Predictions replaced by facts: a keystone species' behavioural responses to declining arctic sea-ice

Since the first documentation of climate-warming induced declines in arctic sea-ice, predictions have been made regarding the expected negative consequences for endemic marine mammals. But, several decades later, little hard evidence exists regarding the responses of these animals to the ongoing environmental changes. Herein, we report the first empirical evidence of a dramatic shift in movement patterns and foraging behaviour of the arctic endemic ringed seal (Pusa hispida), before and after a major collapse in sea-ice in Svalbard, Norway. Among other changes to the ice-regime, this collapse shifted the summer position of the marginal ice zone from over the continental shelf, northward to the deep Arctic Ocean Basin. Following this change, which is thought to be a ‘tipping point’, subadult ringed seals swam greater distances, showed less area-restricted search behaviour, dived for longer periods, exhibited shorter surface intervals, rested less on sea-ice and did less diving directly beneath the ice during post-moulting foraging excursions. In combination, these behavioural changes suggest increased foraging effort and thus also likely increases in the energetic costs of finding food. Continued declines in sea-ice are likely to result in distributional changes, range reductions and population declines in this keystone arctic species.     

Ringed seal (Pusa hispida) tooth annuli as an index of reproduction in the Beaufort Sea

Multi-decadal time-series of biological indices that reflect the state of a population are rare in ecological studies, but invaluable for assessing environmental regulation of population dynamics. We utilized canine teeth extracted from ringed seals (Pusa hispida) killed by polar bears (Ursus maritimus) in the Beaufort Sea, Canada, in 1985–2011, to obtain widths of annual growth layers in the cementum. Canine teeth for 75 individuals were measured and compared across years using a proportional width index (PWI) spanning 1965–2007. PWI was positively correlated with ringed seal ovulation rate obtained independently from other studies and was significantly lower than normal during ringed seal reproductive declines in 1974–75, 1984–87, 1991–93, and 2004–05, suggesting that PWI reflects ringed seal reproductive capacity. The PWI was also examined against climatic and sea ice factors to assess environmental regulation of ringed seal reproduction. Results suggest that ringed seals benefit from cyclonic circulation regimes in the Beaufort Sea, and an earlier breakup of sea ice in summer that may positively influence the quality and quantity of food during the open water season. Results highlight how cementum annuli in the canine teeth of ringed seals can provide an index of body state and linkages to sea ice conditions. Canine teeth from ringed seals can function as a means to monitor the effects of past Arctic marine variability on area-specific populations for which there are few independent empirical data.     

CLIMATE CHANGE AND RINGED SEAL (PHOCA HISPIDA) RECRUITMENT IN WESTERN HUDSON BAY

Climate warming is predicted to reduce the extent of ice cover in the Arctic and, within the Hudson Bay region, the annual ice may be significantly decreased or entirely lost in the foreseeable future. The ringed seal ( Phoca hispida ), a key species that depends on sea ice, will likely be among the first marine mammals to show the negative effects of climatic warming. We used 639 ringed seals killed by Inuit hunters from western Hudson Bay (1991–1992, 1999–2001) to assess trends in recruitment relative to snow depth, snowfall, rainfall, temperature in April and May, North Atlantic Oscillation (NAO) from the previous winter, and timing of spring break-up. Snowfall and ringed seal recruitment varied from lower than average in the 1970s, to higher in 1980s and lower in 1990s. Prior to 1990, seal recruitment appeared to be related to timing of spring ice break-up which was correlated with the NAO. However, recent 1990–2001 environmental data indicate less snowfall, lower snow depth, and warmer temperatures in April and May when pups are born and nursed. Decreased snow depth, particularly below 32 cm, corresponded with a significant decrease in ringed seal recruitment as indicated by pups born and surviving to adults that were later harvested. Earlier spring break-up of sea ice together with snow trends suggest continued low pup survival in western Hudson Bay.     

