Climate change introduces threatened killer whale populations and conservation challenges to the Arctic.

The Arctic is the fastest-warming region on the planet, and the lengthening ice-free season is opening Arctic waters to sub-Arctic species such as the killer whale (Orcinus orca). As apex predators, killer whales can cause significant ecosystem-scale changes. Setting conservation priorities for killer whales and their Arctic prey species requires knowledge of their evolutionary history and demographic trajectory. Using whole-genome resequencing of 24 killer whales sampled in the northwest Atlantic, we first explored the population structure and demographic history of Arctic killer whales. To better understand the broader geographic relationship of these Arctic killer whales to other populations, we compared them to a globally sampled dataset. Finally, we assessed threats to Arctic killer whales due to anthropogenic harvest by reviewing the peer-reviewed and gray literature. We found that there are two highly genetically distinct, non-interbreeding populations of killer whales using the eastern Canadian Arctic. These populations appear to be as genetically different from each other as are ecotypes described elsewhere in the killer whale range; however, our data cannot speak to ecological differences between these populations. One population is newly identified as globally genetically distinct, and the second is genetically similar to individuals sampled from Greenland. The effective sizes of both populations recently declined, and both appear vulnerable to inbreeding and reduced adaptive potential. Our survey of human-caused mortalities suggests that harvest poses an ongoing threat to both populations. The dynamic Arctic environment complicates conservation and management efforts, with killer whales adding top-down pressure on Arctic food webs crucial to northern communities' social and economic well-being. While killer whales represent a conservation priority, they also complicate decisions surrounding wildlife conservation and resource management in the Arctic amid the effects of climate change.

Killer whale presence drives bowhead whale selection for sea ice in Arctic seascapes of fear.

The effects of predator intimidation on habitat use and behavior of prey species are rarely quantified for large marine vertebrates over ecologically relevant scales. Using state space movement models followed by a series of step selection functions, we analyzed movement data of concurrently tracked prey, bowhead whales (Balaena mysticetus; n = 7), and predator, killer whales (Orcinus orca; n = 3), in a large (63,000 km2), partially ice-covered gulf in the Canadian Arctic. Our analysis revealed pronounced predator-mediated shifts in prey habitat use and behavior over much larger spatiotemporal scales than previously documented in any marine or terrestrial ecosystem. The striking shift from use of open water (predator-free) to dense sea ice and shorelines (predators present) was exhibited gulf-wide by all tracked bowheads during the entire 3-wk period killer whales were present, constituting a nonconsumptive effect (NCE) with unknown energetic or fitness costs. Sea ice is considered quintessential habitat for bowhead whales, and ice-covered areas have frequently been interpreted as preferred bowhead foraging habitat in analyses that have not assessed predator effects. Given the NCEs of apex predators demonstrated here, however, unbiased assessment of habitat use and distribution of bowhead whales and many marine species may not be possible without explicitly incorporating spatiotemporal distribution of predation risk. The apparent use of sea ice as a predator refuge also has implications for how bowhead whales, and likely other ice-associated Arctic marine mammals, will cope with changes in Arctic sea ice dynamics as historically ice-covered areas become increasingly ice-free during summer.

How evolutionary biology can explain why human and a few marine mammal females are the only ones that are menopausal.

Two fundamental questions related to menopause that have not been answered are: (1) why does menopause even occur? And, (2) of the more than six thousand known mammals extant today, why human and four whale females are the only ones that are menopausal? Answers to both of these basic questions are provided here on the basis of evolutionary biology. From observational data, it was found that there are three elemental criteria that all menopausal species must fulfill: first, it has to be long-lived (average female lifespan of the species has to be forty years or more); second, it must live in groups; and third, the average female-male lifespan differential has to be at least thirty percent or more. In addition, a corollary criterion for menopause was also established: for a species' females to be menopausal, the Encephalization Quotient (EQ) for the species has to be 2.5 or more. Though humans do not fulfill the third menopausal criterion currently, it has been shown that when the menopausal mechanism first became common in human ancestors, in all likelihood, that principle was conformed to. Of the multitude of mammals around, only a few species satisfy all three menopausal criteria, and hence are the only ones whose females undergo the menopausal process. Many hitherto unanswered questions with respect to menopause, such as, while long and short-finned pilot whales are close to each other both genetically and physiologically, why short-finned females are menopausal while long-finned females are not, why orca females are menopausal while elephant females are not, in spite of both being long-lived, etc., can be answered on the basis of those three criteria. Why there was no selection pressure for males to undergo advanced-age reproductive cessation in those few menopausal species and why the majority of divorces occur in mid-life (40-to-60s) are also explained from a menopausal perspective.

