Shine a light: Under-ice light and its ecological implications in a changing Arctic Ocean

The Arctic marine ecosystem is shaped by the seasonality of the solar cycle, spanning from 24-h light at the sea surface in summer to 24-h darkness in winter. The amount of light available for under-ice ecosystems is the result of different physical and biological processes that affect its path through atmosphere, snow, sea ice and water. In this article, we review the present state of knowledge of the abiotic (clouds, sea ice, snow, suspended matter) and biotic (sea ice algae and phytoplankton) controls on the underwater light field. We focus on how the available light affects the seasonal cycle of primary production (sympagic and pelagic) and discuss the sensitivity of ecosystems to changes in the light field based on model simulations. Lastly, we discuss predicted future changes in under-ice light as a consequence of climate change and their potential ecological implications, with the aim of providing a guide for future research.

Antarctic microalgae: physiological acclimation to environmental change

<p>Sea ice algal communities play a very significant role in primary production in the Southern Ocean, being the only source of fixed carbon for all other life in this habitat and contributing up to 22% of Antarctic primary production in ice-covered regions. Therefore it is important to understand how these organisms adapt to this highly variable and harsh environment Previous studies have described their acclimation to changes in environmental conditions but we still do not understand the physiological basis of these responses. This study examines the effects of varying levels of photosynthetically active radiation (PAR), ultraviolet-B (UV-B) radiation and temperature on bottom ice algal communities and individual algal species using pulse-amplitude modulation (PAM) fluorometry, the production of mycosporine-like amino acids (MAAs) and superoxide dismutase (SOD) activity. The experiments conducted in this thesis show that bottom ice algae are capable of acclimating to the higher levels of PAR and temperature that would likely be experienced during sea ice melt As temperature was increased past a threshold temperature of thylakoid integrity, it became the major stressor, causing decreases in photosynthetic yield at around 14°C, even at ambient PAR exposure. Similarly, a thylakoid integrity experiment independently suggested that the critical temperature for the onset of thylakoid damage was 14°C, which correlated well to the 14°C incubation observations, although this is a temperature that sea ice algae are unlikely to encounter in the polar regions. It is likely that sea ice algae produce additional MAAs, known to be cellular sunscreens, in response to increasing levels of UV-B, allowing tolerance of this stressor. This is the first study in the marine environment to demonstrate that algae can produce MAAs in response to increasing PAR and temperature, even in the absence of UV-B, indicating that MAAs may be more than just sunscreen compounds. The levels of UV-B used in this study were representative of those likely to be faced by the algae during sea ice melt. With increasing temperature, the algae maintained photosynthetic yield and decreased MAA production, implying that the rise in temperature aids the algae with another element of photoprotection such as enzymatic repair. As these results contrasted with previous studies of bottom ice algae that showed no additional MAA production in response to higher levels of PAR and UV-B, it was hypothesized that this difference was attributed to variations in species composition that could modify the productivity of the community. The short-term effects of increasing PAR and UV -B on three unialgal cultures of Thalassiosira sp., Fragilariopsis sp. (from the Ross Sea), and Chaetoceros sp. (from the Antarctic Peninsula) were therefore examined. In unialgal culture studies, these three algal species showed higher tolerance to PAR and UV-B compared to that of the mixed culture of bottom ice algae, although there remained species-specific variation. Both Ross Sea species showed increasing photosynthetic yield with increasing PAR and UV-B exposure, but there was a difference in the tolerance shown by the two species. Thalassiosira sp. tolerated higher PAR and lower UV-B and Fragilariopsis tolerated lower PAR and higher UV-B. Both species produced MAAs in response to these stressors, indicating that these compounds allowed the algae to decrease levels of photoinhibition. In comparison to the Ross Sea, the Antarctic Peninsula is an area of higher environmental variability and change, meaning that the species in both regions could have varying acclimatory capabilities. Although data from three species alone cannot conclusively demonstrate that algae from different regions have different acclimatory capabilities, they do illustrate considerable variation between species. Chaetoceros sp. from the Antarctic Peninsula region showed a higher tolerance to PAR and UV-B compared to the Ross Sea species. The former species showed an increase in photosynthetic yield in response to increasing PAR and this was accompanied by a lack of MAA production in response to the experimental levels of PAR, which indicates that the two Ross Sea species have a higher tolerance to PAR compared to the Antarctic Peninsula species. Chaetoceros sp. from the Antarctic Peninsula showed an increase in photosynthetic yield in response to high UV-B exposures, accompanied by MAA production and had no signs of photoinhibition. A further experiment was conducted to address the weaknesses in the initial methodologies, particularly related to control conditions in the short-term experiments. Common species from the Ross Sea, Antarctic Peninsula and the Arctic were exposed to a combination of increased PAR and UV-B over a period of seven days to compare acclimatory abilities using PAM and SOD activity. Thalassiosira antarctica from the Ross Sea, Chaetoceros socialis from the Antarctic Peninsula and C. socialis from the Arctic showed no significant change in quantum yield over the incubation period. This further highlights the importance of running experiments with compounding factors, as an increase in one factor could alleviate the negative effect of the other. There was an unexpected lack of change in SOD activity for all species under all treatments applied, which could indicate that the levels of PAR and UV-B used were not high enough to cause stress in these species. This work also points to the need to assay for various antioxidants, as algae are known to rely on a network of antioxidants in their defence against environmental stresses. The data from this thesis clarify the influence of PAR, UV-B and temperature on sea ice algae, and could help better evaluate the fate of these communities under various climate change scenarios. This study has made important steps towards understanding the acclimatory abilities of sea ice algae. Increasing knowledge of sea ice algal physiology, particularly of photosynthetic health in response to environmental change, will help improve predictions of productivity in the most productive ocean on this planet. Algal tolerance to increasing PAR, UV-B and temperature is remarkable, and this ability could be crucial in the context of future climate change. The productivity of these autotrophic microorganisms strongly influences secondary production that ties their fate to that of all other life in the Southern Ocean.</p>

