Mesoscale distribution and functional diversity of picoeukaryotes in the first-year sea ice of the Canadian Arctic

Sea ice, a characteristic feature of polar waters, is home to diverse microbial communities. Sea-ice picoeukaryotes (unicellular eukaryotes with cell size <3 μm) have received little attention compared with diatoms that dominate the spring bloom in Arctic first-year sea ice. Here, we investigated the abundance of all picoeukaryotes, and of 11 groups (chlorophytes, cryptophytes, bolidophytes, haptophytes, Pavlovaphyceae, Phaeocystis spp., pedinellales, stramenopiles groups MAST-1, MAST-2 and MAST-6 and Syndiniales Group II) at 13 first-year sea-ice stations localized in Barrow Strait and in the vicinity of Cornwallis Island, Canadian Arctic Archipelago. We applied Catalyzed Reporter Deposition–Fluorescence In Situ Hybridization to identify selected groups at a single cell level. Pavlovaphyceae and stramenopiles from groups MAST-2 and MAST-6 were for the first time reported from sea ice. Total numbers of picoeukaryotes were significantly higher in the vicinity of Cornwallis Island than in Barrow Strait. Similar trend was observed for all the groups except for haptophytes. Chlorophytes and cryptophytes were the dominant plastidic, and MAST-2 most numerous aplastidic of all the groups investigated. Numbers of total picoeukaryotes, chlorophytes and MAST-2 stramenopiles were positively correlated with the thickness of snow cover. All studied algal and MAST groups fed on bacteria. Presence of picoeukaryotes from various trophic groups (mixotrophs, phagotrophic and parasitic heterotrophs) indicates the diverse ecological roles picoeukaryotes have in sea ice. Yet, >50% of total sea-ice picoeukaryote cells remained unidentified, highlighting the need for further study of functional and phylogenetic sea-ice diversity, to elucidate the risks posed by ongoing Arctic changes.     

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.     

Linking ice structure and microscale variability of algal biomass in Arctic first-year sea ice using an in situ photographic technique

Microscale photographs were taken of the ice bottom to examine linkages of algal chlorophyll a (chl a) biomass distribution with bottom ice features in thick Arctic first-year sea ice during a spring field program which took place from May 5 to 21, 2003. The photographic technique developed in this paper has resulted in the first in situ observations of microscale variability in bottom ice algae distribution in Arctic first-year sea ice in relation to ice morphology. Observations of brine channel diameter (1.65–2.68 mm) and number density (5.33–10.35 per 100 cm²) showed that the number of these channels at the bottom of thick first-year sea ice may be greater than previously measured on extracted ice samples. A variogram analysis showed that over areas of low chl a biomass (≤20.7 mg chl a m⁻²), patchiness in bottom ice chl a biomass was at the scale of brine layer spacing and small brine channels (∼1–3 mm). Over areas of high chl a biomass (≥34.6 mg chl a m⁻²), patchiness in biomass was related to the spacing of larger brine channels on the ice bottom (∼10–26 mm). Brine layers and channels are thought to provide microscale maxima of light, nutrient replenishment and space availability which would explain the small scale patchiness over areas of low algal biomass. However, ice melt and erosion near brine channels may play a more important role in areas with high algal biomass and low snow cover.     

Vertical distribution of bacteria in Arctic sea ice from the Barents and Laptev Seas

The vertical distribution of bacterial abundance and biomass was investigated in relation to algal biomass in ice cores taken from drifting ice floes in two Arctic shelf areas: the Barents Sea and the Laptev Sea. Bacteria were not homogeneously distributed throughout the cores but occurred in dense layers. Different types of distribution patterns were found: either a single maximum occurred inside or at the bottom of the ice floe or maxima were found in different parts of the floes. Bacterial concentrations ranged from 0.4 to 36.7 · 10⁵ cells ml⁻¹. The size spectra of sea-ice bacteria were determined by image analysis. Cell sizes showed considerable variation between the ice floes. In multi-year sea ice, the largest bacteria were observed in the area of an internal chlorophyll a maximum. No specific vertical distribution patterns were found in first-year ice floes. Bacterial biomass for the ice cores ranged from 19.2 to 79.2 mg C m⁻², and the ratio of bacterial:ice algal biomass ranged from 0.43 to 10.42. A comparison with data collected from fast ice revealed large differences in terms of cell size, abundance and biomass. Received: 7 September 1995 / Accepted: 10 September 1996     

