Decadal migration phenology of a long-lived Arctic icon keeps pace with climate change.

Animals migrate in response to seasonal environments, to reproduce, to benefit from resource pulses, or to avoid fluctuating hazards. Although climate change is predicted to modify migration, only a few studies to date have demonstrated phenological shifts in marine mammals. In the Arctic, marine mammals are considered among the most sensitive to ongoing climate change due to their narrow habitat preferences and long life spans. Longevity may prove an obstacle for species to evolutionarily respond. For species that exhibit high site fidelity and strong associations with migration routes, adjusting the timing of migration is one of the few recourses available to respond to a changing climate. Here, we demonstrate evidence of significant delays in the timing of narwhal autumn migrations with satellite tracking data spanning 21 y from the Canadian Arctic. Measures of migration phenology varied annually and were explained by sex and climate drivers associated with ice conditions, suggesting that narwhals are adopting strategic migration tactics. Male narwhals were found to lead the migration out of the summering areas, while females, potentially with dependent young, departed later. Narwhals are remaining longer in their summer areas at a rate of 10 d per decade, a similar rate to that observed for climate-driven sea ice loss across the region. The consequences of altered space use and timing have yet to be evaluated but will expose individuals to increasing natural changes and anthropogenic activities on the summering areas.

Population genomics of the muskox' resilience in the near absence of genetic variation.

Genomic studies of species threatened by extinction are providing crucial information about evolutionary mechanisms and genetic consequences of population declines and bottlenecks. However, to understand how species avoid the extinction vortex, insights can be drawn by studying species that thrive despite past declines. Here, we studied the population genomics of the muskox (Ovibos moschatus), an Ice Age relict that was at the brink of extinction for thousands of years at the end of the Pleistocene yet appears to be thriving today. We analysed 108 whole genomes, including present-day individuals representing the current native range of both muskox subspecies, the white-faced and the barren-ground muskox (O. moschatus wardi and O. moschatus moschatus) and a ~21,000-year-old ancient individual from Siberia. We found that the muskox' demographic history was profoundly shaped by past climate changes and post-glacial re-colonizations. In particular, the white-faced muskox has the lowest genome-wide heterozygosity recorded in an ungulate. Yet, there is no evidence of inbreeding depression in native muskox populations. We hypothesize that this can be explained by the effect of long-term gradual population declines that allowed for purging of strongly deleterious mutations. This study provides insights into how species with a history of population bottlenecks, small population sizes and low genetic diversity survive against all odds.

Narwhal (Monodon monoceros) echolocation click rates to support cue counting passive acoustic density estimation.

Estimating animal abundance is fundamental for effective management and conservation. It is increasingly done by combining passive acoustics with knowledge about rates at which animals produce cues (cue rates). Narwhals (Monodon monoceros) are elusive marine mammals for which passive acoustic density estimation might be plausible, but for which cue rates are lacking. Clicking rates in narwhals were investigated using a dataset from sound and movement tag records collected in August 2013-2016 and 2019 in East Greenland. Clicking rates were quantified for ∼1200 one-second-long systematic random samples from 8 different whales. Generalized additive models were used to model (1) the probability of being in a clicking state versus depth and (2) the clicking rate while in a clicking state, versus time and depth. The probability of being in a clicking state increased with depth, reaching ∼1.0 at ∼500 m, while the number of clicks per second (while in a clicking state) increased with depth. The mean cue production rate, weighted by tag duration, was 1.28 clicks per second (se = 0.13, CV = 0.10). This first cue rate for narwhals may be used for cue counting density estimation, but care should be taken if applying it to other geographical areas or seasons, given sample size, geographical, and temporal limitations.

A regime shift in the Southeast Greenland marine ecosystem.

Two major oceanographic changes have recently propagated through several trophic levels in coastal areas of Southeast Greenland (SEG). Firstly, the amount of drift-ice exported from the Fram Strait and transported with the East Greenland Current (EGC) has decreased significantly over the past two decades, and a main tipping element (summer sea ice) has virtually disappeared since 2003 leading to a regime shift in oceanographic and ecological conditions in the region. The following 20-year period with low or no coastal sea ice is unique in the 200-year history of ice observations in the region, and the regime shift is also obvious in the volume of ice export through the Fram Strait after 2013. In the same period, the temperature of the EGC south of 73.5 N has increased significantly (>2°C) since 1980. Secondly, the warm Irminger Current, which advects warm, saline Atlantic Water into the region, has become warmer since 1990. The lack of pack ice in summer together with a warming ocean generated cascading effects on the ecosystem in SEG that are manifested in a changed fish fauna with an influx of boreal species in the south and the subarctic capelin further north. At higher trophic levels there has been an increase in the abundance of several boreal cetaceans (humpback, fin, killer, and pilot whales and dolphins) that are either new to this area or occur in historically large numbers. It is estimated that the new cetacean species in SEG are responsible for an annual predation level of 700,000 tons of fish. In addition, predation on krill species is estimated at >1,500,000 tons mainly consumed by fin whales. Simultaneously, there has been a reduction in the abundance and catches of narwhals and walruses in SEG and it is suggested that these species have been impacted by the habitat changes.

