Dietary plasticity and broad North Atlantic origins inferred from bulk and amino acid-specific δ15N and δ13C favour killer whale range expansions into Arctic waters.

Killer whales (Orcinus orca) occur seasonally in the eastern Canadian Arctic (ECA), where their range expansion associated with declining sea ice have raised questions about the impacts of increasing killer whale predation pressure on Arctic-endemic prey. We assessed diet and distribution of ECA killer whales using bulk and compound-specific stable isotope analysis (CSIA) of amino acids (AA) of 54 skin biopsies collected from 2009 to 2020 around Baffin Island, Canada. Bulk ECA killer whale skin δ15N and δ13C values did not overlap with potential Arctic prey after adjustment for trophic discrimination, and instead reflected foraging history in the North Atlantic prior to their arrival in the ECA. Adjusted killer whale stable isotope (SI) values primarily overlapped with several species of North Atlantic baleen whales or tuna. Amino acid (AA)-specific δ15N values indicated the ECA killer whales fed primarily on marine mammals, having similar glutamic acid δ15N-phenylalanine δ15N (δ15NGlx-Phe) and threonine δ15N (δ15NThr) as mammal-eating killer whales from the eastern North Pacific (ENP) that served as a comparative framework. However, one ECA whale grouped with the fish-eating ENP ecotype based δ15NThr. Distinctive essential AA δ13C of ECA killer whale groups, along with bulk SI similarity to killer whales from different regions of the North Atlantic, indicates different populations converge in Arctic waters from a broad source area. Generalist diet and long-distance dispersal capacity favour range expansions, and integration of these insights will be critical for assessing ecological impacts of increasing killer whale predation pressure on Arctic-endemic species.

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.

Comparison of δ13C and δ15N of ecologically relevant amino acids among beluga whale tissues.

Ecological applications of compound-specific stable isotope analysis (CSIA) of amino acids (AAs) include 1) tracking carbon pathways in food webs using essential AA (AAESS) δ13C values, and 2) estimating consumer trophic position (TP) by comparing relative differences of 'trophic' and 'source' AA δ15N values. Despite the significance of these applications, few studies have examined AA-specific SI patterns among tissues with different AA compositions and metabolism/turnover rates, which could cause differential drawdown of body AA pools and impart tissue-specific isotopic fractionation. To address this knowledge gap, especially in the absence of controlled diet studies examining this issue in captive marine mammals, we used a paired-sample design to compare δ13C and δ15N values of 11 AAs in commonly sampled tissues (skin, muscle, and dentine) from wild beluga whales (Delphinapterus leucas). δ13C of two AAs, glutamic acid/glutamine (Glx, a non-essential AA) and, notably, threonine (an essential AA), differed between skin and muscle. Furthermore, δ15N of three AAs (alanine, glycine, and proline) differed significantly among the three tissues, with glycine δ15N differences of approximately 10 ‰ among tissues supporting recent findings it is unsuitable as a source AA. Significant δ15N differences in AAs such as proline, a trophic AA used as an alternative to Glx in TP estimation, highlight tissue selection as a potential source of error in ecological applications of CSIA-AA. Amino acids that differed among tissues play key roles in metabolic pathways (e.g., ketogenic and gluconeogenic AAs), pointing to potential physiological applications of CSIA-AA in studies of free-ranging animals. These findings underscore the complexity of isotopic dynamics within tissues and emphasize the need for a nuanced approach when applying CSIA-AA in ecological research.

Assessment of persistent organic pollutants in killer whales (Orcinus orca) of the Canadian Arctic: Implications for subsistence consumption and conservation strategies.

