Variability in humpback whale songs reveals how individuals can be distinctive when sharing a complex vocal display.

Individually distinctive acoustic signals in animal vocal communication are taxonomically widespread, however, the investigation of these signal types in marine mammals has focused only on a few species. Humpback whale songs are a stereotyped, hierarchically structured vocal display performed by males, and hence thought to be sexually selected. Within a population, whales conform to a common version of the song despite the song constantly evolving. While humpback songs have been studied extensively at the population level, individual level variation has been rarely described, with inconclusive results. Here, we quantified inter- and intra-individual variability at different levels in the song hierarchy using songs from 25 singers across two song types from the eastern Australian population song of 2002 (12 singers), and the revolutionary song introduced in 2003 (13 singers). Inter-individual variability was found heterogeneously across all hierarchical levels of the song structure. In addition, distinct and individually specific patterns of song production were consistently recorded across song levels, with clear structural differences between the two song types. These results suggest that within the constraints of song conformity, males can produce individually distinctive patterns that could function as an advertisement to females to convey individual qualities.

A deepening understanding of animal culture suggests lessons for conservation.

A key goal of conservation is to protect biodiversity by supporting the long-term persistence of viable, natural populations of wild species. Conservation practice has long been guided by genetic, ecological and demographic indicators of risk. Emerging evidence of animal culture across diverse taxa and its role as a driver of evolutionary diversification, population structure and demographic processes may be essential for augmenting these conventional conservation approaches and decision-making. Animal culture was the focus of a ground-breaking resolution under the Convention on the Conservation of Migratory Species of Wild Animals (CMS), an international treaty operating under the UN Environment Programme. Here, we synthesize existing evidence to demonstrate how social learning and animal culture interact with processes important to conservation management. Specifically, we explore how social learning might influence population viability and be an important resource in response to anthropogenic change, and provide examples of how it can result in phenotypically distinct units with different, socially learnt behavioural strategies. While identifying culture and social learning can be challenging, indirect identification and parsimonious inferences may be informative. Finally, we identify relevant methodologies and provide a framework for viewing behavioural data through a cultural lens which might provide new insights for conservation management.

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.

Network analysis reveals underlying syntactic features in a vocally learnt mammalian display, humpback whale song.

Vocal communication systems have a set of rules that govern the arrangement of acoustic signals, broadly defined as 'syntax'. However, there is a limited understanding of potentially shared or analogous rules across vocal displays in different taxa. Recent work on songbirds has investigated syntax using network-based modelling. This technique quantifies features such as connectivity (adjacent signals in a sequence) and recurring patterns. Here, we apply network-based modelling to the complex, hierarchically structured songs of humpback whales (Megaptera novaeangliae) from east Australia. Given the song's annual evolving pattern and the cultural conformity of males within a population, network modelling captured the patterns of multiple song types over 13 consecutive years. Song arrangements in each year displayed clear 'small-world' network structure, characterized by clusters of highly connected sounds. Transitions between these connected sounds further suggested a combination of both structural stability and variability. Small-world network structure within humpback songs may facilitate the characteristic and persistent vocal learning observed. Similar small-world structures and transition patterns are found in several birdsong displays, indicating common syntactic patterns among vocal learning in multiple taxa. Understanding the syntactic rules governing vocal displays in multiple, independently evolving lineages may indicate what rules or structural features are important to the evolution of complex communication, including human language.

Source levels of humpback whales decrease with frequency suggesting an air-filled resonator is used in sound production.

Source level and frequency are important in determining how far an acoustic signal can travel. However, in some species these sound characteristics have been found to be biomechanically linked, and therefore cannot be modified independently to achieve optimal transmission. This study investigates the variability in source levels and their relationship with frequency in the songs of humpback whales (Megaptera novaeangliae). Songs were recorded off eastern Australia using a fixed hydrophone array deployed on the whales' migratory corridor. Singing whales were acoustically tracked. An empirical, frequency-dependent model was used to estimate transmission loss. Source levels and frequency were measured for 2408 song units from 19 singers. Source levels varied from 138 to 187 dB re 1 µPa at 1 m (root mean squared), while peak frequency ranged between 52 and 3877 Hz. Much of the variability in source levels was accounted for by differences between the unit types, with mean source levels for each unit type varying by up to 17 dB. Source levels were negatively correlated with peak frequency and decreased by 2.3 dB per octave. The negative correlation between source levels and frequency is consistent with the presence of an air-filled resonator in the whales' sound production system.

