Cetaceans are the next frontier for vocal rhythm research.

While rhythm can facilitate and enhance many aspects of behavior, its evolutionary trajectory in vocal communication systems remains enigmatic. We can trace evolutionary processes by investigating rhythmic abilities in different species, but research to date has largely focused on songbirds and primates. We present evidence that cetaceans-whales, dolphins, and porpoises-are a missing piece of the puzzle for understanding why rhythm evolved in vocal communication systems. Cetaceans not only produce rhythmic vocalizations but also exhibit behaviors known or thought to play a role in the evolution of different features of rhythm. These behaviors include vocal learning abilities, advanced breathing control, sexually selected vocal displays, prolonged mother-infant bonds, and behavioral synchronization. The untapped comparative potential of cetaceans is further enhanced by high interspecific diversity, which generates natural ranges of vocal and social complexity for investigating various evolutionary hypotheses. We show that rhythm (particularly isochronous rhythm, when sounds are equally spaced in time) is prevalent in cetacean vocalizations but is used in different contexts by baleen and toothed whales. We also highlight key questions and research areas that will enhance understanding of vocal rhythms across taxa. By coupling an infraorder-level taxonomic assessment of vocal rhythm production with comparisons to other species, we illustrate how broadly comparative research can contribute to a more nuanced understanding of the prevalence, evolution, and possible functions of rhythm in animal communication.

Evidence from sperm whale clans of symbolic marking in non-human cultures.

Culture, a pillar of the remarkable ecological success of humans, is increasingly recognized as a powerful force structuring nonhuman animal populations. A key gap between these two types of culture is quantitative evidence of symbolic markers-seemingly arbitrary traits that function as reliable indicators of cultural group membership to conspecifics. Using acoustic data collected from 23 Pacific Ocean locations, we provide quantitative evidence that certain sperm whale acoustic signals exhibit spatial patterns consistent with a symbolic marker function. Culture segments sperm whale populations into behaviorally distinct clans, which are defined based on dialects of stereotyped click patterns (codas). We classified 23,429 codas into types using contaminated mixture models and hierarchically clustered coda repertoires into seven clans based on similarities in coda usage; then we evaluated whether coda usage varied with geographic distance within clans or with spatial overlap between clans. Similarities in within-clan usage of both "identity codas" (coda types diagnostic of clan identity) and "nonidentity codas" (coda types used by multiple clans) decrease as space between repertoire recording locations increases. However, between-clan similarity in identity, but not nonidentity, coda usage decreases as clan spatial overlap increases. This matches expectations if sympatry is related to a measurable pressure to diversify to make cultural divisions sharper, thereby providing evidence that identity codas function as symbolic markers of clan identity. Our study provides quantitative evidence of arbitrary traits, resembling human ethnic markers, conveying cultural identity outside of humans, and highlights remarkable similarities in the distributions of human ethnolinguistic groups and sperm whale clans.

Long term trends in floating plastic pollution within a marine protected area identifies threats for Endangered northern bottlenose whales.

"The Gully", situated off Nova Scotia, Canada, is the largest submarine canyon in the western North Atlantic. This unique oceanographic feature, which became a Marine Protected Area (MPA) in 2004, is rich in marine biodiversity and is part of the critical habitat of Endangered northern bottlenose whales (Hyperoodon ampullatus). To understand the potential impact of plastic pollution in the MPA and on this Endangered cetacean, we evaluated trends over time in the abundance and composition of plastics and compared these to the stomach contents of recently stranded northern bottlenose whales. From the 1990s-2010s, the median abundance of micro-sized (<5 mm) and small plastics (5 mm-2.5 cm) increased significantly, while the median abundance of large plastics (>2.5 cm) decreased significantly. Plastic abundance from the 2010s for micro-sized and small plastics varied from 5586-438 196 particles km-2, higher than previously measured estimates for surrounding offshore areas. Polymers identified using FTIR spectroscopy included polyethylene, polypropylene, polyethylene terephthalate polyester, nylon, alkyds (paint), and natural and semi-synthetic cellulosic fibers. The abundance of large debris ranged from 0 to 108.6 items km-2 and consisted of plastic sheets and bags, food wrappers and containers, rope, fishing buoys, and small plastic fragments. Whale stomach contents contained fragments of fishing nets, ropes, bottle caps, cups, food wrappers, smaller plastic fragments, fibers, and paint flakes, consistent with the composition and character of items collected from their critical habitat. Despite being far from centres of human population, the unique oceanographic features of The Gully (i.e. currents and bathymetric complexity) may concentrate plastic debris, increasing exposure rates of whales to plastic pollution. The increase in micro-sized and small plastics over time suggests associated health and welfare impacts of ingested plastics should be accounted for in future recovery plans for this Endangered species.