Role of sociality in the response of killer whales to an additive mortality event.

In highly social top predators, group living is an ecological strategy that enhances individual fitness, primarily through increased foraging success. Additive mortality events across multiple social groups in populations may affect the social structure, and therefore the fitness, of surviving individuals. This hypothesis was examined in a killer whale (Orcinus orca) population that experienced a 7-y period of severe additive mortality due to lethal interactions with illegal fishing vessels. Using both social and demographic analyses conducted on a unique long-term dataset encompassing periods before, during, and after this event, results indicated a decrease in both the number and the mean strength of associations of surviving individuals during the additive mortality period. A positive significant correlation between association strength and apparent survival suggested that the fitness of surviving individuals was impacted by the additive mortality event. After this event, individuals responded to the loss of relatives in their social groups by associating with a greater number of other social groups, likely to maintain a functional group size that maximized their foraging success. However, these associations were loose; individuals did not reassociate in highly stable social groups, and their survival remained low years after the mortality event. These findings demonstrate how the disruption of social structure in killer whales may lead to prolonged negative effects of demographic stress beyond an additive mortality event. More importantly, this study shows that sociality has a key role in the resilience of populations to human-induced mortality; this has major implications for the conservation of highly social and long-lived species.

Sustained disruption of narwhal habitat use and behavior in the presence of Arctic killer whales.

Although predators influence behavior of prey, analyses of electronic tracking data in marine environments rarely consider how predators affect the behavior of tracked animals. We collected an unprecedented dataset by synchronously tracking predator (killer whales, [Formula: see text] = 1; representing a family group) and prey (narwhal, [Formula: see text] = 7) via satellite telemetry in Admiralty Inlet, a large fjord in the Eastern Canadian Arctic. Analyzing the movement data with a switching-state space model and a series of mixed effects models, we show that the presence of killer whales strongly alters the behavior and distribution of narwhal. When killer whales were present (within about 100 km), narwhal moved closer to shore, where they were presumably less vulnerable. Under predation threat, narwhal movement patterns were more likely to be transiting, whereas in the absence of threat, more likely resident. Effects extended beyond discrete predatory events and persisted steadily for 10 d, the duration that killer whales remained in Admiralty Inlet. Our findings have two key consequences. First, given current reductions in sea ice and increases in Arctic killer whale sightings, killer whales have the potential to reshape Arctic marine mammal distributions and behavior. Second and of more general importance, predators have the potential to strongly affect movement behavior of tracked marine animals. Understanding predator effects may be as or more important than relating movement behavior to resource distribution or bottom-up drivers traditionally included in analyses of marine animal tracking data.

Kinematic signatures of prey capture from archival tags reveal sex differences in killer whale foraging activity.

Studies of odontocete foraging ecology have been limited by the challenges of observing prey capture events and outcomes underwater. We sought to determine whether subsurface movement behavior recorded from archival tags could accurately identify foraging events by fish-eating killer whales. We used multisensor bio-logging tags attached by suction cups to Southern Resident killer whales (Orcinus orca) to: (1) identify a stereotyped movement signature that co-occurred with visually confirmed prey capture dives; (2) construct a prey capture dive detector and validate it against acoustically confirmed prey capture dives; and (3) demonstrate the utility of the detector by testing hypotheses about foraging ecology. Predation events were significantly predicted by peaks in the rate of change of acceleration ('jerk peak'), roll angle and heading variance. Detection of prey capture dives by movement signatures enabled substantially more dives to be included in subsequent analyses compared with previous surface or acoustic detection methods. Males made significantly more prey capture dives than females and more dives to the depth of their preferred prey, Chinook salmon. Additionally, only half of the tag deployments on females (5 out of 10) included a prey capture dive, whereas all tag deployments on males exhibited at least one prey capture dive (12 out of 12). This dual approach of kinematic detection of prey capture coupled with hypothesis testing can be applied across odontocetes and other marine predators to investigate the impacts of social, environmental and anthropogenic factors on foraging ecology.

Acoustic crypsis in southern right whale mother-calf pairs: infrequent, low-output calls to avoid predation?

