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

Funding was provided by the Bureau of Ocean Energy Management under InterAgency Agreement M09PG00016. E.C.G. was supported by a National Research Council (National Academy of Sciences) Postdoctoral Fellowship.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 clas- sification 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 pas- sive 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.Publisher PDFPeer reviewe

Reproductive tactics in baleen whales

Funding: FE is supported by a University of St Andrews School of Biology Ph.D. scholarship and a Royal Society Research Fellows Enhancement Award (RGF\EA \180213 to ECG), ECG is funded by a Royal Society University Research Fellowship (UF160081 & URF\R\221020), and ELC is funded by a Rutherford Discovery Fellowship from the Royal Society of New Zealand Te Apārangi.While a variety of reproductive tactics are readily witnessed in the odontocetes, such behaviors can be far more elusive, and in some cases, are yet to be observed, in baleen whales. This leads researchers to employ a variety of research methods, some of which have improved greatly in recent decades, to study reproductive behaviors in mysticetes. Genetics and genomics tools can provide invaluable information on maternity, paternity, age, diversity, and kinship, while acoustic tools can provide new insights into the function of sexual displays such as song. In this chapter, we explore what is known about the reproductive strategies and tactics of baleen whales, with a particular focus on the comparatively well-studied right whales (Eubalaena spp.) and humpback whales (Megaptera novaeangliae). Finally, we showcase that by integrating multiple data types, we can explore the interactions between anatomy, physiology, reproductive success, age, population dynamics, and acoustic displays to better understand the mating systems of baleen whales.Publisher PD

Phylogenetically controlled life history trait meta-analysis in cetaceans reveals unexpected negative brain size and longevity correlation

Funding: ELC was supported by a Rutherford Discovery Fellowship from the Royal Society of New Zealand Te Apārangi and EG was supported by a University Research Fellowship from the Royal Society of London.The identification of patterns in trait evolution is essential to understand the interaction of evolutionary forces, and provides useful information for species management. Cetaceans are a phylogenetically well-resolved infraorder that exhibit distinct trait variation across behavioural, molecular and life history dimensions, yet few researchers have applied a meta-analytic or comparative approach to these traits. To understand cetacean trait evolution, we used a phylogenetic generalised least squares approach to examine the cognitive buffer hypothesis (CBH). A large brain should buffer individuals against environmental challenges through increasing survival rates, and a longer lifespan should buffer individuals against the cost of extended development for larger brains according to the CBH, leading to an expected positive correlation between brain size and lifespan. In contrast to this expectation, previously observed in taxa including primates, we found a negative correlation between brain size and lifespan in cetaceans. This suggests cetaceans experience selective pressures different from most other mammals in these traits but may be more similar to some social mammalian carnivores that display alloparenting. We also provide a comprehensive dataset to explore additional aspects of trait evolution but which would greatly benefit from studies on behavioural ecology across cetaceans and increased focus on data deficient species.Publisher PDFPeer reviewe

Global cultural evolutionary model of humpback whale song

Funding: ECG is funded by a Royal Society University Research Fellowship (UF160081). RFL and LZ are funded by the BBSRC (BB/R008736/2). LL was supported by a Leverhulme Trust Grant to Luke Rendell (among other recipients; grant reference RPG-2013-367)Humpback whale song is an extraordinary example of vocal cultural behaviour. In northern popula-tions, the complex songs show long-lasting traditions that slowly evolve, while in the South Pacific, pe-riodic revolutions occur when songs are adopted from neighbouring populations and rapidly spread. In this species, vocal learning cannot be studied in the laboratory, learning is instead inferred from the songs’ complexity and patterns of transmission. Here, we used individual-based cultural evolutionary simulations of the entire Southern and Northern Hemisphere humpback whale populations to formalise this process of inference. We modelled processes of song mutation and patterns of contact among popu-lations and compared our model with patterns of song theme sharing measured in South Pacific popula-tions. Low levels of mutation in combination with rare population interactions were sufficient to closely fit the pattern of diversity in the South Pacific, including the distinctive pattern of West-to-East revolu-tions. Interestingly, the same learning parameters that gave rise to revolutions in the Southern Hemi-sphere simulations gave rise to evolutionary patterns of cultural evolution in the Northern Hemisphere populations. Our study demonstrates how cultural evolutionary approaches can be used to make infer-ences about the learning processes underlying cultural transmission and how they might generate emergent population-level processes.Publisher PDFPeer reviewe

Humpback whale song revolutions continue to spread from the central into the eastern South Pacific