Combined Genetic and Telemetry Data Reveal High Rates of Gene Flow,Migration, and Long-Distance Dispersal Potential in Arctic Ringed Seals (Pusa hispida)

Ringed seals (Pusa hispida) are broadly distributed in seasonally ice covered seas, and their survival and reproductive success is intricately linked to sea ice and snow. Climatic warming is diminishing Arctic snow and sea ice and threatens to endanger ringed seals in the foreseeable future. We investigated the population structure and connectedness within and among three subspecies: Arctic (P. hispida hispida), Baltic (P. hispida botnica), and Lake Saimaa (P. hispida saimensis) ringed seals to assess their capacity to respond to rapid environmental changes. We consider (a) the geographical scale of migration, (b) use of sea ice, and (c) the amount of gene flow between subspecies. Seasonal movements and use of sea ice were determined for 27 seals tracked via satellite telemetry. Additionally, population genetic analyses were conducted using 354 seals representative of each subspecies and 11 breeding sites. Genetic analyses included sequences from two mitochondrial regions and genotypes of 9 microsatellite loci. We found that ringed seals disperse on a pan-Arctic scale and both males and females may migrate long distances during the summer months when sea ice extent is minimal. Gene flow among Arctic breeding sites and between the Arctic and the Baltic Sea subspecies was high; these two subspecies are interconnected as are breeding sites within the Arctic subspecies.     

Habitat use by harbour seals (Phoca vitulina) in a seasonally ice-covered region, the western Hudson Bay

Over the last few decades, the period of ice cover in Hudson Bay has decreased, owing to climate warming, with breakup occurring approximately 3 weeks earlier than it did 30 years ago. The trend towards lengthening of the open water season has led to speculation that ringed seal numbers would decline, but then harbour seals might become numerous enough to replace ringed seals in the diet of polar bears. The movement patterns of 18 harbour seals equipped with satellite-linked transmitters in the Churchill River estuary (western Hudson Bay) were examined, as well as the dive behaviour of 11 of these seals. During the ice-free period, seals followed a general central place-foraging strategy, making repeated trips between their haul-out site in the Churchill River estuary and nearshore areas (<20 km) near the river mouth and estuary. Seal behaviour changed significantly as ice started to form along the coast of western Hudson Bay: animals remained significantly farther from the Churchill River haul-out site and from the coast and performed longer and deeper dives. However, throughout the entire tracking period, whether ice was present or not, all animals restricted their movements to a narrow band of shallow coastal waters (<50 m depth) along a 600-km stretch of the western Hudson Bay coastline, centred on the Churchill River estuary haul-out site. This natural self-limitation to nearshore shallow waters could restrict the potential for the population to increase in size and replace ringed seals as a primary energy resource for polar bears.     

Temporal variation in distribution and density of ice-obligated seals in western Hudson Bay, Canada

Recent unidirectional climatic trends and changes in top predator population ecology suggest that long-term modifications may be happening in Hudson Bay, Canada. Effects of such changes on ice-obligated seal populations are expected but long-term studies are required to differentiate climate-induced changes from natural variation. We conducted strip-transect surveys in late spring in 1995–1997, 1999–2000 and 2007–2008 to estimate distribution, density and abundance of ice-obligated ringed (Phoca hispida) and bearded (Erignathus barbatus) seals in western Hudson Bay. When hauled out, ringed seals preferred land-fast and consolidated pack ice, whereas bearded seals preferred unconsolidated pack ice. Bearded and ringed seal density estimates varied from 0.0036 to 0.0229 seals/km² of ice and from 0.46 to 1.60 seals/km² of ice, respectively. Strong inter-annual variations were recorded in the abundance estimates of both species, with the largest abundance estimates in 1995 (104,162 and 1,494 ringed and bearded seals, respectively) and the lowest in 2008 for ringed seals (33,701) and 1997 for bearded seals (278). A sine function best described seal density estimates in western Hudson Bay and suggested a decadal cycle. Previous studies that reported low ringed seal demographic parameters in the 1990s and a recovery in the 2000s supported our interpretation of the survey results. We discuss our results in the context of climate warming and suggest that a long-term decline in ice-obligated seal density estimates may overlay a possible natural decadal cycle.     