Southern right whales (Eubalaena australis) invest substantial amounts of energy in their calves, while facing the risk of having them predated upon by eavesdropping killer whales (Orcinus orca). We tested the hypothesis that southern right whale mother-calf pairs employ acoustic crypsis to reduce acoustic detectability by such predators. Specifically, we deployed multi-sensor DTAGs on nine lactating whales for a total of 62.9 h in a Western Australian breeding ground, and used a SoundTrap to estimate the concomitant acoustic background noise. Vocalisations were recorded at low rates of <10 calls h-1 (1 call per dive) and at low received levels between 123±8 and 134±10 dB re. 1 µPa RMS depending on call type. We conclude that such acoustic crypsis in southern right whales and other baleen whales decreases the risk of alerting potential predators and hence jeopardizing a substantial energetic investment by the mother.

The evolution of the human menopause.

The females of most species die soon after ceasing to reproduce, their purpose in life being to ensure survival of their kin. Human females may live more than one-third of their lives after they cease to reproduce, a property shared by few species, one of which is Orca whales. Orcas have been extensively studied because families live together in stable units or pods and individual whales have distinctive markings, enabling them to be identified. The females survive long after the menopause, one possible reason for this being that the older females provide a survival advantage since they are seen to lead the pods more often than younger females or males, thus providing a survival advantage in times of food shortage. The female lifespan is increasing in most countries worldwide, principally due to decreased infection and maternal mortality. Women are now more active through middle and into older age. Whatever sort of life they wish to lead, women need to be as fit as possible to facilitate healthy aging. Chronic diseases that affect millions of women are cardiovascular disease, osteoporosis, cancer, and dementia. The incidence of all these is increased by obesity, the prevention of which is a major challenge in our society. Hormone therapy may have a place for some women but for many others taking control of their health by lifestyle intervention is a major contributor to disease prevention. It is our duty as doctors to encourage this at every opportunity to help all women live a fruitful and healthy old age.

Automated localization of whales in coastal fjords.

Localization and tracking of vocalizing marine mammals are powerful tools for understanding and mitigating the impacts of anthropogenic stressors such as vessel noise on habitat use of cetaceans. A large-aperture hydrophone network has been installed in the Kitimat Fjord System, an ecologically, culturally, and economically valued marine environment in northern British Columbia, Canada. This network consists of four synchronized bottom-mounted hydrophones that permanently record and radio-transmit data to a land-based laboratory. An automated system has been developed which includes routines to localize transient bio-acoustic signals from three or more streaming hydrophones in near real-time. These routines comprise the correlation of hydrophone signals, the construction of a time lag model, and signal localization and error estimation from a spatial likelihood surface. The localization method was tested experimentally and subsequently applied to vocalizations from humpback whales, fin whales, and killer whales. Refractive and reflective sound propagation effects in the confined fjords are assessed using ray tracing propagation models. Automated localization results are compared to ground-truth data and shown to provide good accuracy.

Aquatic animal colors and skin temperature: Biology's selection for reducing oceanic dolphin's skin friction drag.

There is currently a growing interest in the area of drag reduction. In this work, the thermal effects of body color of some species of aquatics like Orcas and Dusky dolphins are investigated with respect to their swimming routes and geometric and behavioral characteristics. Considering the marine and atmospheric characteristics of these aquatics' routes, a thermal analysis is performed. The surrounding fluxes including the water flux, sun irradiation, and core temperature are considered in an energy balance to determine the skin temperature of the top side of the animal/organism's body. To study the effects of color on the surface temperature of the aquatic species, an experiment is carried out in the water on a flat plate with black and white color. Applying a turbulent analytical solution for heated boundary layers, it will be shown that the black color on the top of the bodies of these marine organisms is very efficient in terms of skin drag reduction. Moreover, to investigate the effects of the temperature on underwater skin friction drag reduction, the turbulent flow is simulated around a flat plate and a 2- dimensional modeled Killer whale at different temperatures. The results show that the top black body color of Orca and Dusky dolphin decreases their skin friction drag by 7%. This study will also provide the reason for this evolution of color scheme of other extremely fast marine animals, such as billfish, whales, and sharks. This method of drag reduction can be considered as one of the effective factors in skin drag reduction of underwater robots.

Social interaction analysis in captive orcas (Orcinus orca).

