Quantitative fatty acid signature analysis reveals a high level of dietary specialization in killer whales across the North Atlantic.

Quantifying the diet composition of apex marine predators such as killer whales (Orcinus orca) is critical to assessing their food web impacts. Yet, with few exceptions, the feeding ecology of these apex predators remains poorly understood. Here, we use our newly validated quantitative fatty acid signature analysis (QFASA) approach on nearly 200 killer whales and over 900 potential prey to model their diets across the 5000 km span of the North Atlantic. Diet estimates show that killer whales mainly consume other whales in the western North Atlantic (Canadian Arctic, Eastern Canada), seals in the mid-North Atlantic (Greenland), and fish in the eastern North Atlantic (Iceland, Faroe Islands, Norway). Nonetheless, diet estimates also varied widely among individuals within most regions. This level of inter-individual feeding variation should be considered for future ecological studies focusing on killer whales in the North Atlantic and other oceans. These estimates reveal remarkable population- and individual-level variation in the trophic ecology of these killer whales, which can help to assess how their predation impacts community and ecosystem dynamics in changing North Atlantic marine ecosystems. This new approach provides researchers with an invaluable tool to study the feeding ecology of oceanic top predators.

Connaître en détails la composition du régime alimentaire des grands prédateurs marins tels que les orques (Orcinus orca) est primordial afin d'évaluer leurs impacts sur les écosystèmes. Pourtant, à quelques exceptions près, l'écologie alimentaire de ces super-prédateurs reste mal comprise. Ici, nous utilisons notre nouvelle approche d'analyse quantitative des signatures d'acides gras (QFASA) sur près de 200 orques et plus de 900 proies potentielles pour modéliser leur régime alimentaire à travers l'Atlantique Nord. Les estimations de leurs régimes alimentaires montrent que les orques consomment principalement d'autres baleines dans l'ouest de l'Atlantique Nord (Arctique canadien, Est du Canada), des phoques dans le milieu de l'Atlantique Nord (Groenland) et des poissons dans l'est de l'Atlantique Nord (Islande, îles Féroé, Norvège). Néanmoins, ces estimations varient considérablement d'un individu à l'autre dans la plupart des régions. Cette variation alimentaire importante entre les individus doit être prise en compte dans les futures études écologiques qui s'intéressent aux orques de l'Atlantique Nord et d'ailleurs. Ces estimations révèlent des variations remarquables dans l'écologie trophique des orques tant au niveau des population que de l'individu, ce qui peut aider à évaluer l'impact de leur prédation sur la dynamique des communautés et des écosystèmes dans un contexte de changements climatiques en l'Atlantique Nord. Cette nouvelle approche fournit aux chercheurs un outil inestimable pour étudier l'écologie alimentaire des super-prédateurs océaniques.

Varying Diet Composition Causes Striking Differences in Legacy and Emerging Contaminant Concentrations in Killer Whales across the North Atlantic.

Lipophilic persistent organic pollutants (POPs) tend to biomagnify in food chains, resulting in higher concentrations in species such as killer whales (Orcinus orca) feeding on marine mammals compared to those consuming fish. Advancements in dietary studies include the use of quantitative fatty acid signature analysis (QFASA) and differentiation of feeding habits within and between populations of North Atlantic (NA) killer whales. This comprehensive study assessed the concentrations of legacy and emerging POPs in 162 killer whales from across the NA. We report significantly higher mean levels of polychlorinated biphenyls (PCBs), organochlorine pesticides, and flame retardants in Western NA killer whales compared to those of Eastern NA conspecifics. Mean ∑PCBs ranged from ∼100 mg/kg lipid weight (lw) in the Western NA (Canadian Arctic, Eastern Canada) to ∼50 mg/kg lw in the mid-NA (Greenland, Iceland) to ∼10 mg/kg lw in the Eastern NA (Norway, Faroe Islands). The observed variations in contaminant levels were strongly correlated with diet composition across locations (inferred from QFASA), emphasizing that diet and not environmental variation in contaminant concentrations among locations is crucial in assessing contaminant-associated health risks in killer whales. These findings highlight the urgency for implementing enhanced measures to safely dispose of POP-contaminated waste, prevent further environmental contamination, and mitigate the release of newer and potentially harmful contaminants.

