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Review

Spatial Variability in the Primary Production Rates and Biomasses (Chl a) of Sea Ice Algae in the Canadian Arctic–Greenland Region: A Review

by
Laura Martín García
1,
Brian Sorrell
1,
Dorte Haubjerg Søgaard
1,2 and
Lars Chresten Lund-Hansen
1,*
1
Department of Biology, Arctic Research Center, Aquatic Biology, Aarhus University, 8000 Aarhus, Denmark
2
Greenland Climate Research Center, Greenland Institute of Natural Resources, 3900 Nuuk, Greenland
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2023, 11(11), 2063; https://doi.org/10.3390/jmse11112063
Submission received: 22 September 2023 / Revised: 25 October 2023 / Accepted: 26 October 2023 / Published: 28 October 2023
(This article belongs to the Section Marine Biology)
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Abstract

:
The aims of this review are to elucidate the spatial variation in the primary production rates and biomasses (Chl a) of sea ice algae in the Canadian Arctic–Greenland region, characterized by its comparable physical settings. A database was compiled from 30 studies of the production rates and biomasses (Chl a) of sea ice algae, the snow and ice thicknesses, ice types, nutrients (Si(OH)4, PO4, (NO3 + NO2)), and NH4 concentrations in the ice and below the ice from the region. Production rates were significantly higher (463 mg C m−2 d−1) in Resolute Bay and Northern Baffin Bay (317 mg C m−2 d−1), both in the Canadian Arctic, compared to a rate of 0.2 mg C m−2 d−1 in northeast Greenland. The biomasses reached 340 mg Chl a m−2 in Resolute Bay in comparison to 0.02 mg Chl a m−2 in southwest Greenland. Primary production at other Canadian and Greenland sites was comparable, but sea ice Chl a was higher (15.0 ± 13.4 mg Chl a m−2) at Canadian sites compared to Greenland ones (0.8 ± 0.5 mg Chl a m−2). Resolute and Northern Baffin Bay production rates were significantly higher when compared to other Arctic Ocean sites outside the studied region. The review concludes that the high production rates and biomasses in Resolute and Northern Baffin Bay are related to the inflow and mixing of nutrient-rich waters of Pacific origin. A conceptual model with drivers and inhibitors of the primary production of sea ice algae is proposed, and the database is compiled into a dataset of published data for further studies.

