Temporal dynamics of mother-offspring relationships in Bigg's killer whales: opportunities for kin-directed help by post-reproductive females.

Age-related changes in the patterns of local relatedness (kinship dynamics) can be a significant selective force shaping the evolution of life history and social behaviour. In humans and some species of toothed whales, average female relatedness increases with age, which can select for a prolonged post-reproductive lifespan in older females due to both costs of reproductive conflict and benefits of late-life helping of kin. Killer whales (Orcinus orca) provide a valuable system for exploring social dynamics related to such costs and benefits in a mammal with an extended post-reproductive female lifespan. We use more than 40 years of demographic and association data on the mammal-eating Bigg's killer whale to quantify how mother-offspring social relationships change with offspring age and identify opportunities for late-life helping and the potential for an intergenerational reproductive conflict. Our results suggest a high degree of male philopatry and female-biased budding dispersal in Bigg's killer whales, with some variability in the dispersal rate for both sexes. These patterns of dispersal provide opportunities for late-life helping particularly between mothers and their adult sons, while partly mitigating the costs of mother-daughter reproductive conflict. Our results provide an important step towards understanding why and how menopause has evolved in Bigg's killer whales.

A collaborative and near-comprehensive North Pacific humpback whale photo-ID dataset.

We present an ocean-basin-scale dataset that includes tail fluke photographic identification (photo-ID) and encounter data for most living individual humpback whales (Megaptera novaeangliae) in the North Pacific Ocean. The dataset was built through a broad collaboration combining 39 separate curated photo-ID catalogs, supplemented with community science data. Data from throughout the North Pacific were aggregated into 13 regions, including six breeding regions, six feeding regions, and one migratory corridor. All images were compared with minimal pre-processing using a recently developed image recognition algorithm based on machine learning through artificial intelligence; this system is capable of rapidly detecting matches between individuals with an estimated 97-99% accuracy. For the 2001-2021 study period, a total of 27,956 unique individuals were documented in 157,350 encounters. Each individual was encountered, on average, in 5.6 sampling periods (i.e., breeding and feeding seasons), with an annual average of 87% of whales encountered in more than one season. The combined dataset and image recognition tool represents a living and accessible resource for collaborative, basin-wide studies of a keystone marine mammal in a time of rapid ecological change.

Behavioral context of echolocation and prey-handling sounds produced by killer whales (Orcinus orca) during pursuit and capture of Pacific salmon (Oncorhynchus spp.).

Availability of preferred salmonid prey and a sufficiently quiet acoustic environment in which to forage are critical to the survival of resident killer whales (Orcinus orca) in the northeastern Pacific. Although piscivorous killer whales rely on echolocation to locate and track prey, the relationship between echolocation, movement, and prey capture during foraging by wild individuals is poorly understood. We used acoustic biologging tags to relate echolocation behavior to prey pursuit and capture during successful feeding dives by fish-eating killer whales in coastal British Columbia, Canada. The significantly higher incidence and rate of echolocation prior to fish captures compared to afterward confirms its importance in prey detection and tracking. Extremely rapid click sequences (buzzes) were produced before or concurrent with captures of salmon at depths typically exceeding 50 m, and were likely used by killer whales for close-range prey targeting, as in other odontocetes. Distinctive crunching and tearing sounds indicative of prey-handling behavior occurred at relatively shallow depths following fish captures, matching concurrent observations that whales surfaced with fish prior to consumption and often shared prey. Buzzes and prey-handling sounds are potentially useful acoustic signals for estimating foraging efficiency and determining if resident killer whales are meeting their energetic requirements.

Epizootiology of a Cryptococcus gattii outbreak in porpoises and dolphins from the Salish Sea.

Cryptococcus gattii is a fungal pathogen that primarily affects the respiratory and nervous systems of humans and other animals. C. gattii emerged in temperate North America in 1999 as a multispecies outbreak of cryptococcosis in British Columbia (Canada) and Washington State and Oregon (USA), affecting humans, domestic animals, and wildlife. Here we describe the C. gattii epizootic in odontocetes. Cases of C. gattii were identified in 42 odontocetes in Washington and British Columbia between 1997 and 2016. Species affected included harbor porpoises Phocoena phocoena (n = 26), Dall's porpoises Phocoenoides dalli (n = 14), and Pacific white-sided dolphins Lagenorhynchus obliquidens (n = 2). The probable index case was identified in an adult male Dall's porpoise in 1997, 2 yr prior to the initial terrestrial outbreak. The spatiotemporal extent of the C. gattii epizootic was defined, and cases in odontocetes were found to be clustered around terrestrial C. gattii hotspots. Case-control analyses with stranded, uninfected odontocetes revealed that risk factors for infection were species (Dall's porpoises), age class (adult animals), and season (winter). This study suggests that mycoses are an emerging source of mortality for odontocetes, and that outbreaks may be associated with anthropogenic environmental disturbance.