Cultural revolutions reduce complexity in the songs of humpback whales.

Much evidence for non-human culture comes from vocally learned displays, such as the vocal dialects and song displays of birds and cetaceans. While many oscine birds use song complexity to assess male fitness, the role of complexity in humpback whale (Megaptera novaeangliae) song is uncertain owing to population-wide conformity to one song pattern. Although songs change gradually each year, the eastern Australian population also completely replaces their song every few years in cultural 'revolutions'. Revolutions involve learning large amounts of novel material introduced from the Western Australian population. We examined two measures of song structure, complexity and entropy, in the eastern Australian population over 13 consecutive years. These measures aimed to identify the role of complexity and information content in the vocal learning processes of humpback whales. Complexity was quantified at two hierarchical levels: the entire sequence of individual sound 'units' and the stereotyped arrangements of units which comprise a 'theme'. Complexity increased as songs evolved over time but decreased when revolutions occurred. No correlation between complexity and entropy estimates suggests that changes to complexity may represent embellishment to the song which could allow males to stand out amidst population-wide conformity. The consistent reduction in complexity during song revolutions suggests a potential limit to the social learning capacity of novel material in humpback whales.

Stereotypic and complex phrase types provide structural evidence for a multi-message display in humpback whales (Megaptera novaeangliae).

Male humpback whales produce a mating display called "song." Behavioral studies indicate song has inter- and/or intra-sexual functionality, suggesting song may be a multi-message display. Multi-message displays often include stereotypic components that convey group membership for mate attraction and/or male-male interactions, and complex components that convey individual quality for courtship. Humpback whale song contains sounds ("units") arranged into sequences ("phrases"). Repetitions of a specific phrase create a "theme." Within a theme, imperfect phrase repetitions ("phrase variants") create variability among phrases of the same type ("phrase type"). The hypothesis that song contains stereotypic and complex phrase types, structural characteristics consistent with a multi-message display, is investigated using recordings of 17 east Australian males (8:2004, 9:2011). Phrase types are categorized as stereotypic or complex using number of unit types, number of phrase variants, and the proportion of phrases that is unique to an individual versus shared amongst males. Unit types are determined using self-organizing maps. Phrase variants are determined by Levenshtein distances between phrases. Stereotypic phrase types have smaller numbers of unit types and shared phrase variants. Complex phrase types have larger numbers of unit types and unique phrase variants. This study supports the hypothesis that song could be a multi-message display.

The behavioural response of migrating humpback whales to a full seismic airgun array.

Despite concerns on the effects of noise from seismic survey airguns on marine organisms, there remains uncertainty as to the biological significance of any response. This study quantifies and interprets the response of migrating humpback whales (Megaptera novaeangliae) to a 3130 in3 (51.3l) commercial airgun array. We compare the behavioural responses to active trials (array operational; n = 34 whale groups), with responses to control trials (source vessel towing the array while silent; n = 33) and baseline studies of normal behaviour in the absence of the vessel (n = 85). No abnormal behaviours were recorded during the trials. However, in response to the active seismic array and the controls, the whales displayed changes in behaviour. Changes in respiration rate were of a similar magnitude to changes in baseline groups being joined by other animals suggesting any change group energetics was within their behavioural repertoire. However, the reduced progression southwards in response to the active treatments, for some cohorts, was below typical migratory speeds. This response was more likely to occur within 4 km from the array at received levels over 135 dB re 1 µPa2s.

Determining the behavioural dose-response relationship of marine mammals to air gun noise and source proximity.