Antarctic microalgae: physiological acclimation to environmental change

<p>Sea ice algal communities play a very significant role in primary production in the Southern Ocean, being the only source of fixed carbon for all other life in this habitat and contributing up to 22% of Antarctic primary production in ice-covered regions. Therefore it is important to understand how these organisms adapt to this highly variable and harsh environment Previous studies have described their acclimation to changes in environmental conditions but we still do not understand the physiological basis of these responses. This study examines the effects of varying levels of photosynthetically active radiation (PAR), ultraviolet-B (UV-B) radiation and temperature on bottom ice algal communities and individual algal species using pulse-amplitude modulation (PAM) fluorometry, the production of mycosporine-like amino acids (MAAs) and superoxide dismutase (SOD) activity. The experiments conducted in this thesis show that bottom ice algae are capable of acclimating to the higher levels of PAR and temperature that would likely be experienced during sea ice melt As temperature was increased past a threshold temperature of thylakoid integrity, it became the major stressor, causing decreases in photosynthetic yield at around 14°C, even at ambient PAR exposure. Similarly, a thylakoid integrity experiment independently suggested that the critical temperature for the onset of thylakoid damage was 14°C, which correlated well to the 14°C incubation observations, although this is a temperature that sea ice algae are unlikely to encounter in the polar regions. It is likely that sea ice algae produce additional MAAs, known to be cellular sunscreens, in response to increasing levels of UV-B, allowing tolerance of this stressor. This is the first study in the marine environment to demonstrate that algae can produce MAAs in response to increasing PAR and temperature, even in the absence of UV-B, indicating that MAAs may be more than just sunscreen compounds. The levels of UV-B used in this study were representative of those likely to be faced by the algae during sea ice melt. With increasing temperature, the algae maintained photosynthetic yield and decreased MAA production, implying that the rise in temperature aids the algae with another element of photoprotection such as enzymatic repair. As these results contrasted with previous studies of bottom ice algae that showed no additional MAA production in response to higher levels of PAR and UV-B, it was hypothesized that this difference was attributed to variations in species composition that could modify the productivity of the community. The short-term effects of increasing PAR and UV -B on three unialgal cultures of Thalassiosira sp., Fragilariopsis sp. (from the Ross Sea), and Chaetoceros sp. (from the Antarctic Peninsula) were therefore examined. In unialgal culture studies, these three algal species showed higher tolerance to PAR and UV-B compared to that of the mixed culture of bottom ice algae, although there remained species-specific variation. Both Ross Sea species showed increasing photosynthetic yield with increasing PAR and UV-B exposure, but there was a difference in the tolerance shown by the two species. Thalassiosira sp. tolerated higher PAR and lower UV-B and Fragilariopsis tolerated lower PAR and higher UV-B. Both species produced MAAs in response to these stressors, indicating that these compounds allowed the algae to decrease levels of photoinhibition. In comparison to the Ross Sea, the Antarctic Peninsula is an area of higher environmental variability and change, meaning that the species in both regions could have varying acclimatory capabilities. Although data from three species alone cannot conclusively demonstrate that algae from different regions have different acclimatory capabilities, they do illustrate considerable variation between species. Chaetoceros sp. from the Antarctic Peninsula region showed a higher tolerance to PAR and UV-B compared to the Ross Sea species. The former species showed an increase in photosynthetic yield in response to increasing PAR and this was accompanied by a lack of MAA production in response to the experimental levels of PAR, which indicates that the two Ross Sea species have a higher tolerance to PAR compared to the Antarctic Peninsula species. Chaetoceros sp. from the Antarctic Peninsula showed an increase in photosynthetic yield in response to high UV-B exposures, accompanied by MAA production and had no signs of photoinhibition. A further experiment was conducted to address the weaknesses in the initial methodologies, particularly related to control conditions in the short-term experiments. Common species from the Ross Sea, Antarctic Peninsula and the Arctic were exposed to a combination of increased PAR and UV-B over a period of seven days to compare acclimatory abilities using PAM and SOD activity. Thalassiosira antarctica from the Ross Sea, Chaetoceros socialis from the Antarctic Peninsula and C. socialis from the Arctic showed no significant change in quantum yield over the incubation period. This further highlights the importance of running experiments with compounding factors, as an increase in one factor could alleviate the negative effect of the other. There was an unexpected lack of change in SOD activity for all species under all treatments applied, which could indicate that the levels of PAR and UV-B used were not high enough to cause stress in these species. This work also points to the need to assay for various antioxidants, as algae are known to rely on a network of antioxidants in their defence against environmental stresses. The data from this thesis clarify the influence of PAR, UV-B and temperature on sea ice algae, and could help better evaluate the fate of these communities under various climate change scenarios. This study has made important steps towards understanding the acclimatory abilities of sea ice algae. Increasing knowledge of sea ice algal physiology, particularly of photosynthetic health in response to environmental change, will help improve predictions of productivity in the most productive ocean on this planet. Algal tolerance to increasing PAR, UV-B and temperature is remarkable, and this ability could be crucial in the context of future climate change. The productivity of these autotrophic microorganisms strongly influences secondary production that ties their fate to that of all other life in the Southern Ocean.</p>