Using stable isotopes to understand changes in ringed seal foraging ecology as a response to a warming environment

Trends toward increased temperatures, reduced sea ice extent, and longer open water seasons have resulted in changing Arctic ecosystem dynamics. Expected changes include shifts in distribution and abundance of prey species for seabirds and marine mammals. Using stable isotope analysis, we studied spatial and interannual variation in ringed seal (Pusa hispida) feeding ecology in Hudson Bay in relation to environmental variables, between 2003 and 2010. Ringed seal muscle and hair samples collected from Arviat and Sanikiluaq, Nunavut, were analyzed for stable isotope ratios of nitrogen (δ¹⁵N) and carbon (δ¹³C). Seals from western Hudson Bay (Arviat) had higher δ¹⁵N and lower δ¹³C than seals from eastern Hudson Bay (Sanikiluaq), and stable isotope ratios varied interannually within each region. Peak δ¹⁵N occurred in years with spring air temperatures between approximately ?5°C and ?2°C. This temperature range was characteristic of warm years in western Hudson Bay and cool years in eastern Hudson Bay. We hypothesize that the high δ¹⁵N observed in ringed seals is indicative of greater importance of capelin (Mallotus villosus) in ringed seal diet. A comparison of ringed seal isotopic niche widths indicated greater dietary differences between western and eastern Hudson Bay with warming, suggesting a possible ecological divergence related to climate change.     

Exploring Linkages between Abiotic Oceanographic Processes and a Top-trophic Predator in an Antarctic Ecosystem

Climatic variation affects the physical and biological components of ecosystems, and global-climate models predict enhanced sensitivity in polar regions, raising concern for Antarctic animal populations that may show direct responses to changes in sea-ice distribution and extent, or indirect responses to changes in prey distribution and abundance. Here, we show that over a 30-year period in the Ross Sea, average weaning masses of Weddell seals, Leptonychotes weddellii, varied strongly among years and were correlated to large-scale climatic and oceanographic variations. Foraging success of pregnant seals (reflected by weaning mass the following pupping season) increased during summers characterized by reduced sea-ice cover and positive phases of the southern oscillation. These results demonstrate a correlation between environmental variation and an important life history characteristic (weaning mass) of an Antarctic marine mammal. Understanding the mechanisms that link climatic variation and animal life history characteristics will contribute to understanding both population dynamics and global climatic processes. For the world’s most southerly distributed mammal species, the projected trend of increasing global climate change raises concern because increasing sea-ice trends in the Ross Sea sector of Antarctica will likely reduce populations due to reduced access to prey as expressed through declines in body condition and reproductive performance.     

Effects of climate warming on polar bears: a review of the evidence

Climate warming is causing unidirectional changes to annual patterns of sea ice distribution, structure, and freeze‐up. We summarize evidence that documents how loss of sea ice, the primary habitat of polar bears (Ursus maritimus), negatively affects their long‐term survival. To maintain viable subpopulations, polar bears depend on sea ice as a platform from which to hunt seals for long enough each year to accumulate sufficient energy (fat) to survive periods when seals are unavailable. Less time to access to prey, because of progressively earlier breakup in spring, when newly weaned ringed seal (Pusa hispida) young are available, results in longer periods of fasting, lower body condition, decreased access to denning areas, fewer and smaller cubs, lower survival of cubs as well as bears of other age classes and, finally, subpopulation decline toward eventual extirpation. The chronology of climate‐driven changes will vary between subpopulations, with quantifiable negative effects being documented first in the more southerly subpopulations, such as those in Hudson Bay or the southern Beaufort Sea. As the bears' body condition declines, more seek alternate food resources so the frequency of conflicts between bears and humans increases. In the most northerly areas, thick multiyear ice, through which little light penetrates to stimulate biological growth on the underside, will be replaced by annual ice, which facilitates greater productivity and may create habitat more favorable to polar bears over continental shelf areas in the short term. If the climate continues to warm and eliminate sea ice as predicted, polar bears will largely disappear from the southern portions of their range by mid‐century. They may persist in the northern Canadian Arctic Islands and northern Greenland for the foreseeable future, but their long‐term viability, with a much reduced global population size in a remnant of their former range, is uncertain.     

