Multi-decadal trends in biomarkers in harp seal teeth from the North Atlantic reveal the influence of prey availability on seal trophic position.

Arctic food webs are being impacted by borealisation and environmental change. To quantify the impact of these multiple forcings, it is crucial to accurately determine the temporal change in key ecosystem metrics, such as trophic position of top predators. Here, we measured stable nitrogen isotopes (δ15 N) in amino acids in harp seal teeth from across the North Atlantic spanning a period of 60 years to robustly assess multi-decadal trends in harp seal trophic position, accounting for changes in δ15 N at the base of the food web. We reveal long-term variations in trophic position of harp seals which are likely to reflect fluctuations in prey availability, specifically fish- or invertebrate-dominated diets. We show that the temporal trends in harp seal trophic position differ between the Northwest Atlantic, Greenland Sea and Barents Sea, suggesting divergent changes in each local ecosystem. Our results provide invaluable data for population dynamic and ecotoxicology studies.

Emerging and legacy contaminants in common minke whale from the Barents sea.

Persistent organic pollutants (POPs), including brominated flame retardants (BFRs), perfluoroalkyl substances (PFAS) and metals, can accumulate in marine mammals and be transferred to offspring. In this study, we analyzed 64 lipophilic POPs, including four emerging BFRs, in the blubber, liver and muscle of 17 adult common minke whales (Balaenoptera acutorostrata) from the Barents Sea to investigate occurrence and tissue partitioning. In addition, the placental transfer concentration ratios of 14 PFAS and 17 metals were quantified in the muscle of nine female-fetus pairs to investigate placental transfer. Legacy lipophilic POPs were the dominating compound group in every tissue, and we observed generally lower levels compared to previous studies from 1992 to 2001. We detected the emerging BFRs hexabromobenzene (HBB) and pentabromotoluene (PBT), but in low levels compared to the legacy POPs. We detected nine PFAS, and levels of perfluorooctane sulfonate (PFOS) were higher than detected from the same population in 2011, whilst levels of Hg were comparable to 2011. Levels of lipophilic contaminants were higher in blubber compared to muscle and liver on both a wet weight and lipid adjusted basis, but tissue partitioning of the emerging BFRs could not be determined due to the high number of samples below the limit of detection. The highest muscle ΣPFAS levels were quantified in fetuses (23 ± 8.7 ng/g ww), followed by adult males (7.2 ± 2.0 ng/gg ww) and adult females (4.5 ± 1.1 ng/g ww), showing substantial placental transfer from mother to fetus. In contrast, Hg levels in the fetus were lower than the mother. Levels were under thresholds for risk of health effects in the whales. This study is the first to report occurrence and placental transfer of emerging contaminants in common minke whales from the Barents Sea, contributing valuable new data on pollutant levels in Arctic wildlife.

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.

Multi-decadal environmental change in the Barents Sea recorded by seal teeth.

Multiple environmental forcings, such as warming and changes in ocean circulation and nutrient supply, are affecting the base of Arctic marine ecosystems, with cascading effects on the entire food web through bottom-up control. Stable nitrogen isotopes (δ15 N) can be used to detect and unravel the impact of these forcings on this unique ecosystem, if the many processes that affect the δ15 N values are constrained. Combining unique 60-year records from compound specific δ15 N biomarkers on harp seal teeth alongside state-of-the-art ocean modelling, we observed a significant decline in the δ15 N values at the base of the Barents Sea food web from 1951 to 2012. This strong and persistent decadal trend emerges due to the combination of anthropogenic atmospheric nitrogen deposition in the Atlantic, increased northward transport of Atlantic water through Arctic gateways and local feedbacks from increasing Arctic primary production. Our results suggest that the Arctic ecosystem has been responding to anthropogenically induced local and remote drivers, linked to changing ocean biology, chemistry and physics, for at least 60 years. Accounting for these trends in δ15 N values at the base of the food web is essential to accurately detect ecosystem restructuring in this rapidly changing environment.

Hooded seal Cystophora cristata foraging areas in the Northeast Atlantic Ocean-Investigated using three complementary methods.