1. Introduction

Winter sea ice covers the entire Arctic Ocean, Canadian Archipelago, Hudson and Baffin Bays [1], and east and west Greenland [2] with a 15.9 × 106 km2 median maximum surface area during March [3]. In contrast, the aerial extent of the summer (June) sea ice in the Arctic Ocean has been decreasing since late 1970, from 12.5 × 106 km2 in 1980 to 10.6 × 106 km2 in 2022, equal to a loss of summer sea ice of 2.0 × 106 km2 [3,4,5]. The decrease in the extent of summer extent is mainly driven by increasing temperatures in the Arctic [6], and it is predicted that the Arctic Ocean will reach an ice-free state in summer within the next two decades [7]. From a biological point of view, sea ice is an ecosystem with defined pathways of matter and energy [8] with microorganisms, zooplankton, fish, seals, walruses, and polar bears, which rely and depend on sea ice for maintaining their life cycles [9]. Microorganisms living in the sea ice include bacteria [10], viruses [11], fungi [12], and heterotrophic and autotrophic protists [13]. Most of the autotrophic organisms such as sea ice algae are located at the ice–seawater interface [14,15] where biomasses can reach concentrations 50–100 times higher than concentrations of pelagic phytoplankton [16]. It has been estimated that sea ice algae contribute about 10% of the total marine-produced carbon in the Arctic Ocean [16]. The important ecological functioning of sea ice algae in polar marine ecosystems is to establish an early carbon source for planktonic grazers during the ice-covered winter and early spring [17,18]. Sea ice algae are later released from the melting ice and can seed the water column below the sea ice and ignite pelagic primary production [19,20] or sink to the bottom of the ocean where benthic living organisms can decompose the organic material [21]. Nevertheless, an initial literature-based survey of the primary production of sea ice algae revealed some significant differences in production rates among sites in the Canadian Arctic–Greenland region. This is exemplified by high rates of 463 mg C m−2 d−1 in Resolute Bay [22] and 317 mg C m−2 d−1 in Northern Baffin Bay [23] in the Canadian Arctic, compared to the 0.2 mg C m−2 d−1 in Young Sound, northeast Greenland [24]. Differences in production rates are also mirrored in the biomasses produced, from 340 mg Chl a m−2 in Resolute Bay [25] to 0.02 mg Chl a m−2 in Kapisillit, west Greenland [26]. Nonetheless, morphology, climatology, light, and oceanographic conditions in the region are comparable and generally similar. This raises the following questions, addressed in the present review: (1) Why are there significant spatial differences in the primary production rates and biomasses of sea ice algae in the Canadian Artic–Greenland region in spite of comparable physical settings, and (2) what are the driving forces of the differences? (3) Are the differences explained by differences in sea ice conditions, snow cover, nutrients in the ice and below the ice? The extended spatial variation in primary production is a conundrum considering the comparable physical settings in the region whereby drivers other than light [15] could not be part of the explanation. These questions are investigated by means of a literature study, where data have been extracted from a total of 30 studies from study sites in Hudson Bay, the Canadian Arctic Archipelago, and around Greenland (Figure 1). Data on study sites including position, time of sampling, methods applied for measuring primary production, ice types, ice and snow thickness, rates of primary production, and Chl a, were extracted with references and are provided in Table S1 (S1 in Supplementary Material). Data on nutrients Si(OH)4, PO4, (NO3 + NO2), NH4 concentrations in the ice and in the water below, and N:P ratios, are provided in Table S2 (S2 in Supplementary Material). All production rates and concentrations are given for the lower-most section (5–10 cm) of the ice. In the following text primary production is abbreviated (PP), as are Canadian Arctic (CA) and Greenland (GL), for brevity. Note the CA and GL refer to the two specific regions, and not any specific locality.

2. Physical and Biological Parameters of the Sea Ice

2.1. Ice, Snow, Production Rates, and Chl a

All CA samples were collected from land-fast first-year ice (FYI) except for two samplings in a mixture of pack and land-fast ice in northern BB and drift ice in FB, while all GL samples were collected from land-fast FYI. The sea ice thickness was high (1.44 ± 0.28 m) at CA sites and less than half that (0.63 ± 0.41 m) at GL sites except for YS (1.31 ± 0.42 m) (Figure 2a). Snow thickness was comparable at all sites except for 38 cm (FO) and 42 cm (YS) at a CA and GL site, respectively (Figure 2b). The highest average PP rates were found at the two CA sites RB (147 ± 19.1 mg C m−2 d−1) and Northern BB (97.1 ± 75.2 mg C m−2 d−1). The rates at the other CA sites, HB (3.05 ± 4.1 mg C m−2 d−1) and FB (4.5 ± 0.7 mg C m−2 d−1), were similar to the average PP at GL sites (4.5 ± 0.7 mg C m−2 d−1) (Figure 2c). The average sea ice Chl a concentration reached a maximum at the RB (79.9 mg m−2) CA site, with an average at the other CA sites—excluding RB—of 13.5 ± 12.7 mg m−2, but significantly higher than the average (0.8 ± 0.5 mg m−2) at the GL sites (Figure 2d)

