than predatory lunges. The most expensive breaches approach the upper limits of vertebrate muscle performance, and the energetic cost of breaching is high enough that repeated breaching events may serve as honest signaling of body condition. Furthermore, the confluence of muscle contractile properties, hydrodynamics, and the high speeds required likely impose an upper limit to the body size and effectiveness of breaching whales.

Humpback whale song occurrence reflects ecosystem variability in feeding and migratory habitat of the northeast Pacific.

This study examines the occurrence of humpback whale (Megaptera novaeangliae) song in the northeast Pacific from three years of continuous recordings off central California (36.713°N, 122.186°W). Song is prevalent in this feeding and migratory habitat, spanning nine months of the year (September-May), peaking in winter (November-January), and reaching a maximum of 86% temporal coverage (during November 2017). From the rise of song in fall through the end of peak occurrence in winter, song length increases significantly from month to month. The seasonal peak in song coincides with the seasonal trough in day length and sighting-based evidence of whales leaving Monterey Bay, consistent with seasonal migration. During the seasonal song peak, diel variation shows maximum occurrence at night (69% of the time), decreasing during dawn and dusk (52%), and further decreasing with increasing solar elevation during the day, reaching a minimum near solar noon (30%). Song occurrence increased 44% and 55% between successive years. Sighting data within the acoustic detection range of the hydrophone indicate that variation in local population density was an unlikely cause of this large interannual variation. Hydrographic data and modeling of acoustic transmission indicate that changes in neither habitat occupancy nor acoustic transmission were probable causes. Conversely, the positive interannual trend in song paralleled major ecosystem variations, including similarly large positive trends in wind-driven upwelling, primary productivity, and krill abundance. Further, the lowest song occurrence during the first year coincided with anomalously warm ocean temperatures and an extremely toxic harmful algal bloom that affected whales and other marine mammals in the region. These major ecosystem variations may have influenced the health and behavior of humpback whales during the study period.

Acoustic influence of underwater mobile survey vehicles on the soundscape of Pacific rockfish habitat.

Noise produced by scientific equipment during fisheries surveys is largely unstudied, though these sound sources may have an effect on the organisms of interest and on their resultant stock assessments. This paper describes acoustic signatures of two underwater mobile vehicles and accompanying research ships used to survey demersal fishes, and discusses the acoustic contributions of the survey equipment to rockfish habitat. Increases in noise over ambient levels were high, but the majority of sound energy was generated by communication and navigation instrumentation on the ships and survey vehicles, and was out of the expected sensitivity range for fish hearing.

Behavioral responses of individual blue whales (Balaenoptera musculus) to mid-frequency military sonar.

This study measured the degree of behavioral responses in blue whales (Balaenoptera musculus) to controlled noise exposure off the southern California coast. High-resolution movement and passive acoustic data were obtained from non-invasive archival tags (n=42) whereas surface positions were obtained with visual focal follows. Controlled exposure experiments (CEEs) were used to obtain direct behavioral measurements before, during and after simulated and operational military mid-frequency active sonar (MFAS), pseudorandom noise (PRN) and controls (no noise exposure). For a subset of deep-feeding animals (n=21), active acoustic measurements of prey were obtained and used as contextual covariates in response analyses. To investigate potential behavioral changes within individuals as a function of controlled noise exposure conditions, two parallel analyses of time-series data for selected behavioral parameters (e.g. diving, horizontal movement and feeding) were conducted. This included expert scoring of responses according to a specified behavioral severity rating paradigm and quantitative change-point analyses using Mahalanobis distance statistics. Both methods identified clear changes in some conditions. More than 50% of blue whales in deep-feeding states responded during CEEs, whereas no changes in behavior were identified in shallow-feeding blue whales. Overall, responses were generally brief, of low to moderate severity, and highly dependent on exposure context such as behavioral state, source-to-whale horizontal range and prey availability. Response probability did not follow a simple exposure-response model based on received exposure level. These results, in combination with additional analytical methods to investigate different aspects of potential responses within and among individuals, provide a comprehensive evaluation of how free-ranging blue whales responded to mid-frequency military sonar.

Context-dependent variability in blue whale acoustic behaviour.

Acoustic communication is an important aspect of reproductive, foraging and social behaviours for many marine species. Northeast Pacific blue whales (Balaenoptera musculus) produce three different call types-A, B and D calls. All may be produced as singular calls, but A and B calls also occur in phrases to form songs. To evaluate the behavioural context of singular call and phrase production in blue whales, the acoustic and dive profile data from tags deployed on individuals off southern California were assessed using generalized estimating equations. Only 22% of all deployments contained sounds attributed to the tagged animal. A larger proportion of tagged animals were female (47%) than male (13%), with 40% of unknown sex. Fifty per cent of tags deployed on males contained sounds attributed to the tagged whale, while only a few (5%) deployed on females did. Most calls were produced at shallow depths (less than 30 m). Repetitive phrasing (singing) and production of singular calls were most common during shallow, non-lunging dives, with the latter also common during surface behaviour. Higher sound production rates occurred during autumn than summer and they varied with time-of-day: singular call rates were higher at dawn and dusk, while phrase production rates were highest at dusk and night.