Upwelling Irradiance below Sea Ice—PAR Intensities and Spectral Distributions

Upwelling and downwelling spectral (320–920 nm) distributions and photosynthetic active radiation (PAR) intensities were measured below a first-year land-fast sea ice in a western Greenland fjord with and without a snow cover. Time-series of surface upwelling PAR, downwelling PAR, and under-ice PAR were also obtained. Spectral distributions of upwelling and downwelling irradiances were similar except for reduced intensities in the UV, the red, and NIR parts of the spectrum when the ice was snow-covered. Upwelling PAR amounted to about 10% of downwelling intensities, giving 5.1 µmol photons m−2 s−1 at the bottom of the ice with a snow cover and 8.2 µmol photons m−2 s−1 without. PAR partitioning analyses showed that the upwelling was related to scattering by suspended particles in the water column. A snow melt increased under-ice daily maximum downwelling PAR from 50 to 180 µmol photons m−2 s−1 and overall under-ice PAR of 55 and 198 µmol photons m−2 s−1 with 10% upwelling. It is concluded that upwelling PAR below sea ice might be an important factor regarding sea ice algae photophysiology and performance with a 10% higher PAR; specifically when PAR > Ek the light saturation point of the sea ice algae.

Winter Carnivory and Diapause Counteract the Reliance on Ice Algae by Barents Sea Zooplankton