Runs of homozygosity in killer whale genomes provide a global record of demographic histories.

Runs of homozygosity (ROH) occur when offspring inherit haplotypes that are identical by descent from each parent. Length distributions of ROH are informative about population history; specifically, the probability of inbreeding mediated by mating system and/or population demography. Here, we investigated whether variation in killer whale (Orcinus orca) demographic history is reflected in genome-wide heterozygosity and ROH length distributions, using a global data set of 26 genomes representative of geographic and ecotypic variation in this species, and two F1 admixed individuals with Pacific-Atlantic parentage. We first reconstructed demographic history for each population as changes in effective population size through time using the pairwise sequential Markovian coalescent (PSMC) method. We found a subset of populations declined in effective population size during the Late Pleistocene, while others had more stable demography. Genomes inferred to have undergone ancestral declines in effective population size, were autozygous at hundreds of short ROH (<1 Mb), reflecting high background relatedness due to coalescence of haplotypes deep within the pedigree. In contrast, longer and therefore younger ROH (>1.5 Mb) were found in low latitude populations, and populations of known conservation concern. These include a Scottish killer whale, for which 37.8% of the autosomes were comprised of ROH >1.5 Mb in length. The fate of this population, in which only two adult males have been sighted in the past five years, and zero fecundity over the last two decades, may be inextricably linked to its demographic history and consequential inbreeding depression.

Individual Prey Specialization Drives PCBs in Icelandic Killer Whales.

Interindividual variation in prey specialization is an essential yet overlooked aspect of wildlife feeding ecology, especially as it relates to intrapopulation variation in exposure to toxic contaminants. Here, we assessed blubber concentrations of an extensive suite of persistent organic pollutants in Icelandic killer whales (Orcinus orca). Polychlorinated biphenyl (PCB) concentrations in blubber were >300-fold higher in the most contaminated individual relative to the least contaminated, ranging from 1.3 to 428.6 mg·kg-1 lw. Mean PCB concentrations were 6-to-9-fold greater in individuals with a mixed diet including marine mammals than in fish specialist individuals, whereas males showed PCB concentrations 4-fold higher than females. Given PCBs have been identified as potentially impacting killer whale population growth, and levels in mixed feeders specifically exceeded known thresholds, the ecology of individuals must be recognized to accurately forecast how contaminants may threaten the long-term persistence of the world's ultimate marine predator.

Killer whale genomes reveal a complex history of recurrent admixture and vicariance.

Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree-like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidate complex population histories. Killer whales have limited extrinsic barriers to dispersal and have radiated globally, and are therefore a good candidate model for the application of such tools. Here, we analyse a global data set of killer whale genomes in a rare attempt to elucidate global population structure in a nonhuman species. We identify a pattern of genetic homogenisation at lower latitudes and the greatest differentiation at high latitudes, even between currently sympatric lineages. The processes underlying the major axis of structure include high drift at the edge of species' range, likely associated with founder effects and allelic surfing during postglacial range expansion. Divergence between Antarctic and non-Antarctic lineages is further driven by ancestry segments with up to four-fold older coalescence time than the genome-wide average; relicts of a previous vicariance during an earlier glacial cycle. Our study further underpins that episodic gene flow is ubiquitous in natural populations, and can occur across great distances and after substantial periods of isolation between populations. Thus, understanding the evolutionary history of a species requires comprehensive geographic sampling and genome-wide data to sample the variation in ancestry within individuals.

Separating underwater ambient noise from flow noise recorded on stereo acoustic tags attached to marine mammals.

Sound-recording acoustic tags attached to marine animals are commonly used in behavioural studies. Measuring ambient noise is of interest to efforts to understand responses of marine mammals to anthropogenic underwater sound, or to assess their communication space. Noise of water flowing around the tag reflects the speed of the animal, but hinders ambient noise measurement. Here, we describe a correlation-based method for stereo acoustic tags to separate the relative contributions of flow and ambient noise. The uncorrelated part of the noise measured in digital acoustic recording tag (DTAG) recordings related well to swim speed of a humpback whale (Megaptera novaeangliae), thus providing a robust measure of flow noise over a wide frequency bandwidth. By removing measurements affected by flow noise, consistent ambient noise estimates were made for two killer whales (Orcinus orca) with DTAGs attached simultaneously. The method is applicable to any multi-channel acoustic tag, enabling application to a wide range of marine species.