Strange attractor of a narwhal (Monodon monoceros).

Detecting structures within the continuous diving behavior of marine animals is challenging, and no universal framework is available. We captured such diverse structures using chaos theory. By applying time-delay embedding to exceptionally long dive records (83 d) from the narwhal, we reconstructed the state-space portrait. Using measures of chaos, we detected a diurnal pattern and its seasonal modulation, classified data, and found how sea-ice appearance shifts time budgets. There is more near-surface rest but deeper dives at solar noon, and more intense diving during twilight and at night but to shallower depths (likely following squid); sea-ice appearance reduces rest. The introduced geometrical approach is simple to implement and potentially helpful for mapping and labeling long-term behavioral data, identifying differences between individual animals and species, and detecting perturbations.

Correction: Understanding narwhal diving behaviour using Hidden Markov Models with dependent state distributions and long range dependence.

[This corrects the article DOI: 10.1371/journal.pcbi.1006425.].

Extremely low seasonal prey capture efficiency in a deep-diving whale, the narwhal.

Successful foraging is essential for individuals to maintain the positive energy balance required for survival and reproduction. Yet, prey capture efficiency is poorly documented in marine apex predators, especially deep-diving mammals. We deployed acoustic tags and stomach temperature pills in summer to collect concurrent information on presumed foraging activity (through buzz detection) and successful prey captures (through drops in stomach temperature), providing estimates of feeding efficiency in narwhals. Compared to the daily number of buzzes (707 ± 368), the daily rate of feeding events was particularly low in summer (19.8 ± 8.9) and only 8-14% of the foraging dives were successful (i.e. with a detectable prey capture). This extremely low success rate resulted in a very low daily food consumption rate (less than 0.5% of body mass), suggesting that narwhals rely on body reserves accumulated in winter to sustain year-round activities. The expected changes or disappearance of their wintering habitats in response to climate change may therefore have severe fitness consequences for narwhal populations.

Strong and lasting impacts of past global warming on baleen whales and their prey.

Global warming is affecting the population dynamics and trophic interactions across a wide range of ecosystems and habitats. Translating these real-time effects into their long-term consequences remains a challenge. The rapid and extreme warming period that occurred after the Last Glacial Maximum (LGM) during the Pleistocene-Holocene transition (7-12 thousand years ago) provides an opportunity to gain insights into the long-term responses of natural populations to periods with global warming. The effects of this post-LGM warming period have been assessed in many terrestrial taxa, whereas insights into the impacts of rapid global warming on marine taxa remain limited, especially for megafauna. In order to understand how large-scale climate fluctuations during the post-LGM affected baleen whales and their prey, we conducted an extensive, large-scale analysis of the long-term effects of the post-LGM warming on abundance and inter-ocean connectivity in eight baleen whale and seven prey (fish and invertebrates) species across the Southern and the North Atlantic Ocean; two ocean basins that differ in key oceanographic features. The analysis was based upon 7032 mitochondrial DNA sequences as well as genome-wide DNA sequence variation in 100 individuals. The estimated temporal changes in genetic diversity during the last 30,000 years indicated that most baleen whale populations underwent post-LGM expansions in both ocean basins. The increase in baleen whale abundance during the Holocene was associated with simultaneous changes in their prey and climate. Highly correlated, synchronized and exponential increases in abundance in both baleen whales and their prey in the Southern Ocean were indicative of a dramatic increase in ocean productivity. In contrast, the demographic fluctuations observed in baleen whales and their prey in the North Atlantic Ocean were subtle, varying across taxa and time. Perhaps most important was the observation that the ocean-wide expansions and decreases in abundance that were initiated by the post-LGM global warming, continued for millennia after global temperatures stabilized, reflecting persistent, long-lasting impacts of global warming on marine fauna.

