Ellen C. Garland

Acoustic sequences in non-human animals: a tutorial review and prospectus

Animal acoustic communication often takes the form of complex sequences, made up of multiple distinct acoustic units. Apart from the well‐known example of birdsong, other animals such as insects, amphibians, and mammals (including bats, rodents, primates, and cetaceans) also generate complex acoustic sequences. Occasionally, such as with birdsong, the adaptive role of these sequences seems clear (e.g. mate attraction and territorial defence). More often however, researchers have only begun to characterise – let alone understand – the significance and meaning of acoustic sequences. Hypotheses abound, but there is little agreement as to how sequences should be defined and analysed. Our review aims to outline suitable methods for testing these hypotheses, and to describe the major limitations to our current and near‐future knowledge on questions of acoustic sequences. This review and prospectus is the result of a collaborative effort between 43 scientists from the fields of animal behaviour, ecology and evolution, signal processing, machine learning, quantitative linguistics, and information theory, who gathered for a 2013 workshop entitled, ‘Analysing vocal sequences in animals’. Our goal is to present not just a review of the state of the art, but to propose a methodological framework that summarises what we suggest are the best practices for research in this field, across taxa and across disciplines. We also provide a tutorial‐style introduction to some of the most promising algorithmic approaches for analysing sequences. We divide our review into three sections: identifying the distinct units of an acoustic sequence, describing the different ways that information can be contained within a sequence, and analysing the structure of that sequence. Each of these sections is further subdivided to address the key questions and approaches in that area. We propose a uniform, systematic, and comprehensive approach to studying sequences, with the goal of clarifying research terms used in different fields, and facilitating collaboration and comparative studies. Allowing greater interdisciplinary collaboration will facilitate the investigation of many important questions in the evolution of communication and sociality.

Humpback whale song on the southern ocean feeding grounds : implications for cultural transmission

Male humpback whales produce a long, complex, and stereotyped song on low-latitude breeding grounds; they also sing while migrating to and from these locations, and occasionally in high-latitude summer feeding areas. All males in a population sing the current version of the constantly evolving display and, within an ocean basin, populations sing similar songs; however, this sharing can be complex. In the western and central South Pacific region there is repeated cultural transmission of song types from eastern Australia to other populations eastward. Song sharing is hypothesized to occur through several possible mechanisms. Here, we present the first example of feeding ground song from the Southern Ocean Antarctic Area V and compare it to song from the two closest breeding populations. The early 2010 song contained at least four distinct themes; these matched four themes from the eastern Australian 2009 song, and the same four themes from the New Caledonian 2010 song recorded later in the year. This provides evidence for at least one of the hypothesized mechanisms of song transmission between these two populations, singing while on shared summer feeding grounds. In addition, the feeding grounds may provide a point of acoustic contact to allow the rapid horizontal cultural transmission of song within the western and central South Pacific region and the wider Southern Ocean.

Improved versions of the Levenshtein distance method for comparing sequence information in animals’ vocalisations: tests using humpback whale song

Animals can communicate using visual and acoustic displays to convey information to conspecifics. In some cases, such displays are produced in highly stereotyped and repetitive sequences. Here we use a quantitative analysis technique, the Levenshtein distance, to assess similarity in sequences of displays at both the population and individual levels. We review two existing variations of the method and present two new variations that complement and extend these existing techniques. Three of the methods include the use of a median string sequence and three use a normalisation of the original equation. Humpback whale song theme sequences from multiple populations, years and song types (different variations of the display) are used as examples to illustrate the application and success of each variation. A novel outcome of this technique is that it can produce a threshold measure of similarity to assess when behavioural sequences are so dissimilar that they must be considered different, with a measure of the probability of such clusters being distinct. The Levenshtein distance is applicable to all behavioural data produced in sequences and its use should not be limited to acoustical studies.