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.

Pathology findings and correlation with body condition index in stranded killer whales (Orcinus orca) in the northeastern Pacific and Hawaii from 2004 to 2013.

Understanding health and mortality in killer whales (Orcinus orca) is crucial for management and conservation actions. We reviewed pathology reports from 53 animals that stranded in the eastern Pacific Ocean and Hawaii between 2004 and 2013 and used data from 35 animals that stranded from 2001 to 2017 to assess association with morphometrics, blubber thickness, body condition and cause of death. Of the 53 cases, cause of death was determined for 22 (42%) and nine additional animals demonstrated findings of significant importance for population health. Causes of calf mortalities included infectious disease, nutritional, and congenital malformations. Mortalities in sub-adults were due to trauma, malnutrition, and infectious disease and in adults due to bacterial infections, emaciation and blunt force trauma. Death related to human interaction was found in every age class. Important incidental findings included concurrent sarcocystosis and toxoplasmosis, uterine leiomyoma, vertebral periosteal proliferations, cookiecutter shark (Isistius sp.) bite wounds, excessive tooth wear and an ingested fish hook. Blubber thickness increased significantly with body length (all p < 0.001). In contrast, there was no relationship between body length and an index of body condition (BCI). BCI was higher in animals that died from trauma. This study establishes a baseline for understanding health, nutritional status and causes of mortality in stranded killer whales. Given the evidence of direct human interactions on all age classes, in order to be most successful recovery efforts should address the threat of human interactions, especially for small endangered groups of killer whales that occur in close proximity to large human populations, interact with recreational and commercial fishers and transit established shipping lanes.

Postreproductive killer whale grandmothers improve the survival of their grandoffspring.

Understanding why females of some mammalian species cease ovulation prior to the end of life is a long-standing interdisciplinary and evolutionary challenge. In humans and some species of toothed whales, females can live for decades after stopping reproduction. This unusual life history trait is thought to have evolved, in part, due to the inclusive fitness benefits that postreproductive females gain by helping kin. In humans, grandmothers gain inclusive fitness benefits by increasing their number of surviving grandoffspring, referred to as the grandmother effect. Among toothed whales, the grandmother effect has not been rigorously tested. Here, we test for the grandmother effect in killer whales, by quantifying grandoffspring survival with living or recently deceased reproductive and postreproductive grandmothers, and show that postreproductive grandmothers provide significant survival benefits to their grandoffspring above that provided by reproductive grandmothers. This provides evidence of the grandmother effect in a nonhuman menopausal species. By stopping reproduction, grandmothers avoid reproductive conflict with their daughters, and offer increased benefits to their grandoffspring. The benefits postreproductive grandmothers provide to their grandoffspring are shown to be most important in difficult times where the salmon abundance is low to moderate. The postreproductive grandmother effect we report, together with the known costs of late-life reproduction in killer whales, can help explain the long postreproductive life spans of resident killer whales.

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.

Infanticide in a mammal-eating killer whale population.

Infanticide can be an extreme result of sexual conflict that drives selection in species in which it occurs. It is a rarely observed behaviour but some evidence for its occurrence in cetaceans exists in three species of dolphin. Here we describe observations of an adult male killer whale (Orcinus orca) and his post-reproductive mother killing a neonate belonging to an unrelated female from the same population in the North Pacific. This is the first account of infanticide reported in killer whales and the only case committed jointly by an adult male and his mother outside of humans. Consistent with findings in other social mammals, we suggest that infanticide is a sexually selected behaviour in killer whales that could provide subsequent mating opportunities for the infanticidal male and thereby provide inclusive fitness benefits for his mother.

Fine-scale foraging movements by fish-eating killer whales (Orcinus orca) relate to the vertical distributions and escape responses of salmonid prey (Oncorhynchus spp.).

