Foraging habits of Northwest Atlantic hooded seals over the past 30 years: Future habitat suitability under global warming.

The Arctic is a global warming 'hot-spot' that is experiencing rapid increases in air and ocean temperatures and concomitant decreases in sea ice cover. These environmental changes are having major consequences on Arctic ecosystems. All Arctic endemic marine mammals are highly dependent on ice-associated ecosystems for at least part of their life cycle and thus are sensitive to the changes occurring in their habitats. Understanding the biological consequences of changes in these environments is essential for ecosystem management and conservation. However, our ability to study climate change impacts on Arctic marine mammals is generally limited by the lack of sufficiently long data time series. In this study, we took advantage of a unique dataset on hooded seal (Cystophora cristata) movements (and serum samples) that spans more than 30 years in the Northwest Atlantic to (i) investigate foraging (distribution and habitat use) and dietary (trophic level of prey and location) habits over the last three decades and (ii) predict future locations of suitable habitat given a projected global warming scenario. We found that, despite a change in isotopic signatures that might suggest prey changes over the 30-year period, hooded seals from the Northwest Atlantic appeared to target similar oceanographic characteristics throughout the study period. However, over decades, they have moved northward to find food. Somewhat surprisingly, foraging habits differed between seals breeding in the Gulf of St Lawrence vs those breeding at the "Front" (off Newfoundland). Seals from the Gulf favoured colder waters while Front seals favoured warmer waters. We predict that foraging habitats for hooded seals will continue to shift northwards and that Front seals are likely to have the greatest resilience. This study shows how hooded seals are responding to rapid environmental change and provides an indication of future trends for the species-information essential for effective ecosystem management and conservation.

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.

Environmental drivers of population-level variation in the migratory and diving ontogeny of an Arctic top predator.

The development of migratory strategies that enable juveniles to survive to sexual maturity is critical for species that exploit seasonal niches. For animals that forage via breath-hold diving, this requires a combination of both physiological and foraging skill development. Here, we assess how migratory and dive behaviour develop over the first year of life for a migratory Arctic top predator, the harp seal Pagophilus groenlandicus, tracked using animal-borne satellite relay data loggers. We reveal similarities in migratory movements and differences in diving behaviour between 38 juveniles tracked from the Greenland Sea and Northwest Atlantic breeding populations. In both regions, periods of resident and transitory behaviour during migration were associated with proxies for food availability: sea ice concentration and bathymetric depth. However, while ontogenetic development of dive behaviour was similar for both populations of juveniles over the first 25 days, after this time Greenland Sea animals performed shorter and shallower dives and were more closely associated with sea ice than Northwest Atlantic animals. Together, these results highlight the role of both intrinsic and extrinsic factors in shaping early life behaviour. Variation in the environmental conditions experienced during early life may shape how different populations respond to the rapid changes occurring in the Arctic ocean ecosystem.

The caval sphincter in cetaceans and its predicted role in controlling venous flow during a dive.

A sphincter on the inferior vena cava can protect the heart of a diving mammal from overload when elevated abdominal pressures increase venous return, yet sphincters are reported incompetent or absent in some cetacean species. We previously hypothesized that abdominal pressures are elevated and pulsatile in fluking cetaceans, and that collagen is deposited on the diaphragm according to pressure levels to resist deformation. Here, we tested the hypothesis that cetaceans generating high abdominal pressures need a more robust sphincter than those generating low pressures. We examined diaphragm morphology in seven cetacean and five pinniped species. All odontocetes had morphologically similar sphincters despite large differences in collagen content, and mysticetes had muscle that could modulate caval flow. These findings do not support the hypothesis that sphincter structure correlates with abdominal pressures. To understand why a sphincter is needed, we simulated the impact of oscillating abdominal pressures on caval flow. Under low abdominal pressures, simulated flow oscillated with each downstroke. Under elevated pressures, a vascular waterfall formed, greatly smoothing flow. We hypothesize that cetaceans maintain high abdominal pressures to moderate venous return and protect the heart while fluking, and use their sphincters only during low-fluking periods when abdominal pressures are low. We suggest that pinnipeds, which do not fluke, maintain low abdominal pressures. Simulations also showed that retrograde oscillations could be transmitted upstream from the cetacean abdomen and into the extradural veins, with potentially adverse repercussions for the cerebral circulation. We propose that locomotion-generated pressures have influenced multiple aspects of the cetacean vascular system.

