Marla M Holt

• Ph.D.
• Researcher at National Oceanic and Atmospheric Administration

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...

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 acidi...

Introduction Eastern Boundary Upwelling Systems are some of the most productive marine ecosystems in the world. Little is known about habitat associations and spatial distributions of marine predators during seasonal periods of low productivity because there are few at-sea surveys during this period. During low productivity or prey scarcity, predat...

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 f...

The Southern Resident Killer Whale (SRKW; Orcinus orca) population in Canadian Pacific waters is listed as Endangered under the Species at Risk Act. Efforts in support of recovery are underway from numerous government sectors, stakeholders, industry and others. Critical habitat has been identified for this population and includes the waters on the...

No PDF available ABSTRACT Killer whales face many anthropogenic threats including vessel traffic, noise, and reduced prey availability. Here, we use high-resolution suction-cup Dtags to study the behavior of endangered Southern Resident killer whales that rely on biosonar to hunt salmon, and investigate how proximate vessels affect foraging behavio...

No PDF available ABSTRACT Understanding ambient noise effects on foraging ecology of endangered killer whales is a necessary step toward predicting population-level consequences of acoustic disturbance. However, this has been limited by the difficulty of identifying prey capture which typically occurs out of sight, and by the challenge of obtaining...

No PDF available ABSTRACT Killer whales are the largest delphinid odontocete, a top predator and are globally distributed. Southern resident killer whales, which inhabit the Pacific coastal region of the northwest United States and Canada, are listed as endangered. Anthropogenic noise has been identified as a major threat to this populations of kil...

No PDF available ABSTRACT Since 2006, a network of hydrophones has been deployed along the outer coasts of Washington, Oregon, and California to improve our understanding of endangered Southern Resident killer whale (SRKW) movements outside the inland waters of the Salish Sea and refine Critical Habitat designation. During this time period, improve...

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 end...

No PDF available ABSTRACT Southern Resident killer whales (SRKW) were listed as endangered in 2005, requiring designation of Critical Habitat. At that time little was known about SRKW distribution in winter/spring along the outer coast. From 2004 to 2016, we conducted nine winter/spring surveys aboard NOAA ocean-class vessels to locate and follow S...

Accurate knowledge of behavior is necessary to effectively manage the effects of human activities on wildlife, including vessel-based whale-watching. Yet, the wholly aquatic nature of cetaceans makes understanding their basic behavioral ecology quite challenging. An endangered population of killer whales faces several identified threats including p...

Anthropogenic activities that have negative consequences on foraging outcomes warrant special concern in endangered species. Prey availability and vessel disturbance are identified risk factors of endangered Southern Resident killer whales (SRKW) as vessels and associated sounds can mask echolocation signals used for foraging and/or disrupt foragin...

It's the prey that matters Although many people think of dinosaurs as being the largest creatures to have lived on Earth, the true largest known animal is still here today—the blue whale. How whales were able to become so large has long been of interest. Goldbogen et al. used field-collected data on feeding and diving events across different types...

Northern elephant seals (Mirounga angustirostris) are massive, land-breeding marine mammals that produce loud, stereotyped calls during annual breeding seasons. To determine vocalization source levels emitted by competing males on a mainland breeding rookery, aerial calls were measured on-axis at 1 m from adult males using three different sound pre...

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 fo...

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 pop...

No PDF available ABSTRACT Animal Bioacoustics as a field of research involves the study of sound in non-human animals. The range of this field is wide and includes all aspects of sound production and reception, communication and associated behaviors, acoustic ecology and effects of noise/sound, and passive and active acoustic methods for monitoring...

No PDF available ABSTRACT Foraging in toothed whales and dolphins is fundamentally tied to the use of sound. Resident-type killer whales (Orcinus orca) use echolocation to locate and capture fast-moving salmon and other fish prey. In addition to prey availability, disturbance from vessels and noise is a threat to the endangered Southern Resident ki...

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...