Killer whales (Orcinus orca) historically restricted to certain Arctic regions due to extensive sea ice have recently been documented farther north and for longer durations in the Canadian Arctic. These apex predators accumulate high levels of persistent organic pollutants (POPs). The objective of this study was to evaluate the concentrations and profiles of POPs in killer whales of the Canadian Arctic, thus determining potential risks for Inuit communities if consumed. Biopsies were collected from 33 killer whales across areas of the Canadian Arctic between 2009 and 2021. Significant variability in POP concentrations was observed among whales. The cumulative POP concentrations ranged from 12 to >2270 mg/kg lw, representing ∼200-fold increase from the least to the most contaminated individual. The rank order of concentrations of the top five contaminant classes was ∑DDT, ∑PCB, ∑CHL, ∑Toxaphene, and Dieldrin. Several emerging Arctic contaminants were detected, including chlorpyrifos, endosulfan, pentachloroanisole, and polychlorinated naphthalenes, although at relatively lower concentrations than legacy POPs. Considering the elevated blubber POP levels in killer whales, recommended daily consumption thresholds, established based on human tolerable daily intake (TDI) values, were notably restricted for ∑PCB (<0.14 g), ∑DDT (<6.9 g), ∑CHL (<13 g), dieldrin (<8 g) and heptachlor epoxide (<5 g). Killer whales in the Canadian Arctic exhibited higher POP concentrations than other commonly hunted species such as polar bears, ringed seals, and Arctic char. We acknowledge that a more holistic risk assessment of diet is required to assess the cumulative impacts of contaminant mixtures as well as nutritional quality of tissues commonly consumed by northern communities.

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.

Investigating the Relationship Between Body Shape and Life History Traits in Toothed Whales: Can Body Shape Predict Fast-Slow Life Histories?

A widespread pattern in vertebrate life-history evolution is for species to evolve towards either fast or slow life histories; however, the underlying causes of this pattern remain unclear. Toothed whales (Odontoceti) are a diverse group with a range of body sizes and life histories, making them an ideal model to investigate potential drivers of this dichotomy. Using ancestral reconstruction, we identified that certain groups of odontocetes evolved more-streamlined, presumably faster, body shapes around the same time that killer whales (Orcinus orca) evolved into whale predators approximately 1 Mya during the Pleistocene. This suggests that the evolution of a streamlined body shape may have been an adaptation to escape killer whale predation, leading to longer life-history events. To test this hypothesis, we performed a cluster analysis of odontocete whales and confirmed the dual pattern of life-history traits, with one group referred to as 'reproducers' characterized by early age of maturity, short gestation, short interbirth interval, and short lifespan, and the other group referred to as 'bet-hedgers' exhibiting the opposite pattern. However, we found that life history grouping was relatively unrelated to whale shape (i.e., more streamlined or less streamlined). Therefore, we incorporated principal component results into mixed effects models, and the model results indicated that body shape was positively related to neonate length (a measure of investment in progeny), but not significantly related to the temporal life-history traits. Thus, whale body shape is not a sufficient explanation for the evolution of fast-slow life histories in odontocete whales. Supplementary Information: The online version contains supplementary material available at 10.1007/s11692-023-09605-4.

Patterns of trace element deposition in beluga whale teeth reflect early life history.

Determination of trace element concentrations in continuously growing biological structures such as otoliths, whiskers, and teeth can provide important insight into physiological and ontogenetic processes. We examined concentrations of 11 trace elements (Li, Mg, Mn, Cu, Zn, Se, Rb, Sr, Cs, Ba, Pb) in the annual dentine growth layer groups (GLGs) of teeth of 66 Eastern Canadian Arctic belugas (Delphinapterus leucas). Several of these trace elements displayed clear and consistent patterns in early life, though few longer term trends or signals were present in trace element data for either females or males. Large changes in Sr and Ba concentrations in fetal dentine reflected in utero shifts in element deposition in the teeth of developing belugas. Marked changes in these elements during the first years after birth were likely associated with the onset of nursing and subsequent weaning. Mg, Mn, and Zn also displayed clear and consistent patterns in early life that correlated strongly with dentine stable nitrogen isotope (δ15N) data, suggesting these elements merit further study as potential tools for studying nursing and weaning. Depositional patterns of Zn and Pb, which have been linked to sexual maturation in female Pacific walruses (Odobenus rosmarus divergens), were inconsistent in beluga teeth. Some individuals (including males) displayed patterns strongly resembling those observed in female walruses, whereas many animals did not, perhaps because they had not yet reached sexual maturity. The lack of clear patterns in trace element deposition after the first few years of life may have resulted from pooling samples from multiple populations/regions collected across more than two decades, but may also indicate that elemental concentrations are primarily driven by other, extrinsic processes later in life, and might be useful as biomonitors of environmental element concentrations or tools for delineating population structure.

Mercury accumulation, biomagnification, and relationships to δ13C, δ15N and δ34S of fishes and marine mammals in a coastal Arctic marine food web.

