Abundant dissolved genetic material in Arctic sea ice Part I: Extracellular DNA

The porous medium of sea ice, a surface-rich environment characterized by low temperature and high salinity, has been proposed as a favorable site for horizontal gene transfer, but few measurements are available to assess the possibility of this mode of evolution in ice. Here, we report the first measurements of dissolved DNA in sea ice, measured by fluorescent dye staining of centrifugal-filter-concentrated samples of melted ice. Newly formed landfast and pack ice on the Canadian Arctic Shelf (ca. 71°N, 125°W) contained higher concentrations (scaled to volume of brine) of the major components of dissolved DNA—extracellular DNA and viruses—than the underlying seawater. Dissolved DNA was dominated by extracellular DNA in surface seawater (up to 95%), with viruses making up relatively larger fractions at depths below 100 m (up to 27%) and in thick sea ice (66–78 cm; up to 100%). Extracellular DNA was heterogeneously distributed, with concentrations up to 135 μg DNA L⁻¹ brine detected in landfast sea ice, higher than previously reported from any marine environment. Additionally, extracellular DNA was significantly highly enriched at the base of ice of medium thickness (33–37 cm), suggestive of in situ production. Relative to underlying seawater, higher concentrations of extracellular DNA, viruses, and bacteria, and the availability of numerous surfaces for attachment within the ice matrix suggest that sea ice may be a hotspot for HGT in the marine environment.     

Unusual narwhal sea ice entrapments and delayed autumn freeze-up trends

Sea ice entrapments of narwhals (Monodon monoceros) occur when rapid changes in weather and wind conditions create a formation of fast ice in bays or passages used by whales. Between 2008 and 2010, four entrapments of narwhals were reported in Canada and Greenland. In each case, large groups (40–600 individuals) succumbed in the sea ice at three separate summering localities, two of these where entrapments had never before been reported. We examined long-term trends in autumn freeze-up timing (date when sea ice concentration rises above some threshold) on the 6 largest narwhal summering areas using sea ice concentration from satellite passive microwave data (1979–2009). We found strongly positive and significant trends (P < 0.001) in progressively later dates of autumn freeze-up in all summering areas. Autumn freeze-up occurs between 0.5 and 1 day later per year, or roughly 2–4 weeks later, over the 31-year time series. This indicates that sea ice conditions on narwhal summering areas are changing rapidly. The question remains whether entrapment events on summering areas are random or whether narwhals are adapting to changes in sea ice freeze-up by prolonging their summer residence time.     

Population dynamics of bacteria in Arctic sea ice

The dynamics of bacterial populations in annual sea ice were measured throughout the vernal bloom of ice algae near Resolute in the Canadian Arctic. The maximum concentration of bacteria was 6.0·10¹¹ cells·m^–2 (about 2.0·10¹⁰ cells·l^–1) and average cell volume was 0.473 m³ in the lower 4 cm of the ice sheet. On average, 37% of the bacteria were epiphytic and were most commonly attached (70%) to the dominant alga,Nitzschia frigida (58% of total algal numbers). Bacterial population dynamics appeared exponential, and specific growth rates were higher in the early season (0.058 day^–1), when algal biomass was increasing, than in the later season (0.0247 day^–1), when algal biomass was declining. The proportion of epiphytes and the average number of epiphytes per alga increased significantly (P<0.05) through the course of the algal bloom. The net production of bacteria was 67.1 mgC·m^–2 throughout the algal bloom period, of which 45.5 mgC·m^–2 occurred during the phase of declining algal biomass. Net algal production was 1942 mgC·m^–2. Sea ice bacteria (both arctic and antarctic) are more abundant than expected on the basis of relationships between bacterioplankton and chlorophyll concentrations in temperate waters, but ice bacteria biomass and net production are nonetheless small compared with the ice algal blooms that presumably support them.     