Context-dependent lateralized feeding strategies in blue whales.

Lateralized behaviors benefit individuals by increasing task efficiency in foraging and anti-predator behaviors [1-4]. The conventional lateralization paradigm suggests individuals are left or right lateralized, although the direction of this laterality can vary for different tasks (e.g. foraging or predator inspection/avoidance). By fitting tri-axial movement sensors to blue whales (Balaenoptera musculus), and by recording the direction and size of their rolls during lunge feeding events, we show how these animals differ from such a paradigm. The strength and direction of individuals' lateralization were related to where and how the whales were feeding in the water column. Smaller rolls (≤180°) predominantly occurred at depth (>70 m), with whales being more likely to rotate clockwise around their longest axis (right lateralized). Larger rolls (>180°), conversely, occurred more often at shallower depths (<70 m) and were more likely to be performed anti-clockwise (left lateralized). More acrobatic rolls are typically used to target small, less dense krill patches near the water's surface [5,6], and we posit that the specialization of lateralized feeding strategies may enhance foraging efficiency in environments with heterogeneous prey distributions.

Measurements of humpback whale song sound levels received by a calf in association with a singer.

Male humpback whales produce loud "songs" on the wintering grounds and some sing while escorting mother-calf pairs, exposing them to near-continuous sounds at close proximity. An Acousonde acoustic and movement recording tag deployed on a calf off Maui, Hawaii captured sounds produced by a singing male escort. Root-mean-square received levels ranged from 126 to 158 dB re 1 µPa. These levels represent rare direct measurements of sound to which a newly born humpback calf may be naturally exposed by a conspecific, and may provide a basis for informed decisions regarding anthropogenic sound levels projected near calves.

Multiple-stage decisions in a marine central-place forager.

Air-breathing marine animals face a complex set of physical challenges associated with diving that affect the decisions of how to optimize feeding. Baleen whales (Mysticeti) have evolved bulk-filter feeding mechanisms to efficiently feed on dense prey patches. Baleen whales are central place foragers where oxygen at the surface represents the central place and depth acts as the distance to prey. Although hypothesized that baleen whales will target the densest prey patches anywhere in the water column, how depth and density interact to influence foraging behaviour is poorly understood. We used multi-sensor archival tags and active acoustics to quantify Antarctic humpback whale foraging behaviour relative to prey. Our analyses reveal multi-stage foraging decisions driven by both krill depth and density. During daylight hours when whales did not feed, krill were found in deep high-density patches. As krill migrated vertically into larger and less dense patches near the surface, whales began to forage. During foraging bouts, we found that feeding rates (number of feeding lunges per hour) were greatest when prey was shallowest, and feeding rates decreased with increasing dive depth. This strategy is consistent with previous models of how air-breathing diving animals optimize foraging efficiency. Thus, humpback whales forage mainly when prey is more broadly distributed and shallower, presumably to minimize diving and searching costs and to increase feeding rates overall and thus foraging efficiency. Using direct measurements of feeding behaviour from animal-borne tags and prey availability from echosounders, our study demonstrates a multi-stage foraging process in a central place forager that we suggest acts to optimize overall efficiency by maximizing net energy gain over time. These data reveal a previously unrecognized level of complexity in predator-prey interactions and underscores the need to simultaneously measure prey distribution in marine central place forager studies.

Radiated Sound of a High-Speed Water-Jet-Propelled Transportation Vessel.

The radiated noise from a high-speed water-jet-propelled catamaran was measured for catamaran speeds of 12, 24, and 37 kn. The radiated noise increased with catamaran speed, although the shape of the noise spectrum was similar for all speeds and measuring hydrophone depth. The spectra peaked at ~200 Hz and dropped off continuously at higher frequencies. The radiated noise was 10-20 dB lower than noise from propeller-driven ships at comparable speeds. The combination of low radiated noise and high speed could be a factor in the detection and avoidance of water-jet-propelled ships by baleen whales.

Evidence for acoustic communication among bottom foraging humpback whales.

Humpback whales (Megaptera novaeangliae), a mysticete with a cosmopolitan distribution, demonstrate marked behavioural plasticity. Recent studies show evidence of social learning in the transmission of specific population level traits ranging from complex singing to stereotyped prey capturing behaviour. Humpback whales have been observed to employ group foraging techniques, however details on how individuals coordinate behaviour in these groups is challenging to obtain. This study investigates the role of a novel broadband patterned pulsed sound produced by humpback whales engaged in bottom-feeding behaviours, referred to here as a 'paired burst' sound. Data collected from 56 archival acoustic tag deployments were investigated to determine the functional significance of these signals. Paired burst sound production was associated exclusively with bottom feeding under low-light conditions, predominantly with evidence of associated conspecifics nearby suggesting that the sound likely serves either as a communicative signal to conspecifics, a signal to affect prey behaviour, or possibly both. This study provides additional evidence for individual variation and phenotypic plasticity of foraging behaviours in humpback whales and provides important evidence for the use of acoustic signals among foraging individuals in this species.