Controlling thoracic pressures in cetaceans during a breath-hold dive: importance of the diaphragm.

Internal pressures change throughout a cetacean's body during swimming or diving, and uneven pressures between the thoracic and abdominal compartments can affect the cardiovascular system. Pressure differentials could arise from ventral compression on each fluke downstroke or by a faster equilibration of the abdominal compartment with changing ambient ocean pressures compared with the thoracic compartment. If significant pressure differentials do develop, we would expect the morphology of the diaphragm to adapt to its in vivo loading. Here, we tested the hypothesis that significant pressure differentials develop between the thoracic and abdominal cavities in diving cetaceans by examining diaphragms from several cetacean and pinniped species. We found that: (1) regions of cetacean diaphragms possess subserosal collagen fibres that would stabilize the diaphragm against craniocaudal stretch; (2) subserosal collagen covers 5-60% of the thoracic diaphragm surface, and area correlates strongly with published values for swimming speed of each cetacean species (P<0.001); and (3) pinnipeds, which do not locomote by vertical fluking, do not possess this subserosal collagen. These results strongly suggest that this collagen is associated with loads experienced during a dive, and they support the hypothesis that diving cetaceans experience periods during which abdominal pressures significantly exceed thoracic pressures. Our results are consistent with the generation of pressure differentials by fluking and by different compartmental equilibration rates. Pressure differentials during diving would affect venous and arterial perfusion and alter transmural pressures in abdominal arteries.

Quantitative Phylogenomics of Within-Species Mitogenome Variation: Monte Carlo and Non-Parametric Analysis of Phylogeographic Structure among Discrete Transatlantic Breeding Areas of Harp Seals (Pagophilus groenlandicus).

Phylogenomic analysis of highly-resolved intraspecific phylogenies obtained from complete mitochondrial DNA genomes has had great success in clarifying relationships within and among human populations, but has found limited application in other wild species. Analytical challenges include assessment of random versus non-random phylogeographic distributions, and quantification of differences in tree topologies among populations. Harp Seals (Pagophilus groenlandicus Erxleben, 1777) have a biogeographic distribution based on four discrete trans-Atlantic breeding and whelping populations located on "fast ice" attached to land in the White Sea, Greenland Sea, the Labrador ice Front, and Southern Gulf of St Lawrence. This East to West distribution provides a set of a priori phylogeographic hypotheses. Outstanding biogeographic questions include the degree of genetic distinctiveness among these populations, in particular between the Greenland Sea and White Sea grounds. We obtained complete coding-region DNA sequences (15,825 bp) for 53 seals. Each seal has a unique mtDNA genome sequence, which differ by 6 ~ 107 substitutions. Six major clades / groups are detectable by parsimony, neighbor-joining, and Bayesian methods, all of which are found in breeding populations on either side of the Atlantic. The species coalescent is at 180 KYA; the most recent clade, which accounts for 66% of the diversity, reflects an expansion during the mid-Wisconsinan glaciation 40~60 KYA. FST is significant only between the White Sea and Greenland Sea or Ice Front populations. Hierarchal AMOVA of 2-, 3-, or 4-island models identifies small but significant ΦSC among populations within groups, but not among groups. A novel Monte-Carlo simulation indicates that the observed distribution of individuals within breeding populations over the phylogenetic tree requires significantly fewer dispersal events than random expectation, consistent with island or a priori East to West 2- or 3-stepping-stone biogeographic models, but not a simple 1-step trans-Atlantic model. Plots of the cumulative pairwise sequence difference curves among seals in each of the four populations provide continuous proxies for phylogenetic diversification within each. Non-parametric Kolmogorov-Smirnov (K-S) tests of maximum pairwise differences between these curves indicates that the Greenland Sea population has a markedly younger phylogenetic structure than either the White Sea population or the two Northwest Atlantic populations, which are of intermediate age and homogeneous structure. The Monte Carlo and K-S assessments provide sensitive quantitative tests of within-species mitogenomic phylogeography. This is the first study to indicate that the White Sea and Greenland Sea populations have different population genetic histories. The analysis supports the hypothesis that Harp Seals comprises three genetically distinguishable breeding populations, in the White Sea, Greenland Sea, and Northwest Atlantic. Implications for an ice-dependent species during ongoing climate change are discussed.

