Currently, there are several research programs being carried out by our staff in the lab and in the field. Our underwater laboratory research takes place in outdoor, saltwater pools surrounded by haul out space for the animals. Much of our ongoing lab research occurs in our aerial testing facility, a hemi-anechoic aerial chamber that is located near the pools and animal living spaces. This facility is a unique research tool that is allowing us to investigate many fine-scale aspects of hearing and cognition in marine mammals.

We also conduct research at other facilities and field sites, including behavioral and neurophysiological research with pinnipeds at The Marine Mammal Center in Sausalito, California, research on sea otter acoustics with the Monterey Bay Aquarium, work on vocal learning with walruses at Six Flags Discovery Kingdom in Vallejo, California, hearing research with steller sea lions at Vancouver Aquarium and the University of British Columbia, and field research at various sites in California including Año Nuevo State Reserve.
 

Our current research programs include:
Hearing and the effects of noise on pinnipeds
Psychoacoustics of arctic seals
Underwater high-frequency hearing in pinnipeds and humans
Sensorimotor synchronization to rhythmic auditory stimuli in California sea lions
Field research on elephant seal acoustics
Vocal learning in seals and walruses
Underwater wake detection and tracking by harbor seals
Bioacoustics of southern sea otters
Cognitive effects of neurotoxic domoic acid exposure on California sea lions
Cross-modal classification in California sea lions
Neurophysiological auditory processing in pinnipeds
Hearing and the effects of noise on pinnipeds
Our lab has been focused primarily on the investigation of pinniped acoustics since 1994. The main impetus for this work was growing concern about increasing levels of noise in the oceans, from sources including shipping, ocean exploration, and military operations. At the time this work was begun, relatively little was known about hearing in pinnipeds, although many species occupy particularly noisy regions close to shore. We have established auditory profiles for each of our three resident species (California sea lion, harbor seal, and northern elephant seal) by testing their hearing in air and under water at a range of different frequencies. From this information, we can generate audiograms, or hearing curves, that allow us to determine frequency ranges of hearing, regions of best hearing sensitivity, and how hearing sensitivities in different media correlate to differences in life history. To expand these auditory profiles, we examine effects of noise on hearing using two different experimental procedures. Masking experiments, which involve signal detection against a noisy background, help us to assess how the simultaneous presence of noise effects hearing, while the temporary threshold shift (TTS) experiments, which involve signal detection following exposure to a noisy background, allow us to evaluate the residual effects of noise exposure on hearing. The results of these experiments are used to generate models which predict how noise of a given intensity, duration, or character will effect the hearing of free-ranging pinnipeds. These data are useful by regulatory agencies charged with establishing policies to protect pinnipeds and other marine mammals from the damaging effects of anthropogenic noise.

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Psychoacoustics of arctic seals
Ongoing work in our lab is examining the auditory capabilities of Arctic seals, specifically spotted (Phoca largha), ringed (Pusa hispida), and bearded seals (Erignathus barbatus). Our goal is to characterize hearing sensitivity in these species, and to learn more about how noise may interfere with their ability to detect important sounds in the environment. Because seals are amphibious—foraging at sea but remaining tied to land for activities such as pupping and molting—we are investigating their hearing both above and below the water's surface. Hearing in spotted seals has not previously been measured, either in terms of basic capabilities or susceptibility to noise effects. While there are some published hearing data for ringed seals, we know very little about their sensitivity to low-frequency sounds, which is a substantial knowledge gap considering that many anthropogenic noise sources have significant energy at low frequencies. Finally, nothing is currently known about the hearing sensitivity of bearded seals, a more distantly related species that is known to produce unique underwater vocalizations associated with breeding. Our work will provide new data about hearing for these three under-studied seal species, and will also address the effects of common industry noises on their hearing. More specifically, we are also working to measure the simultaneous and residual auditory effects of seismic airguns, which are increasingly used in the Arctic for oil and gas exploration. The results of these studies will give us a broader understanding of hearing in ice-living seal species, and pinnipeds (seals, sea lions, and walruses) in general. Ultimately, this work will also inform best management practices regarding the effects of anthropogenic noise on ice-living seals. This project is being funded by the OGP E&P Sound and Marine Life Joint Industry Programme. Graduate student Jillian Sills is leading this effort in our laboratory.

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Underwater high-frequency hearing in pinnipeds and humans
Current work at our lab includes investigating how seals, sea lions, and humans hear underwater sounds at very high frequencies. We are particularly interested in how diving mammals perceive sound at frequencies considered to be beyond the limits of their functional hearing range. This work began as a collaborative effort between our team and fisheries biologists to examine the ability of trained pinnipeds to detect the outputs of ultrasonic acoustic tags that are typically used to track anadromous fish. The motivation behind this project was to test the viability of the so-called "dinner bell" hypothesis: marine mammals that can detect acoustic tag outputs use this information to selectively predate tagged fish. Despite the fact that the frequency of the acoustic tag we tested was approximately twice the high-frequency hearing limit for a sea lion subject, our experiment showed that the tag was clearly audible to this animal. This is one example of how the current lack of understanding about pinniped hearing at high frequencies can have detrimental effects. More research is needed in this area given the recent proliferation of high-frequency marine technologies, and we are currently working to extend this research to even higher frequencies. Our ongoing study should generate ultra-high frequency hearing profiles for seals and sea lions, as well as allow us to examine how sound energy is transmitted to the ear in underwater hearing. Similar research with human divers should enable us to determine how well humans can hear ultrasound in water and give us insight into the mechanisms underlying this ability. Graduate student Kane Cunningham is leading this research effort in our laboratory.