The effect of various anthropogenic sources of noise (e.g. sonar, seismic surveys) on the behaviour of marine mammals is sometimes quantified as a dose-response relationship, where the probability of an animal behaviourally 'responding' (e.g. avoiding the source) increases with 'dose' (or received level of noise). To do this, however, requires a definition of a 'significant' response (avoidance), which can be difficult to quantify. There is also the potential that the animal 'avoids' not only the source of noise but also the vessel operating the source, complicating the relationship. The proximity of the source is an important variable to consider in the response, yet difficult to account for given that received level and proximity are highly correlated. This study used the behavioural response of humpback whales to noise from two different air gun arrays (20 and 140 cubic inch air gun array) to determine whether a dose-response relationship existed. To do this, a measure of avoidance of the source was developed, and the magnitude (rather than probability) of this response was tested against dose. The proximity to the source, and the vessel itself, was included within the one-analysis model. Humpback whales were more likely to avoid the air gun arrays (but not the controls) within 3 km of the source at levels over 140 re. 1 µPa2 s-1, meaning that both the proximity and the received level were important factors and the relationship between dose (received level) and response is not a simple one.

Changes in humpback whale singing behavior with abundance: Implications for the development of acoustic surveys of cetaceans.

Acoustic surveys of vocal animals can have significant advantages over visual surveys, particularly for marine mammals. For acoustic density estimates to be viable, however, the vocal output of the animals surveyed needs to be determined under a range of conditions and shown to be a robust predictor of abundance. In this study, the songs of humpback whales, one of the most vocal and best studied species of marine mammals, were tested as predictors of abundance. Two acoustic metrics, the number of singing whales and amount of songs produced, were compared with the number of whales seen traversing a study site on the eastern coast of Australia over an 18 year period. Although there were predictive relationships between both metrics and numbers of passing whales, these relationships changed significantly as the population grew in size. The proportion of passing whales that sang decreased as the population increased. Singing in humpback whales, therefore, is a poor predictor even of relative abundance and illustrates the caution required when developing acoustic survey techniques particularly when using social vocalizations.

Using self-organizing maps to classify humpback whale song units and quantify their similarity.

Classification of vocal signals can be undertaken using a wide variety of qualitative and quantitative techniques. Using east Australian humpback whale song from 2002 to 2014, a subset of vocal signals was acoustically measured and then classified using a Self-Organizing Map (SOM). The SOM created (1) an acoustic dictionary of units representing the song's repertoire, and (2) Cartesian distance measurements among all unit types (SOM nodes). Utilizing the SOM dictionary as a guide, additional song recordings from east Australia were rapidly (manually) transcribed. To assess the similarity in song sequences, the Cartesian distance output from the SOM was applied in Levenshtein distance similarity analyses as a weighting factor to better incorporate unit similarity in the calculation (previously a qualitative process). SOMs provide a more robust and repeatable means of categorizing acoustic signals along with a clear quantitative measurement of sound type similarity based on acoustic features. This method can be utilized for a wide variety of acoustic databases especially those containing very large datasets and can be applied across the vocalization research community to help address concerns surrounding inconsistency in manual classification.

The devil is in the detail: Quantifying vocal variation in a complex, multi-levelled, and rapidly evolving display.

Identifying and quantifying variation in vocalizations is fundamental to advancing our understanding of processes such as speciation, sexual selection, and cultural evolution. The song of the humpback whale (Megaptera novaeangliae) presents an extreme example of complexity and cultural evolution. It is a long, hierarchically structured vocal display that undergoes constant evolutionary change. Obtaining robust metrics to quantify song variation at multiple scales (from a sound through to population variation across the seascape) is a substantial challenge. Here, the authors present a method to quantify song similarity at multiple levels within the hierarchy. To incorporate the complexity of these multiple levels, the calculation of similarity is weighted by measurements of sound units (lower levels within the display) to bridge the gap in information between upper and lower levels. Results demonstrate that the inclusion of weighting provides a more realistic and robust representation of song similarity at multiple levels within the display. This method permits robust quantification of cultural patterns and processes that will also contribute to the conservation management of endangered humpback whale populations, and is applicable to any hierarchically structured signal sequence.

Addressing Challenges in Studies of Behavioral Responses of Whales to Noise.

Studying the behavioral response of whales to noise presents numerous challenges. In addition to the characteristics of the noise exposure, many factors may affect the response and these must be measured and accounted for in the analysis. An adequate sample size that includes matching controls is crucial if meaningful results are to be obtained. Field work is thus complicated, logistically difficult, and expensive. This paper discusses some of the challenges and how they are being met in a large-scale multiplatform project in which humpback whales are exposed to the noise of seismic air guns.