Respiration and bacterial carbon dynamics in Arctic sea ice

Bacterial carbon demand, an important component of ecosystem dynamics in polar waters and sea ice, is a function of both bacterial production (BP) and respiration (BR). BP has been found to be generally higher in sea ice than underlying waters, but rates of BR and bacterial growth efficiency (BGE) are poorly characterized in sea ice. Using melted ice core incubations, community respiration (CR), BP, and bacterial abundance (BA) were studied in sea ice and at the ice–water interface (IWI) in the Western Canadian Arctic during the spring and summer 2008. CR was converted to BR empirically. BP increased over the season and was on average 22 times higher in sea ice as compared with the IWI. Rates in ice samples were highly variable ranging from 0.2 to 18.3 μg C l⁻¹ d⁻¹. BR was also higher in ice and on average ~10 times higher than BP but was less variable ranging from 2.39 to 22.5 μg C l⁻¹ d⁻¹. Given the high variability in BP and the relatively more stable rates of BR, BP was the main driver of estimated BGE (r ² = 0.97, P < 0.0001). We conclude that microbial respiration can consume a significant proportion of primary production in sea ice and may play an important role in biogenic CO₂ fluxes between the sea ice and atmosphere.     

Denitrification activity and oxygen dynamics in Arctic sea ice

Denitrification and oxygen dynamics were investigated in the sea ice of Franklin Bay (70°N), Canada. These investigations were complemented with measurements of denitrification rates in sea ice from different parts of the Arctic (69°N–85°N). Potential for bacterial denitrification activity (5–194 μmol N m⁻² day⁻¹) and anammox activity (3–5 μmol N m⁻² day⁻¹) in melt water from both first-year and multi-year sea ice was found. These values correspond to 27 and 7%, respectively, of the benthic denitrification and anammox activities in Arctic sediments. Although we report only potential denitrification and anammox rates, we present several indications that active denitrification in sea ice may occur in Franklin Bay (and elsewhere): (1) despite sea ice-algal primary production in the lower sea ice layers, heterotrophic activity resulted in net oxygen consumption in the sea ice of 1–3 μmol l⁻¹ sea ice per day at in situ light conditions, suggesting that O₂ depletion may occur prior to the spring bloom. (2) The ample organic carbon (DOC) and NO₃ ⁻ present in sea ice may support an active denitrification population. (3) Measurements of O₂ conditions in melted sea ice cores showed very low bulk concentrations, and in some cases anoxic conditions prevailed. (4) Laboratory studies using planar optodes for measuring the high-resolution two-dimensional O₂ distributions in sea ice confirmed the very dynamic and heterogeneous O₂ distribution in sea ice, displaying a mosaic of microsites of high and low O₂ concentrations. Brine enclosures and channels were strongly O₂ depleted in actively melting sea ice, and anoxic conditions in parts of the brine system would favour anaerobic processes.     

Dissolved organic matter in Arctic multi-year sea ice during winter: major components and relationship to ice characteristics

Ice cores were collected between 10.03.93 and 15.03.93 along a 200 m profile on a large ice floe in Fram Strait. The ice was typical of Arctic multi-year ice, having a mean thickness along the profile of 2.56 ±0.53 m. It consisted mostly of columnar ice (83%) grown through congelation of seawater at the ice bottom, and the salinity profiles were characterized by a linear increase from 0 psu at the top to values ranging between 3 and 5 psu at depth. Distributions of dissolved organic carbon (DOC) and nitrogen (DON) and major nutrients were compared with ice texture, salinity and chlorophyll a. DOC, DON, dissolved inorganic nitrogen (DIN), NH₄ ⁺ and NO₂ ^– were present in concentrations in excess of that predicted by dilution curves derived from Arctic surface water values. Only NO₃ ^– was depleted, although not exhausted. High DOC and DON values in conjunction with high NH₄ ⁺ levels indicated that a significant proportion of the dissolved organic matter (DOM) was a result of decomposition/grazing of ice algae and/or detritus. The combination of high NH₄ ⁺ and NO₂ ^– points to regeneration of nitrogen compounds. There was no significant correlation between DOC and Chl a in contrast to DON, which had a positively significant correlation with both salinity and Chl a, and the distribution of DOM in the cores might best be described as a combination of both physical and biological processes. There was no correlation between DOC and DON suggesting an uncoupling of DOC and DON dynamics in multi year ice.     