Funding: COCIBA grants of USFQ National Geographic Society - W396-15; NERC Sea Mammal Research Unit - NE/R015007/1; Project CETACEA Ecuador Royal Society - NF140667, UF160081; Rufford Foundation.Cultural transmission of behaviour is an important aspect of many animal communities ranging from humans to birds. Male humpback whales (Megaptera novaeangliae) sing a repetitive, stereotyped, socially learnt and culturally transmitted song display that slowly evolves each year. Most males within a population sing the same, slow-evolving song type; but in the South Pacific, song ‘revolutions’ have led to rapid and complete replacement of one song type by another introduced from a neighbouring population. Songs spread eastwards, from eastern Australia to French Polynesia, but the easterly extent of this transmission was unknown. Here, we investigated whether song revolutions continue to spread from the central (French Polynesia) into the eastern (Ecuador) South Pacific region. Similarity analyses using three consecutive years of song data (2016–2018) revealed that song themes recorded in 2016–2018 French Polynesian song matched song themes sung in 2018 Ecuadorian song, suggesting continued easterly transmission of song to Ecuador, and vocal connectivity across the entire South Pacific Ocean basin. This study demonstrates songs first identified in western populations can be transmitted across the entire South Pacific, supporting the potential for a circumpolar Southern Hemisphere cultural transmission of song and a vocal culture rivalled in its extent only by our own.Publisher PDFPeer reviewe

A pan-cetacean MHC amplicon sequencing panel developed and evaluated in combination with genome assemblies

This study was funded by a Royal Society Research Grants for Research Fellows (RGF\R1\181014) to E.C.G. E.C.G. is funded by a Royal Society University Research Fellowship (UF160081 & URF\R\221020). F.E. is supported by a University of St Andrews School of Biology Ph.D. scholarship and a Royal Society Research Fellows Enhancement Award (RGF\EA\180213 to E.C.G). E.L.C. is funded by a Rutherford Discovery Fellowship from the Royal Society of New Zealand Te Apārangi.The major histocompatibility complex (MHC) is a highly polymorphic gene family that is crucial in immunity, and its diversity can be effectively used as a fitness marker for populations. Despite this, MHC remains poorly characterised in non-model species (e.g., cetaceans: whales, dolphins and porpoises) as high gene copy number variation, especially in the fast-evolving class I region, makes analyses of genomic sequences difficult. To date, only small sections of class I and IIa genes have been used to assess functional diversity in cetacean populations. Here, we undertook a systematic characterisation of the MHC class I and IIa regions in available cetacean genomes. We extracted full-length gene sequences to design pan-cetacean primers that amplified the complete exon2 from MHC class I and IIa genes in one combined sequencing panel. We validated this panel in 19 cetacean species and described 354 alleles for both classes. Furthermore, we identified likely assembly artefacts for many MHC class I assemblies based on the presence of class I genes in the amplicon data compared to missing genes from genomes. Finally, we investigated MHC diversity using the panel in 25 humpback and 30 southern right whales, including four paternity trios for humpback whales. This revealed copy-number variable class I haplotypes in humpback whales, which is likely a common phenomenon across cetaceans. These MHC alleles will form the basis for a cetacean branch of the Immuno-Polymorphism Database (IPD-MHC), a curated resource intended to aid in the systematic compilation of MHC alleles across several species, to support conservation initiatives.Peer reviewe

Culturally transmitted song exchange between humpback whales (Megaptera novaeangliae) in the southeast Atlantic and southwest Indian Ocean basins

Funding: E.C.G. was funded by a Royal Society Newton International Fellowship and Royal Society University Research Fellowship.In migratory marine species, investigating population connectivity and structure can be challenging given barriers to dispersal are less evident and multiple factors may influence individual movement patterns. Male humpback whales sing a song display that can provide insights into contemporary connectivity patterns, as there can be a cultural exchange of a single, population-wide shared song type with neighbouring populations in acoustic contact. Here, we investigated song exchange between populations located on the east and west coasts of Africa using 5 years of concurrent data (2001–2005). Songs were qualitatively and quantitatively transcribed by measuring acoustic features of all song units and then compared using both Dice’s similarity index and the Levenshtein distance similarity index (LSI) to quantitatively calculate song similarity. Song similarity varied among individuals and potentially between populations depending on the year (Dice: 36–100%, LSI: 21–100%), suggesting varying levels of population connectivity and/or interchange among years. The high degree of song sharing indicated in this study further supports genetic studies that demonstrate interchange between these two populations and reinforces the emerging picture of broad-scale connectivity in Southern Hemisphere populations. Further research incorporating additional populations and years would be invaluable for better understanding of fine-scale, song interchange patterns between Southern Hemisphere male humpback whales.Publisher PDFPeer reviewe

Management of acoustic metadata for bioacoustics

Recent expansion in the capabilities of passive acoustic monitoring of sound-producing animals is providing expansive data sets in many locations. These long-termdata sets will allowthe investigation of questions related to the ecology of sound-producing animals on time scales ranging fromdiel 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 froma 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.) fromawide 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.Publisher PDFPeer reviewe