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.

Estructura Poblacional de las Yubartas en el Centro y Occidente del Sur del Océano Pacífico, Determinada por el Intercambio Vocal entre las Poblaciones Resumen La estructura poblacional de los cetáceos se determina tradicionalmente por medio de genética molecular o individuos identificados fotográficamente. Sin embargo, los datos acústicos han proporcionado información sobre el movimiento y la estructura poblacional de una variedad de taxones con menos esfuerzo y menos costo que los métodos tradicionales. Las yubartas macho (Megaptera novaeangliae) producen una demostración vocal sexual, o canto, en continua evolución que es similar entre todos los machos en una población. La transmisión cultural rápida (la transferencia de información o comportamientos entre co-específicos por medio del aprendizaje social) de diferentes versiones de esta demostración entre poblaciones distintas pero interconectadas en el centro y occidente en la región del sur del Pacífico presenta una manera única para investigar la estructura poblacional con base en las dinámicas de movimiento de la demostración del canto (acústico). Al usar once años de datos, con base en la acústica investigamos a una estructura poblacional de la región al comparar secuencias estereotipadas de cantos entre las poblaciones y los años. Usamos la técnica de la distancia Levenshtein para agrupar poblaciones previamente definidas en grupos (con base vocal) basados en la similitud general de su canto en el espacio y el tiempo. Identificamos a los siguientes grupos vocales perceptibles: grupo occidental, una población al este de Australia; grupo central, poblaciones alrededor de Nueva Caledonia, Tonga y Samoa Americana; y región oriental, ya sea un grupo único o dos grupos, uno alrededor de las Islas Cook y el otro cerca de la Polinesia Francesa. Estos resultados son consistentes con la hipótesis de que cada conjunto reproductivo representa a una población distinta (cada una ocupó un nodo terminal único) en una meta-población, similar al entendimiento actual de la estructura poblacional con base en los estudios genéticos y de foto-identificación. Sin embargo, el grupo vocal central tuvo niveles más altos de cantos compartidos entre las poblaciones que en los otros grupos, lo que indica que los niveles de conectividad vocal variaron dentro de la región. Nuestros resultados demuestran la utilidad y el valor de usar patrones vocales transmitidos culturalmente como una forma de definir la conectividad para inferir la estructura poblacional. Sugerimos que los patrones vocales sean incorporados por la Comisión Internacional de Caza de Ballenas en conjunto con los métodos tradicionales de evaluación de la estructura.

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.

Evidence of a Lombard response in migrating humpback whales (Megaptera novaeangliae).

The Lombard reflex is an increase in the subject's vocal levels in response to increased noise levels. This functions to maintain an adequate signal-to-noise ratio at the position of the receiver when noise levels vary. While it has been demonstrated in a small number of mammals and birds including some whales, it has not yet been shown to occur in one of the most vocal species of baleen whale, the humpback whale (Megaptera novaeangliae). Humpback whales were simultaneously visually and acoustically tracked (using an array of calibrated hydrophone buoys) as they migrated southward. Source levels of social vocalizations were estimated from measured received levels and a site-specific empirical sound propagation model developed. In total, 226 social vocalizations from 16 passing groups of whales were selected for final analysis. Noise levels were predominantly wind-dependent (from sea surface motion) and ranged from 81 to 108 dB re 1 µPa in the 36 Hz-2.8 kHz band. Vocalization source levels increased by 0.9 dB for every 1 dB increase in wind-dependent background noise levels, with source levels (at 1 m) being maintained ∼60 dB above the noise level.

Blubber gene expression and cortisol concentrations reveal changing physiological stress in a Southern ocean sentinel species.