Anthropogenic and Climatic Drivers of Long-Term Changes of Mercury and Feeding Ecology in Arctic Beluga (Delphinapterus leucas) Populations.

We assessed long-term changes in the feeding ecology and mercury (Hg) accumulation in Eastern High Arctic-Baffin Bay beluga (Delphinapterus leucas) using total Hg and stable isotope (δ13C, δ15N) assays in teeth samples from historical (1854-1905) and modern (1985-2000) populations. Mean δ13C values in teeth declined significantly over time, from -13.01 ± 0.55‰ historically to -14.41 ± 0.28‰ in 2000, while no consistent pattern was evident for δ15N due to high individual variability within each period. The temporal shift in isotopic niche is consistent with beluga feeding ecology changing in recent decades to a more pelagic and less isotopically diverse diet or an ecosystem wide change in isotope profiles. Mercury concentrations in modern beluga teeth were 3-5 times higher on average than those in historical beluga. These results are similar to the long-term trends of Hg and feeding ecology reported in other beluga populations and in other Arctic marine predators. Similar feeding ecology shifts across regions and species indicate a consistent increased pelagic diet response to climate change as the Arctic Ocean progressively warmed and lost sea ice. Previously, significant temporal Hg increase in beluga and other Arctic animals was attributed solely to direct inputs of anthropogenic Hg from long-range sources. Recent advances in understanding the Arctic marine Hg cycle suggest an additional, complementary possibility─increased inputs of terrestrial Hg of mixed anthropogenic-natural origin, mobilized from permafrost and other Arctic soils by climate warming. At present, it is not possible to assign relative importance to the two processes in explaining the rise of Hg concentrations in modern Arctic marine predators.

Circumpolar phylogeography and demographic history of beluga whales reflect past climatic fluctuations.

Several Arctic marine mammal species are predicted to be negatively impacted by rapid sea ice loss associated with ongoing ocean warming. However, consequences for Arctic whales remain uncertain. To investigate how Arctic whales responded to past climatic fluctuations, we analysed 206 mitochondrial genomes from beluga whales (Delphinapterus leucas) sampled across their circumpolar range, and four nuclear genomes, covering both the Atlantic and the Pacific Arctic region. We found four well-differentiated mitochondrial lineages, which were established before the onset of the last glacial expansion ~110 thousand years ago. Our findings suggested these lineages diverged in allopatry, reflecting isolation of populations during glacial periods when the Arctic sea-shelf was covered by multiyear sea ice. Subsequent population expansion and secondary contact between the Atlantic and Pacific Oceans shaped the current geographic distribution of lineages, and may have facilitated mitochondrial introgression. Our demographic reconstructions based on both mitochondrial and nuclear genomes showed markedly lower population sizes during the Last Glacial Maximum (LGM) compared to the preceding Eemian and current Holocene interglacial periods. Habitat modelling similarly revealed less suitable habitat during the LGM (glacial) than at present (interglacial). Together, our findings suggested the association between climate, population size, and available habitat in belugas. Forecasts for year 2100 showed that beluga habitat will decrease and shift northwards as oceans continue to warm, putatively leading to population declines in some beluga populations. Finally, we identified vulnerable populations which, if extirpated as a consequence of ocean warming, will lead to a substantial decline of species-wide haplotype diversity.

Population genomics of grey wolves and wolf-like canids in North America.

North America is currently home to a number of grey wolf (Canis lupus) and wolf-like canid populations, including the coyote (Canis latrans) and the taxonomically controversial red, Eastern timber and Great Lakes wolves. We explored their population structure and regional gene flow using a dataset of 40 full genome sequences that represent the extant diversity of North American wolves and wolf-like canid populations. This included 15 new genomes (13 North American grey wolves, 1 red wolf and 1 Eastern timber/Great Lakes wolf), ranging from 0.4 to 15x coverage. In addition to providing full genome support for the previously proposed coyote-wolf admixture origin for the taxonomically controversial red, Eastern timber and Great Lakes wolves, the discriminatory power offered by our dataset suggests all North American grey wolves, including the Mexican form, are monophyletic, and thus share a common ancestor to the exclusion of all other wolves. Furthermore, we identify three distinct populations in the high arctic, one being a previously unidentified "Polar wolf" population endemic to Ellesmere Island and Greenland. Genetic diversity analyses reveal particularly high inbreeding and low heterozygosity in these Polar wolves, consistent with long-term isolation from the other North American wolves.

Influence of past climate change on phylogeography and demographic history of narwhals, Monodon monoceros.