BACKGROUND: We sought to quantitatively describe the fine-scale foraging behavior of northern resident killer whales (Orcinus orca), a population of fish-eating killer whales that feeds almost exclusively on Pacific salmon (Oncorhynchus spp.). To reconstruct the underwater movements of these specialist predators, we deployed 34 biologging Dtags on 32 individuals and collected high-resolution, three-dimensional accelerometry and acoustic data. We used the resulting dive paths to compare killer whale foraging behavior to the distributions of different salmonid prey species. Understanding the foraging movements of these threatened predators is important from a conservation standpoint, since prey availability has been identified as a limiting factor in their population dynamics and recovery. RESULTS: Three-dimensional dive tracks indicated that foraging (N = 701) and non-foraging dives (N = 10,618) were kinematically distinct (Wilks' lambda: λ16 = 0.321, P < 0.001). While foraging, killer whales dove deeper, remained submerged longer, swam faster, increased their dive path tortuosity, and rolled their bodies to a greater extent than during other activities. Maximum foraging dive depths reflected the deeper vertical distribution of Chinook (compared to other salmonids) and the tendency of Pacific salmon to evade predators by diving steeply. Kinematic characteristics of prey pursuit by resident killer whales also revealed several other escape strategies employed by salmon attempting to avoid predation, including increased swimming speeds and evasive maneuvering. CONCLUSIONS: High-resolution dive tracks reconstructed using data collected by multi-sensor accelerometer tags found that movements by resident killer whales relate significantly to the vertical distributions and escape responses of their primary prey, Pacific salmon.

Reproductive Conflict and the Evolution of Menopause in Killer Whales.

Why females of some species cease ovulation prior to the end of their natural lifespan is a long-standing evolutionary puzzle [1-4]. The fitness benefits of post-reproductive helping could in principle select for menopause [1, 2, 5], but the magnitude of these benefits appears insufficient to explain the timing of menopause [6-8]. Recent theory suggests that the cost of inter-generational reproductive conflict between younger and older females of the same social unit is a critical missing term in classical inclusive fitness calculations (the "reproductive conflict hypothesis" [6, 9]). Using a unique long-term dataset on wild resident killer whales, where females can live decades after their final parturition, we provide the first test of this hypothesis in a non-human animal. First, we confirm previous theoretical predictions that local relatedness increases with female age up to the end of reproduction. Second, we construct a new evolutionary model and show that given these kinship dynamics, selection will favor younger females that invest more in competition, and thus have greater reproductive success, than older females (their mothers) when breeding at the same time. Third, we test this prediction using 43 years of individual-based demographic data in resident killer whales and show that when mothers and daughters co-breed, the mortality hazard of calves from older-generation females is 1.7 times that of calves from younger-generation females. Intergenerational conflict combined with the known benefits conveyed to kin by post-reproductive females can explain why killer whales have evolved the longest post-reproductive lifespan of all non-human animals.

Causes of mortality of harbor porpoises Phocoena phocoena along the Atlantic and Pacific coasts of Canada.

There is increasing public interest in the overall health of the marine environment. Harbor porpoises Phocoena phocoena have a coastal distribution, and stranded animals function as sentinels for population and ecosystem health. The goal of this retrospective study was to join datasets from the western Atlantic and eastern Pacific coasts of Canada to investigate causes of morbidity and mortality in this species. A total of 241 necropsy records were reviewed including 147 (61%) from the Pacific region and 94 (39%) from the Atlantic region from 1988 to 2011. A cause of death could be determined with confidence in 118 (49%) of these cases. Of these 118 cases, the leading cause of mortality for both regions, together and separately, was infectious disease. In the Pacific region, this was followed by traumatic and anthropogenic causes, whereas in the Atlantic region, it was followed by emaciation/starvation, mortality of dependent calves, and anthropogenic causes. Pathogens of potential zoonotic significance or indicative of environmental contamination, e.g. Salmonella sp. and Cryptococcus gattii, were identified. Numerous parasitic species were observed within the lungs, liver, stomach, middle ear, and subcutaneous tissues, although they were usually interpreted as incidental findings. Anthropogenic causes may be underrepresented as they are notoriously difficult to diagnose with certainty, thereby making up a proportion of the 'unknown causes of death' (51%) category. Improved standardization of data collection and documentation is required to better understand harbor porpoise and ecosystem health.

Physical constraints of cultural evolution of dialects in killer whales.

Odontocete sounds are produced by two pairs of phonic lips situated in soft nares below the blowhole; the right pair is larger and is more likely to produce clicks, while the left pair is more likely to produce whistles. This has important implications for the cultural evolution of delphinid sounds: the greater the physical constraints, the greater the probability of random convergence. In this paper the authors examine the call structure of eight killer whale populations to identify structural constraints and to determine if they are consistent among all populations. Constraints were especially pronounced in two-voiced calls. In the calls of all eight populations, the lower component of two-voiced (biphonic) calls was typically centered below 4 kHz, while the upper component was typically above that value. The lower component of two-voiced calls had a narrower frequency range than single-voiced calls in all populations. This may be because some single-voiced calls are homologous to the lower component, while others are homologous to the higher component of two-voiced calls. Physical constraints on the call structure reduce the possible variation and increase the probability of random convergence, producing similar calls in different populations.

