Postglacial climate changes and rise of three ecotypes of harbour porpoises, Phocoena phocoena, in western Palearctic waters.

Despite no obvious barriers to gene flow in the marine realm, environmental variation and ecological specializations can lead to genetic differentiation in highly mobile predators. Here, we investigated the genetic structure of the harbour porpoise over the entire species distribution range in western Palearctic waters. Combined analyses of 10 microsatellite loci and a 5085 base-pair portion of the mitochondrial genome revealed the existence of three ecotypes, equally divergent at the mitochondrial genome, distributed in the Black Sea (BS), the European continental shelf waters, and a previously overlooked ecotype in the upwelling zones of Iberia and Mauritania. Historical demographic inferences using approximate Bayesian computation (ABC) suggest that these ecotypes diverged during the last glacial maximum (c. 23-19 kilo-years ago, kyrbp). ABC supports the hypothesis that the BS and upwelling ecotypes share a more recent common ancestor (c. 14 kyrbp) than either does with the European continental shelf ecotype (c. 28 kyrbp), suggesting they probably descended from the extinct populations that once inhabited the Mediterranean during the glacial and post-glacial period. We showed that the two Atlantic ecotypes established a narrow admixture zone in the Bay of Biscay during the last millennium, with highly asymmetric gene flow. This study highlights the impacts that climate change may have on the distribution and speciation process in pelagic predators and shows that allopatric divergence can occur in these highly mobile species and be a source of genetic diversity.

Minke whales maximise energy storage on their feeding grounds.

Seasonal trends in energy storage of the minke whale (Balaenoptera acutorostrata), a capital breeder, were investigated in Iceland, a North Atlantic feeding ground. The aim was to better understand the energy acquisition strategies of minke whales and the energetic costs that different reproductive classes face during the breeding season. We modelled total blubber volume, using blubber thickness and morphometric measurements of individual whales. Blubber volume was influenced by body length, and was higher for pregnant females than mature whales. Blubber volume increased linearly through the feeding season at the same rate for mature (mean ± s.e.m.=0.0028 ± 0.00103 m(3) day(-1); N=61 male, 5 female) and pregnant whales (0.0024 ± 0.00100 m(3) day(-1); N=49), suggesting that minke whales aim to maximise energy storage while on the feeding grounds. The total amount of blubber accumulated over the feeding season (0.51 ± 0.119 m(3) for mature and 0.43 ± 0.112 m(3) for pregnant whales), together with energy stored as muscle and intra-abdominal fats, constitutes the total amount of energy available for reproduction (fetus development and lactation) on the breeding grounds, as well as migration, daily field metabolic rates, growth and body maintenance. No seasonal variation was observed for immature whales (N=4 male, 12 female), suggesting that they are investing most of their excess energy into growth rather than reproduction, in order to reach the length of sexual maturity faster and start reproducing earlier. Our novel modelling approach provides insight into large whale bioenergetics and life history strategies, as well as the relationship between single-site measurement of blubber thickness and total blubber volume.

Transplacental transfer of plasticizers and flame retardants in fin whales (Balaenoptera physalus) from the North Atlantic Ocean.

Marine mammals are one of the groups of animals most affected by marine pollution including that by organic compounds which, besides bearing recognised harmful effects to adults, they may also affect foetuses through placental transfer. In this study we analysed samples of fin whale (Balaenoptera physalus) females and their foetuses collected in the western Iceland summer feeding grounds in 2018. Three different families of organic pollutants: organophosphate esters (OPEs); halogenated flame retardants (HFRs); and short chain chlorinated paraffins (SCCPs), were analysed and their placental transfer investigated. HFRs were detected in 87.5% of females and 100% of foetus samples with concentrations that ranged between nd-15.4 and 6.37-101 ng/g lipid weight (lw), respectively. OPEs were detected in all samples, both from females (85.8-567 ng/g lw) and foetuses (nq-1130 ng/g lw). SCCPs were detected in 87.5% of female samples and 100% of foetal samples with concentrations that ranged between nd-30.9 and nq-574 ng/g lw, respectively. For OPE compounds, a significant negative correlation was observed between the logarithm maternal transfer ratio and their log Kow, indicating that a high lipophilicity reduced placental transfer rate. Interestingly, the decabromodiphenyl ethane (DBDPE) was the compound with the highest log Kow but also the one that was transferred the most from mothers to foetuses, calling for in-depth research on this pollutant. These results constitute the first evidence of mother-calf transfer of plasticizers and flame retardants in fin whales. Further investigations are needed to determine their potential effects on this species and other groups of animals.

Intrapopulation and temporal differences of phthalate concentrations in North Atlantic fin whales (Balaenoptera physalus).