Biogenic silica recycling in sea ice inferred from Si-isotopes: constraints from Arctic winter first-year sea ice

We report silicon isotopic composition (δ³⁰Si vs. NBS28) in Arctic sea ice, based on sampling of silicic acid from both brine and seawater in a small Greenlandic bay in March 2010. Our measurements show that just before the productive period, δ³⁰Si of sea-ice brine similar to δ³⁰Si of the underlying seawater. Hence, there is no Si isotopic fractionation during sea-ice growth by physical processes such as brine convection. This finding brings credit and support to the conclusions of previous work on the impact of biogenic processes on sea ice δ³⁰Si: any δ³⁰Si change results from a combination of biogenic silica production and dissolution. We use this insight to interpret data from an earlier study of sea-ice δ³⁰Si in Antarctic pack ice that show a large accumulation of biogenic silica. Based on these data, we estimate a significant contribution of biogenic silica dissolution (D) to production (P), with a D:P ratio between 0.4 and 0.9. This finding has significant implications for the understanding and parameterization of the sea ice Si-biogeochemical cycle, i.e. previous studies assumed little or no biogenic silica dissolution in sea ice.     

Decadal shifts in autumn migration timing by Pacific Arctic beluga whales are related to delayed annual sea ice formation

Migrations are often influenced by seasonal environmental gradients that are increasingly being altered by climate change. The consequences of rapid changes in Arctic sea ice have the potential to affect migrations of a number of marine species whose timing is temporally matched to seasonal sea ice cover. This topic has not been investigated for Pacific Arctic beluga whales (Delphinapterus leucas) that follow matrilineally maintained autumn migrations in the waters around Alaska and Russia. For the sympatric Eastern Chukchi Sea (‘Chukchi’) and Eastern Beaufort Sea (‘Beaufort’) beluga populations, we examined changes in autumn migration timing as related to delayed regional sea ice freeze‐up since the 1990s, using two independent data sources (satellite telemetry data and passive acoustics) for both populations. We compared dates of migration between ‘early’ (1993–2002) and ‘late’ (2004–2012) tagging periods. During the late tagging period, Chukchi belugas had significantly delayed migrations (by 2 to >4 weeks, depending on location) from the Beaufort and Chukchi seas. Spatial analyses also revealed that departure from Beaufort Sea foraging regions by Chukchi whales was postponed in the late period. Chukchi beluga autumn migration timing occurred significantly later as regional sea ice freeze‐up timing became later in the Beaufort, Chukchi, and Bering seas. In contrast, Beaufort belugas did not shift migration timing between periods, nor was migration timing related to freeze‐up timing, other than for southward migration at the Bering Strait. Passive acoustic data from 2008 to 2014 provided independent and supplementary support for delayed migration from the Beaufort Sea (4 day yr^?1) by Chukchi belugas. Here, we report the first phenological study examining beluga whale migrations within the context of their rapidly transforming Pacific Arctic ecosystem, suggesting flexible responses that may enable their persistence yet also complicate predictions of how belugas may fare in the future.     

Identification of the sea ice diatom biomarker IP25 in Arctic benthic macrofauna: direct evidence for a sea ice diatom diet in Arctic heterotrophs

