Colleen Reichmuth

Why pinnipeds don’t echolocate

Odontocete cetaceans have evolved a highly advanced system of active biosonar. It has been hypothesized that other groups of marine animals, such as the pinnipeds, possess analogous sound production, reception, and processing mechanisms that allow for underwater orientation using active echolocation. Despite sporadic investigation over the past 30 years, the accumulated evidence in favor of the pinniped echolocation hypothesis is unconvincing. We argue that an advanced echolocation system is unlikely to have evolved in pinnipeds primarily because of constraints imposed by the obligate amphibious functioning of the pinniped auditory system. As a result of these constraints, pinnipeds have not developed highly acute, aquatic, high frequency sound production or reception systems required for underwater echolocation. Instead, it appears that pinnipeds have evolved enhanced visual, tactile, and passive listening skills. The evolutionary refinement of alternative sensory systems allows pinnipeds to effectively forage, navigate, and avoid predators under water despite the lack of active biosonar capabilities.

How Animals Classify Friends and Foes

A model of stimulus equivalence, which describes how non-similarity-based categories are formed, is used to describe aspects of animal social and communicative interactions such as kinship, friendship, coalitions, territorial behavior, and referential calling. Although this model was originally designed to deal with stimulus relations in linguistic behavior, it can be readily applied to understanding the cognitive mechanisms that underlie social as well as non-social categorizations in numerous taxa. This approach provides a new, parsimonious, and experimentally based understanding of how animals without language deal with problems of classification in their environment.

Communication masking in marine mammals: A review and research strategy

Underwater noise, whether of natural or anthropogenic origin, has the ability to interfere with the way in which marine mammals receive acoustic signals (i.e., for communication, social interaction, foraging, navigation, etc.). This phenomenon, termed auditory masking, has been well studied in humans and terrestrial vertebrates (in particular birds), but less so in marine mammals. Anthropogenic underwater noise seems to be increasing in parts of the worlds oceans and concerns about associated bioacoustic effects, including masking, are growing. In this article, we review our understanding of masking in marine mammals, summarise data on marine mammal hearing as they relate to masking (including audiograms, critical ratios, critical bandwidths, and auditory integration times), discuss masking release processes of receivers (including comodulation masking release and spatial release from masking) and anti-masking strategies of signalers (e.g. Lombard effect), and set a research framework for improved assessment of potential masking in marine mammals.

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.

Vocal learning in seals, sea lions, and walruses

The pinnipeds provide a variety of clues to those interested in the vocal learning capabilities of non-human animals. Observational and experimental studies of seals, sea lions, and walruses reveal elements of vocal development, contextual control, plasticity in expression and learning, and even imitation of complex sounds. Consideration of the factors that influence the expression of these capabilities informs understanding of the behavioral and structural mechanisms that support vocal learning in mammals and the evolutionary forces shaping these capabilities.

Algal toxin impairs sea lion memory and hippocampal connectivity, with implications for strandings

Red tides make dinner hard to find Domoic acid (DA) is a neurotoxin produced by marine algae. When present in large amounts, it is harmful to marine organisms and to humans. Cook et al. tested California sea lions being treated at a marine mammal rescue facility. Animals that had evidence of exposure to DA had lesions in their hippocampus and displayed reduced performance on spatial memory tasks. Because such tasks are essential to foraging in a marine environment, increasing exposure to DA may be contributing to increasing sea lion strandings. Science, this issue p. 1545 Domoic acid reduces spatial memory and, likely, foraging ability in California sea lions. Domoic acid (DA) is a naturally occurring neurotoxin known to harm marine animals. DA-producing algal blooms are increasing in size and frequency. Although chronic exposure is known to produce brain lesions, the influence of DA toxicosis on behavior in wild animals is unknown. We showed, in a large sample of wild sea lions, that spatial memory deficits are predicted by the extent of right dorsal hippocampal lesions related to natural exposure to DA and that exposure also disrupts hippocampal-thalamic brain networks. Because sea lions are dynamic foragers that rely on flexible navigation, impaired spatial memory may affect survival in the wild.