The health of migratory eastern Australian humpback whales (Megaptera novaeangliae) can reflect the condition of their remote polar foraging environments. This study used gene expression (LEP, LEPR, ADIQ, AhR, TNF-α, HSP-70), blubber hormone concentrations (cortisol, testosterone), and photogrammetric body condition to assess this sentinel species during a period of unprecedented changes to anthropogenic activity and natural processes. The results revealed higher cortisol concentrations in 2020 compared to 2021, suggesting a decline in physiological stress between years. Additionally, metabolic transcripts LEPR, and AhR, which is also linked to xenobiotic metabolism, were upregulated during the 2020 southbound migration. These differences suggest that one or more environmental stressors were reduced between 2020 and 2021, with upregulated AhR possibly indicating a Southern Ocean pollutant declined between the years. This research confirms a Southern Ocean-wide decrease in whale stress during the study period and informs efforts to identify key stressors on Antarctic marine ecosystems.

Multivariate analysis of behavioural response experiments in humpback whales (Megaptera novaeangliae).

The behavioural response study (BRS) is an experimental design used by field biologists to determine the function and/or behavioural effects of conspecific, heterospecific or anthropogenic stimuli. When carrying out these studies in marine mammals it is difficult to make basic observations and achieve sufficient samples sizes because of the high cost and logistical difficulties. Rarely are other factors such as social context or the physical environment considered in the analysis because of these difficulties. This paper presents results of a BRS carried out in humpback whales to test the response of groups to one recording of conspecific social sounds and an artificially generated tone stimulus. Experiments were carried out in September/October 2004 and 2008 during the humpback whale southward migration along the east coast of Australia. In total, 13 'tone' experiments, 15 'social sound' experiments (using one recording of social sounds) and three silent controls were carried out over two field seasons. The results (using a mixed model statistical analysis) suggested that humpback whales responded differently to the two stimuli, measured by changes in course travelled and dive behaviour. Although the response to 'tones' was consistent, in that groups moved offshore and surfaced more often (suggesting an aversion to the stimulus), the response to 'social sounds' was highly variable and dependent upon the composition of the social group. The change in course and dive behaviour in response to 'tones' was found to be related to proximity to the source, the received signal level and signal-to-noise ratio (SNR). This study demonstrates that the behavioural responses of marine mammals to acoustic stimuli are complex. In order to tease out such multifaceted interactions, the number of replicates and factors measured must be sufficient for multivariate analysis.

Temporal stability and change in the social call repertoire of migrating humpback whales.

Quantifying the stability of a species vocal repertoire is fundamental for further investigations into repertoire function and geographic variation. Changes to the repertoire of sounds used in the song displays of male humpback whales have been well studied. In contrast, little is known about the stability of this species' non-song vocal calls. The stability of the social call repertoire of east Australian humpback whales was investigated from 1997, 2003-2004, and 2008. Out of 46 qualitatively defined call types, 19 were classified as "song-unit calls" that tended to change with the song, and 15 were "inconsistent" and only found in one or two years. Twelve call types were "stable" and present in all years and were commonly produced (64.2% of calls). Stable calls tended to vary in some of the measured call parameters but there was no clear trend between years. This result could indicate that minor changes to calls are not permanent, but reflect individual differences in call production or the graded nature of calls within different social environments. This research has clearly identified stable calls in the call repertoire of humpback whales and while their function is not well understood, their stability suggests an important role in social interactions.

Source levels of social sounds in migrating humpback whales (Megaptera novaeangliae).

The source level of an animal sound is important in communication, since it affects the distance over which the sound is audible. Several measurements of source levels of whale sounds have been reported, but the accuracy of many is limited because the distance to the source and the acoustic transmission loss were estimated rather than measured. This paper presents measurements of source levels of social sounds (surface-generated and vocal sounds) of humpback whales from a sample of 998 sounds recorded from 49 migrating humpback whale groups. Sources were localized using a wide baseline five hydrophone array and transmission loss was measured for the site. Social vocalization source levels were found to range from 123 to 183 dB re 1 µPa @ 1 m with a median of 158 dB re 1 µPa @ 1 m. Source levels of surface-generated social sounds ("breaches" and "slaps") were narrower in range (133 to 171 dB re 1 µPa @ 1 m) but slightly higher in level (median of 162 dB re 1 µPa @ 1 m) compared to vocalizations. The data suggest that group composition has an effect on group vocalization source levels in that singletons and mother-calf-singing escort groups tend to vocalize at higher levels compared to other group compositions.