Auditory sensitivity in aquatic animals.

A critical concern with respect to marine animal acoustics is the issue of hearing "sensitivity," as it is widely used as a criterion for the onset of noise-induced effects. Important aspects of research on sensitivity to sound by marine animals include: uncertainties regarding how well these species detect and respond to different sounds; the masking effects of man-made sounds on the detection of biologically important sounds; the question how internal state, motivation, context, and previous experience affect their behavioral responses; and the long-term and cumulative effects of sound exposure. If we are to better understand the sensitivity of marine animals to sound we must concentrate research on these questions. In order to assess population level and ecological community impacts new approaches can possibly be adopted from other disciplines and applied to marine fauna.

Grey seals use anthropogenic signals from acoustic tags to locate fish: evidence from a simulated foraging task.

Anthropogenic noise can have negative effects on animal behaviour and physiology. However, noise is often introduced systematically and potentially provides information for navigation or prey detection. Here, we show that grey seals (Halichoerus grypus) learn to use sounds from acoustic fish tags as an indicator of food location. In 20 randomized trials each, 10 grey seals individually explored 20 foraging boxes, with one box containing a tagged fish, one containing an untagged fish and all other boxes being empty. The tagged box was found after significantly fewer non-tag box visits across trials, and seals revisited boxes containing the tag more often than any other box. The time and number of boxes needed to find both fish decreased significantly throughout consecutive trials. Two additional controls were conducted to investigate the role of the acoustic signal: (i) tags were placed in one box, with no fish present in any boxes and (ii) additional pieces of fish, inaccessible to the seal, were placed in the previously empty 18 boxes, making possible alternative chemosensory cues less reliable. During these controls, the acoustically tagged box was generally found significantly faster than the control box. Our results show that animals learn to use information provided by anthropogenic signals to enhance foraging success.

The role of vocal learning in call acquisition of wild grey seal pups.

Pinnipeds have been identified as one of the best available models for the study of vocal learning. Experimental evidence for their learning skills is demonstrated with advanced copying skills, particularly in formant structure when copying human speech sounds and melodies. By contrast, almost no data are available on how learning skills are used in their own communication systems. We investigated the impact of playing modified seal sounds in a breeding colony of grey seals (Halichoerus grypus) to study how acoustic input influenced vocal development of eight pups. Sequences of two or three seal pup calls were edited so that the average peak frequency between calls in a sequence changed up or down. We found that seals copied the specific stimuli played to them and that copies became more accurate over time. The differential response of different groups showed that vocal production learning was used to achieve conformity, suggesting that geographical variation in seal calls can be caused by horizontal cultural transmission. While learning of pup calls appears to have few benefits, we suggest that it also affects the development of the adult repertoire, which may facilitate social interactions such as mate choice. This article is part of the theme issue 'Vocal learning in animals and humans'.

Formant Modification through Vocal Production Learning in Gray Seals.

Vocal production learning is a rare communication skill and has only been found in selected avian and mammalian species [1-4]. Although humans use learned formants and voiceless sounds to encode most lexical information [5], evidence for vocal learning in other animals tends to focus on the modulation pattern of the fundamental frequency [3, 4]. Attempts to teach mammals to produce human speech sounds have largely been unsuccessful, most notably in extensive studies on great apes [5]. The limited evidence for formant copying in mammals raises the question whether advanced learned control over formant production is uniquely human. We show that gray seals (Halichoerus grypus) have the ability to match modulations in peak frequency patterns of call sequences or melodies by modifying the formants in their own calls, moving outside of their normal repertoire's distribution of frequencies and even copying human vowel sounds. Seals also demonstrated enhanced auditory memory for call sequences by accurately copying sequential changes in peak frequency and the number of calls played to them. Our results demonstrate that formants can be influenced by vocal production learning in non-human vocal learners, providing a mammalian substrate for the evolution of flexible information coding in formants as found in human language.

Can a gray seal (Halichoerus grypus) generalize call classes?

Past researchers have found that gray seals (Halichoerus grypus) are capable of classifying vocal signals by call type using a trained set, but were unable to generalize to novel exemplars (Shapiro, Slater, & Janik, 2004). Given the importance of auditory categorization in communication, it would be surprising if the animals were unable to generalize acoustically similar calls into classes. Here, we trained a juvenile gray seal to discriminate novel calls into 2 classes, "growls" and "moans," by vocally matching call types (i.e., the seal moaned when played a moan and growled when played a growl). Our method differed from the previous study as we trained the animal using a comparatively large set of exemplars with standardized durations, consisting of both the seal's own calls and those of 2 other seals. The seal successfully discriminated growls and moans for both her own (94% correct choices) and the other seals' (87% correct choices) calls. We used a generalized linear model (GLM) and found that the seal's performance significantly improved across test sessions, and that accuracy was higher during the first presentation of a sound from her own repertoire but decreased after multiple exposures. This pattern was not found for calls from unknown seals. Factor analysis for mixed data (FAMD) identified acoustic parameters that could be used to discriminate between call types and individuals. Growls and moans differed in noise, duration and frequency parameters, whereas individuals differed only in frequency. These data suggest that the seal could have gained information about both call type and caller identity using frequency cues.