Vertical distribution of sympagic meiofauna in sea ice in the Canadian Beaufort Sea

This is the first study to determine vertical distribution patterns of sympagic meiofauna, including metazoans, protozoans and eggs >20 μm, in the Amundsen Gulf (southeastern Beaufort Sea, Arctic). Full sea-ice cores were sampled from mid of March to end of May 2008 (Circumpolar Flaw Lead system study). Investigations were performed on first-year ice from three pack- and three fast-ice stations. Additionally, 5-cm bottom-ice sections were sampled at 13 pack-ice and 5 fast-ice stations. The metazoan community was composed of nematodes, rotifers, copepods, copepod nauplii, platyhelminthes and a few rare taxa such as mollusks, cnidarians and nemerteans. High numbers of eggs, between 50 and 2,188 eggs L⁻¹, particularly of nematodes and copepods, were present in the ice. Investigations revealed also eggs of the pelagic species Calanus hyperboreus and Sagitta spp. within the ice, so that further research is needed to clarify whether more organisms than expected might use this habitat as a reproduction ground. Many different morphotypes of protozoans were observed in the samples, especially ciliates of the order Euplotida. The highest abundance was always found in the lowermost 5 cm of the ice cores, nevertheless sympagic meiofauna was not restricted to that part of the ice. Integrated meiofauna abundance ranged between 41 and 4,738 × 10² Ind. m⁻² and was highest in the fast ice in early May. Differences between pack and fast ice in terms of integrated meiofauna communities and vertical distribution were not significant, while the analysis of the bottom-ice sections indicated both a temporal development and ice-type-specific differences.     

Molecular diversity and temporal variation of picoeukaryotes in two Arctic fjords,Svalbard

Picoeukaryotes (protists <3 μm) form an important component of Arctic marine ecosystems, although knowledge of their diversity and ecosystem functioning is limited. In this study, the molecular diversity and autotrophic biomass contribution of picoeukaryotes from January to June 2009 in two Arctic fjords at Svalbard were examined using 18S environmental cloning and size-fractioned chlorophyll a measurements. A total of 62 putative picoeukaryotic phylotypes were recovered from 337 positive clones. Putative picoeukaryotic autotrophs were mostly limited to one species: Micromonas pusilla, while the putative heterotrophic picoeukaryote assemblage was more diverse and dominated by uncultured marine stramenopiles (MAST) and marine alveolate groups. One MAST-1A phylotype was the only phylotype to be found in all clone libraries. The diversity of picoeukaryotes in general showed an inverse relationship with total autotrophic biomass, suggesting that the conditions dominating during the peak of the spring bloom may have a negative impact on picoeukaryote diversity. Picoplankton could contribute more than half of total autotrophic biomass before and after the spring bloom and benefited from an early onset of the growth season, whereas larger cells dominated the bloom itself.     

Viable bacterial biomass and functional diversity in fresh and marine waters in the Canadian Arctic

Bacterial biomass and functional diversity in four marine and four freshwater samples, collected from Resolute Bay, Nunavut, Canada, were studied using fluorescent nucleic-acid staining and sole-carbon-source utilization. Viable microbial counts using the LIVE/DEAD BacLight Viability Kit estimated viable marine bacterial numbers from 0.7 to 1.8᎒⁶ cells/l, which were lower than viable bacterial numbers in freshwater samples (2.1-9.9᎒⁶ cells/l) (RCBD-ANOVA). Calculations of the Shannon-Wiener diversity index and average well colour development were based on substrate utilization in ECO-Biolog plates incubated at 4°C and 20°C for 38 and 24 days, respectively. The Shannon-Wiener diversity of the marine water samples was significantly greater ( x _H'=2.40ǂ.08, P <0.005; RCBD-ANOVA) than that of freshwater samples ( x _H'=1.20ǂ.00, P <0.005; RCBD-ANOVA). Differences in microbial diversity between fresh and marine water samples at 4°C ( x _4°C =2.01) and 20°C (x_20°C =2.31) were also detected by RCBD-ANOVA analysis. Interactions between water type and incubation temperature were not significant ( F =1.926, F _c=5.12). Principal component analysis revealed differences in metabolic substrate utilization patterns and, consequently, the microbial diversity between water types and samples.     

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.     