Assessing social structure: a data-driven approach to define associations between individuals.

Our interpretation of animal social structures is inherently dependent on our ability to define association criteria that are biologically meaningful. However, association thresholds are often based upon generalized preconceptions of a species' social behaviour, and the impact of using these arbitrary definitions has been largely overlooked. In this study we suggest a probability-based method for defining association thresholds using lagged identification rates on photographic records of identifiable individuals. This technique uses a simple model of emigration/immigration from photographable clusters to identify the time-dependent lag value between identifications of two individuals that corresponds to approximately 75% probability of being in close spatial proximity and likely associating. This lag value is then used as the threshold to define associations for social analyses. We applied the technique to a dataset of northern resident killer whales (Orcinus orca) in the Northeast Pacific and tested its performance against two arbitrary thresholds. The probabilistic association maximized the variation in association strengths at different levels of the social structure, in line with known social patterns in this population. Furthermore, variability in inferred social structure metrics generated by different association criteria highlighted the consequential effect of choosing arbitrary thresholds. Data-driven association thresholds are a promising approach to study populations without the need to subjectively define associations in the field, especially in societies with prominent fission-fusion dynamics. This method is applicable to any dataset of sequential identifications where it can be assumed that associated individuals will tend to be identified in close proximity. Supplementary Information: The online version contains supplementary material available at 10.1007/s42991-022-00231-9.

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.

Adaptation of sperm whales to open-boat whalers: rapid social learning on a large scale?

Animals can mitigate human threats, but how do they do this, and how fast can they adapt? Hunting sperm whales was a major nineteenth century industry. Analysis of data from digitized logbooks of American whalers in the North Pacific found that the rate at which whalers succeeded in harpooning ('striking') sighted whales fell by about 58% over the first few years of exploitation in a region. This decline cannot be explained by the earliest whalers being more competent, as their strike rates outside the North Pacific, where whaling had a longer history, were not elevated. The initial killing of particularly vulnerable individuals would not have produced the observed rapid decline in strike rate. It appears that whales swiftly learned effective defensive behaviour. Sperm whales live in kin-based social units. Our models show that social learning, in which naive social units, when confronted by whalers, learned defensive measures from grouped social units with experience, could lead to the documented rapid decline in strike rate. This rapid, large-scale adoption of new behaviour enlarges our concept of the spatio-temporal dynamics of non-human culture.

Cultural specialization and genetic diversity: Killer whales and beyond.

Culturally-transmitted ecological specialization can reduce niche breadths with demographic and ecological consequences. I use agent-based models, grounded in killer whale biology, to investigate the potential consequences of cultural specialization for genetic diversity. In these models, cultural specialization typically reduces the number of mitochondrial haplotypes, mitochondrial haplotype diversity, mitochondrial nucleotide diversity, and heterozygosity at nuclear loci. The causal route of this decline is mostly indirect, being ascribed to a reduction in absolute population size resulting from cultural specialization. However, small group size exacerbates the decline in genetic diversity, presumably because of increased founder effects at the initiation of each cultural ecotype. These results are concordant with measures of low genetic diversity in the killer whale, although culturally-transmitted ecological specialization alone might not be sufficient to fully account for the species' very low mitochondrial diversity. The process may also operate in other species.

Gene-culture coevolution in whales and dolphins.