The fin whale (Balaenoptera physalus) is a migratory filter-feeding species that is susceptible to ingest plastics while lunge feeding across the oceans. Plastic additives, such as phthalates, are compounds that are added to plastics to give them specific characteristics, such as flexibility. These so-called plasticizers are currently raising major concern because of their potential adverse effects on marine fauna. However, little is known about phthalate concentrations in tissues of baleen whales as well as their potential relation with biological variables (i.e., sex, body length and age) and their trends with time. In this study, we assessed the concentration of 13 phthalates in the muscle of 31 fin whales sampled in the feeding grounds off western Iceland between 1986 and 2015. We detected 5 of the 13 phthalates investigated, with di-n-butylphthalate (DBP), diethylphthalate (DEP) and bis(2-ethylhexyl) phthalate (DEHP) being the most abundant. None of the biological variables examined showed a statistically significant relationship with phthalate concentrations. Also, phthalate concentrations did not significantly vary over the 29-year period studied, a surprising result given the global scenario of increasing plastic pollution in the seas. The lack of time trends in phthalate concentration may be due in part to the fact that phthalates also originate from other sources. Although no adverse effects of phthalates on fin whales have been detected to date, further monitoring of these pollutants is required to identify potential toxic effects in the future.

A risk assessment review of mercury exposure in Arctic marine and terrestrial mammals.

There has been a considerable number of reports on Hg concentrations in Arctic mammals since the last Arctic Monitoring and Assessment Programme (AMAP) effort to review biological effects of the exposure to mercury (Hg) in Arctic biota in 2010 and 2018. Here, we provide an update on the state of the knowledge of health risk associated with Hg concentrations in Arctic marine and terrestrial mammal species. Using available population-specific data post-2000, our ultimate goal is to provide an updated evidence-based estimate of the risk for adverse health effects from Hg exposure in Arctic mammal species at the individual and population level. Tissue residues of Hg in 13 species across the Arctic were classified into five risk categories (from No risk to Severe risk) based on critical tissue concentrations derived from experimental studies on harp seals and mink. Exposure to Hg lead to low or no risk for health effects in most populations of marine and terrestrial mammals, however, subpopulations of polar bears, pilot whales, narwhals, beluga and hooded seals are highly exposed in geographic hotspots raising concern for Hg-induced toxicological effects. About 6% of a total of 3500 individuals, across different marine mammal species, age groups and regions, are at high or severe risk of health effects from Hg exposure. The corresponding figure for the 12 terrestrial species, regions and age groups was as low as 0.3% of a total of 731 individuals analyzed for their Hg loads. Temporal analyses indicated that the proportion of polar bears at low or moderate risk has increased in East/West Greenland and Western Hudson Bay, respectively. However, there remain numerous knowledge gaps to improve risk assessments of Hg exposure in Arctic mammalian species, including the establishment of improved concentration thresholds and upscaling to the assessment of population-level effects.

Genetic differentiation among North Atlantic killer whale populations.

Population genetic structure of North Atlantic killer whale samples was resolved from differences in allele frequencies of 17 microsatellite loci, mtDNA control region haplotype frequencies and for a subset of samples, using complete mitogenome sequences. Three significantly differentiated populations were identified. Differentiation based on microsatellite allele frequencies was greater between the two allopatric populations than between the two pairs of partially sympatric populations. Spatial clustering of individuals within each of these populations overlaps with the distribution of particular prey resources: herring, mackerel and tuna, which each population has been seen predating. Phylogenetic analyses using complete mitogenomes suggested two populations could have resulted from single founding events and subsequent matrilineal expansion. The third population, which was sampled at lower latitudes and lower density, consisted of maternal lineages from three highly divergent clades. Pairwise population differentiation was greater for estimates based on mtDNA control region haplotype frequencies than for estimates based on microsatellite allele frequencies, and there were no mitogenome haplotypes shared among populations. This suggests low or no female migration and that gene flow was primarily male mediated when populations spatially and temporally overlap. These results demonstrate that genetic differentiation can arise through resource specialization in the absence of physical barriers to gene flow.

Ingestion of synthetic particles by fin whales feeding off western Iceland in summer.

In this study we aim to assess the daily ingestion rates of synthetic particles by the fin whales (Balaenoptera physalus) that feed off the western coast of Iceland. To do so, we collected and analysed samples from the stomach content of 25 fin whales, consisting solely of northern krill (Meganyctiphanes norvegica). The particles found consisted of fibres and fragments, mainly blue, black and red, with an average size of 1.2 ± 1.3 mm. To confirm the synthetic nature of these particles, we used Micro-Fourier Transform Infrared Spectroscopy and comparison with a polymer library. The mean concentration of synthetic particles in the krill samples found in the stomachs of whales was 0.057 particles per gram, a value much lower than that previously reported for particle uptake by krill. From this concentration in krill, we estimated that the daily intake of synthetic particles for the North Atlantic fin whale would be ranging from 38,646 ± 43,392 to 77,292 ± 86,784 particles per day. Although at this level it is not possible to assess the impact of synthetic particles and their associated chemicals on the North Atlantic fin whale population, concentrations of these contaminants are likely to increase in the future, potentially causing adverse effects on whales and other marine mammals.