Killer whale call frequency is similar across the oceans, but varies across sympatric ecotypes.

Killer whale populations may differ in genetics, morphology, ecology, and behavior. In the North Pacific, two sympatric populations ("resident" and "transient") specialize on different prey (fish and marine mammals) and retain reproductive isolation. In the eastern North Atlantic, whales from the same populations have been observed feeding on both fish and marine mammals. Fish-eating North Pacific "residents" are more genetically related to eastern North Atlantic killer whales than to sympatric mammal-eating "transients." In this paper, a comparison of frequency variables in killer whale calls recorded from four North Pacific resident, two North Pacific transient, and two eastern North Atlantic populations is reported to assess which factors drive the large-scale changes in call structure. Both low-frequency and high-frequency components of North Pacific transient killer whale calls have significantly lower frequencies than those of the North Pacific resident and North Atlantic populations. The difference in frequencies could be related to ecological specialization or to the phylogenetic history of these populations. North Pacific transient killer whales may have genetically inherited predisposition toward lower frequencies that may shape their learned repertoires.

Ultrasonic whistles of killer whales (Orcinus orca) recorded in the North Pacific (L).

Ultrasonic whistles were previously found in North Atlantic killer whales and were suggested to occur in eastern North Pacific killer whales based on the data from autonomous recorders. In this study ultrasonic whistles were found in the recordings from two encounters with the eastern North Pacific offshore ecotype killer whales and one encounter with the western North Pacific killer whales of unknown ecotype. All ultrasonic whistles were highly stereotyped and all but two had downsweep contours. These results demonstrate that specific sound categories can be shared by killer whales from different ocean basins.

Habitat-based PCB environmental quality criteria for the protection of endangered killer whales (Orcinus orca).

The development of an area-based polychlorinated biphenyl (PCB) food-web bioaccumulation model enabled a critical evaluation of the efficacy of sediment quality criteria and prey tissue residue guidelines in protecting fish-eating resident killer whales of British Columbia and adjacent waters. Model-predicted and observed PCB concentrations in resident killer whales and Chinook salmon were in good agreement, supporting the model's application for risk assessment and criteria development. Model application shows that PCB concentrations in the sediments from the resident killer whale's Critical Habitats and entire foraging range leads to PCB concentrations in most killer whales that exceed PCB toxicity threshold concentrations reported for marine mammals. Results further indicate that current PCB sediment quality and prey tissue residue criteria for fish-eating wildlife are not protective of killer whales and are not appropriate for assessing risks of PCB-contaminated sediments to high trophic level biota. We present a novel methodology for deriving sediment quality criteria and tissue residue guidelines that protect biota of high trophic levels under various PCB management scenarios. PCB concentrations in sediments and in prey that are deemed protective of resident killer whale health are much lower than current criteria values, underscoring the extreme vulnerability of high trophic level marine mammals to persistent and bioaccumulative contaminants.

Adaptive prolonged postreproductive life span in killer whales.

Prolonged life after reproduction is difficult to explain evolutionarily unless it arises as a physiological side effect of increased longevity or it benefits related individuals (i.e., increases inclusive fitness). There is little evidence that postreproductive life spans are adaptive in nonhuman animals. By using multigenerational records for two killer whale (Orcinus orca) populations in which females can live for decades after their final parturition, we show that postreproductive mothers increase the survival of offspring, particularly their older male offspring. This finding may explain why female killer whales have evolved the longest postreproductive life span of all nonhuman animals.

PCB-associated changes in mRNA expression in killer whales (Orcinus orca) from the NE Pacific Ocean.

Killer whales in the NE Pacific Ocean are among the world's most PCB-contaminated marine mammals, raising concerns about implications for their health. Sixteen health-related killer whale mRNA transcripts were analyzed in blubber biopsies collected from 35 free-ranging killer whales in British Columbia using real-time quantitative polymerase chain reaction. We observed PCB-related increases in the expression of five gene targets, including the aryl hydrocarbon receptor (AhR; r(2) = 0.83; p < 0.001), thyroid hormone α receptor (TRα; r(2) = 0.64; p < 0.001), estrogen α receptor (ERα; r(2) = 0.70; p < 0.001), interleukin 10 (IL-10; r(2) = 0.74 and 0.68, males and females, respectively; p < 0.001), and metallothionein 1 (MT1; r(2) = 0.58; p < 0.001). Best-fit models indicated that population (dietary preference), age, and sex were not confounding factors, except for IL-10, where males differed from females. While the population-level consequences are unclear, the PCB-associated alterations in mRNA abundance of such pivotal end points provide compelling evidence of adverse physiological effects of persistent environmental contaminants in these endangered killer whales.