Underwater acrobatics by the world's largest predator: 360° rolling manoeuvres by lunge-feeding blue whales.

The extreme body size of blue whales requires a high energy intake and therefore demands efficient foraging strategies. As an obligate lunge feeder on aggregations of small zooplankton, blue whales engulf a large volume of prey-laden water in a single, rapid gulp. The efficiency of this feeding mechanism is strongly dependent on the amount of prey that can be captured during each lunge, yet food resources tend to be patchily distributed in both space and time. Here, we measured the three-dimensional kinematics and foraging behaviour of blue whales feeding on krill, using suction-cup attached multi-sensor tags. Our analyses revealed 360° rolling lunge-feeding manoeuvres that reorient the body and position the lower jaws so that a krill patch can be engulfed with the whale's body inverted. We also recorded these rolling behaviours when whales were in a searching mode in between lunges, suggesting that this behaviour also enables the whale to visually process the prey field and maximize foraging efficiency by surveying for the densest prey aggregations. These results reveal the complex manoeuvrability that is required for large rorqual whales to exploit prey patches and highlight the need to fully understand the three-dimensional interactions between predator and prey in the natural environment.

Humpback whale song and foraging behavior on an antarctic feeding ground.

Reports of humpback whale (Megaptera novaeangliae) song chorusing occurring outside the breeding grounds are becoming more common, but song structure and underwater behavior of individual singers on feeding grounds and migration routes remain unknown. Here, ten humpback whales in the Western Antarctic Peninsula were tagged in May 2010 with non-invasive, suction-cup attached tags to study foraging ecology and acoustic behavior. Background song was identified on all ten records, but additionally, acoustic records of two whales showed intense and continuous singing, with a level of organization and structure approaching that of typical breeding ground song. The songs, produced either by the tagged animals or close associates, shared phrase types and theme structure with one another, and some song bouts lasted close to an hour. Dive behavior of tagged animals during the time of sound production showed song occurring during periods of active diving, sometimes to depths greater than 100 m. One tag record also contained song in the presence of feeding lunges identified from the behavioral sensors, indicating that mating displays occur in areas worthy of foraging. These data show behavioral flexibility as the humpbacks manage competing needs to continue to feed and to prepare for the breeding season during late fall. This may also signify an ability to engage in breeding activities outside of the traditional, warm water breeding ground locations.

Common humpback whale (Megaptera novaeangliae) sound types for passive acoustic monitoring.

Humpback whales (Megaptera novaeangliae) are one of several baleen whale species in the Northwest Atlantic that coexist with vessel traffic and anthropogenic noise. Passive acoustic monitoring strategies can be used in conservation management, but the first step toward understanding the acoustic behavior of a species is a good description of its acoustic repertoire. Digital acoustic tags (DTAGs) were placed on humpback whales in the Stellwagen Bank National Marine Sanctuary to record and describe the non-song sounds being produced in conjunction with foraging activities. Peak frequencies of sounds were generally less than 1 kHz, but ranged as high as 6 kHz, and sounds were generally less than 1 s in duration. Cluster analysis distilled the dataset into eight groups of sounds with similar acoustic properties. The two most stereotyped and distinctive types ("wops" and "grunts") were also identified aurally as candidates for use in passive acoustic monitoring. This identification of two of the most common sound types will be useful for moving forward conservation efforts on this Northwest Atlantic feeding ground.

Humpback whales harbour a combination of specific and variable skin bacteria.

Investigations of marine mammal skin-associated microbiota are limited to cultivation-based studies of lesioned individuals, resulting in a lack of understanding about the composition of 'normal' skin-associated microbial communities, their variation among individuals, and whether or not the microbial communities change with host health or environmental exposures. In this study, bacterial communities associated with the skin of 19 North Pacific humpback whales (Megaptera novaeangliae), including skin from three health-compromised individuals, were examined using small subunit ribosomal RNA gene-based culture-independent techniques. These analyses revealed that the skin-associated bacteria were significantly different from free-living bacterial communities in the surrounding seawater. Two novel groups within the Flavobacteriaceae family of the Bacteroidetes phylum were found to be associated with multiple whales, including a species within the Tenacibaculum genus that associated with 95% of the individuals. Statistical analyses revealed that a group of eight 'healthy' whales harboured similar microbial communities, while the health-compromised and other 'healthy' animals harboured communities that were unique to the specific animal. These results describe two components of the whale skin bacterial community: a specific and potentially co-evolved fraction, and a more variable microbial community fraction that may offer a diagnostic-type tool for investigating the health and life-related events of these endangered animals.