Currently, the impact of declining seasonal sea ice extent in the Arctic on polar food webs remains uncertain. Previously, a range of proxy techniques has been employed to determine links between sea ice or phytoplankton primary production and the Arctic marine food web, although it is accepted that such approaches have their limitations. Here, we propose a novel approach to tracing sea ice primary production through Arctic food webs using the sea ice diatom biomarker, IP₂₅. Various benthic macrofaunal specimens were collected between March and May 2008 from Franklin Bay in the Amundsen Gulf, Arctic Canada, as part of the International Polar Year–Circumpolar Flaw Lead system study. Each specimen was analysed for the presence of the sea ice diatom biomarker IP₂₅ in order to provide evidence for feeding by benthic organisms on sea ice algae. IP₂₅ was found in nineteen out of the twenty-one specimens analysed, often as the most abundant of the highly branched isoprenoid biomarkers detected. The stable isotope composition of IP₂₅ (δ¹³C = −17.1 ± 0.5‰) in the sea urchin (Strongylocentrotus sp.) specimens was similar to that reported previously for this biomarker in Arctic sea ice, sedimenting particles and sediments. It is concluded that detection of IP₂₅ in Arctic benthic macrofauna represents a novel approach to providing convincing evidence for feeding on sea ice algae. It is also proposed that analysis of IP₂₅ may be used to trace trophic transfer of sea ice algal-derived organic matter through Arctic food webs in the future.     

Protists in Arctic drift and land‐fast sea ice

Global climate change is having profound impacts on polar ice with changes in the duration and extent of both land‐fast ice and drift ice, which is part of the polar ice pack. Sea ice is a distinct habitat and the morphologically identifiable sympagic community living within sea ice can be readily distinguished from pelagic species. Sympagic metazoa and diatoms have been studied extensively since they can be identified using microscopy techniques. However, non‐diatom eukaryotic cells living in ice have received much less attention despite taxa such as the dinoflagellate Polarella and the cercozoan Cryothecomonas being isolated from sea ice. Other small flagellates have also been reported, suggesting complex microbial food webs. Since smaller flagellates are fragile, often poorly preserved, and are difficult for non‐experts to identify, we applied high throughput tag sequencing of the V4 region of the 18S rRNA gene to investigate the eukaryotic microbiome within the ice. The sea ice communities were diverse (190 taxa) and included many heterotrophic and mixotrophic species. Dinoflagellates (43 taxa), diatoms (29 taxa) and cercozoans (12 taxa) accounted for ~80% of the sequences. The sympagic communities living within drift ice and land‐fast ice harbored taxonomically distinct communities and we highlight specific taxa of dinoflagellates and diatoms that may be indicators of land‐fast and drift ice.     

Sea ice occurrence predicts genetic isolation in the Arctic fox

Unlike Oceanic islands, the islands of the Arctic Sea are not completely isolated from migration by terrestrial vertebrates. The pack ice connects many Arctic Sea islands to the mainland during winter months. The Arctic fox (Alopex lagopus), which has a circumpolar distribution, populates numerous islands in the Arctic Sea. In this study, we used genetic data from 20 different populations, spanning the entire distribution of the Arctic fox, to identify barriers to dispersal. Specifically, we considered geographical distance, occurrence of sea ice, winter temperature, ecotype, and the presence of red fox and polar bear as nonexclusive factors that influence the dispersal behaviour of individuals. Using distance-based redundancy analysis and the BIOENV procedure, we showed that occurrence of sea ice is the key predictor and explained 40-60% of the genetic distance among populations. In addition, our analysis identified the Commander and Pribilof Islands Arctic populations as genetically unique suggesting they deserve special attention from a conservation perspective.     

The role of sea ice for vascular plant dispersal in the Arctic

Sea ice has been suggested to be an important factor for dispersal of vascular plants in the Arctic. To assess its role for postglacial colonization in the North Atlantic region, we compiled data on the first Late Glacial to Holocene occurrence of vascular plant species in East Greenland, Iceland, the Faroe Islands and Svalbard. For each record, we reconstructed likely past dispersal events using data on species distributions and genetics. We compared these data to sea-ice reconstructions to evaluate the potential role of sea ice in these past colonization events and finally evaluated these results using a compilation of driftwood records as an independent source of evidence that sea ice can disperse biological material. Our results show that sea ice was, in general, more prevalent along the most likely dispersal routes at times of assumed first colonization than along other possible routes. Also, driftwood is frequently dispersed in regions that have sea ice today. Thus, sea ice may act as an important dispersal agent. Melting sea ice may hamper future dispersal of Arctic plants and thereby cause more genetic differentiation. It may also limit the northwards expansion of competing boreal species, and hence favour the persistence of Arctic species.     