Identifying Variations in Baseline Behavior of Killer Whales (Orcinus orca) to Contextualize Their Responses to Anthropogenic Noise.

Determining the baseline behavior of a whale requires understanding natural variations occurring due to environmental context, such as changes in prey behavior. Killer whales feeding on herring consistently encircle herring schools; however, depth of feeding differs from near the surface in winter to deeper than 10 m in spring and summer. These variations in feeding depth are probably due to the depth of the prey and the balance between the costs and benefits of bringing schools of herring to the surface. Such variation in baseline behavior may incur different energetic costs and consequently change the motivation of whales to avoid a feeding area. Here, we discuss these variations in feeding behavior in the context of exposure to noise and interpret observed responses to simulated navy sonar signals.

Low-frequency signals produced by Northeast Atlantic killer whales (Orcinus orca).

Killer whale acoustic behavior has been extensively investigated; however, most studies have focused on pulsed calls and whistles. This study reports the production of low-frequency signals by killer whales at frequencies below 300 Hz. Recordings were made in Iceland and Norway when killer whales were observed feeding on herring and no other marine mammal species were nearby. Low-frequency sounds were identified in Iceland and ranged in duration between 0.14 and 2.77 s and in frequency between 50 and 270 Hz, well below the previously reported lower limit for killer whale tonal sounds of 500 Hz. Low-frequency sounds appeared to be produced close in time to tail slaps, which are indicative of feeding attempts, suggesting that these sounds may be related to a feeding context. However, their precise function is unknown, and they could be the by-product of a non-vocal behavior rather than a vocal signal deliberately produced by the whales. Although killer whales in Norway exhibit similar feeding behavior, this sound has not been detected in recordings from Norway to date. This study suggests that, like other delphinids, killer whales produce low-frequency sounds, but further studies will be required to understand whether similar sounds exist in other killer whale populations.

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.

Dose-response relationships for the onset of avoidance of sonar by free-ranging killer whales.

Eight experimentally controlled exposures to 1-2 kHz or 6-7 kHz sonar signals were conducted with four killer whale groups. The source level and proximity of the source were increased during each exposure in order to reveal response thresholds. Detailed inspection of movements during each exposure session revealed sustained changes in speed and travel direction judged to be avoidance responses during six of eight sessions. Following methods developed for Phase-I clinical trials in human medicine, response thresholds ranging from 94 to 164 dB re 1 µPa received sound pressure level (SPL) were fitted to Bayesian dose-response functions. Thresholds did not consistently differ by sonar frequency or whether a group had previously been exposed, with a mean SPL response threshold of 142 ± 15 dB (mean ± s.d.). High levels of between- and within-individual variability were identified, indicating that thresholds depended upon other undefined contextual variables. The dose-response functions indicate that some killer whales started to avoid sonar at received SPL below thresholds assumed by the U.S. Navy. The predicted extent of habitat over which avoidance reactions occur depends upon whether whales responded to proximity or received SPL of the sonar or both, but was large enough to raise concerns about biological consequences to the whales.

Call combination patterns in Icelandic killer whales (Orcinus orca).

Acoustic sequences have been described in a range of species and in varying complexity. Cetaceans are known to produce complex song displays but these are generally limited to mysticetes; little is known about call combinations in odontocetes. Here we investigate call combinations produced by killer whales (Orcinus orca), a highly social and vocal species. Using acoustic recordings from 22 multisensor tags, we use a first order Markov model to show that transitions between call types or subtypes were significantly different from random, with repetitions and specific call combinations occurring more often than expected by chance. The mixed call combinations were composed of two or three calls and were part of three call combination clusters. Call combinations were recorded over several years, from different individuals, and several social clusters. The most common call combination cluster consisted of six call (sub-)types. Although different combinations were generated, there were clear rules regarding which were the first and last call types produced, and combinations were highly stereotyped. Two of the three call combination clusters were produced outside of feeding contexts, but their function remains unclear and further research is required to determine possible functions and whether these combinations could be behaviour- or group-specific.

