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.

Spatial release from masking of aerial tones in pinnipeds.

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 lacks pinnae, and California sea lion, who possesses reduced pinnae. Subjects had to detect aerial tones at 1, 8, and 16 kHz in the presence of octave bands of white noise centered at the tone frequency. While the masker occurred in front of the subject (0 degree), the tone occurred at 0, 45, or 90 degrees in the horizontal plane. Unmasked thresholds were also measured at these angles to determine sensitivity differences based on source azimuth. Compared to when signal and masker where co-located, masked thresholds were lower by as much as 19 and 12 dB in the harbor seal and sea lion, respectively, when signal and masker were separated. Masked threshold differences of the harbor seal were larger than those previously measured under water. Performance was consistent with some measurements collected on terrestrial animals but differences between subjects at the highest frequency likely reflect variations in pinna anatomy.

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.

Underwater temporary threshold shift in pinnipeds: effects of noise level and duration.

Behavioral psychophysical techniques were used to evaluate the residual effects of underwater noise on the hearing sensitivity of three pinnipeds: a California sea lion (Zalophus californianus), a harbor seal (Phoca vitulina), and a northern elephant seal (Mirounga angustirostris). Temporary threshold shift (TTS), defined as the difference between auditory thresholds obtained before and after noise exposure, was assessed. The subjects were exposed to octave-band noise centered at 2500 Hz at two sound pressure levels: 80 and 95 dB SL (re: auditory threshold at 2500 Hz). Noise exposure durations were 22, 25, and 50 min. Threshold shifts were assessed at 2500 and 3530 Hz. Mean threshold shifts ranged from 2.9-12.2 dB. Full recovery of auditory sensitivity occurred within 24 h of noise exposure. Control sequences, comprising sham noise exposures, did not result in significant mean threshold shifts for any subject. Threshold shift magnitudes increased with increasing noise sound exposure level (SEL) for two of the three subjects. The results underscore the importance of including sound exposure metrics (incorporating sound pressure level and exposure duration) in order to fully assess the effects of noise on marine mammal hearing.

Localization of aerial pure tones by pinnipeds.

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 sea lion in a hemi-anechoic chamber using a left/right psychophysical procedure. Performance for the same frequencies was also quantified for discrete speaker separation of 5 degrees from the mid-line. For all subjects, MAAs ranged from approximately 3 degrees to 15 degrees and were generally equal to or larger than those previously measured in the same subjects with a broadband signal. Performance at 5 degrees ranged from chance to 97% correct, depending on frequency and subject. Poorest performance in the sea lion and harbor seal occurred at intermediate frequencies, which is consistent with the duplex theory of sound localization. In contrast, the elephant seal's poorest performance occurred at higher frequencies. The elephant seal's result suggests an inferior ability to utilize interaural level differences and is perhaps related to best hearing sensitivity shifted toward lower frequencies in this species relative to other pinnipeds.

Localization of aerial broadband noise by pinnipeds.

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 (Phoca vitulina), and a female California sea lion (Zalophus californianus) were measured in the horizontal plane. The stimulus was broadband white noise that was band pass filtered between 1.2 and 15 kHz. Testing was conducted in a hemi-anechoic chamber using a left/right forced choice procedure to measure the minimum audible angle (MAA) for each subject. MAAs were defined as half the angular separation of two sound sources bisected by a subject's midline that corresponded to 75% correct discrimination. MAAs were 4.7 degrees, 3.6 degrees, and 4.2 degrees for the northern elephant seal, harbor seal, and California sea lion, respectively. These results demonstrate that individuals of these pinniped species have sound localization abilities comparable to the domestic cat and rhesus macaque. The acuity differences between our subjects were small and not predicted by head size. These results likely reflect the relatively acute general abilities of pinnipeds to localize aerial broadband signals.

Auditory masking in three pinnipeds: aerial critical ratios and direct critical bandwidth measurements.