Identifying environmental characteristics that define the ecological niche of a species is essential to understanding how changes in physical conditions might affect its distribution and other aspects of its ecology. The present study used satellite relay data loggers (SRDLs) to study habitat use by Northeast Atlantic hooded seals (N = 20; 9 adult females, 3 adult males, and 8 juveniles). Three different methods were used in combination to achieve maximum insight regarding key foraging areas for hooded seals in this region, which have decline by 85% in recent decades: 1) first passage time (FPT); 2) vertical transit rate and; 3) change in dive drift rate. Generalized additive mixed models (GAMM) were applied to each method to determine whether specific habitat characteristics were associated with foraging. Separate models were run for the post-molting and the post-breeding seasons; sex and age classes were included in the GAMMs. All three methods highlighted a few common geographic areas as being important foraging zones; however, there were also some different areas identified by the different methods, which highlights the importance of using multiple indexes when analyzing tracking and diving data to study foraging behavior. Foraging occurred most commonly in relatively shallow areas with high Sea Surface Temperatures (SST), corresponding to continental shelf areas with Atlantic Water masses. All age and sex classes overlapped spatially to some extent, but the different age and sex groups showed differences in the bathymetry of their foraging areas as well as in their vertical use of the water column. When foraging, pups dove in the upper part of the water column in relatively deep areas. Adult females foraged relatively shallowly in deep water areas too, though in shallower areas than pups. Adult males foraged close to the bottom in shallower areas.

Whole genome resequencing reveals diagnostic markers for investigating global migration and hybridization between minke whale species.

BACKGROUND: In the marine environment, where there are few absolute physical barriers, contemporary contact between previously isolated species can occur across great distances, and in some cases, may be inter-oceanic. An example of this can be seen in the minke whale species complex. Antarctic minke whales are genetically and morphologically distinct from the common minke found in the north Atlantic and Pacific oceans, and the two species are estimated to have been isolated from each other for 5 million years or more. Recent atypical migrations from the southern to the northern hemisphere have been documented and fertile hybrids and back-crossed individuals between both species have also been identified. However, it is not known whether this represents a contemporary event, potentially driven by ecosystem changes in the Antarctic, or a sporadic occurrence happening over an evolutionary time-scale. We successfully used whole genome resequencing to identify a panel of diagnostic SNPs which now enable us address this evolutionary question. RESULTS: A large number of SNPs displaying fixed or nearly fixed allele frequency differences among the minke whale species were identified from the sequence data. Five panels of putatively diagnostic markers were established on a genotyping platform for validation of allele frequencies; two panels (26 and 24 SNPs) separating the two species of minke whale, and three panels (22, 23, and 24 SNPs) differentiating the three subspecies of common minke whale. The panels were validated against a set of reference samples, demonstrating the ability to accurately identify back-crossed whales up to three generations. CONCLUSIONS: This work has resulted in the development of a panel of novel diagnostic genetic markers to address inter-oceanic and global contact among the genetically isolated minke whale species and sub-species. These markers, including a globally relevant genetic reference data set for this species complex, are now openly available for researchers interested in identifying other potential whale hybrids in the world's oceans. The approach used here, combining whole genome resequencing and high-throughput genotyping, represents a universal approach to develop similar tools for other species and population complexes.

Investigating population genetic structure in a highly mobile marine organism: the minke whale Balaenoptera acutorostrata acutorostrata in the North East Atlantic.

Inferring the number of genetically distinct populations and their levels of connectivity is of key importance for the sustainable management and conservation of wildlife. This represents an extra challenge in the marine environment where there are few physical barriers to gene-flow, and populations may overlap in time and space. Several studies have investigated the population genetic structure within the North Atlantic minke whale with contrasting results. In order to address this issue, we analyzed ten microsatellite loci and 331 bp of the mitochondrial D-loop on 2990 whales sampled in the North East Atlantic in the period 2004 and 2007-2011. The primary findings were: (1) No spatial or temporal genetic differentiations were observed for either class of genetic marker. (2) mtDNA identified three distinct mitochondrial lineages without any underlying geographical pattern. (3) Nuclear markers showed evidence of a single panmictic population in the NE Atlantic according STRUCTURE's highest average likelihood found at K = 1. (4) When K = 2 was accepted, based on the Evanno's test, whales were divided into two more or less equally sized groups that showed significant genetic differentiation between them but without any sign of underlying geographic pattern. However, mtDNA for these individuals did not corroborate the differentiation. (5) In order to further evaluate the potential for cryptic structuring, a set of 100 in silico generated panmictic populations was examined using the same procedures as above showing genetic differentiation between two artificially divided groups, similar to the aforementioned observations. This demonstrates that clustering methods may spuriously reveal cryptic genetic structure. Based upon these data, we find no evidence to support the existence of spatial or cryptic population genetic structure of minke whales within the NE Atlantic. However, in order to conclusively evaluate population structure within this highly mobile species, more markers will be required.

Age-dependent prevalence of anti-Brucella antibodies in hooded seals Cystophora cristata.