Beluga whale (Delphinapterus leucas) vocalizations and call classification from the eastern Beaufort Sea population

Beluga whales, Delphinapterus leucas, have a graded call system; call types exist on a continuum making classification challenging. A description of vocalizations from the eastern Beaufort Sea beluga population during its spring migration are presented here, using both a non-parametric classification tree analysis (CART), and a Random Forest analysis. Twelve frequency and duration measurements were made on 1019 calls recorded over 14 days off Icy Cape, Alaska, resulting in 34 identifiable call types with 83% agreement in classification for both CART and Random Forest analyses. This high level of agreement in classification, with an initial subjective classification of calls into 36 categories, demonstrates that the methods applied here provide a quantitative analysis of a graded call dataset. Further, as calls cannot be attributed to individuals using single sensor passive acoustic monitoring efforts, these methods provide a comprehensive analysis of data where the influence of pseudo-replication of calls from individuals is unknown. This study is the first to describe the vocal repertoire of a beluga population using a robust and repeatable methodology. A baseline eastern Beaufort Sea beluga population repertoire is presented here, against which the call repertoire of other seasonally sympatric Alaskan beluga populations can be compared.

Non-song social call bouts of migrating humpback whales

The use of stereotyped calls within structured bouts has been described for a number of species and may increase the information potential of call repertoires. Humpback whales produce a repertoire of social calls, although little is known about the complexity or function of these calls. In this study, digital acoustic tag recordings were used to investigate social call use within bouts, the use of bouts across different social contexts, and whether particular call type combinations were favored. Call order within bouts was investigated using call transition frequencies and information theory techniques. Call bouts were defined through analysis of inter-call intervals, as any calls within 3.9 s of each other. Bouts were produced significantly more when new whales joined a group compared to groups that did not change membership, and in groups containing multiple adults escorting a female and calf compared to adult only groups. Although social calls tended to be produced in bouts, there were few repeated bout types. However, the order in which most call types were produced within bouts was non-random and dependent on the preceding call type. These bouts appear to be at least partially governed by rules for how individual components are combined.

Population structure of humpback whales in the western and central South Pacific Ocean as determined by vocal exchange among populations

For cetaceans, population structure is traditionally determined by molecular genetics or photographically identified individuals. Acoustic data, however, has provided information on movement and population structure with less effort and cost than traditional methods in an array of taxa. Male humpback whales (Megaptera novaeangliae) produce a continually evolving vocal sexual display, or song, that is similar among all males in a population. The rapid cultural transmission (the transfer of information or behavior between conspecifics through social learning) of different versions of this display between distinct but interconnected populations in the western and central South Pacific region presents a unique way to investigate population structure based on the movement dynamics of a song (acoustic) display. Using 11 years of data, we investigated an acoustically based population structure for the region by comparing stereotyped song sequences among populations and years. We used the Levenshtein distance technique to group previously defined populations into (vocally based) clusters based on the overall similarity of their song display in space and time. We identified the following distinct vocal clusters: western cluster, 1 population off eastern Australia; central cluster, populations around New Caledonia, Tonga, and American Samoa; and eastern region, either a single cluster or 2 clusters, one around the Cook Islands and the other off French Polynesia. These results are consistent with the hypothesis that each breeding aggregation represents a distinct population (each occupied a single, terminal node) in a metapopulation, similar to the current understanding of population structure based on genetic and photo-identification studies. However, the central vocal cluster had higher levels of song-sharing among populations than the other clusters, indicating that levels of vocal connectivity varied within the region. Our results demonstrate the utility and value of using culturally transmitted vocal patterns as a way of defining connectivity to infer population structure. We suggest vocal patterns be incorporated by the International Whaling Commission in conjunction with traditional methods in the assessment of structure.