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Sensorimotor synchronization to rhythmic auditory stimuli in California sea lions
The capability to synchronize movement to a steady beat (called "sensorimotor synchronization") is a behavioral capability once thought to be unique to humans. Recently, this ability has been identified in a few other species, most notably the sulfur-crested cockatoo. Previously, this ability had only been shown in animals demonstrating vocal mimicry. Due to this, it has been suggested that sensorimotor synchronization to rhythmic stimuli could be a byproduct of evolutionary adaptations supporting complex vocal learning. In order to explicitly test this hypothesis, graduate student Peter Cook and researcher Andrew Rouse have trained and tested sensorimotor synchronization in a mammal widely regarded as being vocally stereotypic: the California sea lion. Our sea lion subject, Ronan, has learned not only to reliably synchronize a continuous head bob to simple rhythmic sounds, but successfully demonstrated the ability to synchronize her movements with music at different tempos. These results present a strong challenge to the supposed primacy of vocal mimicry and indicate that the capacity for rhythmic entrainment might be more widespread than previously thought, an argument described in a 2013 publication highlighting Ronan's results in The Journal of Comparative Psychology.

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Field research on elephant seal acoustics
We are interested in studying sound production, as well as sound reception, and in using our understanding of sensory systems to inform our understanding of naturally occurring behavior. Our ongoing research on northern elephant seal acoustics is conducted seasonally at Ano Nuevo State Reserve, which is located about 20 miles north of our laboratory. The general aims of this work have included measuring the source levels of aerial vocalizations produced by all age and sex classes of northern elephant seals and measuring ambient noise levels in the seal rookeries during the breeding season. In the past few years we have expanded to recording and analyzing temporal and spectral components of male vocalizations to investigate whether or not dominance information is contained within calls, which vary greatly by individual. We are also looking at amphibious sound production by males stationed along the shoreline during the breeding season. These data provide a useful complement to our research on elephant seal hearing. The combination of our field studies with our laboratory data on elephant seal acoustics is yielding insight into intraspecific communication by allowing us to predict the distances over which an individual's calls may be detected by other seals; for example, the effective communication ranges of a mother vocalizing to her pup or an alpha male's rumbling threats directed towards a breeding rival. Additionally, we have uncovered several interesting characteristics of vocal and visual signaling in sub-adult male and adult female elephant seals, which have led us to investigate aspects of vocalization stereotypy and the influence of social context on vocal communication. This work is being led by graduate student Caroline Casey, who works closely with Dr. Reichmuth and several international collaborators on this effort. For some photos and a more detailed project description, please click here.

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Vocal learning in seals and walruses
Many of our field studies deal generally with sound production and acoustic communication in pinnipeds, especially in noisy environments. However, there are some interesting aspects of sound production that are difficult to study in wild animals. Our ongoing research with captive seals at Long Marine Lab and captive walruses at Six Flags Discovery Kingdom concerns the extent to which pinnipeds are capable of vocal learning. While evidence for vocal production learning is limited in most nonhuman mammals, marine mammals appear to have a unique propensity for learning how to modify their sounds as a result of interactions with the social and physical environment. Our work involves looking at spontaneous (untrained) components of vocalizations, such as annual cycles in vocal behavior, the types of sounds emitted, and the behavioral contexts in which these sounds are produced. We also use food reinforcement and operant conditioning in order to determine how plastic these sound emissions are. Such studies help us to better understand the innate vs. learned aspects of acoustic communication in these animals. We are also interested in examining the proximal mechanisms that underlie sound production in these animals. As walruses produce a variety of unusual sounds using laryngeal, supra-laryngeal, and sub-laryngeal structures, they are ideal subjects for this research. We are collaborating with Dr. Ole Naesbye Larsen, a neurobiologist specializing in animal communication from Southern Denmark University to apply a variety of acoustic and imaging techniques.

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Underwater wake detection and tracking by harbor seals
We are conducting research on a fascinating but poorly understood sensory modality--that of hydrodynamic reception--in harbor seals. This work is inspired in part by the research findings of our colleagues in Germany, who have shown that harbor seals are capable of detecting and following underwater wakes as they decay in time. We are currently cooperating with partners at the University of Virginia who are tackling this research area from an engineering standpoint. Our studies with a trained seal have informed the development and fabrication of bio-inspired prototypes and instrumentation to be used for real world flow-field characterization. Motion analysis on the behavioral performance of a seal trained to follow underwater wakes while wearing a blindfold is enabling us to characterize the detection and discrimination capabilities of this specialized sensory system.