Reproductive rates of ringed seals and survival of pups in Northwestern Hudson Bay, Canada, 1991–2000

Reproductive parameters were determined from a sample of ringed seals collected by Inuit hunters during their annual open water harvest in autumn at Arviat, Nunavut, on the western coast of Hudson Bay, Canada, in 1991–1992 and 1998–2000. Ovulation rates of adult females were high and similar to rates recorded from studies of ringed seals in other geographic areas. However, pregnancy rates averaged only 55% and were significantly lower than in other studies, and the proportions of young-of-the-year were only 4.8, 4.2, 7.5, 4.1, and 23% for the mentioned years, respectively, instead of being >30% as expected. These results appear to indicate that reproductive parameters of ringed seals and survival of their young are exhibiting long-term shifts rather than short-term fluctuations, and that the trend is downward. Furthermore, these downward trends in reproduction, in conjunction with changes in the proportions of different seal species in the diet of polar bears, climatic warming in western Hudson Bay, and progressively earlier breakup of sea ice over the last 25 years, suggest that major changes are occurring in the marine ecosystem of Hudson Bay. The pathways involved are poorly understood and merit further study.     

ABUNDANCE OF RINGED SEALS (PUSA HISPIDA) IN THE FJORDS OF SPITSBERGEN, SVALBARD, DURING THE PEAK MOLTING PERIOD

Ringed seal (Pusa hispida) abundance in Spitsbergen, Svalbard, was estimated during the peak molting period via aerial, digital photographic surveys. A total of 9,145 images, covering 41.7%–100% of the total fast‐ice cover (1,496 km²) of 18 different fjords and bays, were inspected for the presence of ringed seals. A total of 1,708 seals were counted, and when accounting for ice areas that were not covered by images, a total of 3,254 (95% CI: 3,071–3,449) ringed seals were estimated to be hauled out during the surveys. Extensive behavioral data from radio‐tagged ringed seals (collected in a companion study) from one of the highest density fjords during the molting period were used to create a model that predicts the proportion of seals hauled out on any given date, time of day, and under various meteorological conditions. Applying this model to the count data from each fjord, we estimated that a total of 7,585 (95% CI: 6,332–9,085) ringed seals were present in the surveyed area during the peak molting period. Data on interannual variability in ringed seal abundance suggested higher numbers of seals in Van Keulenfjorden in 2002 compared to 2003, while other fjords with very stable ice cover showed no statistical differences. Poor ice conditions in general in 2002 probably resulted in seals from a wide area coming to Van Keulenfjorden (a large fjord with stable ice in 2002). The total estimated number of ringed seals present in the study area at the time of the survey must be regarded as a population index, or at least a minimum estimate for the area, because it does not account for individuals leaving and arriving, which might account for a considerable number of animals. The same situation is likely the case for many other studies reporting aerial census data for ringed seals. To achieve accurate estimates of population sizes from aerial surveys, more extensive knowledge of ringed seal behavior will be required.     

Seasonal and developmental changes of reproductive organs of male ringed seals (Phoca hispida) in the Svalbard area

The weights of testes, prostate gland and baculum of ringed seal males were related to age, season and differences in body size. There was a significant seasonal variation in testes and prostate gland size of sexually mature males, with a maximum occurring in early April. There were no seasonal changes in prostate weight of immature males, but some of the older immatures had elevated testes weights in April. Testes weight was significantly correlated with lean body mass. The increase in testes size with increasing body weight was greater for seals six years of age or older than for younger males. We suggest that some testicular growth and a seasonal cycle in testes growth occur before the testes become functional endocrinologically. We also believe that the primary event leading to puberty in ringed seals is an age-dependent shift in metabolic processes, directing a larger percentage of available energy towards the reproductive organs.     