Whales and dolphins (Cetacea) have excellent social learning skills as well as a long and strong mother-calf bond. These features produce stable cultures, and, in some species, sympatric groups with different cultures. There is evidence and speculation that this cultural transmission of behavior has affected gene distributions. Culture seems to have driven killer whales into distinct ecotypes, which may be incipient species or subspecies. There are ecotype-specific signals of selection in functional genes that correspond to cultural foraging behavior and habitat use by the different ecotypes. The five species of whale with matrilineal social systems have remarkably low diversity of mtDNA. Cultural hitchhiking, the transmission of functionally neutral genes in parallel with selective cultural traits, is a plausible hypothesis for this low diversity, especially in sperm whales. In killer whales the ecotype divisions, together with founding bottlenecks, selection, and cultural hitchhiking, likely explain the low mtDNA diversity. Several cetacean species show habitat-specific distributions of mtDNA haplotypes, probably the result of mother-offspring cultural transmission of migration routes or destinations. In bottlenose dolphins, remarkable small-scale differences in haplotype distribution result from maternal cultural transmission of foraging methods, and large-scale redistributions of sperm whale cultural clans in the Pacific have likely changed mitochondrial genetic geography. With the acceleration of genomics new results should come fast, but understanding gene-culture coevolution will be hampered by the measured pace of research on the socio-cultural side of cetacean biology.

Consequences of culturally-driven ecological specialization: Killer whales and beyond.

Culturally-transmitted ecological specialization occurs in killer whales, as well as other species. We hypothesize that some of the remarkable demographic and ecological attributes of killer whales result from this process. We formalize and model (using agent-based stochastic models parametrized using killer whale life history) the cultural evolution of specialization by social groups, in which a narrowing of niche breadth is spread and maintained in a group through social learning. We compare the demographic and ecological results of cultural specialization to those of a similar model of specialization through natural selection. We found that specialization, through either the cultural or natural selection routes, is adaptive in the short term with specialization often increasing fitness. Generalization, in contrast, is rarely adaptive. The cultural evolution of specialization can lead to increased rates of group extirpation. Specialization has little effect on group size but tends to reduce population size and resource abundance. While the two specialization processes produce similar results, cultural specialization can be very much faster. The results are generally consistent with what we know of the formation and maintenance of specialist ecotypes in killer whales, and have implications for the persistence, nature and ecological effects of these apex predators.

Automatic acoustic estimation of sperm whale size distributions achieved through machine recognition of on-axis clicks.

The waveforms of individual sperm whale clicks often appear as multiple pulses, which are the product of a single pulse reverberating throughout the spermaceti organ. Since there is a relationship between spermaceti organ size and total body size, it is possible to estimate a whale's length by measuring the inter-pulse intervals (IPIs) within its clicks. However, if a click is recorded off-axis, the IPI corresponding to spermaceti organ length is usually obscured. This paper presents an algorithm for automatically estimating the "true" IPIs of sperm whales in a recording by measuring them from on-axis clicks only. The routine works by classifying detected clicks with a support vector machine, assessing the stability of their IPIs, and then clustering the stable IPIs using Gaussian mixture models. Results show that the routine is very accurate in obtaining reliable IPIs, but has a high false negative rate. Nonetheless, since sperm whales click very frequently, it is possible to obtain useful IPI distributions with only a few minutes of recording. This algorithm makes it possible to estimate the body lengths of multiple sperm whales automatically with only one hydrophone. An implementation is available for download at http://whitelab.biology.dal.ca/CABLE/cable.htm.

Variability of the inter-pulse interval in sperm whale clicks with implications for size estimation and individual identification.

Sperm whales generate multi-pulsed clicks for echolocation and communication with an inter-pulse interval (IPI) determined by the size of their hypertrophied sound producing nose. The IPI has therefore been used to estimate body size and distinguish between individuals, and it has been hypothesized that conspecifics may use IPIs to recognize each other. However, the degree to which IPIs vary within individuals has not explicitly been tested, and therefore the inherent precision of this measure and its applicability for size estimation for researchers and sperm whales alike remain unknown. Here, the variability in IPI from both animal-borne Dtags and far-field recordings from echolocating and communicating sperm whales is quantified. Three different automatic methods (envelope, cepstrum, and cross-correlation) are tested and it is found that the envelope approach results in the least dispersion. Furthermore, it is shown that neither growth, depth, nor recording aspect fully explains the observed variability among clicks recorded from the same individual. It is proposed that dynamics in the soft structures of the nose are affecting IPIs, resulting in a variation of approximately 0.2 ms. Therefore, it is recommended that this variation be considered in IPI studies and that IPIs may have limited functionality as an identity cue among large groups of conspecifics.

Cultural Hitchhiking in the Matrilineal Whales.