Prey availability and disturbance from vessels and noise are identified threats to endangered Southern Resident killer whales. Vessel noise can mask echolocation signals used for hunting and/or disrupt foraging with implications for energy acquisition in a likely prey-limited population. We utilized suction cup-attached digital acoustic recording t...

The National Oceanic and Atmospheric Administration (NOAA)/National Park Service (NPS) Ocean Noise Reference Station (NRS) Network is an array of currently twelve calibrated autonomous passive acoustic recorders. The first NRS was deployed in June 2014, and eleven additional stations were added to the network during the following two years. The twe...

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 (β), fiber-type profiles, and myosin heavy chain expression of vocal musculature in two odontocetes: the...

Toothed whales use echolocation to sense their environment and capture prey. However, their reliance on acoustic information makes them vulnerable to sound exposure. Odontocetes modify echolocation signals in response to ambient noise levels, yet the metabolic cost of producing and modifying echolocation signals are unknown. Studies on bats found t...

Whale-watching is often conducted from motorized vessels, which contribute to underwater noise pollution and can disturb marine mammals. Protective measures can ameliorate some effects of disturbance but it is crucial to empirically assess effectiveness of such measures, particularly for endangered species. We quantitatively compared noise exposure...

Killer whales are apex predators with diet specializations that vary among ecotypes. Resident killer whales use broadband echolocation clicks to detect and capture fish prey in their underwater environment. Here, we describe the echolocation behavior of endangered Southern Resident killer whales using DTAGs to determine subsurface foraging activity...

Cetaceans produce different types of sounds that vary according to behavioral context. They also modify their acoustic signals in response to noise. The metabolic costs of producing social sounds and clicks were recently measured in two bottlenose dolphins using flow-through respirometry methods. For both sound types, metabolic rates significantly...

Odontocetes respond to vessels and anthropogenic noise by modifying vocal behavior, surface active behaviors, dive patterns, swim speed, direction of travel, and activity budgets. Exposure scenarios and behavioral responses vary across odontocetes. A literature review was conducted to determine relevant sources of disturbance and associated behavio...

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...

Analysis of qualitative characteristics as factors. The qualitative vessel characteristics: type, orientation and propulsion system, were also analyzed as factors in the negative log likelihood model. (PDF)

Noise levels and average vessel length. There was no significant relationship between received noise levels (dB re 1 μPa) and average vessel length (m) per interval. Variation in average vessel length was skewed toward the smaller vessels. (TIF)

Noise levels and average vessel type. There was no significant relationship between received noise levels (dB re 1 μPa) and the average vessel type per interval. Variation in average vessel type was heavily skewed toward inflatables and no intervals where vessels were on average of the medium or large hard bottom distinction. (TIF)

Average distance of vessels to tagged whales and average vessel type. The average distance (m) of vessels to tagged whales had a highly significant correlation with average vessel type per interval (F1, 55 = 27.77, p<0.001). (TIF)

Noise levels and average vessel orientation. There was no significant relationship between received noise levels (dB re 1 μPa) and the average vessel orientation per interval. Orientation descriptions are relating the motor’s relationship to the whale (i.e. motor away indicates the motor is facing away from the whale, see Table 1). There was little...

Noise levels and average distance of vessels to tagged whales. There was no significant relationship between received noise levels (dB re 1 μPa) and the average distance of vessels to tagged whales (m) per interval. Variation in average vessel distance was slightly skewed toward closer distances. (TIF)

Average distance of vessels to tagged whales and average vessel length. The average distance (m) of vessels to tagged whales had a highly significant correlation with average vessel length (m) per interval (F1, 55 = 30.62, p<0.001). (TIF)

Average vessel length and average vessel type. The average vessel length (m) had a highly significant correlation with average vessel type per interval (F1, 55 = 67.47, p<0.001). (TIF)

Underlying data for analyses. Spreadsheet includes: whale and vessel locations, vessel characteristics, and received noise levels for all intervals in this study. (XLSX)

