Memory for own behaviour in pinnipeds.

Pinnipeds are aquatic predators feeding on a vast range of prey, and their social behaviour differs greatly between species (from extreme polygyny in some sea lions to monogamy in some true seals). It has been hypothesised that the foraging and social complexity of their lifestyle should drive the evolution of their cognitive abilities. To investigate how aware pinnipeds are of their own behaviour, a grey seal (Halichoerus grypus), two harbour seals (Phoca vitulina) and four South American sea lions (Otaria flavescens) were trained to repeat their own behaviour on command. Three already trained behaviours were used, and the animal was asked to repeat the behaviour twice to ensure that the animal recalled its own behaviour and not the command given for the previous behaviour. All three species could recall their own behaviour significantly better than by chance. The duration for which the animals could recall their behaviour was tested using a staircase paradigm. A delay was implemented between the completion of the behaviour and the command to repeat it. The delay was increased after correct responses and decreased after incorrect responses. The performance of all species fell towards chance level after 12-18 s, with no significant difference between species. These results indicate that sea lions and true seals are aware of their own behaviour and that true seals have similar short-term memory abilities. It also shows that pinnipeds have less developed short-term memory abilities compared to other aquatic predators, such as the bottlenose dolphin. The complexity of pinniped foraging and social behaviour does not seem to have driven the evolution of short-term memory abilities in these animals but might have contributed to their ability to recall their own behaviour.

The role of visual cues in mother-pup reunions in a colonially breeding mammal.

Parental care is an important factor influencing offspring survival and adult reproductive success in many vertebrates. Parent-offspring recognition ensures care is only directed to filial young, avoiding the costs of misallocated resource transfer. It is essential in colonial mammal species, such as otariids (fur seals and sea lions), in which repeated mother-offspring separations increase the risk of misdirecting maternal effort. Identification of otariid pups by mothers is known to be multi-modal, yet the role of visual cues in this process remains uncertain. We used three-dimensional visual models to investigate the importance of visual cues in maternal recognition of pups in Australian sea lions (Neophoca cinerea). We showed that the colour pattern of pup pelage in the absence of any other sensory cues served to attract the attention of females and prompt investigation. Furthermore, females were capable of accurately distinguishing between models imitating the age-class of their own pup and those resembling older or younger age-classes. Our results suggest that visual cues facilitate age-class discrimination of pups by females and so are likely to play an important role in mother-pup reunions and recognition in otariid species.

Relaxed Open Mouth reciprocity favours playful contacts in South American sea lions (Otaria flavescens).

Fine-tuning communication is well documented in mammalian social play which relies on a large variety of specific and non-specific signals. Facial expressions are one of the most frequent patterns in play communication. The reciprocity of facial signals expressed by the players provides information on their reciprocal attentional state and on the correct perception/decoding of the signal itself. Here, for the first time, we explored the Relaxed Open Mouth (ROM), a widespread playful facial expression among mammals, in the South American sea lion (Otaria flavescens). In this species, like many others, ROM appears to be used as a playful signal as distinct from merely being a biting action. ROM was often reciprocated by players. Even though ROM did not vary in frequency of emission as a function of the number of players involved, it was reciprocated more often during dyadic encounters, in which the players had the highest probability to engage in a face-to-face interaction. Finally, we found that it was the reciprocation of ROMs, more than their frequency performance, that was effective in prolonging playful bouts. In conclusion, ROM is widespread in many social mammals and O. flavescens is not an exception. At least in those species for which quantitative data are available, ROM seems to be characterized by similar design features clearly indicating that the signal underwent to similar selective pressures.

Olfactory Enrichment in California Sea Lions (Zalophus californianus): An Effective Tool for Captive Welfare?

In the wild, California sea lions (Zalophus californianus) are exposed to a wide variety of sensory information, which cannot be replicated in captive environments. Therefore, unique procedures are necessary for maintaining physiological and psychological health in nonhuman animals in captivity. The effects of introducing natural scents to captive enclosures have been investigated in a variety of species, yet they have not been examined in marine mammals. This project explored the behavioral effect of scent added to the environment, with the goal of improving the welfare of sea lions in captivity. Two scent types were introduced: (a) natural scents, found in their native environment, and (b) non-natural scents, not found in their native environment. This study examined not only scent enrichment but also the possible evolutionary underpinnings of pinniped olfaction. Scent enrichment was found to significantly impact sea lion behavior as demonstrated by a reduction in pattern swimming, an increase in habitat utilization, and a reduction in stereotypical behavior. However, there were no differences in behavior between natural and non-natural scent conditions.