SEASONAL CHANGES IN BLUBBER DISTRIBUTION IN ATLANTIC HARBOR SEALS: INDICATIONS OF THERMODYNAMIC CONSIDERATIONS

Among its functions, the hypodermal blubber layer of pinnipeds serves as both an energy reserve and insulation. This study examined seasonal changes in blubber distribution and body morphology in a group of captive changesharbor seals to test whether these changes were designed to maximize insulative effectiveness. Seasonal changes were found in girth, blubber volume, mean blubber depth, and the ratio of blubber depth to body radius (d/r ratio). These changes were more evident in older seals. The d/r ratio demonstrated a smaller relative annual change than mean blubber depth. The d/r ratio also exhibited less variation along the length of the seal than blubber depth at any given time. Similar to reports for ringed seals, and contrary to those for southern elephant seals, the harbor seals preferentially lost blubber from overinsulated areas of the body. These results suggest that core tissue and blubber mass are lost in a manner that maximizes insulative effectiveness.     

Spatio-temporal variability of snow over sea ice in western Hudson Bay,with reference to ringed seal pup survival

Snow-covered sea ice plays a significant role in the ecology of the Arctic marine system and is a critical habitat for ice-adapted ringed seals; however, limited research has focused on the role of snow. The first two objectives of this study characterize the spatial and temporal variability in snow over the sea ice of western Hudson Bay measured from satellite (2002–2010) and how this variability relates to ringed seal pup demographic parameters. The final objective uses a regional circulation model (RCM) to estimate the future snow cover within the study area. Results indicated that the snow cover experienced interannual and interseasonal variability, however, typically increased in late spring. In addition, the Moran’s I statistics indicated clustering at small spatial lags for both seasons, suggesting similar snow depths (i.e., large-scale drifting) occurring at distances of 125 km. There was greater interannual variability in the clustering of snow during spring, compared to the winter season. These trends in snow depth were related to variability in seal pup survival; however, seal pup growth and body condition were not related to winter/spring snow conditions. The results from the RCM member runs suggest that snow will decrease by the end of this century, with a larger decrease occurring in the spring period. In addition, there will also be an increase in interannual and spatial variability during both seasons, which may have significant consequences to ringed seal population abundance through reduced pup survival within the study area.     

Do intraspecific life history patterns follow interspecific predictions? A test using latitudinal variation in ringed seals

Mammals adapted to unpredictable and low-energy environments often evolve a “bet-hedging” life history strategy characterized by less costly reproductive outputs over a longer and slower-growing life. In contrast, species adapted to more predictable (i.e., low variation) and higher energy environments may evolve greater fecundity over a shorter and faster-growing life. We tested whether this known interspecific pattern also occurs within a species. We compared life history traits of the ringed seal (Pusa hispida) in the Canadian High Arctic to those closer to the southern limit of the species' circumpolar distribution. We found that northern seals grew slower than southern seals (Brody growth coefficient), achieved a greater asymptotic body weight (82 and 69 kg vs. 74 and 54 kg female and male, respectively), reached sexual maturity later (6.1 years vs. 4.5 years), had lower fecundity (1.8 years vs. 1.3 years interbirth interval), longer average lifespan (5 years vs. 3 years median age), and greater movements (1,269 vs. 681 km). Mating systems also likely differed with northern seals showing morphological evidence of a promiscuous mating system with potential sperm competition as indicated by greater relative testes size. The northern region was also characterized by more unpredictable environmental timing of seasonal events, such as spring sea ice breakup. Life history variation between the intraspecific groups of seals appears to agree with interspecific patterns and provides a better understanding of how species' life history parameters shift in concert with environmental conditions.     

Effect of climatic warming on the Pacific walrus, and potential modification of its helminth fauna

The decreasing extent of sea-ice in the arctic basin as a consequence of climatic warming is modifying the behavior and diets of pagophilic pinnipeds, including the Pacific walrus, Odobenus rosmarus divergens Illiger, the species emphasized here. Mammals such as the walrus and bearded seal, Erignathus barbatus (Erxleben), cannot remain associated with the sea-ice, and continue to feed on their usual diet of benthic invertebrates inhabiting coastal waters to a depth of approximately 100 m, when the northwestward retreating ice reaches deep waters beyond the margins of the continental shelf. With reduction of their customary substrate (ice), the walrus has become more pelagic and preys more often on ringed seals, Phoca hispida Schreber. Dietary changes, with modifications of helminth faunas, may be induced by various factors. Increased consumption of mammals or their remains by walruses may lead to a higher prevalence of trichinellosis in them and to more frequent occurrence in indigenous peoples inhabiting the arctic coasts. To assess predicted effects on the composition of helminth fauna of the walrus, we recommend systematic surveys of their helminths as part of research on effects of climatic warming.     