Noise levels and average propulsion system. There was no significant relationship between received noise levels (dB re 1 μPa) and the average vessel propulsion system per interval. Variation in average vessel propulsion system was very poor with outboard motors present on most vessels per interval. (TIF)

Average number of propellers and average vessel speed. The average number of propellers had a marginally significant correlation with average vessel speed per interval (F1, 55 = 3.385, p = 0.071). (TIF)

AICc results of models with qualitative characteristics as factors. Negative log likelihood model results when vessel type, propulsion system and orientation were included as factors. The AICc value for the full model excluding research vessel-only intervals where each qualitative characteristic was assigned a numerical value (according to Table 1)...

Dolphins produce many types of sounds known to have distinct qualities and functionalities. Whistles, which function in social contexts, are much longer in duration and require close to twice the intranasal air pressure to produce relative to biosonar click production. Thus, it is predicted that whistle production would be energetically more costly...

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 inc...

In this investigation, acoustic tags (DTAGs) allow us to better understand noise exposure and potential behavioral effects in endangered Southern Resident killer whales (SRKWs). Designated critical habit of SRKWs includes summer foraging areas where vessel traffic from commercial shipping, whale-watching, and other boating activities is common. Ris...

Cetaceans that rely on their acoustic environment for key life history strategies are susceptible to noise effects from anthropogenic use such as ecotourism. Endangered Southern Resident killer whales (SRKW) are the primary target for vessel-based whale-watching in the Salish Sea. Vessel interactions and associated noise have been identified as pot...

Many species respond to increases in environmental noise by increasing the amplitude, duration, and/or repetition rate of their vocalizations. Potential costs of noise-induced vocal modifications include increased energetic costs but no empirical data in marine mammals exist. This study's objective was to compare the metabolic costs of communicativ...

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...

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 importa...

One calendar year of Automatic Identification System (AIS) ship-traffic data was paired with hydrophone recordings to assess ambient noise in northern Admiralty Inlet, Puget Sound, WA (USA) and to quantify the contribution of vessel traffic. The study region included inland waters of the Salish Sea within a 20 km radius of the hydrophone deployment...

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 gener...

Investigations on the behavioral responses of cetaceans to a variety of anthropogenic sounds are numerous, with a large proportion of these studies focused on responses to vessels (Nowacek et al. 2007; Richardson et al. 1995). Behavioral responses that affect activities associated with survival and reproduction are of particular concern because the...

Several studies have shown that cetaceans respond to the physical presence and/or acoustic emissions from marine vessels. For example, cetaceans perform surface-active behaviors (SABs) in response to an increase in the number of and/or close approaches by vessels (Lusseau 2006; Noren et al. 2009; Williams et al. 2002, 2009). SABs are often performe...

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 con...

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 s...

Southern resident killer whales (SRKWs) occur along the coastal and inland waters of the northeast Pacific Ocean. They are currently listed as endangered in both the U.S. and Canada. Risk factors that are potentially affecting population recovery include prey availability and quality and acoustic disturbance. This is because SRKWs specialize on Chi...

Harbor porpoise were reported to be the most commonly observed marine mammal in Puget Sound in the 1940s. Although little information on their status is available from the next three decades, by the mid-1970s when greater attention began to be paid to marine mammal distribution and abundance in this region, harbor porpoise appeared to have all but...

Whether an animal truly recognizes an individual or a simple rule-based category (e.g. neighbor or offspring) has important behavioral and evolutionary implications such as the accuracy of social reciprocity. Many tests of individual recognition have focused on neighboring territorial males ("dear enemy" or "neighbour-stranger" recognition). Unfort...

Aerial vocalization source levels were obtained for adult male northern elephant seals from 1999–2010. Vocalizations from known individuals (marked within years) were selected from three breeding seasons (1999–2000, 2004–2005, and 2009–2010) evenly spaced during this interval so that it is unlikely animals were resampled across seasons. Sound press...