Organism incorporation into newly forming Arctic sea ice in the Greenland Sea

New ice formation, protist incorporation and enrichment in differentstages of young Arctic sea ice (grease,nilas and pancake ice)were studied in the Greenland Sea in autumn 1995. Nutrients(nitrite, nitrate, phosphateand silicate), salinity and abundanceestimates of organisms were analysed from surface water andnew ice samples. The abundances of bacteria, diatoms, and photo-and hetero trophic flagellates in the ice and water column weredetermined using epifluorescence microscopy. An enrichment indexwas calculated to compare the abundance of organisms in thewater column with different stages of young sea ice. The resultsclearly show that (i) protist incorporation already begins duringthe first stages of new sea ice formation, (ii) incorporationof protists is selective, showing preference for diatoms witha relatively large cell size and (iii) enrichment of organisms,in particular diatoms, takes place in young sea ice in the GreenlandSea. The selectivity of the incorpor ation process and the evidentpreference for diatoms are presumably a result of the largercell size and/orcertain properties of the cell surface (e.g.stickiness) that enhance their incorporation. The calculatedenrichment indices were relatively low for bacteria and flagellates.     

Notes on the biology of sea ice in the Arctic and Antarctic

The sea ice which covers large areas of the polar regions plays a major role in the marine ecosystem of both the Arctic and Southern Oceans. Not only do warmblooded animals depend on sea ice as a platform, but the sympagic organisms living internally within the sea ice or at the interfaces ice/snow and ice/water provide a substantial part of the total primary production of the ice covered regions. In addition sea ice organisms are an important food source for a variety of pelagic animals and may initiate phytoplankton spring blooms after ice melt by seeding effects.Sea ice organisms often are enriched by some orders of magnitude if the same volume of melted ice is compared to that of the underlying water column. Three hypotheses try to explain this discrepancy and are discussed. Investigations on the nutrient chemistry within the sea ice system and in-situ observations still are rare. Intense growth of sympagic organisms can result in nutrient deficiencies, at least in selected habitats. Advances in endoscopie methods may lead to a better understanding of the life within the sea ice.Paper presented at the Symposium on Polar regions: the challenge for biological and ecological research organised by the Swiss Committee for Polar Research, Basel on 2 October 1992     

Organism losses during ice melting: A serious bias in sea ice community studies

Summary When ice samples are melted, microorganisms living within the brine inclusions are subjected to rapid and extreme changes in salinities. This procedure results in substantial losses of flagellates and ciliates. Most of these losses can be prevented if ice samples are melted in larger volumes of sterile sea water to buffer salinity and osmotic changes. Since most studies on the ice biota have ignored, or have been unable to avoid this bias, current views of the composition and activity of sea ice communities are based on assemblages over-representing organisms with rigid cell material.     

Sea-ice algae in Arctic pack ice during late winter

Pack ice around Svalbard was sampled during the expedition ARK XIX/1 of RV “Polarstern” (March–April 2003) in order to determine environmental conditions, species composition and abundances of sea-ice algae and heterotrophic protists during late winter. As compared to other seasons, species diversity of algae (total 40 taxa) was not low, but abundances (5,000–448,000 cells l⁻¹) were lower by one to two orders of magnitude. Layers of high algal abundances were observed both at the bottom and in the ice interior. Inorganic nutrient concentrations (NO₂, NO₃, PO₄, Si(OH)₄) within the ice were mostly higher than during other seasons, and enriched compared to seawater by enrichment indices of 1.6–24.6 (corrected for losses through the desalination process). Thus, the survival of algae in Arctic pack ice was not limited by nutrients at the beginning of the productive season. Based on less-detailed physical data, light was considered as the most probable factor controlling the onset of the spring ice-algal bloom in the lower part of the ice, while low temperatures and salinities inhibit algal growth in the upper part of the ice at the end of the winter. Incorporation of ice algae probably took place during the entire freezing period. Possible overwintering strategies during the dark period, such as facultative heterotrophy, energy reserves, and resting spores are discussed.     