Psychophysical and electrophysiological aerial audiograms of a Steller sea lion (Eumetopias jubatus) a)

A within-subject comparison of auditory steady-state response (ASSR) and psychophysical measurements of aerial hearing sensitivity was conducted with an individual of the largest otariid species, the Steller sea lion. Psychophysical methods were used to obtain an unmasked aerial audiogram at 13 frequencies, spanning a range of 0.125-34 kHz. The subject had a hearing range (frequencies audible at 60 dB(rms) re 20 microPa) of about 0.250-30 kHz, and a region of best hearing sensitivity from 5-14.1 kHz. The psychophysical aerial audiogram of this Steller sea lion was remarkably similar to aerial audiograms previously obtained for California sea lions and northern fur seals, suggesting that the otariid pinnipeds form a functional hearing group. ASSR thresholds, measured at frequencies of 1, 2, 5, 10, 20, and 32 kHz, were elevated relative to corresponding psychophysical thresholds, ranging from +1 dB at 20 kHz, to +31 dB at 1 kHz. The ASSR audiogram accurately predicted the subjects high-frequency cutoff, and provided a reasonable estimate of hearing sensitivity at frequencies above 2 kHz. In testing situations where psychophysical methods are not possible, ASSR methods may provide an objective and efficient estimate of behavioral hearing sensitivity in otariid pinnipeds.

Novel sound production through contingency learning in the Pacific walrus (Odobenus rosmarus divergens)

Walruses (Odobenus rosmarus) are highly vocal amphibious mammals with a range of anatomical specializations that can provide plasticity to their sound emissions. The objective of this descriptive study was to determine whether contingency learning could be used to increase variability and induce novelty in the acoustic behavior of walruses. The subjects were two twelve-year-old captive walruses, a male and a female that had previously been conditioned using food reinforcement to produce several specific sounds in response to different discriminative cues. In the current task, these individuals were encouraged to produce novel sounds and novel sound combinations in air by withholding reinforcement for sounds previously emitted in a given session and providing reinforcement only for qualitative differences in emitted sounds. Following training in air, the walruses were tested under water with the same reinforcement contingency. The subjects responded as they had done in air, by varying their underwater sound emissions until reinforcement was provided. Many of the sounds and sound combinations produced by the subjects during underwater testing were quite different from those produced during training in air and those produced under water during baseline observations. Both the male and female spontaneously emitted knocks and soft bells which are components of the songs known to be emitted by mature male walruses during the breeding season. The finding that reinforced variability can induce creativity in sound production is consistent with recent experiments on budgerigar birds showing that vocal topographies, like motor responses, may be influenced by contingency learning.

Electrophysiological Assessment of Temporal Resolution in Pinnipeds

Studies of auditory temporal processing in marine mammals have traditionally focused on the highly refined temporal resolution capabilities of dolphins and other odontocete cetaceans. However, a recent electrophysiological investigation of manatee (Trichechus manatus) hearing has shown their temporal resolution to be better than expected, leading to speculation that enhanced temporal processing capabilities are adaptive for underwater sound localization. This study measured evoked responses from several California sea lions (Zalophus californianus), a harbor seal (Phoca vitulina), and a northern elephant seal (Mirounga angustirostris) to determine how well the auditory systems of these amphibious mammals resolve rhythmic stimuli. Trains of broadband clicks were presented in air at repetition rates from 125 to 1,500 s -1 , and the averaged evoked responses elicited by these stimuli were recorded from the skin. Rate-following responses were detected in the sea lions at rates up to 1,000 s -1 , with an estimated upper limit of temporal resolution between 875 to 1,000 s -1 . This upper limit is better than previously anticipated and was further substantiated by limited testing with the harbor seal and northern elephant seal. While these findings might support an underwater sound localization hypothesis, measurements comparable to those of the pinnipeds were also obtained in a phylogenetically similar terrestrial mammal: a domestic dog (Canis familiaris). It is therefore possible that increased temporal resolution in pinnipeds and other nonecholocating marine mammals is not a result of the evolutionary pressure of an aquatic environment.

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.