Prevalence and pathology of nematode infections in the lungs of ringed seals (Phoca hispida) of the western arctic of Canada

Two genera of lung nematodes were found in a sample of 382 wild ringed seals (Phoca hispida). Otostrongylus circumlitus were found mainly in young of the year where they occupied the main stem bronchi causing extensive mucus production, mucosal hyperplasia and peribronchitis. Immature stages of the nematode were found in pulmonary vessels causing end-arteritis. There was only a slight reduction in respiratory parenchyma in infected seals and no correlation between infection and size or body condition. However, the sharp decline of O. circumlitus infection from 32% in young of the year to 0.5% after the first winter suggests that this parasite may play a role in the population dynamics of ringed seals. Filaroides (Parafilaroides) hispidus was found in alveoli of seals throughout all age classes causing no significant lesions. The infection rate increased from 44 to 71% in the 7 to 13-yr-old animals and declined to 38% in older seals. Concurrent infections occurred in 28% of young of the year seals.     

VARIABILITY IN THE BLUBBER FATTY ACID COMPOSITION OF RINGED SEALS (PHOCA HISPIDA) ACROSS THE CANADIAN ARCTIC

We determined the blubber fatty acid (FA) composition of 281 ringed seals ( Phoca hispida ) across the Canadian Arctic to make inferences about spatial, temporal, and demographic patterns of foraging. Seals were sampled in nine locations between 1992 and 2004. Regional differences in FA signatures were related to the distance between groups, with the greatest similarity occurring among seals sampled in three locations within the Beaufort Sea-Amundsen Gulf. Seals in the western and southeastern portions of Hudson Bay also had similar FA signatures. Discriminant analysis on seventeen FAs classified ringed seals to their correct geographic region with 95% accuracy. Although location accounted for most of the variability in FA signatures, adult and juvenile ringed seals in Frobisher Bay-Labrador Sea and Jones Sound showed significant FA differences, as did male and female ringed seals in Jones Sound and Qaanaaq. Demographic differences were not detected among ringed seals in the Beaufort Sea-Amundsen Gulf or in western Hudson Bay. Seals off the coast of Labrador showed significant seasonal variability in FA signatures. Overall, seasonal, regional, and demographic patterns in FA signatures were consistent with differences in ringed seal diets, as inferred from stomach content and stable isotope analyses.     

Distribution and abundance of seabirds and fur seals near the Antarctic Peninsula during the austral winter, 1986

Twenty one species of seabirds plus fur seals were observed at sea near the Antarctic Peninsula, between 60 °–68 °S, in May and June 1986, a season for which few published observations of marine animals are available for this area. Here we describe and quantify the importance of fishing activities as well as sea-ice cover and other environmental variables to the distribution patterns of birds and seals. The most striking aspect of the winter avifauna was its pronounced concentration near fishing trawlers operating on the continental shelf to the north and west of Elephant Island, and its temporal shift in response to the seasonal advance of the ice edge.     

USE OF BIOELECTRICAL IMPEDANCE ANALYSIS TO ASSESS BODY COMPOSITION OF SEALS

Abstract: Bioelectrical impedance analysis (BIA) measures resistance and reactance of a current as it passes through an organism. The validity of using BIA as a tool to measure body water content, and hence body composition and condition, was tested on harp and ringed seals. The resistance and reactance readings from BIA were compared to estimates of total body water (TBW) determined via tritiated water dilution. The relationship between resistance and TBW (% of body mass) was linear after logarithmic transformation and the two variables were highly correlated. We describe the electrode configuration and placements which provide reliable results in these seals. Our findings indicate that BIA has considerable potential as an inexpensive, rapid, and reliable technique for estimating body composition of phocid seals.