Visual predators and the diel vertical migration of copepods under Arctic sea ice during the midnight sun

Despite the midnight sun, herbivore copepods Calanus hyperboreus,C. glacialis and Pseudocalanus acuspes displayed a normal dielvertical migration (NDVM) under the ice cover of Barrow Straitin spring, ascending into the chlorophyll-rich under-ice surfacelayer around maximum relative rate of change in irradiance (     

Dissolved extracellular polymeric substances (dEPS) dynamics and bacterial growth during sea ice formation in an ice tank study

Extracellular polymeric substances (EPS) are known to help microorganisms to survive under extreme conditions in sea ice. High concentrations of EPS are reported in sea ice from both poles; however, production and dynamics of EPS during sea ice formation have been little studied to date. This investigation followed the production and partitioning of existing and newly formed dissolved organic matter (DOM) including dissolved carbohydrates (dCHO), dissolved uronic acids (dUA) and dissolved EPS (dEPS), along with bacterial abundances during early stages of ice formation. Sea ice was formed from North Sea water with (A) ambient DOM (NSW) and (B) with additional algal-derived DOM (ADOM) in a 6d experiment in replicated mesocosms. In ADOM seawater, total bacterial numbers (TBN) increased throughout the experiment, whereas bacterial growth occurred for 5d only in the NSW seawater. TBN progressively decreased within developing sea ice but with a 2-fold greater decline in NSW compared to ADOM ice. There were significant increases in the concentrations of dCHO in ice. Percentage contribution of dEPS was highest (63%) in the colder, uppermost parts in ADOM ice suggesting the development of a cold-adapted community, producing dEPS possibly for cryo-protection and/or protection from high salinity brines. We conclude that in the early stages of ice formation, allochthonous organic matter was incorporated from parent seawater into sea ice and that once ice formation had established, there were significant changes in the concentrations and composition of dissolved organic carbon pool, resulting mainly from the production of autochthonous DOM by the bacteria.     

Zooplankton boom and ice amphipod bust below melting sea ice in the Amundsen Gulf, Arctic Canada

Early summer in the Arctic with extensive ice melt and break-up represents a dramatic change for sympagic–pelagic fauna below seasonal sea ice. As part of the International Polar Year-Circumpolar Flaw Lead system study (IPY-CFL), this investigation quantified zooplankton in the meltwater layer below landfast ice and remaining ice fauna below melting ice during June (2008) in Franklin Bay and Darnley Bay, Amundsen Gulf, Canada. The ice was in a state of advanced melt, with fully developed melt ponds. Intense melting resulted in a 0.3- to 0.5-m-thick meltwater layer below the ice, with a strong halocline to the Arctic water below. Zooplankton under the ice, in and below the meltwater layer, was sampled by SCUBA divers. Dense concentrations (max. 1,400 ind. m⁻³) of Calanus glacialis were associated with the meltwater layer, with dominant copepodid stages CIV and CV and high abundance of nauplii. Less abundant species included Pseudocalanus spp., Oithona similis and C. hyperboreus. The copepods were likely feeding on phytoplankton (0.5–2.3 mg Chl-a m⁻³) in the meltwater layer. Ice amphipods were present at low abundance (<10 ind. m⁻²) and wet biomass (<0.2 g m⁻²). Onisimus glacialis and Apherusa glacialis made up 64 and 51% of the total ice faunal abundance in Darnley Bay and Franklin Bay, respectively. During early summer, the autochthonous ice fauna becomes gradually replaced by allochthonous zooplankton, with an abundance boom near the meltwater layer. The ice amphipod bust occurs during late stages of melting and break-up, when their sympagic habitat is diminished then lost.