Evidence of unidirectional hybridization and second-generation adult hybrid between the two largest animals on Earth, the fin and blue whales.

Biodiversity in the oceans has dramatically declined since the beginning of the industrial era, with accelerated loss of marine biodiversity impairing the ocean's capacity to maintain vital ecosystem services. A few organisms epitomize the damaging and long-lasting effects of anthropogenic exploitation: Some whale species, for instance, were brought to the brink of extinction, with their population sizes reduced to such low levels that may have caused a significant disruption to their reproductive dynamics and facilitated hybridization events. The incidence of hybridization is nevertheless believed to be rare, and very little information exists on its directionality. Here, using genetic markers, we show that all but one whale hybrid sample collected in Icelandic waters originated from the successful mating of male fin whale and female blue whale, thus suggesting unidirectional hybridization. We also demonstrate for the first time the existence of a second-generation adult (male) hybrid resulting from a backcross between a female hybrid and a pure male fin whale. The incidence of hybridization events between fin and blue whales is likely underestimated and the observed unidirectional hybridization (for F1 and F2 hybrids) is likely to induce a reproductive loss in blue whale, which may represent an additional challenge to its recovery in the Atlantic Ocean compared to other rorquals.

Organophosphate contaminants in North Atlantic fin whales.

Pollution of the marine environment by litter composed of plastics is a growing concern. Chemical additives such as organophosphate flame retardants (OPFRs), which are added to plastics to improve their qualities, are in focus because they allegedly cause adverse effects on marine fauna. Here we analyse OPFR levels in the muscle of fin whales because, as a mysticete, this cetacean obtains its food by filter-feeding and is thus highly vulnerable to marine litter. Moreover, the fin whale performs long-range migrations from low-latitude areas in winter to high-latitude areas in summer, a trait that makes it a potentially good large-scale biomonitor of pollution. We also analyse OPFR levels in its main prey, the krill Meganyctiphanes norvegica, to assess transfer through diet. The samples analysed consisted of muscle tissue from 20 fin whales and whole-body homogenates of 10 krill samples, all collected off West Iceland. From the 19 OPFRs analysed, we detected 7 in the fin whale and 5 in the krill samples. Tri-n-butyl phosphate (TNBP), Isopropylated triphenyl phosphate (IPPP) and Triphenylphosphine oxide (TPPO) were the most abundant compounds found in both species. Mean ∑OPFR concentration, expressed on a lipid weight basis, was 985 (SD = 2239) ng g-1 in fin whale muscle, and 949 (SD = 1090) ng g-1 in krill homogenates. These results constitute the first evidence of the presence of OPFRs in the tissues of fin whales. Furthermore, they seem to support the non-significance of bioaccumulation of OPFRs through lifespan and of biomagnification trough the food web.

Wait your turn, North Atlantic fin whales share a common feeding ground sequentially.

Highly migratory marine species pose a challenge for the identification of management units due to the absence of clear oceanographic barriers. The population structure of North Atlantic fin whales has been investigated since the start of whaling operations but is still the subject of an ongoing scientific debate. Here we measured stable isotopes of carbon, nitrogen and oxygen in skin samples collected from 151 individuals from western Iceland, Galicia (NW Spain), the Azores archipelago and the Strait of Gibraltar (SoG). We found spatiotemporal differences in stable isotope ratios suggesting that fin whales sampled in these four areas may share a common feeding ground within the Northeast Atlantic at different times during the year. Our results also suggest that SoG whales use this common feeding ground in summer but exploit Mediterranean resources during the winter months, further supporting the existence of a limited but current exchange of individuals between these two basins.

Mitochondrial genomics reveals the evolutionary history of the porpoises (Phocoenidae) across the speciation continuum.