The Arctic is warming at an unprecedented rate, with unknown consequences for endemic fauna. However, Earth has experienced severe climatic oscillations in the past, and understanding how species responded to them might provide insight into their resilience to near-future climatic predictions. Little is known about the responses of Arctic marine mammals to past climatic shifts, but narwhals (Monodon monoceros) are considered one of the endemic Arctic species most vulnerable to environmental change. Here, we analyse 121 complete mitochondrial genomes from narwhals sampled across their range and use them in combination with species distribution models to elucidate the influence of past and ongoing climatic shifts on their population structure and demographic history. We find low levels of genetic diversity and limited geographic structuring of genetic clades. We show that narwhals experienced a long-term low effective population size, which increased after the Last Glacial Maximum, when the amount of suitable habitat expanded. Similar post-glacial habitat release has been a key driver of population size expansion of other polar marine predators. Our analyses indicate that habitat availability has been critical to the success of narwhals, raising concerns for their fate in an increasingly warming Arctic.

Understanding narwhal diving behaviour using Hidden Markov Models with dependent state distributions and long range dependence.

Diving behaviour of narwhals is still largely unknown. We use Hidden Markov models (HMMs) to describe the diving behaviour of a narwhal and fit the models to a three-dimensional response vector of maximum dive depth, duration of dives and post-dive surface time of 8,609 dives measured in East Greenland over 83 days, an extraordinarily long and rich data set. Narwhal diving patterns have not been analysed like this before, but in studies of other whale species, response variables have been assumed independent. We extend the existing models to allow for dependence between state distributions, and show that the dependence has an impact on the conclusions drawn about the diving behaviour. We try several HMMs with 2, 3 or 4 states, and with independent and dependent log-normal and gamma distributions, respectively, and different covariates to characterize dive patterns. In particular, diurnal patterns in diving behaviour is inferred, by using periodic B-splines with boundary knots in 0 and 24 hours.

The longer the better: evidence that narwhal tusks are sexually selected.

Once thought to be the magical horn of a unicorn, narwhal tusks are one of the most charismatic structures in biology. Despite years of speculation, little is known about the tusk's function, because narwhals spend most of their lives hidden underneath the Arctic ice. Some hypotheses propose that the tusk has sexual functions as a weapon or as a signal. By contrast, other hypotheses propose that the tusk functions as an environmental sensor. Since assessing the tusks function in nature is difficult, we can use the morphological relationships of tusk size with body size to understand this mysterious trait. To do so, we collected morphology data on 245 adult male narwhals over the course of 35 years. Based on the disproportional growth and large variation in tusk length we found, we provide the best evidence to date that narwhal tusks are indeed sexually selected. By combining our results on tusk scaling with known material properties of the tusk, we suggest that the narwhal tusk is a sexually selected signal that is used during male-male contests.

The endangered Spitsbergen bowhead whales' secrets revealed after hundreds of years in hiding.

Spitsbergen's bowhead whales (Balaena mysticetus) were hunted to near extinction in the world's first commercial whaling enterprise; this population clearly remains threatened, but nothing is known about its distribution, making assessment unfeasible. In this study, we document range, movement patterns and habitat preferences of this population, based on tagging done from an icebreaker-based helicopter. Despite their reduced abundance, Spitsbergen's bowhead whales occupy much of their historical range, stretching across the northern Barents Region from East Greenland eastward to Franz Josef Land. Unlike larger bowhead populations to the west, they do not migrate in a classical sense, but rather disperse from wintering grounds in the northernmost parts of their range during spring, returning northward again in autumn, a pattern opposite in terms of directionality compared to other Arctic bowhead whale populations. The extreme affiliation of this population with cold, ice-filled waters is a concern given ongoing climate warming and concomitant rapid sea ice habitat loss.

Fluorine Mass Balance and Suspect Screening in Marine Mammals from the Northern Hemisphere.