This study expands the limited understanding of pinniped aerial auditory masking and includes measurements at some of the relatively low frequencies predominant in many pinniped vocalizations. Behavioral techniques were used to obtain aerial critical ratios (CRs) within a hemianechoic chamber for a northern elephant seal (Mirounga angustirostris), a harbor seal (Phoca vitulina), and a California sea lion (Zalophus californianus). Simultaneous, octave-band noise maskers centered at seven test frequencies (0.2-8.0 kHz) were used to determine aerial CRs. Narrower and variable bandwidth masking noise was also used in order to obtain direct critical bandwidths (CBWs). The aerial CRs are very similar in magnitude and in frequency-specific differences (increasing gradually with test frequency) to underwater CRs for these subjects, demonstrating that pinniped cochlear processes are similar both in air and water. While, like most mammals, these pinniped subjects apparently lack specialization for enhanced detection of specific frequencies over masking noise, they consistently detect signals across a wide range of frequencies at relatively low signal-to-noise ratios. Direct CBWs are 3.2 to 14.2 times wider than estimated based on aerial CRs. The combined masking data are significant in terms of assessing aerial anthropogenic noise impacts, effective aerial communicative ranges, and amphibious aspects of pinniped cochlear mechanics.

Long-term memory for concepts in a California sea lion ( Zalophus californianus).

An adult California sea lion ( Zalophus californianus) with extensive experience in performing discrimination learning tasks was tested to evaluate her long-term memory for two previously learned concepts. An associative concept, that of equivalence classification, was retested after a retention interval of approximately 1 year. The sea lion had originally shown emergent equivalence classification with nonsimilarity-based classes of stimuli in a simple discrimination repeated-reversal procedure as well as in a matching-to-sample procedure. The 1-year memory test revealed no decrement in classification performance in either procedure. A relational concept, that of generalized identity matching, was retested after approximately 10 years. The sea lion had originally received trial-and-error exemplar training with identity matching-to-sample problems prior to transferring the concept to novel stimulus configurations. In the 10-year memory test, the sea lion immediately and reliably applied the previously established identity concept to familiar and novel sets of matching problems. These are the first reports of long-term conceptual memory in a nonprimate species. The experimental findings are consistent with a variety of observations of sea lions in natural settings, which indicate that natal sites, feeding areas, and individuals may be remembered over long periods of time.

Changes in auditory sensitivity with depth in a free-diving California sea lion (Zalophus californianus).

All current data on underwater hearing in pinnipeds are based on tests conducted in small tanks, and may not accurately represent the auditory functioning of free-ranging animals, especially if hearing sensitivity changes with water depth. Underwater auditory thresholds were determined for a California sea lion at depths ranging from 10 to 100 meters. The following results were obtained: (1) False alarm probabilities (responding in the absence of a signal) decreased significantly with depth, indicating that the sea lion adopted a more conservative response criterion in deeper water. (2) Hearing sensitivity generally worsened with depth. (3) There was a significant interaction between depth and frequency, the depth effect being most pronounced at 10 kHz and reversing at 35 kHz. Increasing pressure related to diving probably alters the impedance characteristics of the pinniped ear, in particular affecting the size of the middle-ear air space via expansion of cavernous tissue in the middle-ear cavity. These results show that the middle ear plays a functional role in underwater sound detection in sea lions. However, contrary to previous speculation, the presence of cavernous tissue in the sea lion middle ear does not appear to enhance sensitivity at depth.

Sea lions and equivalence: expanding classes by exclusion.

Experiments have shown that human and nonhuman subjects are capable of performing new arbitrary stimulus-stimulus relations without error. When subjects that are experienced with matching-to-sample procedures are presented with a novel sample, a novel comparison, and a familiar comparison, most respond by correctly selecting the novel comparison in the presence of the new sample. This exclusion paradigm was expanded with two California sea lions that had previously formed two 10-member equivalence classes in a matching-to-sample procedure. Rather than being presented with a novel sample on a given trial, the sea lions were presented with a randomly selected familiar member of one class as the sample. One of the comparisons was a randomly selected familiar member of the alternative class, and the other was a novel stimulus. When required to choose which comparison matched the sample, the subjects reliably rejected the familiar comparison, and instead selected the unfamiliar one. Next, the sea lions were presented with transfer problems that could not be solved by exclusion; they immediately grouped the new stimuli into the appropriate classes. These findings show that exclusion procedures can rapidly generate new stimulus relations that can be used to expand stimulus classes.