Historical variation in food resources is expected to be a major driver of cetacean evolution, especially for the smallest species like porpoises. Despite major conservation issues among porpoise species (e.g., vaquita and finless), their evolutionary history remains understudied. Here, we reconstructed their evolutionary history across the speciation continuum. Phylogenetic analyses of 63 mitochondrial genomes suggest that porpoises radiated during the deep environmental changes of the Pliocene. However, all intra-specific subdivisions were shaped during the Quaternary glaciations. We observed analogous evolutionary patterns in both hemispheres associated with convergent evolution to coastal versus oceanic environments. This suggests that similar mechanisms are driving species diversification in northern (harbor and Dall's) and southern species (spectacled and Burmeister's). In contrast to previous studies, spectacled and Burmeister's porpoises shared a more recent common ancestor than with the vaquita that diverged from southern species during the Pliocene. The low genetic diversity observed in the vaquita carried signatures of a very low population size since the last 5,000 years. Cryptic lineages within Dall's, spectacled and Pacific harbor porpoises suggest a richer evolutionary history than previously suspected. These results provide a new perspective on the mechanisms driving diversification in porpoises and an evolutionary framework for their conservation.

Rise of oceanographic barriers in continuous populations of a cetacean: the genetic structure of harbour porpoises in Old World waters.

BACKGROUND: Understanding the role of seascape in shaping genetic and demographic population structure is highly challenging for marine pelagic species such as cetaceans for which there is generally little evidence of what could effectively restrict their dispersal. In the present work, we applied a combination of recent individual-based landscape genetic approaches to investigate the population genetic structure of a highly mobile extensive range cetacean, the harbour porpoise in the eastern North Atlantic, with regards to oceanographic characteristics that could constrain its dispersal. RESULTS: Analyses of 10 microsatellite loci for 752 individuals revealed that most of the sampled range in the eastern North Atlantic behaves as a 'continuous' population that widely extends over thousands of kilometres with significant isolation by distance (IBD). However, strong barriers to gene flow were detected in the south-eastern part of the range. These barriers coincided with profound changes in environmental characteristics and isolated, on a relatively small scale, porpoises from Iberian waters and on a larger scale porpoises from the Black Sea. CONCLUSION: The presence of these barriers to gene flow that coincide with profound changes in oceanographic features, together with the spatial variation in IBD strength, provide for the first time strong evidence that physical processes have a major impact on the demographic and genetic structure of a cetacean. This genetic pattern further suggests habitat-related fragmentation of the porpoise range that is likely to intensify with predicted surface ocean warming.

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.

Fin whale MDH-1 and MPI allozyme variation is not reflected in the corresponding DNA sequences.

The appeal of genetic inference methods to assess population genetic structure and guide management efforts is grounded in the correlation between the genetic similarity and gene flow among populations. Effects of such gene flow are typically genomewide; however, some loci may appear as outliers, displaying above or below average genetic divergence relative to the genomewide level. Above average population, genetic divergence may be due to divergent selection as a result of local adaptation. Consequently, substantial efforts have been directed toward such outlying loci in order to identify traits subject to local adaptation. Here, we report the results of an investigation into the molecular basis of the substantial degree of genetic divergence previously reported at allozyme loci among North Atlantic fin whale (Balaenoptera physalus) populations. We sequenced the exons encoding for the two most divergent allozyme loci (MDH-1 and MPI) and failed to detect any nonsynonymous substitutions. Following extensive error checking and analysis of additional bioinformatic and morphological data, we hypothesize that the observed allozyme polymorphisms may reflect phenotypic plasticity at the cellular level, perhaps as a response to nutritional stress. While such plasticity is intriguing in itself, and of fundamental evolutionary interest, our key finding is that the observed allozyme variation does not appear to be a result of genetic drift, migration, or selection on the MDH-1 and MPI exons themselves, stressing the importance of interpreting allozyme data with caution. As for North Atlantic fin whale population structure, our findings support the low levels of differentiation found in previous analyses of DNA nucleotide loci.

Temporal trends and spatial differences of perfluoroalkylated substances in livers of harbor porpoise (Phocoena phocoena) populations from Northern Europe, 1991-2008.

Long-term temporal trends (1991-2008) and spatial differences of perfluoroalkylated substances (PFASs) were investigated in harbor porpoise (Phocoena phocoena) liver samples of juvenile females from the Baltic and North Sea. Additionally, spatial differences between the populations in the Baltic Sea and Atlantic Ocean (i.e. Iceland and Norway) and the influence of the body mass, age and sex on the PFAS concentrations were examined. Perfluorooctane sulfonate (PFOS) was the predominant compound with a concentration range of 160-2425 ng/g wet weight (ww), followed by perfluorooctane sulfonamide (PFOSA, 1-237 ng/g ww) and perfluoroundecanoate (PFUnA, 3-124 ng/g ww). In terms of temporal trends, perfluoroalkyl sulfonates (PFSAs) and PFOSA concentrations decreased over time, while, conversely, the C(9)-C(13) perfluoroalkyl carboxylate (PFCA) concentrations increased. Spatial distribution of the contaminant concentrations showed consistently higher concentrations in the Baltic Sea and lowest concentrations in the Icelandic population of the Atlantic Ocean.