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).

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.

Distinctive, fine-scale distribution of Eastern Caribbean sperm whale vocal clans reflects island fidelity rather than environmental variables.

Environmental variables are often the primary drivers of species' distributions as they define their niche. However, individuals, or groups of individuals, may sometimes adopt a limited range within this larger suitable habitat as a result of social and cultural processes. This is the case for Eastern Caribbean sperm whales. While environmental variables are reasonably successful in describing the general distribution of sperm whales in the region, individuals from different cultural groups have distinct distributions around the Lesser Antilles islands. Using data collected over 2 years of dedicated surveys in the Eastern Caribbean, we conducted habitat modeling and habitat suitability analyses to investigate the mechanisms responsible for such fine-scale distribution patterns. Vocal clan-specific models were dramatically more successful at predicting distribution than general species models, showing how a failure to incorporate social factors can impede accurate predictions. Habitat variation between islands did not explain vocal clan distributions, suggesting that cultural group segregation in the Eastern Caribbean sperm whale is driven by traditions of site/island fidelity (most likely maintained through conformism and homophily) rather than habitat type specialization. Our results provide evidence for the key role of cultural knowledge in shaping habitat use of sperm whales within suitable environmental conditions and highlight the importance of cultural factors in shaping sperm whale ecology. We recommend that social and cultural information be incorporated into conservation and management as culture can segregate populations on fine spatial scales in the absence of environmental variability.

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.

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.

Ocean nomads or island specialists? Culturally driven habitat partitioning contrasts in scale between geographically isolated sperm whale populations.

The sperm whale (Physeter macrocephalus) is a deep-diving cetacean with a global distribution and a multi-leveled, culturally segregated, social structure. While sperm whales have previously been described as 'ocean nomads', this might not be universal. We conducted surveys of sperm whales along the Lesser Antilles to document the acoustic repertoires, movements and distributions of Eastern Caribbean (EC) sperm whale cultural groups (called vocal clans). In addition to documenting a potential third vocal clan in the EC, we found strong evidence of fine-scale habitat partitioning between vocal clans with scales of horizontal movements an order of magnitude smaller than from comparable studies on Eastern Tropical Pacific sperm whales. These results suggest that sperm whales can display cultural ecological specialization and habitat partitioning on flexible spatial scales according to local conditions and broadens our perception of the ecological flexibility of the species. This study highlights the importance of incorporating multiple temporal and spatial scales to understand the impact of culture on ecological adaptability, as well as the dangers of extrapolating results across geographical areas and cultural groups.

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.

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.

Long-term associations among male sperm whales (Physeter macrocephalus).

Little is known about the social structure of male sperm whales (Physeter macrocephalus) after they leave their natal units. While previous studies found no evidence for preferred associations among males, the observation of mass-strandings consisting exclusively of males, suggest that they have strong social bonds. To investigate the social associations among male sperm whales, we used half weight index of association, permutation tests and standardized lagged association rate models on a large photo-identification database collected between 2006 and 2017 in Nemuro Strait, Japan. Our results suggest that while male sperm whales are not as social as females, they do form long term associations, have preferred companionship, and forage in social proximity to each other. The best-fitting model to the standardized lagged association rate showed that associations among males last for at least 2.7 years and as most males leave the area after 2 years, associations may last for longer. Twenty dyads were observed associating over more than 2 years, for a maximum 5 years. One dyad was observed associating on 19 different days and clustered on 7 different days. Male associations may function to enhance foraging or to fend off predators. Such relationships seem to be adapted to a pelagic habitat with uncertain resource availability and predation pressure.

Prolonged maternal investment in northern bottlenose whales alters our understanding of beaked whale reproductive life history.

Nursing and weaning periods are poorly understood in cetaceans due to the difficulty of assessing underwater behaviour in the wild. However, the onset and completion of weaning are critical turning points for individual development and survival, with implications for a species' life history including reproductive potential. δ15N and δ13C deposited in odontocete teeth annuli provide a lifetime record of diet, offering an opportunity to investigate variation and trends in fundamental biology. While available reproductive parameters for beaked whales have largely been inferred from single records of stranded or hunted animals and extrapolated across species, here we examine the weaning strategy and nursing duration in northern bottlenose whales (Hyperoodon ampullatus) by measuring stable isotopes deposited in dentine growth layer groups (GLGs). Using a collection of H. ampullatus teeth taken from whales killed during the whaling era (N = 48) and from two stranded specimens, we compared ontogenetic variation of δ15N and δ13C found in annual GLGs across all individuals, by sex and by region. We detected age-based trends in both δ15N and δ13C that are consistent across regions and males and females, and indicate that nursing is prolonged and weaning does not conclude until whales are 3-4 years old, substantially later than previous estimates of 1 year. Incorporating a prolonged period of maternal care into H. ampullatus life history significantly reduces their reproductive potential, with broad implications for models of beaked whale life history, energetics and the species' recovery from whaling.