First record of Risso's dolphin Grampus griseus (Cuvier, 1812) in Icelandic waters.

In July 2022, two Risso's dolphins were reported stranded in Hrútafjörður (N65° 09,503; W21° 05,529), a fjord in northern Iceland. These events represent the first confirmed observations and strandings of Risso's dolphins in Icelandic waters. Given the uniqueness of these events, a decision was made to conduct full necropsies on these individuals. This study reports findings from viral and parasitological investigations, morphological and fitness measurements, as well as stomach and intestine content analysis for each of the Risso's dolphin specimens. The results of the necropsies do not suggest any other cause of death than lack of food and exhaustion. A large plastic fragment in one individual's stomach supports these suggestions. The presence of those specimens in the middle of the subarctic ocean illustrates ongoing changes in spatial distribution expanding northward, impacting not only Risso's dolphins but more generally marine life and biodiversity.

Occurrence of long-finned pilot whales (Globicephala melas) and killer whales (Orcinus orca) in Icelandic coastal waters and their interspecific interactions.

Long-finned pilot whales and killer whales are widely distributed across the North Atlantic, but few studies have reported their occurrence in Icelandic coastal waters. Here, we use sightings data from research platforms and whale watching tours in six regions of Iceland from 2007 to 2020 to show that the occurrence of long-finned pilot and killer whales varied with region and season. Killer whales were regularly encountered in the south of Iceland during summer and west of Iceland during winter/spring. Long-finned pilot whales were only seen during the summer and were most often encountered in the south, west, and northwest of Iceland. Long-finned pilot whale occurrence in the south of Iceland appeared to increase during the study period but killer whale occurrence showed no noticeable changes. Long-finned pilot whales were sighted often in the areas that were also frequented by killer whales and interspecific interactions were commonly observed when both species co-occurred. Interactions appeared to be antagonistic, with killer whales often avoiding long-finned pilot whales and sometimes fleeing at high speed, similar to what has been described elsewhere in the North Atlantic. In the majority of interactions observed (68%), killer whales avoided long-finned pilot whales by moving away, but in 28% avoidance was at high speed with both species porpoising. This variability in the type of behavioural responses indicates that interactions may be more complex than previously described. We discuss regional trends in long-finned pilot whale and killer whale sightings and potential drivers of the observed interactions. Supplementary Information: The online version contains supplementary material available at 10.1007/s10211-022-00394-1.

Killer whales (Orcinus orca) produce ultrasonic whistles.

This study reports that killer whales, the largest dolphin, produce whistles with the highest fundamental frequencies ever reported in a delphinid. Using wide-band acoustic sampling from both animal-attached (Dtag) and remotely deployed hydrophone arrays, ultrasonic whistles were detected in three Northeast Atlantic populations but not in two Northeast Pacific populations. These results are inconsistent with analyses suggesting a correlation of maximum frequency of whistles with body size in delphinids, indicate substantial intraspecific variation in whistle production in killer whales, and highlight the importance of appropriate acoustic sampling techniques when conducting comparative analyses of sound repertoires.

Killer whales (Orcinus orca) in Iceland show weak genetic structure among diverse isotopic signatures and observed movement patterns.

Local adaption through ecological niche specialization can lead to genetic structure between and within populations. In the Northeast Pacific, killer whales (Orcinus orca) of the same population have uniform specialized diets that are non-overlapping with other sympatric, genetically divergent, and socially isolated killer whale ecotypes. However, killer whales in Iceland show intrapopulation variation of isotopic niches and observed movement patterns: some individuals appear to specialize on herring and follow it year-round while others feed upon herring only seasonally or opportunistically. We investigated genetic differentiation among Icelandic killer whales with different isotopic signatures and observed movement patterns. This information is key for management and conservation purposes but also for better understanding how niche specialization drives genetic differentiation. Photo-identified individuals (N = 61) were genotyped for 22 microsatellites and a 611 bp portion of the mitochondrial DNA (mtDNA) control region. Photo-identification of individuals allowed linkage of genetic data to existing data on individual isotopic niche, observed movement patterns, and social associations. Population subdivision into three genetic units was supported by a discriminant analysis of principal components (DAPC). Genetic clustering corresponded to the distribution of isotopic signatures, mtDNA haplotypes, and observed movement patterns, but genetic units were not socially segregated. Genetic differentiation was weak (F ST < 0.1), suggesting ongoing gene flow or recent separation of the genetic units. Our results show that killer whales in Iceland are not as genetically differentiated, ecologically discrete, or socially isolated as the Northeast Pacific prey-specialized killer whales. If any process of ecological divergence and niche specialization is taking place among killer whales in Iceland, it is likely at a very early stage and has not led to the patterns observed in the Northeast Pacific.