Natural exposure to domoic acid causes behavioral perseveration in Wild Sea lions: Neural underpinnings and diagnostic application.

Domoic acid is a naturally occurring algal toxin that causes neurological symptoms and mortality in exposed marine life. California sea lions (Zalophus californianus) are the most visible victims, and suffer epilepsy and progressive hippocampal atrophy. Despite its reliable neurological effects, little is known about how exposure to domoic acid alters behavior, which is critical for understanding the impact of toxic exposure on long-term survival in sea lions and other exposed animals, including humans. Better understanding of the behavioral effects may also inform veterinary diagnosis and treatment. Anecdotally, exposed sea lions have been reported to show enhanced perseverative behavior. To assess the neurobehavioral effects of domoic acid, we compared veterinary diagnoses, measures of hippocampal volume from in vivo MRI, and behavioral measures of habituation and dishabituation in 27 wild sea lions undergoing rehabilitation. The sample was divided post-hoc between subjects with clear veterinary diagnoses of chronic domoic acid toxicosis and those with no evidence of the disease. In the behavioral task, subjects were exposed repeatedly to sounds from two source locations, and, following a short delay, exposed again. Veterinary diagnosis of domoic acid toxicosis was associated with extent of hippocampal damage, predicted delayed habituation in phase 1, and enhanced dishabituation in phase 2. Receiver operating characteristic analysis indicated that delayed habituation in phase 1 was diagnostically predictive. Enhanced dishabituation in phase 2 was correlated with reduced right ventral hippocampal volume. Together, delayed habituation and enhanced dishabituation following domoic acid exposure indicate a clinically relevant and potentially maladaptive behavioral pattern of perseveration.

Sea lions' (Zalophus californianus) use of human pointing gestures as referential cues.

This experiment investigated the ability of four human-socialized sea lions to exploit human communicative gestures in three different object-choice tasks based on directional cues emitted by their caretakers. In Study 1, three of the tested subjects were able to generalize their choice of the pointed target to variations of the basic pointing gestures (i.e., cross-body point, elbow point, foot point, and gaze only), from the very first trials. Study 2 showed that the subjects could follow the pointing gestures geometrically and select the correct target among four possible targets, two on each side of the informant. In Study 3, we tested the robustness of their tendency to follow a pointing gesture by hiding targets behind barriers. One subject was able to follow pointing gestures towards targets not visible at the moment of their decision without any training, despite the presence of another visible and directly accessible one. Taken together, these results suggest that sea lions were able to use the referential property of the human pointing gesture, because they were able to rely on extrapolating precise linear vectors along different pointing body parts in order to identify a precise object rather than merely a general direction. These findings support previous arguments that some non-domesticated species might have as great an ability to respond appropriately to pointing gestures as domesticated dogs. The potential roles of human-socialization and specific features of wild sea lions ecology are discussed.

Object permanence in marine mammals using the violation of expectation procedure.

Object permanence refers to the ability to process information about objects even when they are not visible. One stage of object permanence, called visible displacement, involves being able to find an object that has been fully hidden from view. Visible displacement has been demonstrated in many animal species, yet very little is known about object permanence in marine mammals. In addition, the methodology for testing visible displacement has sometimes been called into question because alternative explanations could account for subjects' success. The current study investigated visible displacement in Atlantic bottlenose dolphins and California sea lions using a methodology called violation of expectation, in which the animal's fish bucket was placed on a table surrounded on three sides by curtains. A solid screen placed in front of the bucket was then rotated in an arc from front to back. The screen was rotated either 120° (possible event) or 180° (surprising event), appearing as if the bucket disappeared. Both dolphins and sea lions looked significantly longer during the 180°, unexpected, trials than the expected event trials. Results suggest that both dolphins and sea lions pass visible displacement tests without the use of perceptual cues. This article is part of a Special Issue entitled: Tribute to Tom Zentall.