Southern resident killer whales (SRKWs) are a fish?eating, endangered population that frequents the inland waters of Washington and British Columbia. Several risk factors have been identified that could hinder population recovery, including prey quantity and/or quality and disturbance by vessel presence and/or noise. There is a well?developed whale...

Killer whales produce population?specific pulsed calls, and remote acoustic monitoring has been utilized to better assess the seasonal distribution and movements of southern resident killer whales (SRKWs) in the coastal waters of Washington State due to the many factors that limit visual sightings. In 2008 and 2009, Ecological Acoustic Recorders (E...

Many animal sounds are directional in which the sound energy is focused in a direction that depends on the signaler?s orientation. In the 1970s, Ron Schusterman quantitatively showed this in barking California sea lions and dogs. Several investigators have suggested ways that such features might be particularly useful among individuals in acoustic...

The use of sound is essential to the survival of cetaceans. Therefore, anthropogenic sound exposure is a concern. Cetaceans can change the amplitude, duration, repetition rate, and/or frequency of sounds they produce to compensate for masking noise. Potential costs of such compensation are unknown, and no empirical data on the metabolic cost of sou...

Several studies have reported source levels for a variety of sounds produced by animals. This information can then be used to predict the range over which sounds may be used among individuals in communication networks and how the active space of such signals are affected by anthropogenic sounds. Some studies have also shown that animals readily mod...

Animals often produce sounds that are focused in a particular direction relative to the caller’s orientation. Although many studies have suggested ways in which directional signal design might have behavioural significance among vocally interacting individuals, there are few direct tests using experimental approaches. During the breeding season and...

Remote acoustic monitoring is often used to determine the seasonal and spatial distributions of vocal animals, particularly when conditions of other monitoring approaches are limited. Additionally, sound production patterns might be used to infer important activities of free-ranging animals in the absence of other cues. Animals produce sounds durin...

In addition to improving the understanding of auditory processing in pinnipeds, direct measures of temporal summation are relevant to the selection of signal parameters when conducting audiometric research, assessing the effects of signal duration on communication ranges, and evaluating the potential auditory impacts of anthropogenic signals. In th...

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 recor...

Anthropogenic sound exposure has been identified as a potential threat to endangered Southern Resident killer whales (SRKWs). Such exposure can mask important biological sounds including those used for social functions. Vocal animals might compensate for increased background noise by calling louder (the Lombard effect). In this study, amplitude com...

This document reviews what is currently known about potential acoustic impacts on endangered Southern Resident killer whales (SRKWs). Killer whales (Orcinus orca) use sound for echolocation, social communication, and passive listening. Ambient noise, including that from natural and anthropogenic sources, has the potential to interfere with the rece...

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...

In most masking experiments, target signals and sound intended to mask are located in the same position. Spatial release from masking (SRM) occurs when signals and maskers are spatially separated, resulting in detection improvement relative to when they are spatially co-located. In this study, SRM was investigated in a harbor seal, who naturally la...

Spatial release from masking (SRM) occurs when a signal and masker are spatially separated, resulting in improvement of signal detection relative to when they are spatially co‐located. Sea lions forage in the water, breed on land, produce airborne vocalizations that are associated with social and reproductive activities, and possess highly reduced...

A California sea lion that had previously been tested under water was assessed for noise‐induced temporary threshold shift (TTS) in air. One hundred ninety‐two controlled exposures of octave‐band noise centered at 2.5 kHz were conducted over a 3‐year period. The noise was varied in level (to 133 dB SPLre: 20 μPa) and duration (to 50 min) to generat...

Walruses (Odobenus rosmarus) have a range of anatomical specializations that can provide plasticity to their vocal emissions. These include respiratory adaptations related to breath‐holding and buoyancy and soft tissue adaptations of the mouth, lips, and tongue related to suction feeding. The aim of this study was to examine the extent to which con...

Pinnipeds (seals, sea lions, and walruses) emit and receive sounds both in air and water. Their amphibious natural history has resulted in a number of fascinating sensory capabilities, including but not limited to hearing, but has apparently precluded the evolution of sophisticated biosonar systems. Pinnipeds produce vocalizations in a variety of s...