The Barents Sea is a hotspot for environmental change due to its rapid warming, and information on dietary preferences of zooplankton is crucial to better understand the impacts of these changes on food-web dynamics. We combined lipid-based trophic marker approaches, namely analysis of fatty acids (FAs), highly branched isoprenoids (HBIs) and sterols, to compare late summer (August) and early winter (November/December) feeding of key Barents Sea zooplankters; the copepods Calanus glacialis, C. hyperboreus and C. finmarchicus and the amphipods Themisto libellula and T. abyssorum. Based on FAs, copepods showed a stronger reliance on a diatom-based diet. Phytosterols, produced mainly by diatoms, declined from summer to winter in C. glacialis and C. hyperboreus, indicating the strong direct linkage of their feeding to primary production. By contrast, C. finmarchicus showed evidence of year-round feeding, indicated by the higher winter carnivory FA ratios of 18:1(n-9)/18:1(n-7) than its larger congeners. This, plus differences in seasonal lipid dynamics, suggests varied overwintering strategies among the copepods; namely diapause in C. glacialis and C. hyperboreus and continued feeding activity in C. finmarchicus. Based on the absence of sea ice algae-associated HBIs (IP25 and IPSO25) in the three copepod species during both seasons, their carbon sources were likely primarily of pelagic origin. In both amphipods, increased FA carnivory ratios during winter indicated that they relied strongly on heterotrophic prey during the polar night. Both amphipod species contained sea ice algae-derived HBIs, present in broadly similar concentrations between species and seasons. Our results indicate that sea ice-derived carbon forms a supplementary food rather than a crucial dietary component for these two amphipod species in summer and winter, with carnivory potentially providing them with a degree of resilience to the rapid decline in Barents Sea (winter) sea-ice extent and thickness. The weak trophic link of both zooplankton taxa to sea ice-derived carbon in our study likely reflects the low abundance and quality of ice-associated carbon during late summer and the inaccessibility of algae trapped inside the ice during winter.

Low Fe Availability for Photosynthesis of Sea-Ice Algae: Ex situ Incubation of the Ice Diatom Fragilariopsis cylindrus in Low-Fe Sea Ice Using an Ice Tank

Sea-ice algae play a crucial role in the ecology and biogeochemistry of sea-ice zones. They not only comprise the base of sea-ice ecosystems, but also seed populations of extensive ice-edge blooms during ice melt. Ice algae must rapidly acclimate to dynamic light environments, from the low light under sea ice to high light within open waters. Recently, iron (Fe) deficiency has been reported for diatoms in eastern Antarctic pack ice. Low Fe availability reduces photosynthetic plasticity, leading to reduced ice-algal primary production. We developed a low-Fe ice tank to manipulate Fe availability in sea ice. Over 20 days in the ice tank, the Antarctic ice diatom Fragilariopsis cylindrus was incubated in artificial low-Fe sea ice ([total Fe] = 20 nM) in high light (HL) and low light (LL) conditions. Melted ice was also exposed to intense light to simulate light conditions typical for melting ice in situ. When diatoms were frozen in, the maximum photochemical quantum efficiency of photosystem II (PSII), Fv/Fm, was suppressed by freezing stress. However, the diatoms maintained photosynthetic capability throughout the ice periods with a stable Fv/Fm value and increased photoprotection through non-photochemical quenching (NPQ) via photoprotective xanthophyll cycling (XC) and increased photoprotective carotenoid levels compared to pre-freeze-up. Photoprotection was more pronounced in the HL treatment due to greater light stress. However, the functional absorption cross section of PSII, σPSII, in F. cylindrus consistently increased after freezing, especially in the LL treatment (σPSII &gt; 10 nm2 PSII–1). Our study is the first to report such a large σPSII in ice diatoms at low Fe conditions. When the melted sea ice was exposed to high light, Fv/Fm was suppressed. NPQ and XC were slightly upregulated, but not to values normally observed when Fe is not limiting, which indicates reduced photosynthetic flexibility to adapt to environmental changes during ice melt under low Fe conditions. Although ice algae can optimize their photosynthesis to sea-ice environments, chronic Fe starvation led to less flexibility of photoacclimation, particularly in low light conditions. This may have detrimental consequences for ice algal production and trophic interactions in sea-ice ecosystems if the recent reduction in sea-ice extent continues.

Multiple Trophic Markers Trace Dietary Carbon Sources in Barents Sea Zooplankton During Late Summer