The management of socially complex species in captivity is challenging. Research on their social behavior improves our understanding of interactions in captive animals and captive-group management. We conducted a detailed analysis of social relationships shown by the orcas kept at Loro Parque zoo and their tendency to reconcile after aggressive episodes. Affiliative interactions were the most frequent social activities compared to agonistic or sexual interactions. Within affiliative behaviors, we documented the pattern "gentle tongue bite", where an animal touches the other's tongue with his teeth but does not bite it. Affiliative interactions between a specific pair of orcas occurred significantly more often than expected by chance, and together with low levels of agonistic interactions, indicated particular affinity between some individuals. The most frequently observed low-level agonistic relationship was that of the two older males (Tekoa-Keto); however, they also showed frequent sexual and affiliative interactions. Sexual-like behaviors (pursuit, mount, and penis between males) were found in both sexes. Finally, the observed corrected conciliatory tendency (31.57%) was within the range described for other primate and cetacean species. This study provides a systematic way to assess social interactions as well as conflict management strategies in cetaceans housed in zoos and zoo-like facilities and may help to improve animal welfare and management of animals in controlled environments.

Imitation of novel conspecific and human speech sounds in the killer whale (Orcinus orca).

Vocal imitation is a hallmark of human spoken language, which, along with other advanced cognitive skills, has fuelled the evolution of human culture. Comparative evidence has revealed that although the ability to copy sounds from conspecifics is mostly uniquely human among primates, a few distantly related taxa of birds and mammals have also independently evolved this capacity. Remarkably, field observations of killer whales have documented the existence of group-differentiated vocal dialects that are often referred to as traditions or cultures and are hypothesized to be acquired non-genetically. Here we use a do-as-I-do paradigm to study the abilities of a killer whale to imitate novel sounds uttered by conspecific (vocal imitative learning) and human models (vocal mimicry). We found that the subject made recognizable copies of all familiar and novel conspecific and human sounds tested and did so relatively quickly (most during the first 10 trials and three in the first attempt). Our results lend support to the hypothesis that the vocal variants observed in natural populations of this species can be socially learned by imitation. The capacity for vocal imitation shown in this study may scaffold the natural vocal traditions of killer whales in the wild.

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.

Mortality risk and social network position in resident killer whales: sex differences and the importance of resource abundance.

An individual's ecological environment affects their mortality risk, which in turn has fundamental consequences for life-history evolution. In many species, social relationships are likely to be an important component of an individual's environment, and therefore their mortality risk. Here, we examine the relationship between social position and mortality risk in resident killer whales (Orcinus orca) using over three decades of social and demographic data. We find that the social position of male, but not female, killer whales in their social unit predicts their mortality risk. More socially integrated males have a significantly lower risk of mortality than socially peripheral males, particularly in years of low prey abundance, suggesting that social position mediates access to resources. Male killer whales are larger and require more resources than females, increasing their vulnerability to starvation in years of low salmon abundance. More socially integrated males are likely to have better access to social information and food-sharing opportunities which may enhance their survival in years of low salmon abundance. Our results show that observable variation in the social environment is linked to variation in mortality risk, and highlight how sex differences in social effects on survival may be linked to sex differences in life-history evolution.

Swimming and diving energetics in dolphins: a stroke-by-stroke analysis for predicting the cost of flight responses in wild odontocetes.

Exponential increases in hydrodynamic drag and physical exertion occur when swimmers move quickly through water, and underlie the preference for relatively slow routine speeds by marine mammals regardless of body size. Because of this and the need to balance limited oxygen stores when submerged, flight (escape) responses may be especially challenging for this group. To examine this, we used open-flow respirometry to measure the energetic cost of producing a swimming stroke during different levels of exercise in bottlenose dolphins (Tursiops truncatus). These data were then used to model the energetic cost of high-speed escape responses by other odontocetes ranging in mass from 42 to 2738 kg. The total cost per stroke during routine swimming by dolphins, 3.31±0.20 J kg-1 stroke-1, was doubled during maximal aerobic performance. A comparative analysis of locomotor costs (LC; in J kg-1 stroke-1), representing the cost of moving the flukes, revealed that LC during routine swimming increased with body mass (M) for odontocetes according to LC=1.46±0.0005M; a separate relationship described LC during high-speed stroking. Using these relationships, we found that continuous stroking coupled with reduced glide time in response to oceanic noise resulted in a 30.5% increase in metabolic rate in the beaked whale, a deep-diving odontocete considered especially sensitive to disturbance. By integrating energetics with swimming behavior and dive characteristics, this study demonstrates the physiological consequences of oceanic noise on diving mammals, and provides a powerful tool for predicting the biological significance of escape responses by cetaceans facing anthropogenic disturbances.