Migratory convergence facilitates cultural transmission of humpback whale song

E.C.G. was supported by a Royal Society Newton International Fellowship and a Royal Society University Research Fellowship. L.R. was supported by the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) and their support is gratefully acknowledged. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions.Cultural transmission of behaviour is important in a wide variety of vertebrate taxa from birds to humans. Vocal traditions and vocal learning provide a strong foundation for studying culture and its transmission in both humans and cetaceans. Male humpback whales (Megaptera novaeangliae) perform complex, culturally transmitted song displays that can change both evolutionarily (through accumulations of small changes) or revolutionarily (where a population rapidly adopts a novel song). The degree of coordination and conformity underlying song revolutions makes their study of particular interest. Acoustic contact on migratory routes may provide a mechanism for cultural revolutions of song, yet these areas of contact remain uncertain. Here, we compared songs recorded from the Kermadec Islands, a recently discovered migratory stopover, to multiple South Pacific wintering grounds. Similarities in song themes from the Kermadec Islands and multiple wintering locations (from New Caledonia across to the Cook Islands) suggest a location allowing cultural transmission of song eastward across the South Pacific, active song learning (hybrid songs) and the potential for cultural convergence after acoustic isolation at the wintering grounds. As with the correlations in humans between genes, communication and migration, the migration patterns of humpback whales are written into their songs.Publisher PDFPeer reviewe

Cultural transmission of humpback whale song and metapopulation structure in the western and central South Pacific Ocean

Male humpback whales produce a long, complex and highly stereotyped acoustic display termed ‘song’. The exact function of song is unclear but it is believed to be involved in sexual selection through mate attraction and/or male social ordering. All males within a population adhere to the current content and arrangement of the display. Song is highly plastic as it progressively evolves over time and all males are required to make similar changes to maintain the observed conformity. Within an ocean basin, populations sing similar songs with the level of similarity based on the geographical distance between populations. This conclusion is based predominately on studies conducted in the North Pacific which have usually been drawn from a single synoptic year of data. Currently, no studies have investigated the long-term dynamics of ocean basin song. Therefore, the primary aim of this thesis was to investigate the dynamics and thus pattern of cultural transmission of humpback whale song within an ocean basin. Secondarily, I aimed to use this information to produce an acoustically-derived understanding of population structure. This was achieved by analysing extensive song data from multiple populations located within the western and central South Pacific region over eleven consecutive years. To investigate song similarity, data were first required to be transcribed by hand to produce a large qualitative description of all songs (termed song types) present within the region over the eleven year time period. Each of the 67 themes identified were assigned to one of the 11 song types which were given arbitrary colour names. This is the largest description to date of different versions of this display and represents a significant foundation for this thesis. Song types were observed to move in an easterly direction from the western-most population of eastern Australia across the region to French Polynesia. The movement of song types frequently caused complete ‘cultural revolution’ to the display. This unidirectional propagation produced multiple ‘cultural waves’ which were regular and repeated, taking approximately two years to transit the region. The only previous documentation of rapid population-wide cultural change occurred in the song of the eastern Australian humpback whales when a new, novel song type was introduced from the western Australian population and rapidly revolutionised the existing song type. This original ‘cultural revolution’ can now be traced moving across the South Pacific region in this thesis and represents the survival of a highly plastic cultural signal (song type) spanning seven years and two ocean basins. To further investigate ocean basin song similarity at both the population and individual level, quantitative analyses were undertaken. The Levenshtein distance method was used to understand the relationship among population or individual displays based on the calculated similarity of call sequences. Humpback whale song is produced in a stereotyped sequence which allowed the quantification of different versions of the display through clustering of similar sequences to assign song types. Clustering did not occur based on geographic location or the year the song was recorded. Thus, it represented an index of similarity based on the cultural signal which allowed the changes to that signal to be quantitatively traced. An acoustically-derived population structure was developed from this quantitative analysis based on yearly similarity due to the dynamic nature of the display. This resulted in three distinct but interconnected population groupings for the region. The western group contained a single population, eastern Australia, the central group was comprised of New Caledonia, Tonga and American Samoa and finally an eastern group contained the Cook Islands and French Polynesia. This broadly agrees with concurrent genetic and photo-identification studies within the region, and suggests the combination of all three platforms will help elucidate the region’s complex metapopulation structure. This thesis describes the rapid, regular and repeated horizontal cultural transmission of multiple song types of a highly plastic display across a vast oceanic region. This is the first study to investigate the previously unknown dynamics of song movement and to use these results to produce, using quantitative techniques, a population structure based on acoustic display similarity. Future work is required to understand the applicability of these large-scale song dynamics to other ocean basins, the fine-scale aspects of song evolution and revolution, and to further investigate the role and conforming influence of culture on this sexually selected display