Prey of killer whales (Orcinus orca) in Iceland.

Killer whales have a cosmopolitan distribution and as a species are generalists, feeding on a variety of prey. However, local populations tend to specialise on specific prey types. In Icelandic waters, killer whales are generally associated with herring and, thus, have been presumed to be herring specialists. However, recent studies suggest a more complex foraging ecology, possibly including a mosaic of strategies. With increased observational effort in recent years due to research and whale-watching activities, there have been several reports of interactions with different prey, including confirmed predation events. In this study we aimed to summarise the range of potential prey of killer whales observed in Icelandic waters. We report on 12 previously unpublished accounts and review 15 accounts published in the scientific literature or local newspapers, making a total of 27 events where killer whales were observed interacting with actual or potential prey. Thirteen different species, including birds (n = 1), cephalopods (n = 1), fish (n = 5) and marine mammals (n = 6), are reported, although herring is by far the species that killer whales are most often observed interacting with. This study provides the first summary of actual and suspected killer whale prey in Icelandic waters, and contributes towards our understanding of this population's prey preferences. However, describing the diet of individuals/groups was not possible and this study points to a need for continued monitoring to understand the intricacies of killer whale foraging behaviour in this area.

Caller sex and orientation influence spectral characteristics of "two-voice" stereotyped calls produced by free-ranging killer whales.

This study investigates how particular received spectral characteristics of stereotyped calls of sexually dimorphic adult killer whales may be influenced by caller sex, orientation, and range. Calls were ascribed to individuals during natural behavior using a towed beamforming array. The fundamental frequency of both high-frequency and low-frequency components did not differ consistently by sex. The ratio of peak energy within the fundamental of the high-frequency component relative to summed peak energy in the first two low-frequency component harmonics, and the number of modulation bands off the high-frequency component, were significantly greater when whales were oriented towards the array, while range and adult sex had little effect. In contrast, the ratio of peak energy in the first versus second harmonics of the low-frequency component was greater in calls produced by adult females than adult males, while orientation and range had little effect. The dispersion of energy across harmonics has been shown to relate to body size or sex in terrestrial species, but pressure effects during diving are thought to make such a signal unreliable in diving animals. The observed spectral differences by signaler sex and orientation suggest that these types of information may be transmitted acoustically by freely diving killer whales.

Icelandic herring-eating killer whales feed at night.

Herring-eating killer whales debilitate herring with underwater tail slaps and likely herd herring into tighter schools using a feeding-specific low-frequency pulsed call ('herding' call). Feeding on herring may be dependent upon daylight, as the whales use their white underside to help herd herring; however, feeding at night has not been investigated. The production of feeding-specific sounds provides an opportunity to use passive acoustic monitoring to investigate feeding behaviour at different times of day. We compared the acoustic behaviour of killer whales between day and night, using an autonomous recorder deployed in Iceland during winter. Based upon acoustic detection of underwater tail slaps used to feed upon herring we found that killer whales fed both at night and day: they spent 50% of their time at night and 73% of daytime feeding. Interestingly, there was a significant diel variation in acoustic behaviour. Herding calls were significantly associated with underwater tail slap rate and were recorded significantly more often at night, suggesting that in low-light conditions killer whales rely more on acoustics to herd herring. Communicative sounds were also related to underwater tail slap rate and produced at different rates during day and night. The capability to adapt feeding behaviour to different light conditions may be particularly relevant for predator species occurring in high latitudes during winter, when light availability is limited.