A California sea lion (Zalophus californianus) can keep the beat: motor entrainment to rhythmic auditory stimuli in a non vocal mimic.

Is the ability to entrain motor activity to a rhythmic auditory stimulus, that is "keep a beat," dependent on neural adaptations supporting vocal mimicry? That is the premise of the vocal learning and synchronization hypothesis, recently advanced to explain the basis of this behavior (A. Patel, 2006, Musical Rhythm, Linguistic Rhythm, and Human Evolution, Music Perception, 24, 99-104). Prior to the current study, only vocal mimics, including humans, cockatoos, and budgerigars, have been shown to be capable of motoric entrainment. Here we demonstrate that a less vocally flexible animal, a California sea lion (Zalophus californianus), can learn to entrain head bobbing to an auditory rhythm meeting three criteria: a behavioral response that does not reproduce the stimulus; performance transfer to a range of novel tempos; and entrainment to complex, musical stimuli. These findings show that the capacity for entrainment of movement to rhythmic sounds does not depend on a capacity for vocal mimicry, and may be more widespread in the animal kingdom than previously hypothesized.

What makes an Australian sea lion (Neophoca cinerea) male's bark threatening?

In mammals, vocal signals are produced in many social contexts and convey diverse information about the emitter (social rank, individual identity, body size-condition). To understand their biological function, the authors find it is not only important to estimate the information about the signaler encoded in the signal but also to determine if and how this information is perceived by the receiver. In male pinnipeds (phocids, otariids, and odobenids) vocal signaling plays an important role in the breeding season during the defense of territories, females, or both. In this article, the authors investigated 2 key acoustic features that Australian sea lion (Neophoca cinerea) males most likely rely on to assess the threat level posed by potential rivals, by manipulating bark rhythmicity and spectral characteristics. Bark series that show accelerated rhythmicity and higher formants elicited stronger responses.

Rapid behavioural diagnosis of domoic acid toxicosis in California sea lions.

Domoic acid is a neurotoxic metabolite of widely occurring algal blooms that has caused multiple marine animal stranding events. Exposure to high doses of domoic acid, a glutamate agonist, may lead to persistent medial temporal seizures and damage to the hippocampus. California sea lions (Zalophus californianus) are among the most visible and frequent mammalian victims of domoic acid poisoning, but rapid, reliable diagnosis in a clinical setting has proved difficult owing to the fast clearance of the toxin from the blood stream. Here, we show that the behavioural orienting responses of stranded sea lions diagnosed with domoic acid toxicosis habituate more slowly to a series of non-aversive auditory stimuli than do those of sea lions with no apparent neurological deficits. A signal detection analysis based on these habituation measures was able to correctly identify 50 per cent of subjects with domoic acid toxicosis while correctly rejecting approximately 93 per cent of controls, suggesting potential diagnostic merit.

Exploring the Link between Genetic Relatedness r and Social Contact Structure k in Animal Social Networks.

Our understanding of how cooperation can arise in a population of selfish individuals has been greatly advanced by theory. More than one approach has been used to explore the effect of population structure. Inclusive fitness theory uses genetic relatedness r to express the role of population structure. Evolutionary graph theory models the evolution of cooperation on network structures and focuses on the number of interacting partners k as a quantity of interest. Here we use empirical data from a hierarchically structured animal contact network to examine the interplay between independent, measurable proxies for these key parameters. We find strong inverse correlations between estimates of r and k over three levels of social organization, suggesting that genetic relatedness and social contact structure capture similar structural information in a real population.

The memory remains: long-term vocal recognition in Australian sea lions.

The ability to recognize other individuals plays an important role in mediating social interactions. As longitudinal studies are challenging, there is only limited evidence of long-term memory of individuals and concepts in mammals. We examined the ability of six wild Australian sea lions to discriminate between the voice of their mother and another adult female, both while they were dependent on their mother and when they were independent, 2 years after weaning. Here, we show that even after a long period of independence, juveniles retain the ability to identify their mother's voice. Both when dependent and independent, animals showed stronger responses to maternal calls than to the calls of another female. This demonstration of recognition provides rare evidence of the long-term memory capabilities of wild mammals.

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

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 subject's 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.

An empirical case study examining effectiveness of environmental enrichment in two captive Australian Sea Lions (Neophoca cinerea).