Five species of whale with matrilineal social systems (daughters remain with mothers) have remarkably low levels of mitochondrial DNA diversity. Non-heritable matriline-level demography could reduce genetic diversity but the required conditions are not consistent with the natural histories of the matrilineal whales. The diversity of nuclear microsatellites is little reduced in the matrilineal whales arguing against bottlenecks. Selective sweeps of the mitochondrial genome are feasible causes but it is not clear why these only occurred in the matrilineal species. Cultural hitchhiking (cultural selection reducing diversity at neutral genetic loci transmitted in parallel to the culture) is supported in sperm whales which possess suitable matrilineal socio-cultural groups (coda clans). Killer whales are delineated into ecotypes which likely originated culturally. Culture, bottlenecks and selection, as well as their interactions, operating between- or within-ecotypes, may have reduced their mitochondrial diversity. The societies, cultures and genetics of false killer and two pilot whale species are insufficiently known to assess drivers of low mitochondrial diversity.

Constructing, conducting and interpreting animal social network analysis.

1. Animal social networks are descriptions of social structure which, aside from their intrinsic interest for understanding sociality, can have significant bearing across many fields of biology. 2. Network analysis provides a flexible toolbox for testing a broad range of hypotheses, and for describing the social system of species or populations in a quantitative and comparable manner. However, it requires careful consideration of underlying assumptions, in particular differentiating real from observed networks and controlling for inherent biases that are common in social data. 3. We provide a practical guide for using this framework to analyse animal social systems and test hypotheses. First, we discuss key considerations when defining nodes and edges, and when designing methods for collecting data. We discuss different approaches for inferring social networks from these data and displaying them. We then provide an overview of methods for quantifying properties of nodes and networks, as well as for testing hypotheses concerning network structure and network processes. Finally, we provide information about assessing the power and accuracy of an observed network. 4. Alongside this manuscript, we provide appendices containing background information on common programming routines and worked examples of how to perform network analysis using the r programming language. 5. We conclude by discussing some of the major current challenges in social network analysis and interesting future directions. In particular, we highlight the under-exploited potential of experimental manipulations on social networks to address research questions.

Sperm whale clans and human societies.

Sperm whale society is structured into clans that are primarily distinguished by vocal dialects, which may be symbolic markers of clan identity. However, clans also differ in non-vocal behaviour. These distinctive behaviours, as well as clan membership itself, are learned socially, largely within matrilines. The clans can contain thousands of whales and span thousands of kilometres. Two or more clans typically use an area, but the whales only socialize with members of their own clan. In many respects the closest parallel may be the ethno-linguistic groups of humans. Patterns and processes of human prehistory that may be instructive in studying sperm whale clans include: the extreme variability of human societies; no clear link between modes of resource acquisition and social structure; that patterns of vocalizations may not map well onto other behavioural distinctions; and that interacting societies may deliberately distinguish their behaviour (schismogenesis). Conversely, while the two species and their societies are very different, the existence of very large-scale social structures in both sperm whales and humans supports some primary drivers of the phenomenon that are common to both species (such as cognition, cooperation, culture and mobility) and contraindicates others (e.g. tool-making and syntactic language).

Calves as social hubs: dynamics of the social network within sperm whale units.

It is hypothesized that the primary function of permanent social relationships among female sperm whales (Physeter macrocephalus) is to provide allomothers for calves at the surface while mothers make foraging dives. In order to investigate how reciprocity of allocare within units of sperm whales facilitates group living, we constructed weighted social networks based on yearly matrices of associations (2005-2010) and correlated them across years, through changes in age and social role, to study changes in social relationships within seven sperm whale units. Pairs of association matrices from sequential years showed a greater positive correlation than expected by chance, but as the time lag increased, the correlation coefficients decreased. Over all units considered, calves had high values for all measured network statistics, while mothers had intermediate values for most of the measures, but high values for connectedness and affinity. Mothers showed sharp drops in strength and connectedness in the first year of their new calves' lives. These broad patterns appear to be consistent across units. Calves appeared to be significant nodes in the network of the social unit, and thus provide quantitative support for the theory in which communal care acts as the evolutionary force behind group formation in this species.

Can genetic differences explain vocal dialect variation in sperm whales, Physeter macrocephalus?