Combining mercury and stable isotope data sets of consumers facilitates the quantification of whether contaminant variation in predators is due to diet, habitat use and/or environmental factors. We investigated inter-species variation in total Hg (THg) concentrations, trophic magnification slope between δ15N and THg, and relationships of THg with δ13C and δ34S in 15 fish and four marine mammal species (249 individuals in total) in coastal Arctic waters. Median THg concentration in muscle varied between species ranging from 0.08 ± 0.04 µg g-1 dw in capelin to 3.10 ± 0.80 µg g-1 dw in beluga whales. Both δ15N (r2 = 0.26) and δ34S (r2 = 0.19) best explained variation in log-THg across consumers. Higher THg concentrations occurred in higher trophic level species that consumed more pelagic-associated prey than consumers that rely on the benthic microbial-based food web. Our study illustrates the importance of using a multi-isotopic approach that includes δ34S when investigating trophic Hg dynamics in coastal marine systems.

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.

Male Bowhead Whale Reproductive Histories Inferred from Baleen Testosterone and Stable Isotopes.

Male mammals of seasonally reproducing species typically have annual testosterone (T) cycles, with T usually peaking during the breeding season, but occurrence of such cycles in male mysticete whales has been difficult to confirm. Baleen, a keratinized filter-feeding apparatus of mysticetes, incorporates hormones as it grows, such that a single baleen plate can record years of endocrine history with sufficient temporal resolution to discern seasonal patterns. We analyzed patterns of T every 2 cm across the full length of baleen plates from nine male bowhead whales (Balaena mysticetus) to investigate occurrence and regularity of T cycles and potential inferences about timing of breeding season, sexual maturation, and reproductive senescence. Baleen specimens ranged from 181-330 cm in length, representing an estimated 11 years (smallest whale) to 22 years (largest whale) of continuous baleen growth, as indicated by annual cycles in stable isotopes. All baleen specimens contained regularly spaced areas of high T content (T peaks) confirmed by time series analysis to be cyclic, with periods matching annual stable isotope cycles of the same individuals. In 8 of the 9 whales, T peaks preceded putative summer isotope peaks by a mean of 2.8 months, suggesting a mating season in late winter / early spring. The only exception to this pattern was the smallest and youngest male, which had T peaks synchronous with isotope peaks. This smallest, youngest whale also did not have T peaks in the first half of the plate, suggesting initiation of T cycling during the period of baleen growth. Linear mixed effect models suggest that whale age influences T concentrations, with the two largest and oldest males exhibiting a dramatic decline in T peak concentration across the period of baleen growth. Overall, these patterns are consistent with onset of sexual maturity in younger males and possible reproductive senescence in older males. We conclude that adult male bowheads undergo annual T cycles, and that analyses of T in baleen may enable investigation of reproductive seasonality, timing of the breeding season, and life history of male whales.

Amino acid δ15N differences consistent with killer whale ecotypes in the Arctic and Northwest Atlantic.

Ecotypes are groups within a species with different ecological adaptations than their conspecifics. Eastern North Pacific (ENP) killer whale (Orcinus orca) ecotypes differ in their diet, behavior, and morphology, but the same is not known for this species in the eastern Canadian Arctic (ECA) and Northwest Atlantic (NWA). Using compound-specific stable isotope analysis (CSIA) of amino acids (AAs), we compared δ15N patterns of the primary trophic and source AA pair, glutamic acid/glutamine (Glx) and phenylalanine (Phe), in dentine collagen of (1) sympatric ENP killer whale ecotypes with well-characterized diet differences and (2) ECA/NWA killer whales with unknown diets. δ15NGlx-Phe was significantly higher in the ENP fish-eating (FE) than mammal-eating (ME) ecotype (19.2 ± 0.4‰ vs. 13.5 ± 0.7‰, respectively). Similar bimodal variation in δ15NGlx-Phe indicated analogous dietary divisions among ECA/NWA killer whales, with two killer whales having higher δ15NGlx-Phe (16.5 ± 0.0‰) than the others (13.5 ± 0.6‰). Inferences of dietary divisions between these killer whales were supported by parallel differences in threonine δ15N (-33.5 ± 1.6‰ and -40.4 ± 1.1‰, respectively), given the negative correlation between δ15NThr and TP across a range of marine consumers. CSIA-AA results for ECA/NWA whales, coupled with differences in tooth wear (a correlate for diet), are consistent with ecotype characteristics reported in ENP and other killer whale populations, thus adding to documented ecological divergence in this species worldwide.