Spatial release from masking (SRM) occurs when a signal and masker are spatially separated, resulting in improvement of signal detection relative to when they are spatially coincident. Harbor seals feed in the water but haul out on land for a variety of activities. There have been no SRM investigations conducted on harbor seals in air. In this stud...

In this study, minimum audible angles (MAAs) of aerial pure tones were measured in and compared between a northern elephant seal (Mirounga angustirostris), a harbor seal (Phoca vitulina), and a California sea lion (Zalophus californianus). Testing was conducted between 0.8 and 16 kHz in the elephant seal and 0.8 and 20 kHz in the harbor seal and se...

While attempting to gain access to receptive females, male northern elephant seals form dominance hierarchies through multiple dyadic interactions involving visual and acoustic signals. These signals are both highly stereotyped and directional. Previous behavioral observations suggested that males attend to the directional cues of these signals. We...

Recent work has shown that several pinniped species localize aerial broadband signals as accurately as some terrestrial carnivores. Additionally, both harbor seals and California sea lions can better localize both the lower and higher frequencies of their hearing range compared to performance at intermediate frequencies. These results are congruent...

A brief survey of the literature in animal behavioral psychophysics shows that researchers use numerous methods to obtain information on sound detection,discrimination, and identification. Behavioral methodology in animal psychoacoustics includes both classical and operant conditioning, go/no‐go or multiple alternative forced‐choice tasks, and vari...

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 Pa to generate a variety of equal sound exposure level conditions. Hearing thresholds were measured at the cent...

Stimulus durations shorter than some critical value result in elevated signal‐detection thresholds due to temporal integration (or temporal summation) properties of the auditory system. These properties are important from a theoretical perspective in terms of the trade‐offs of stimulus duration and intensity on sensitivity. From a methodological pe...

Although many pinnipeds (seals, sea lions, and walruses) emit broadband calls on land as part of their communication system, few studies have addressed these animals' ability to localize aerial broadband sounds. In this study, the aerial sound localization acuities of a female northern elephant seal (Mirounga angustirostris), a male harbor seal (Ph...

Pinnipeds (seals, sea lions, and walruses) emit broadband calls on land as part of their communication system in order to coordinate their reproductive activities. How well do they localize these types of signals? In this study, the aerial sound localization acuities of a harbor seal (Phoca vitulina), a California sea lion (Zalophus californianus),...

Our behavioral studies of pinniped auditory processing, including amphibious hearing, auditory masking, and temporary threshold shift (TTS), have provided comparative data on hearing and the potential effects of anthropogenic noise for three pinniped species. Differences for one harbor seal between aerial thresholds measured using headphones in a n...

Although all pinnipeds communicate acoustically in air, most previous research on sound localization has been done under water. We have recently shown that several pinniped species localize aerial broadband signals as well as some terrestrial carnivores [Holt et al., J. Acoust. Soc. Am. 113 (2003)]. However, it is unclear which frequencies are part...

There is no convincing evidence that any of the 33 pinniped species evolved acoustic specializations for echolocation. However, all species produce and localize signals amphibiously in different communicative contexts. In the setting of sexual selection, aquatic mating male phocids and walruses tend to emit underwater calls, while male otariids and...

Aerial hearing sensitivity was measured in pinnipeds in a sound attenuating, hemi-anechoic chamber. Thresholds at 12 frequencies between 0.1 and 32.5 kHz were obtained behaviorally for three individuals (a California sea lion, a harbor seal, and a northern elephant seal) and compared to thresholds obtained using headphones in less controlled testin...

Animals often increase the amplitude (the Lombard effect), duration, and/or repetition rate of their acoustic signals as a strategy to help reduce the probability of masking from environmental sounds (NRC 2003). Although accumulating evidence from recent research (Scheifele et al. 2005, Holt et al. 2009, Parks et al. 2010) illustrates that several...