Killer whale (Orcinus orca) behavioral audiograms.

Killer whales (Orcinus orca) are one of the most cosmopolitan marine mammal species with potential widespread exposure to anthropogenic noise impacts. Previous audiometric data on this species were from two adult females [Szymanski, Bain, Kiehl, Pennington, Wong, and Henry (1999). J. Acoust. Soc. Am. 108, 1322-1326] and one sub-adult male [Hall and Johnson (1972). J. Acoust. Soc. Am. 51, 515-517] with apparent high-frequency hearing loss. All three killer whales had best sensitivity between 15 and 20 kHz, with thresholds lower than any odontocete tested to date, suggesting this species might be particularly sensitive to acoustic disturbance. The current study reports the behavioral audiograms of eight killer whales at two different facilities. Hearing sensitivity was measured from 100 Hz to 160 kHz in killer whales ranging in age from 12 to 52 year. Previously measured low thresholds at 20 kHz were not replicated in any individual. Hearing in the killer whales was generally similar to other delphinids, with lowest threshold (49 dB re 1 µPa) at approximately 34 kHz, good hearing (i.e., within 20 dB of best sensitivity) from 5 to 81 kHz, and low- and high-frequency hearing cutoffs (>100 dB re µPa) of 600 Hz and 114 kHz, respectively.

Oil Spills and Marine Mammals in British Columbia, Canada: Development and Application of a Risk-Based Conceptual Framework.

Marine mammals are inherently vulnerable to oil spills. We developed a conceptual framework to evaluate the impacts of potential oil exposure on marine mammals and applied it to 21 species inhabiting coastal British Columbia (BC), Canada. Oil spill vulnerability was determined by examining both the likelihood of species-specific (individual) oil exposure and the consequent likelihood of population-level effects. Oil exposure pathways, ecology, and physiological characteristics were first used to assign species-specific vulnerability rankings. Baleen whales were found to be highly vulnerable due to blowhole breathing, surface filter feeding, and invertebrate prey. Sea otters (Enhydra lutris) were ranked as highly vulnerable due to their time spent at the ocean surface, dense pelage, and benthic feeding techniques. Species-specific vulnerabilities were considered to estimate the likelihood of population-level effects occurring after oil exposure. Killer whale (Orcinus orca) populations were deemed at highest risk due to small population sizes, complex social structure, long lives, slow reproductive turnover, and dietary specialization. Finally, we related the species-specific and population-level vulnerabilities. In BC, vulnerability was deemed highest for Northern and Southern Resident killer whales and sea otters, followed by Bigg's killer whales and Steller sea lions (Eumetopias jubatus). Our findings challenge the typical "indicator species" approach routinely used and underscore the need to examine marine mammals at a species and population level for risk-based oil spill predictions. This conceptual framework can be combined with spill probabilities and volumes to develop more robust risk assessments and may be applied elsewhere to identify vulnerability themes for marine mammals.

Development of sociality and emergence of independence in a killer whale (Orcinus orca) calf from birth to 36 months.

Dolphin calves spend most of their time swimming with their mother immediately after birth. As they mature, the calves become increasingly independent, and begin to interact more often with other calves, juveniles, and sub-adults. For bottlenose dolphin calves, sociality is related to maternal behaviors. Unfortunately, much less is known about the development of sociality and emergence of independence for killer whale calves. The purpose of this study was to examine the developmental changes in social behaviors and solitary activities of a killer whale calf across a 36-month period. Focal follow video recordings of a mother-calf pair housed at SeaWorld San Antonio were collected 2-6 times a day for 5-15 min at 6-month intervals. Using a sample of randomly selected video recordings at each month, developmental changes in swims and social interactions with her mother, swims and social interactions with non-maternal partners, and solitary activities (e.g., solitary swims, solitary play) were observed across the months. The calf spent most of her time swimming with the mother across the 36-month period. The time the calf socialized with her mother was greater than the time she socialized with others at each month. Besides her mother, the calf socialized more often with the other adult female compared to adult males. As the calf matured, the increase in the time she spent socializing with adult killer whales other than the mother corresponded with an increase in the rate and time spent in solitary play. The developmental trends of sociality and emerging independence replicate research conducted with calves of other dolphin species. Zoo Biol. 36:11-20, 2017. © 2016 Wiley Periodicals, Inc.