Distributions of Arctic and Northwest Atlantic killer whales inferred from oxygen isotopes.

Killer whales (Orcinus orca) are distributed widely in all oceans, although they are most common in coastal waters of temperate and high-latitude regions. The species' distribution has not been fully described in the northwest Atlantic (NWA), where killer whales move into seasonally ice-free waters of the eastern Canadian Arctic (ECA) and occur year-round off the coast of Newfoundland and Labrador farther south. We measured stable oxygen and carbon isotope ratios in dentine phosphate (δ18OP) and structural carbonate (δ18OSC, δ13CSC) of whole teeth and annual growth layers from killer whales that stranded in the ECA (n = 11) and NWA (n = 7). Source δ18O of marine water (δ18Omarine) at location of origin was estimated from dentine δ18OP values, and then compared with predicted isoscape values to assign individual distributions. Dentine δ18OP values were also assessed against those of other known-origin North Atlantic odontocetes for spatial reference. Most ECA and NWA killer whales had mean δ18OP and estimated δ18Omarine values consistent with 18O-depleted, high-latitude waters north of the Gulf Stream, above which a marked decrease in baseline δ18O values occurs. Several individuals, however, had relatively high values that reflected origins in 18O-enriched, low-latitude waters below this boundary. Within-tooth δ18OSC ranges on the order of 1-2‰ indicated interannual variation in distribution. Different distributions inferred from oxygen isotopes suggest there is not a single killer whale population distributed across the northwest Atlantic, and corroborate dietary and morphological differences of purported ecotypes in the region.

Detection of steroid and thyroid hormones in mammalian teeth.

Endocrine tools can provide an avenue to better understand mammalian life histories and predict how individuals and populations may respond to environmental stressors; however, few options exist for studying long-term endocrine patterns in individual marine mammals. Here, we (i) determined whether hormones could be measured in teeth from four marine mammal species: narwhal (Monodon monoceros), beluga (Delphinapterus leucas), killer whale (Orcinus orca) and Atlantic walrus (Odobenus rosmarus rosmarus); (ii) validated commercially available enzyme immunoassay kits for use with tooth extracts; and (iii) conducted biological validations for each species to determine whether reproductive hormone concentrations in teeth correlated with age of sexual maturity. Tooth extracts from all species had measurable concentrations of progesterone, testosterone, 17ß-estradiol, corticosterone, aldosterone and triiodothyronine (T3); however, cortisol was undetectable. Parallelism between the binding curves of assay kit standards and serially diluted pools of tooth extract for each species was observed for all measurable hormones. Slopes of accuracy tests ranged from 0.750 to 1.116, with r2 values ranging from 0.977 to 1.000, indicating acceptable accuracy. Biological validations were inconsistent with predictions for each species, with the exception of female killer whales (n = 2), which assumed higher progesterone and testosterone concentrations in mature individuals than immature individuals. Instead, we observed a decline in progesterone and testosterone concentrations from infancy through adulthood in narwhal (n = 1) and walruses (n = 2) and higher reproductive hormone concentrations in immature individuals than mature individuals in belugas (n = 8 and 10, respectively) and male killer whales (n = 1 and 2, respectively). While unexpected, this pattern has been observed in other taxa; however, further analytical and biological validations are necessary before this technique can be used to assess individual mammalian endocrine patterns.

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.

Amino acid δ15N underestimation of cetacean trophic positions highlights limited understanding of isotopic fractionation in higher marine consumers.

Compound-specific stable isotope analysis (CSIA) of amino acids (AAs) has been rapidly incorporated in ecological studies to resolve consumer trophic position (TP). Differential 15N fractionation of "trophic" AAs, which undergo trophic 15N enrichment, and "source" AAs, which undergo minimal trophic 15N enrichment and serve as a proxy for primary producer δ15N values, allows for internal calibration of TP. Recent studies, however, have shown the difference between source and trophic AA δ15N values in higher marine consumers is less than predicted from empirical studies of invertebrates and fish. To evaluate CSIA-AA for estimating TP of cetaceans, we compared source and trophic AA δ15N values of multiple tissues (skin, baleen, and dentine collagen) from five species representing a range of TPs: bowhead whales, beluga whales, short-beaked common dolphins, sperm whales, and fish-eating (FE) and marine mammal-eating (MME) killer whale ecotypes. TP estimates (TPCSIA) using several empirically derived equations and trophic discrimination factors (TDFs) were 1-2.5 trophic steps lower than stomach content-derived estimates (TPSC) for all species. Although TPCSIA estimates using dual TDF equations were in better agreement with TPSC estimates, our data do not support the application of universal or currently available dual TDFs to estimate cetacean TPs. Discrepancies were not simply due to inaccurate TDFs, however, because the difference between consumer glutamic acid/glutamine (Glx) and phenylalanine (Phe) δ15N values (δ15NGlx-Phe) did not follow expected TP order. In contrast to pioneering studies on invertebrates and fish, our data suggest trophic 15N enrichment of Phe is not negligible and should be examined among the potential mechanisms driving "compressed" and variable δ15NGlx-Phe values at high TPs. We emphasize the need for controlled diet studies to understand mechanisms driving AA-specific isotopic fractionation before widespread application of CSIA-AA in ecological studies of cetaceans and other marine consumers.