This case study examined the effect of environmental enrichment on the activity budgets of a male and female Australian Sea Lion (Neophoca cinerea) housed together at Adelaide Zoo. Using non-food-related (intrinsic) and food-related (extrinsic) enrichment objects, the study conducted an ABABA (withdrawal) experimental design over a 30-day period (180 hr). The study expected extrinsically reinforcing objects to be more effective than intrinsically reinforcing objects in reducing pattern swimming. The male sea lion spent more than 45% of scans engaged in pattern swimming during the initial baseline, which was reduced by at least 25% when enrichment items were present. However, there was no evidence of stereotypic behavior in the female sea lion, indicating that individual differences may exist. When enrichment was present, the study observed more active behaviors in both nonhuman animals. They spent more time interacting with the non-food-related objects overall. Therefore, introducing simple enrichment devices offers a cheap, practical, and effective method of adding complexity to the environment, which is likely to benefit the animals' welfare and enhance the zoo-visitor experience.

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.

Lateralised swimming behaviour in the California sea lion.

Lateralised motor behaviour in the pinnipeds has been subject to little investigation. This study examined the swimming behaviour of seven zoo-housed California sea lions to determine whether they exhibited a directional bias in their motor behaviour. Data were collected on the direction of the animals' swimming patterns from the point of entering a pool of water from dry land. Each animal was studied for 100 episodes of swimming. All seven of the sea lions showed significant (P<0.001) bias in the direction of their swimming, although unidirectional bias was not observed at the level of the population. The direction of the sea lions' swimming patterns varied significantly according to the animals' sex. Males showed a preference at the level of the population for swimming in a clockwise direction, while females showed a population-level counterclockwise swimming preference. Overall, the findings appear to suggest that California sea lions, like other marine mammals, exhibit motor bias in the direction of their swimming patterns, although further work using larger sample sizes is needed before more firm conclusions regarding motor laterality in this species can be reached.

Mental rotation of perspective stimuli in a California sea lion (Zalophus californianus).

The time it takes humans to discriminate rotated objects from their mirror images increases linearly with the rotation angle. This phenomenon is probably due to an analogue mode of visual information processing during which an object's mental representation is rotated in a time-consuming process called mental rotation. As the speed of mental rotation in humans depends on rotation axis, we tested the ability of a California sea lion to mentally rotate perspective line drawings of three-dimensional objects about four axes. In a matching-to-sample experiment the animal was presented with the image and a mirror image of a block sample that had previously been shown upright. Both image and mirror image were rotated by a multiple of 60 degrees about the object's x-, y-, z-axis, or a skew axis (an axis oblique to these standard orthogonal axes). The animal's choice and reaction times were recorded using a computer-controlled touch-screen device. Mean reaction times and errors generally increased with angular disparity supporting the model of mental rotation for three-dimensional objects. Linear regression analysis of mean reaction times yielded high correlation coefficients only for three axes. The slope of reaction time functions indicated the highest mental rotation speed for the skew axis. This contrasts with the priority of mental rotation axes in humans suggesting that due to special ecological demands a different mode of orientation invariance evolved in marine mammals.

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.

Acoustic identification of female Steller sea lions (Eumetopias jubatus).

Steller sea lion (Eumetopias jubatus) mothers and pups establish and maintain contact with individually distinctive vocalizations. Our objective was to develop a robust neural network to classify females based on their mother-pup contact calls. We catalogued 573 contact calls from 25 females in 1998 and 1323 calls from 46 females in 1999. From this database, a subset of 26 females with sufficient samples of calls was selected for further study. Each female was identified visually by marking patterns, which provided the verification for acoustic identification. Average logarithmic spectra were extracted for each call, and standardized training and generalization datasets created for the neural network classifier. A family of backpropagation networks was generated to assess relative contribution of spectral input bandwidth, frequency resolution, and network architectural variables to classification accuracy. The network with best overall generalization accuracy (71%) used an input representation of 0-3 kHz of bandwidth at 10.77 Hz/bin frequency resolution, and a 2:1 hidden:output layer neural ratio. The network was analyzed to reveal which portions of the call spectra were most influential for identification of each female. Acoustical identification of distinctive female acoustic signatures has several potentially important conservation applications for this endangered species, such as rapid survey of females present on a rookery.

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.