There is increasing evidence that the ∼20 routinely monitored perfluoroalkyl and polyfluoroalkyl substances (PFASs) account for only a fraction of extractable organofluorine (EOF) occurring in the environment. To assess whether PFAS exposure is being underestimated in marine mammals from the Northern Hemisphere, we performed a fluorine mass balance on liver tissues from 11 different species using a combination of targeted PFAS analysis, EOF and total fluorine determination, and suspect screening. Samples were obtained from the east coast United States (US), west and east coast of Greenland, Iceland, and Sweden from 2000 to 2017. Of the 36 target PFASs, perfluorooctane sulfonate (PFOS) dominated in all but one Icelandic and three US samples, where the 7:3 fluorotelomer carboxylic acid (7:3 FTCA) was prevalent. This is the first report of 7:3 FTCA in polar bears (∼1000 ng/g, ww) and cetaceans (<6-190 ng/g, ww). In 18 out of 25 samples, EOF was not significantly greater than fluorine concentrations derived from sum target PFASs. For the remaining 7 samples (mostly from the US east coast), 30-75% of the EOF was unidentified. Suspect screening revealed an additional 37 PFASs (not included in the targeted analysis) bringing the total to 63 detected PFASs from 12 different classes. Overall, these results highlight the importance of a multiplatform approach for accurately characterizing PFAS exposure in marine mammals.

Specialized sledge dogs accompanied Inuit dispersal across the North American Arctic.

Domestic dogs have been central to life in the North American Arctic for millennia. The ancestors of the Inuit were the first to introduce the widespread usage of dog sledge transportation technology to the Americas, but whether the Inuit adopted local Palaeo-Inuit dogs or introduced a new dog population to the region remains unknown. To test these hypotheses, we generated mitochondrial DNA and geometric morphometric data of skull and dental elements from a total of 922 North American Arctic dogs and wolves spanning over 4500 years. Our analyses revealed that dogs from Inuit sites dating from 2000 BP possess morphological and genetic signatures that distinguish them from earlier Palaeo-Inuit dogs, and identified a novel mitochondrial clade in eastern Siberia and Alaska. The genetic legacy of these Inuit dogs survives today in modern Arctic sledge dogs despite phenotypic differences between archaeological and modern Arctic dogs. Together, our data reveal that Inuit dogs derive from a secondary pre-contact migration of dogs distinct from Palaeo-Inuit dogs, and probably aided the Inuit expansion across the North American Arctic beginning around 1000 BP.

Use of glacial fronts by narwhals (Monodon monoceros) in West Greenland.

Glacial fronts are important summer habitat for narwhals (Monodon monoceros); however, no studies have quantified which glacial properties attract whales. We investigated the importance of glacial habitats using telemetry data from n = 15 whales tagged in September of 1993, 1994, 2006 and 2007 in Melville Bay, West Greenland. For 41 marine-terminating glaciers, we estimated (i) narwhal presence/absence, (ii) number of 24 h periods spent at glaciers and (iii) the fraction of narwhals that visited each glacier (at 5, 7 and 10 km) in autumn. We also compiled data on glacier width, ice thickness, ice velocity, front advance/retreat, area and extent of iceberg discharge, bathymetry, subglacial freshwater run-off and sediment flux. Narwhal use of glacial habitats expanded in the 2000s probably due to reduced summer fast ice and later autumn freeze-up. Using a generalized multivariate framework, glacier ice front thickness (vertical height in the water column) was a significant covariate in all models. A negative relationship with glacier velocity was included in several models and glacier front width was a significant predictor in the 2000s. Results suggest narwhals prefer glaciers with potential for higher ambient freshwater melt over glaciers with silt-laden discharge. This may represent a preference for summer freshwater habitat, similar to other Arctic monodontids.

West Greenland harbour porpoises assayed for antibodies against Toxoplasma gondii: false positives with the direct agglutination method.

We assayed blood/tissue fluid samples from 20 harbour porpoises Phocoena phocoena from western Greenland coastal waters for antibodies against the protozoan parasite Toxoplasma gondii by the direct agglutination test (DAT). Nine individuals (45%) were interpreted to be seropositive at 1:40 dilution and 4 (20%) were seropositive up to 1:160. Samples from these individuals were assayed by an enzyme-linked immunosorbent assay (ELISA), and tissue samples of the DAT-positive animals were tested by a nested polymerase chain reaction (nPCR). Results from both methods were negative, suggesting the absence of infection in the tested animals. After chloroform clean-up, all were negative when re-assayed by DAT. We concluded that infection with T. gondii was absent in all 20 animals, despite the initially positive DAT results, and that the false positives resulted from non-specific adherence to tachyzoites in the DAT assay which could be removed by the chloroform clean-up method. Our results suggest that detecting antibodies against T. gondii using the DAT or the modified agglutination technique, particularly on samples from Arctic marine animals which often are rich in lipids, may lead to false positive results. For such samples, the use of ELISA or PCR on available tissue samples may be advocated as confirmatory tests in order to avoid false positives and overestimating seroprevalence.