Investigations of hooded seals Cystophora cristata have revealed high prevalences of Brucella-positive seals in the reduced Northeast Atlantic stock, compared to the increasing Northwest Atlantic stock. This study evaluated the relation between Brucella-serostatus in seals in the Northeast Atlantic stock and age, sex, body condition and reproduction. Bacteriology documented which animals and organs were B. pinnipedialis positive. No relationship was observed between Brucella-serostatus and body condition or reproductive traits. Pups (<1 mo old) had a substantially lower probability of being seropositive (4/159, 2.5%) than yearlings (6/17, 35.3%), suggesting that exposure may occur post-weaning, during the first year of life. For seals >1 yr old, the mean probability of being seropositive decreased with age, with no seropositives older than 5 yr, indicating loss of antibody titre with either chronicity or clearance of infection. The latter explanation seems to be most likely as B. pinnipedialis has never been isolated from a hooded seal >18 mo old, which is consistent with findings in this study; B. pinnipedialis was isolated from the retropharyngeal lymph node in 1 seropositive yearling (1/21, 5%). We hypothesize that this serological and bacteriological pattern is due to environmental exposure to B. pinnipedialis early in life, with a subsequent clearance of infection. This raises the question of a reservoir of B. pinnipedialis in the hooded seal food web.

Hybrids between common and Antarctic minke whales are fertile and can back-cross.

BACKGROUND: Minke whales are separated into two genetically distinct species: the Antarctic minke whale found in the southern hemisphere, and the common minke whale which is cosmopolitan. The common minke whale is further divided into three allopatric sub-species found in the North Pacific, southern hemisphere, and the North Atlantic. Here, we aimed to identify the genetic ancestry of a pregnant female minke whale captured in the North Atlantic in 2010, and her fetus, using data from the mtDNA control region, 11 microsatellite loci and a sex determining marker. RESULTS: All statistical parameters demonstrated that the mother was a hybrid displaying maternal and paternal contribution from North Atlantic common and Antarctic minke whales respectively. Her female fetus displayed greater genetic similarity to North Atlantic common minke whales than herself, strongly suggesting that the hybrid mother had paired with a North Atlantic common minke whale. CONCLUSION: This study clearly demonstrates, for the first time, that hybrids between minke whale species may be fertile, and that they can back-cross. Whether contact between these species represents a contemporary event linked with documented recent changes in the Antarctic ecosystem, or has occurred at a low frequency over many years, remains open.

Helminth parasites in ringed seals (Pusa hispida) from Svalbard, Norway with special emphasis on nematodes: variation with age, sex, diet, and location of host.

Complete gastrointestinal tracts from 257 ringed seals (Pusa hispida) from Svalbard, Norway, were examined for helminth parasites. Three different helminth groups were recorded (acanthocephalans 61.1%; nematodes 38%; cestodes 0.9%). Acanthocephalans (Polymorphidae) and cestodes (Anophryocephalus and Diphyllobothrium sp(p)., as well as unidentified species, were confined to the intestines. The anisakid nematodes Phocascaris phocae, Pseudoterranova sp(p)., Anisakis sp(p)., and Phocascaris/Contracaecum sp(p). were recorded in both stomachs and the anterior part of the small intestines. The abundance of nematodes and acanthocephalans varied significantly with sampling location of the seal hosts. This is likely due to the relative prevalence of Arctic versus Atlantic water in the different fjord systems, which strongly influences the age class and species of fish available as prey for the seals. Adult male ringed seals had significantly higher abundances of nematodes than did adult females or juveniles. Adult males also had significantly higher abundances of acanthocephalans than did adult females, but were not significantly different from juveniles in this regard. Nematode abundance increased significantly with age of male hosts, but this trend was lacking in female seals. Infection parameters appeared to be related to differences in the age of polar cod (Boreogadus saida) exploited by male, female, and juvenile seals.

Migration of Antarctic minke whales to the Arctic.

The Antarctic minke whale (Balaenoptera bonaerensis), and the common minke whale found in the North Atlantic (Balaenoptera acutorostrata acutorostrata), undertake synchronized seasonal migrations to feeding areas at their respective poles during spring, and to the tropics in the autumn where they overwinter. Differences in the timing of seasons between hemispheres prevent these species from mixing. Here, based upon analysis of mitochondrial and microsatellite DNA profiles, we report the observation of a single B. bonaerensis in 1996, and a hybrid with maternal contribution from B. bonaerensis in 2007, in the Arctic Northeast Atlantic. Paternal contribution was not conclusively resolved. This is the first documentation of B. bonaerensis north of the tropics, and, the first documentation of hybridization between minke whale species.