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.

Evolutionary impacts differ between two exploited populations of northern bottlenose whale (Hyperoodon ampullatus).

Interpretation of conservation status should be informed by an appreciation of genetic diversity, past demography, and overall trends in population size, which contribute to a species' evolutionary potential and resilience to genetic risks. Low genetic diversity can be symptomatic of rapid demographic declines and impose genetic risks to populations, but can also be maintained by natural processes. The northern bottlenose whale Hyperoodon ampullatus has the lowest known mitochondrial diversity of any cetacean and was intensely whaled in the Northwest Atlantic over the last century, but whether exploitation imposed genetic risks that could limit recovery is unknown. We sequenced full mitogenomes and genotyped 37 novel microsatellites for 128 individuals from known areas of abundance in the Scotian Shelf, Northern and Southern Labrador, Davis Strait, and Iceland, and a newly discovered group off Newfoundland. Despite low diversity and shared haplotypes across all regions, both markers supported the Endangered Scotian Shelf population as distinct from the combined northern regions. The genetic affinity of Newfoundland was uncertain, suggesting an area of mixing with no clear population distinction for the region. Demographic reconstruction using mitogenomes suggests that the northern region underwent population expansion following the last glacial maximum, but for the peripheral Scotian Shelf population, a stable demographic trend was followed by a drastic decline over a temporal scale consistent with increasing human activity in the Northwest Atlantic. Low connectivity between the Scotian Shelf and the rest of the Atlantic likely compounded the impact of intensive whaling for this species, potentially imposing genetic risks affecting recovery of this population. We highlight how the combination of historical environmental conditions and modern exploitation of this species has had very different evolutionary impacts on structured populations of northern bottlenose whales across the western North Atlantic.

Causes and consequences of female centrality in cetacean societies.

Cetaceans are fully aquatic predatory mammals that have successfully colonized virtually all marine habitats. Their adaptation to these habitats, so radically different from those of their terrestrial ancestors, can give us comparative insights into the evolution of female roles and kinship in mammalian societies. We provide a review of the diversity of such roles across the Cetacea, which are unified by some key and apparently invariable life-history features. Mothers are uniparous, while paternal care is completely absent as far as we currently know. Maternal input is extensive, lasting months to many years. Hence, female reproductive rates are low, every cetacean calf is a significant investment, and offspring care is central to female fitness. Here strategies diverge, especially between toothed and baleen whales, in terms of mother-calf association and related social structures, which range from ephemeral grouping patterns to stable, multi-level, societies in which social groups are strongly organized around female kinship. Some species exhibit social and/or spatial philopatry in both sexes, a rare phenomenon in vertebrates. Communal care can be vital, especially among deep-diving species, and can be supported by female kinship. Female-based sociality, in its diverse forms, is therefore a prevailing feature of cetacean societies. Beyond the key role in offspring survival, it provides the substrate for significant vertical and horizontal cultural transmission, as well as the only definitive non-human examples of menopause. This article is part of the theme issue 'The evolution of female-biased kinship in humans and other mammals'.

The reach of gene-culture coevolution in animals.

Culture (behaviour based on socially transmitted information) is present in diverse animal species, yet how it interacts with genetic evolution remains largely unexplored. Here, we review the evidence for gene-culture coevolution in animals, especially birds, cetaceans and primates. We describe how culture can relax or intensify selection under different circumstances, create new selection pressures by changing ecology or behaviour, and favour adaptations, including in other species. Finally, we illustrate how, through culturally mediated migration and assortative mating, culture can shape population genetic structure and diversity. This evidence suggests strongly that animal culture plays an important evolutionary role, and we encourage explicit analyses of gene-culture coevolution in nature.

Kinship influences sperm whale social organization within, but generally not among, social units.

Sperm whales have a multi-level social structure based upon long-term, cooperative social units. What role kinship plays in structuring this society is poorly understood. We combined extensive association data (518 days, during 2005-2016) and genetic data (18 microsatellites and 346 bp mitochondrial DNA (mtDNA) control region sequences) for 65 individuals from 12 social units from the Eastern Caribbean to examine patterns of kinship and social behaviour. Social units were clearly matrilineally based, evidenced by greater relatedness within social units (mean r = 0.14) than between them (mean r = 0.00) and uniform mtDNA haplotypes within social units. Additionally, most individuals (82.5%) had a first-degree relative in their social unit, while we found no first-degree relatives between social units. Generally and within social units, individuals associated more with their closer relatives (matrix correlations: 0.18-0.25). However, excepting a highly related pair of social units that merged over the study period, associations between social units were not correlated with kinship (p > 0.1). These results are the first to robustly demonstrate kinship's contribution to social unit composition and association preferences, though they also reveal variability in association preferences that is unexplained by kinship. Comparisons with other matrilineal species highlight the range of possible matrilineal societies and how they can vary between and even within species.

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.