Microbial diversity and activity through a permafrost/ground ice core profile from the Canadian high Arctic

Culture‐dependent and culture‐independent methods were used in an investigation of the microbial diversity in a permafrost/massive ground ice core from the Canadian high Arctic. Denaturing gradient gel electrophoresis as well as Bacteria and Archaea 16S rRNA gene clone libraries showed differences in the composition of the microbial communities in the distinct core horizons. Microbial diversity was similar in the active layer (surface) soil, permafrost table and permafrost horizons while the ground ice microbial community showed low diversity. Bacteria and Archaea sequences related to the Actinobacteria (54%) and Crenarchaeota (100%) respectively were predominant in the active layer while the majority of sequences in the permafrost were related to the Proteobacteria (57%) and Euryarchaeota (76%). The most abundant phyla in the ground ice clone libraries were the Firmicutes (59%) and Crenarchaeota (82%). Isolates from the permafrost were both less abundant and diverse than in the active layer soil, while no culturable cells were recovered from the ground ice. Mineralization of [1‐¹⁴C] acetic acid and [2‐¹⁴C] glucose was used to detect microbial activity in the different horizons in the core. Mineralization was detected at near ambient permafrost temperatures (?15°C), indicating that permafrost may harbour an active microbial population, while the low microbial diversity, abundance and activity in ground ice suggests a less hospitable microbial habitat.     

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.     

In situ spectroradiometric estimation of microalgal biomass in first-year sea ice

Summary First- and multi-year sea ice are colonized by microalgae, whose biomass modifies the spectral distribution of underice downwelling irradiance. It is proposed that an index of algal biomass in the first-year ice may be derived from the ratio of underice irradiance at a wavelength where absorption by chlorophyll a is high to a wavelength where absorption by the photosynthetic pigments is low and transmission through the ice is high. In southeastern Hudson Bay (Canadian Arctic), the irradiance ratio (671540 nm) accounts for 55% of the variance in chlorophyll a, indicating that the in situ biomass of algae in first-year ice can be estimated from spectral measurements of underice downwelling irradiance.Contribution to the programme of GIROQ (Groupe interuniversitaire de recherches océanographiques du Québec)     

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     

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.     

Molecular relationships of gammaridean amphipods from Arctic sea ice

The information on the biology and ecology of the Arctic sea ice-associated amphipods (Apherusa glacialis, Gammarus wilkitzkii, Onisimus glacialis, and O. nanseni) has increased, but their molecular taxonomic information still remains undisclosed. In the present study, we investigated long-range DNA sequences spanning 18S to 28S rDNA of these four sea ice-associated amphipods and analyzed their genetic relationships with other amphipod taxa. Variations of rDNA within the individuals of the same species were not detected. Phylogenetic analyses showed that each ice amphipod was separated, forming clusters with other conspecifics. Pairwise comparisons led to similar phylogenetic results, showing that the molecular taxonomy of the ice amphipods was in accordance with morphological systematics. In addition, these findings suggest that all four amphipods have little genetic variation compared with their morphologically defined conspecifics from temperate regions. Based on DNA taxonomy, G. wilkitzkii was supported as a species in good standing, refuting a recent synonymization with Gammarus duebeni. Considerably low genetic divergences of O. glacialis and O. nanseni in 18S, ITS, and 28S rDNA suggest the presence of population distinctions within species.     

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.     

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.     

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.     

In-situ observations on the distribution and behavior of amphipods and Arctic cod (Boreogadus saida) under the sea ice of the High Arctic Canada Basin

The occurrence and behavior of sympagic amphipods and Arctic cod (Boreogadus saida) were studied in the High Arctic Canada Basin by diving under the ice at seven stations in summer 2002. Still images of video-transects were used to obtain animal abundances and information on the structure of the ice environment. Mean amphipod abundances for the stations varied between 1 and 23 individuals m^–2, with an increase towards the western part of the basin. The standard deviation within the 31–51 images analyzed per station was small (<1 individual m^–2). Gammarus wilkitzkii was found in low abundances, often hiding in small ice gaps. Small amphipods (Onisimus spp., Apherusa glacialis, and juveniles of all species) tended to move freely along the bottom of the floes. B. saida occurred in narrow wedges of seawater along the edges of melting ice floes at three stations in water depths of 10–50 cm and was never found under the ice. The fish occurred in schools of 1–28 per wedge. Fish were inactive and did not escape the approaching diver. Resting in the wedges may be a strategy to reduce energetic requirements and avoid predators.We dedicate this publication to Professor Dr. J. Lenz (Kiel University).