Drift diving by hooded seals (Cystophora cristata) in the Northwest Atlantic Ocean.

Many pinniped species perform a specific dive type, referred to as a 'drift dive', where they drift passively through the water column. This dive type has been suggested to function as a resting/sleeping or food processing dive, and can be used as an indication of feeding success by calculating the daily change in vertical drift rates over time, which reflects the relative fluctuations in buoyancy of the animal as the proportion of lipids in the body change. Northwest Atlantic hooded seals perform drift dives at regular intervals throughout their annual migration across the Northwest Atlantic Ocean. We found that the daily change in drift rate varied with geographic location and the time of year and that this differed between sexes. Positive changes in buoyancy (reflecting increased lipid stores) were evident throughout their migration range and although overlapping somewhat, they were not statistically associated with high use areas as indicated by First Passage Time (FPT). Differences in the seasonal fluctuations of buoyancy between males and females suggest that they experience a difference in patterns of energy gain and loss during winter and spring, associated with breeding. The fluctuations in buoyancy around the moulting period were similar between sexes.

Investigating annual diving behaviour by hooded seals (Cystophora cristata) within the Northwest Atlantic Ocean.

With the exception of relatively brief periods when they reproduce and moult, hooded seals, Cystophora cristata, spend most of the year in the open ocean where they undergo feeding migrations to either recover or prepare for the next fasting period. Valuable insights into habitat use and diving behaviour during these periods have been obtained by attaching Satellite Relay Data Loggers (SRDLs) to 51 Northwest (NW) Atlantic hooded seals (33 females and 18 males) during ice-bound fasting periods (2004-2008). Using General Additive Models (GAMs) we describe habitat use in terms of First Passage Time (FPT) and analyse how bathymetry, seasonality and FPT influence the hooded seals' diving behaviour described by maximum dive depth, dive duration and surface duration. Adult NW Atlantic hooded seals exhibit a change in diving activity in areas where they spend >20 h by increasing maximum dive depth, dive duration and surface duration, indicating a restricted search behaviour. We found that male and female hooded seals are spatially segregated and that diving behaviour varies between sexes in relation to habitat properties and seasonality. Migration periods are described by increased dive duration for both sexes with a peak in May, October and January. Males demonstrated an increase in dive depth and dive duration towards May (post-breeding/pre-moult) and August-October (post-moult/pre-breeding) but did not show any pronounced increase in surface duration. Females dived deepest and had the highest surface duration between December and January (post-moult/pre-breeding). Our results suggest that the smaller females may have a greater need to recover from dives than that of the larger males. Horizontal segregation could have evolved as a result of a resource partitioning strategy to avoid sexual competition or that the energy requirements of males and females are different due to different energy expenditure during fasting periods.

How many seals were there? The global shelf loss during the last glacial maximum and its effect on the size and distribution of grey seal populations.

Predicting how marine mammal populations respond to habitat changes will be essential for developing conservation management strategies in the 21st century. Responses to previous environmental change may be informative in the development of predictive models. Here we describe the likely effects of the last ice age on grey seal population size and distribution. We use satellite telemetry data to define grey seal foraging habitat in terms of the temperature and depth ranges exploited by the contemporary populations. We estimate the available extent of such habitat in the North Atlantic at present (between 1.42 · 10(6) km(2) and 2.07 · 10(6) km(2)) and at the last glacial maximum (between 4.74 · 10(4) km(2) and 2.11 · 10(5) km(2)); taking account of glacial and seasonal sea-ice coverage, estimated reductions of sea-level (123 m) and sea surface temperature hind-casts. Most of the extensive continental shelf waters (North Sea, Baltic Sea and Scotian Shelf), currently supporting >95% of grey seals, were unavailable during the last glacial maximum. A combination of lower sea-level and extensive ice-sheets, massively increased seasonal sea-ice coverage and southerly extent of cold water would have pushed grey seals into areas with no significant shelf waters. The habitat during the last glacial maximum might have been as small as 3% of today's extent and grey seal populations may have fallen to similarly low numbers. An alternative scenario involving a major change to a pelagic or bathy-pelagic foraging niche cannot be discounted. However, hooded seals currently dominate that niche and may have excluded grey seals from such habitat. If as seems likely, the grey seal population fell to very low levels it would have remained low for several thousand years before expanding into current habitats over the past 12,000 years or so.