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.

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.

Multi-year patterns in testosterone, cortisol and corticosterone in baleen from adult males of three whale species.

Male baleen whales have long been suspected to have annual cycles in testosterone, but due to difficulty in collecting endocrine samples, little direct evidence exists to confirm this hypothesis. Potential influences of stress or adrenal stress hormones (cortisol, corticosterone) on male reproduction have also been difficult to study. Baleen has recently been shown to accumulate steroid hormones during growth, such that a single baleen plate contains a continuous, multi-year retrospective record of the whale's endocrine history. As a preliminary investigation into potential testosterone cyclicity in male whales and influences of stress, we determined patterns in immunoreactive testosterone, two glucocorticoids (cortisol and corticosterone), and stable-isotope (SI) ratios, across the full length of baleen plates from a bowhead whale (Balaena mysticetus), a North Atlantic right whale (Eubalaena glacialis) and a blue whale (Balaenoptera musculus), all adult males. Baleen was subsampled at 2 cm (bowhead, right) or 1 cm (blue) intervals and hormones were extracted from baleen powder with methanol, followed by quantification of all three hormones using enzyme immunoassays validated for baleen extract of these species. Baleen of all three males contained regularly spaced peaks in testosterone content, with number and spacing of testosterone peaks corresponding well to SI data and to species-specific estimates of annual baleen growth rate. Cortisol and corticosterone exhibited some peaks that co-occurred with testosterone peaks, while other glucocorticoid peaks occurred independent of testosterone peaks. The right whale had unusually high glucocorticoids during a period with a known entanglement in fishing gear and a possible disease episode; in the subsequent year, testosterone was unusually low. Further study of baleen testosterone patterns in male whales could help clarify conservation- and management-related questions such as age of sexual maturity, location and season of breeding, and the potential effect of anthropogenic and natural stressors on male testosterone cycles.

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.

Dentine oxygen isotopes (δ (18)O) as a proxy for odontocete distributions and movements.

Spatial variation in marine oxygen isotope ratios (δ (18)O) resulting from differential evaporation rates and precipitation inputs is potentially useful for characterizing marine mammal distributions and tracking movements across δ (18)O gradients. Dentine hydroxyapatite contains carbonate and phosphate that precipitate in oxygen isotopic equilibrium with body water, which in odontocetes closely tracks the isotopic composition of ambient water. To test whether dentine oxygen isotope composition reliably records that of ambient water and can therefore serve as a proxy for odontocete distribution and movement patterns, we measured δ (18)O values of dentine structural carbonate (δ (18) OSC) and phosphate (δ (18) OP) of seven odontocete species (n = 55 individuals) from regional marine water bodies spanning a surface water δ (18)O range of several per mil. Mean dentine δ (18) OSC (range +21.2 to +25.5‰ VSMOW) and δ (18) OP (+16.7 to +20.3‰) values were strongly correlated with marine surface water δ (18)O values, with lower dentine δ (18) OSC and δ (18) OP values in high-latitude regions (Arctic and Eastern North Pacific) and higher values in the Gulf of California, Gulf of Mexico, and Mediterranean Sea. Correlations between dentine δ (18) OSC and δ (18) OP values with marine surface water δ (18)O values indicate that sequential δ (18)O measurements along dentine, which grows incrementally and archives intra- and interannual isotopic composition over the lifetime of the animal, would be useful for characterizing residency within and movements among water bodies with strong δ (18)O gradients, particularly between polar and lower latitudes, or between oceans and marginal basins.