Sperm whale social groups can be assigned to vocal clans based on their production of codas, short stereotyped patterns of clicks. It is currently unclear whether genetic variation could account for these behavioural differences. We studied mitochondrial DNA (mtDNA) variation among sympatric vocal clans in the Pacific Ocean, using sequences extracted from sloughed skin samples. We sampled 194 individuals from 30 social groups belonging to one of three vocal clans. As in previous studies of sperm whales, mtDNA control region diversity was low (π = 0.003), with just 14 haplotypes present in our sample. Both hierarchical AMOVAs and partial Mantel tests showed that vocal clan was a more important factor in matrilineal population genetic structure than geography, even though our sampling spanned thousands of kilometres. The variance component attributed to vocal dialects (7.7%) was an order of magnitude higher than those previously reported in birds, while the variance component attributed to geographic area was negligible. Despite this, the two most common haplotypes were present in significant quantities in each clan, meaning that variation in the control region cannot account for behavioural variation between clans, and instead parallels the situation in humans where parent-offspring transmission of language variation has resulted in correlations with neutral genes. Our results also raise questions for the management of sperm whale populations, which has traditionally been based on dividing populations into geographic 'stocks', suggesting that culturally-defined vocal clans may be more appropriate management units.

Animal social networks as substrate for cultural behavioural diversity.

We used individual-based stochastic models to examine how social structure influences the diversity of socially learned behaviour within a non-human population. For continuous behavioural variables we modelled three forms of dyadic social learning, averaging the behavioural value of the two individuals, random transfer of information from one individual to the other, and directional transfer from the individual with highest behavioural value to the other. Learning had potential error. We also examined the transfer of categorical behaviour between individuals with random directionality and two forms of error, the adoption of a randomly chosen existing behavioural category or the innovation of a new type of behaviour. In populations without social structuring the diversity of culturally transmitted behaviour increased with learning error and population size. When the populations were structured socially either by making individuals members of permanent social units or by giving them overlapping ranges, behavioural diversity increased with network modularity under all scenarios, although the proportional increase varied considerably between continuous and categorical behaviour, with transmission mechanism, and population size. Although functions of the form e(c)¹(m)⁻(c)² + (c)³(Log(N)) predicted the mean increase in diversity with modularity (m) and population size (N), behavioural diversity could be highly unpredictable both between simulations with the same set of parameters, and within runs. Errors in social learning and social structuring generally promote behavioural diversity. Consequently, social learning may be considered to produce culture in populations whose social structure is sufficiently modular.

Current global population size, post-whaling trend and historical trajectory of sperm whales.

The sperm whale lives in most deep ice-free waters of the globe. It was targeted during two periods of whaling peaking in the 1840's and 1960's. Using a habitat suitability model, we extrapolated estimates of abundance from visual and acoustic surveys to give a global estimate of 736,053 sperm whales (CV = 0.218) in 1993. Estimates of trends in the post-whaling era suggest that: whaling, by affecting the sex ratio and/or the social cohesion of females, reduced recovery rates well after whaling ceased; preferentially-targeted adult males show the best evidence of recovery, presumably due to recruitment from breeding populations; several decades post-whaling, sperm whale populations not facing much human impact are recovering slowly, but populations may be declining in areas with substantial anthropogenic footprint. A theta-logistic population model enhanced to simulate spatial structure and the non-removal impacts of whaling indicated a pre-whaling population of 1,949,698 (CV = 0.178) in 1710 being reduced by whaling, and then then recovering a little to about 844,761 (CV = 0.209) in 2022. There is much uncertainty about these numbers and trends. A larger population estimate than produced by a similar analysis in 2002 is principally due to a better assessment of ascertainment bias.

Posterior probabilities of membership of repertoires in acoustic clades.

Recordings of calls may be used to assess population structure for acoustic species. This can be particularly effective if there are identity calls, produced nearly exclusively by just one population segment. The identity call method, IDcall, classifies calls into types using contaminated mixture models, and then clusters repertoires of calls into identity clades (potential population segments) using identity calls that are characteristic of the repertoires in each identity clade. We show how to calculate the Bayesian posterior probabilities that each repertoire is a member of each identity clade, and display this information as a stacked bar graph. This methodology (IDcallPP) is introduced using the output of IDcall but could easily be adapted to estimate posterior probabilities of clade membership when acoustic clades are delineated using other methods. This output is similar to that of the STRUCTURE software which uses molecular genetic data to assess population structure and has become a standard in conservation genetics. The technique introduced here should be a valuable asset to those who use acoustic data to address evolution, ecology, or conservation, and creates a methodological and conceptual bridge between geneticists and acousticians who aim to assess population structure.