We investigated diets of 24 Barents Sea zooplankton taxa to understand pelagic food-web processes during late summer, including the importance of sea ice algae-produced carbon. This was achieved by combining insights derived from multiple and complementary trophic marker approaches to construct individual aspects of feeding. Specifically, we determined proportions of algal-produced fatty acids (FAs) to reflect the reliance on diatom- versus dinoflagellate-derived carbon, highly branched isoprenoid (HBI) lipids that distinguish between ice-associated and pelagic carbon sources, and sterols to indicate the degree of carnivory. Copepods had the strongest diatom signal based on FAs, while a lack of sea ice algae-associated HBIs (IP25, IPSO25) suggested that they fed on pelagic rather than ice-associated diatoms. The amphipod Themisto libellula and the ctenophores Beroë cucumis and Mertensia ovum had a higher contribution of dinoflagellate-produced FAs. There was a high degree of carnivory in this food web, as indicated by the FA carnivory index 18:1(n−9)/18:1(n−7) (mean value &lt; 1 only in the pteropod Clione limacina), the presence of copepod-associated FAs in most of the taxa, and the absence of algal-produced HBIs in small copepod taxa, such as Oithona similis and Pseudocalanus spp. The coherence between concentrations of HBIs and phytosterols within individuals suggested that phytosterols provide a good additional indication for algal ingestion. Sea ice algae-associated HBIs were detected in six zooplankton species (occurring in krill, amphipods, pteropods, and appendicularians), indicating an overall low to moderate contribution of ice-associated carbon from late-summer sea ice to pelagic consumption. The unexpected occurrence of ice-derived HBIs in pteropods and appendicularians, however, suggests an importance of sedimenting ice-derived material at least for filter feeders within the water column at this time of year.

Spatial and seasonal distribution of dissolved and particulate bioactive metals in Antarctic sea ice

Iron (Fe) has been shown to limit growth of marine phytoplankton in the Southern Ocean, regulating phytoplankton productivity and species composition, yet does not seem to limit primary productivity in Antarctic sea ice. Little is known, however, about the potential impact of other metals in controlling sea-ice algae growth. Here, we report on the distribution of dissolved and particulate cadmium (Cd), cobalt (Co), copper (Cu), manganese (Mn), nickel (Ni), and zinc (Zn) concentrations in sea-ice cores collected during 3 Antarctic expeditions off East Antarctica spanning the winter, spring, and summer seasons. Bulk sea ice was generally enriched in particulate metals but dissolved concentrations were similar to the underlying seawater. These results point toward an environment controlled by a subtle balance between thermodynamic and biological processes, where metal availability does not appear to limit sea-ice algal growth. Yet the high concentrations of dissolved Cu and Zn found in our sea-ice samples raise concern about their potential toxicity if unchelated by organic ligands. Finally, the particulate metal-to-phosphorus (P) ratios of Cu, Mn, Ni, and Zn calculated from our pack ice samples are higher than values previously reported for pelagic marine particles. However, these values were all consistently lower than the sea-ice Fe:P ratios calculated from the available literature, indicating a large accumulation of Fe relative to other metals in sea ice. We report for the first time a P-normalized sea-ice particulate metal abundance ranking of Fe &gt;&gt; Zn ≈ Ni ≈ Cu ≈ Mn &gt; Co ≈ Cd. We encourage future sea-ice work to assess cellular metal quotas through existing and new approaches. Such work, together with a better understanding of the nature of ligand complexation to different metals in the sea-ice environment, would improve the evaluation of metal bioavailability, limitation, and potential toxicity to sea-ice algae.

Rapid Manipulation in Irradiance Induces Oxidative Free-Radical Release in a Fast-Ice Algal Community (McMurdo Sound, Antarctica)

Sea ice supports a unique assemblage of microorganisms that underpin Antarctic coastal food-webs, but reduced ice thickness coupled with increased snow cover will modify energy flow and could lead to photodamage in ice-associated microalgae. In this study, microsensors were used to examine the influence of rapid shifts in irradiance on extracellular oxidative free radicals produced by sea-ice algae. Bottom-ice algal communities were exposed to one of three levels of incident light for 10 days: low (0.5 μmol photons m−2 s−1, 30 cm snow cover), mid-range (5 μmol photons m−2 s−1, 10 cm snow), or high light (13 μmol photons m−2 s−1, no snow). After 10 days, the snow cover was reversed (either removed or added), resulting in a rapid change in irradiance at the ice-water interface. In treatments acclimated to low light, the subsequent exposure to high irradiance resulted in a ~400× increase in the production of hydrogen peroxide (H2O2) and a 10× increase in nitric oxide (NO) concentration after 24 h. The observed increase in oxidative free radicals also resulted in significant changes in photosynthetic electron flow, RNA-oxidative damage, and community structural dynamics. In contrast, there was no significant response in sea-ice algae acclimated to high light and then exposed to a significantly lower irradiance at either 24 or 72 h. Our results demonstrate that microsensors can be used to track real-time in-situ stress in sea-ice microbial communities. Extrapolating to ecologically relevant spatiotemporal scales remains a significant challenge, but this approach offers a fundamentally enhanced level of resolution for quantifying the microbial response to global change.