Song hybridization events during revolutionary song change provide insights into cultural transmission in humpback whales

Cultural processes occur in a wide variety of animal taxa, from insects to cetaceans. The songs of humpback whales are one of the most striking examples of the transmission of a cultural trait and social learning in any nonhuman animal. To understand how songs are learned, we investigate rare cases of song hybridization, where parts of an existing song are spliced with a new one, likely before an individual totally adopts the new song. Song unit sequences were extracted from over 9,300 phrases recorded during two song revolutions across the South Pacific Ocean, allowing fine-scale analysis of composition and sequencing. In hybrid songs the current and new songs were spliced together in two specific ways: (i) singers placed a single hybrid phrase, in which content from both songs were combined, between the two song types when transitioning from one to the other, and/or (ii) singers spliced complete themes from the revolutionary song into the current song. Sequence analysis indicated that both processes were governed by structural similarity rules. Hybrid phrases or theme substitutions occurred at points in the songs where both songs contained “similar sounds arranged in a similar pattern.” Songs appear to be learned as segments (themes/phrase types), akin to birdsong and human language acquisition, and these can be combined in predictable ways if the underlying structural pattern is similar. These snapshots of song change provide insights into the mechanisms underlying song learning in humpback whales, and comparative perspectives on the evolution of human language and culture.

Management of acoustic metadata for bioacoustics

Abstract Recent expansion in the capabilities of passive acoustic monitoring of sound-producing animals is providing expansive data sets in many locations. These long-term data sets will allow the investigation of questions related to the ecology of sound-producing animals on time scales ranging from diel and seasonal to inter-annual and decadal. Analyses of these data often span multiple analysts from various research groups over several years of effort and, as a consequence, have begun to generate large amounts of scattered acoustic metadata. It has therefore become imperative to standardize the types of metadata being generated. A critical aspect of being able to learn from such large and varied acoustic data sets is providing consistent and transparent access that can enable the integration of various analysis efforts. This is juxtaposed with the need to include new information for specific research questions that evolve over time. Hence, a method is proposed for organizing acoustic metadata that addresses many of the problems associated with the retention of metadata from large passive acoustic data sets. A structure was developed for organizing acoustic metadata in a consistent manner, specifying required and optional terms to describe acoustic information derived from a recording. A client-server database was created to implement this data representation as a networked data service that can be accessed from several programming languages. Support for data import from a wide variety of sources such as spreadsheets and databases is provided. The implementation was extended to access Internet-available data products, permitting access to a variety of environmental information types (e.g. sea surface temperature, sunrise/sunset, etc.) from a wide range of sources as if they were part of the data service. This metadata service is in use at several institutions and has been used to track and analyze millions of acoustic detections from marine mammals, fish, elephants, and anthropogenic sound sources.

Temporal peaks in beluga whale (Delphinapterus leucas) acoustic detections in the northern Bering, northeastern Chukchi, and western Beaufort Seas: 2010–2011

Two populations of beluga whales (Delphinapterus leucas) migrate annually between their summering grounds in the eastern Chukchi and eastern Beaufort Seas, and overwintering areas in the Bering Sea. To contribute to the understanding of migratory streams of this highly vocal species, we investigated temporal peaks in acoustic detections from 4-year-long (2010–2011) recorders located in the northeastern Chukchi (inshore and offshore), western Beaufort, and northern Bering Seas. Beluga calls were detected throughout summer (July–August) in the western Beaufort; other studies suggest these animals are likely from the eastern Chukchi population. In autumn (September–November), calls were detected in the western Beaufort and northeastern Chukchi, which were likely from both the eastern Beaufort and eastern Chukchi populations. A strong peak at the inshore northeastern Chukchi site occurred in late-November; this peak is likely to be from the eastern Chukchi population. During spring, beluga calls were detected in the northeastern Chukchi and western Beaufort in two distinct vocal peaks (early- and late-May). The timing was consistent with the hypothesis that both vocal peaks were caused by the eastern Beaufort population. This suggests that migration of populations can be discriminated when temporal differences between vocal peaks are large enough to be identified as independent events. Our study results complement and support the population identity of peaks suggested by satellite telemetry, aerial surveys, and other acoustical studies. Passive acoustic monitoring improves our understanding of the migratory timing of beluga populations for management and conservation in a region undergoing rapid change.

Quantifying similarity in animal vocal sequences: which metric performs best?

E.C.G is supported by a Newton International Fellowship. Part of this work was conducted while E.C.G. was supported by a National Research Council (National Academy of Sciences) Postdoctoral Fellowship at the National Marine Mammal Laboratory, AFSC, NMFS, NOAA.