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Bioacoustics of southern sea otters
In 2007, our lab began an investigation into the bioacoustics of the southern sea otter, an amphibious marine mammal whose sensory biology we know surprisingly little about. Sea otters are coastal-living animals with a unique life history—while they spend nearly all of their time in the water, they carry out many important life functions at the surface. Studying sea otter sensory biology will provide us with a better understanding of their evolutionary biology and behavioral ecology, as well as the evolutionary pressures shaping underwater perception in marine mammals. This information will also be beneficial to management of critical coastal habitats. In an effort to better understand the role that sound plays in the perceptual world of sea otters, we are investigating their auditory capabilities using a behavioral approach. Led by former graduate student Asila Ghoul, the main focus of this project is to measure hearing sensitivity by obtaining in-air and under-water hearing curves, or audiograms. This work is conducted in cooperation with our partners at the Monterey Bay Aquarium and the Aquarium of the Pacific, with animal research conducted in our laboratory in Santa Cruz. The audiograms obtained have been compared to available data collected on other marine mammals (such as pinnipeds), as well as terrestrial carnivores (such as other mustelids) in order to understand better understand the hearing specializations of sea otters. Research on auditory masking (the simultaneous effects of noise on hearing) is also part of this study. This project concluded in 2013 and is being prepared for publication.

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Cognitive effects of neurotoxic domoic acid exposure on California sea lions
Our lab has recently completed data collection on a suite of studies featuring wild California sea lions with naturally occurring brain damage. Led by Psychology doctoral student Peter Cook, this represents one of the first efforts to develop a natural model for brain and behavior research. Over recent years, large numbers of sea lions have stranded in distress from toxic exposure to domoic acid, an excitotoxic algal metabolite that can cause seizures and hippocampal damage. Many of these animals are taken to The Marine Mammal Center (TMMC), the largest marine mammal rehabilitation facility on the West Coast, where they are available for limited study during the course of treatment. Working closely with TMMC, we have developed rapid behavioral assays for use in diagnosing domoic acid exposure. We have also brought a number of subjects to our facility at Long Marine Lab for more in-depth testing and acquired in vivo measurements of brain damage in these animals via MRI. By examining the effects of hippocampal damage on spatial and experiential memory in this patient population, we are helping inform veterinary and rehabilitation decisions. Simultaneously, we are able to capitalize on a unique opportunity to examine brain function in a group of animals not restricted by the extreme genetic and developmental constraints of traditional laboratory animal models. Although using this wild population introduces noise into our data, and quite a few logistical hurdles into the course of training and testing, it also vests our results with a rare commodity in animal lesion research: ecological validity. In a related line of work, we have embarked on a new course of brain imaging research. With collaborators at UC Davis, TMMC, and Animal Scan imaging center in Redwood City, we are using functional connectivity MRI to examine brain networks both in healthy sea lions and those with domoic acid toxicosis.

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Cross-modal classification in California sea lions
Ron Schusterman and his past and present research groups have spent over 25 years studying the cognitive abilities of marine mammals. This area of research is concerned with how information gathered from different sensory systems is used by animals in decision-making, problem solving, learning, and memory. Our work in this area has spanned studies of artificial sign language comprehension, short- and long-term memory, discrimination learning, associative learning, and concept formation. Recently, our studies of sea lion cognition have emphasized 'equivalence' classification, or the ability to recognize relationships between stimuli that are not based on similar features, but rather, on similar function or through connections with shared associates. This cognitive skill is shared by humans, sea lions, and some birds and mammals, and is an important topic of study among human and animal psychologists. Our current research investigates the conditions under which equivalence relationships emerge between stimuli, responses and reinforcers, how equivalence relationships form across sensory modalities, and how equivalence relationships are remembered over short and long time scales. At present, we are particularly interested studying the learning mechanisms that support sensory integration between visual and auditory cues.

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Neurophysiological auditory processing in pinnipeds
Our electrophysiological research focuses on evaluating auditory processing in pinnipeds at the level of the level of the brainstem. In these measurements, extremely small neural potentials are evoked in response to aerial acoustic stimuli. These auditory evoked potentials (AEPs) are recorded by small sub-dermal electrodes placed just under the subject’s skin, amplified using a high-gain bio-potential amplifier, and recorded to a laptop computer. Many aspects of pinniped hearing that are difficult to examine with traditional behavioral hearing methodologies are available for study using AEP techniques. For example, the project is currently working on the measurement of auditory sensitivity in a relatively large sample of wild California sea lions housed for rehabilitation at The Marine Mammal Center in Sausalito, California. As current data on aerial hearing in pinnipeds is limited to measurements made with a few captive subjects, we hope that this effort will also us to better understand the variability of hearing in wild California sea lion populations. Future projects will extend electrophysiological methods to other aspects of the amphibious nature of pinniped hearing, such as sound localization, and the nature of sound conduction to the pinniped inner ear.

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