2.2. Nutrients in Sea Ice and in the Water Below

Si(OH)4 in the ice reached between 2.0 and 4.0 µM L−1 at the CA sites, and similar at the GL sites, except for the high concentrations (8.9 µM L−1) at KL (Figure 2e). The below-sea-ice water’s average concentrations of Si(OH)4 were about three times higher (9.6 ± 3.1 µM L−1) than the in-ice concentrations (2.8 ± 1.0 µM L−1) at CA sites. Below-ice Si(OH)4 average concentrations at GL sites (6.4 ± 1.3 µM L−1) were just slightly higher compared to the Si(OH)4 in ice (4.9 ± 2.9 µM L−1) at the same sites (Figure 2e,f). PO4 concentrations in below-ice water were similar at all locations except for the low (0.01 µM L−1) PO4 concentration at KL (Figure 2g,h). The GL in-ice (NO3 + NO2) concentrations (2.9 ± 0.5 µM L−1) were comparable to the CA sites’ (2.5 ± 1.6 µM L−1) which were slightly higher than in below-ice water at both GL (5.0 ± 3.1 µM L−1) and CA sites (3.9 ± 3.3 µM L−1) (Figure 2i,j). The average N:P ratio was two times higher in CA sea ice (6.4 ± 6.3) compared to GL (3.0 ± 1.3), but comparable in the water in CA (5.0 ± 2.5) and GL (6.3 ± 5.0). Correlation analyses of physical and biological drivers regarding both PP and Chl a concentrations showed a statistically significant (p < 0.05) correlation between under-ice Si(OH)4 concentrations and PP rates (Table S3) (S3 in Supplementary Materials). Only a qualitative compilation of the composition of ice algae species from the study sites was possible, as only some studies provided this information, but this shows that diatoms were the most prevalent species at sites (Table S4) (S4 in Supplementary Materials).

2.3. Primary Production at Other Arctic sites

The average RB and northern BB PP rates were also higher than PP rates measured at other Arctic locations, including the central Arctic Ocean, the Beaufort Sea, Chukchi Sea, Beaufort Shelf, and the Baltic Sea (Table 1). The exception is a very high PP of 310 mg C m−2 d−1 in the central Arctic Ocean [27], exceeded only by a rate of 463 mg C m−2 d−1 measured in RB [22]. Studies outside the CA–GL region were not included in this review as they were obtained at shelf seas and more open water sites.

3. Discussion

There is a general Arctic seasonal signal in sea ice PP rates and Chl a, with low winter–early spring rates and Chl a concentrations which both reach a maximum in the transition from winter to spring [8,33]. All CA studies were carried out between April and June, where ice algae spring bloom occurs during early and late May at 70° N [33,35], whereas spring blooms occur earlier, around March–April, in southwest GL [36,37]. All samplings were carried out as time-series studies covering several weeks, which ensures that the seasonal variability in PP rates and biomasses (Chl a) were included in the studies. The use of core barrels, either SIPRE or Mark II Kovacs corers, for the sampling of ice cores in all studies further ensured comparability. The majority of the 30 independent studies were conducted on land-fast first-year ice (FYI) including all GL, and two CA FYI/pack ice and 1 land-fast/drifting ice, which emphasizes further the comparability between the studies and sites. There were no significant differences in biomass or PP rates between land-fast and pack ice locations, which is in line with [38], who found that maximum Chl a did not significantly differ between land-fast- and pack-ice stations. The 14C method [39] was applied in most of the studies with laboratory incubations of melted ice samples [40,41] in separate bottles inoculated with 14C in a light gradient and 2–4 h of incubation in most cases. The 2–4 h incubation time provides a PP rate between net and gross PP [42]. A study of in situ and laboratory-based 14C PP incubations showed some 10 times lower PP rates measured in situ compared to laboratory-based incubations [43]. Reasons for the significant differences are unclear and, accordingly, in situ data were excluded and only laboratory-based PP rates included, such as for Frobisher Bay in CA where PP rates were measured in situ [44]. The in situ Diving-PAM fluorometer [45], laboratory-based biomass accumulation rates [46], and O2 concentration changes [22,47] have been applied in the studies. These are all considered robust methods for estimating PP [48,49] and accordingly included in the review. The methodological variations and differences in analytical procedures between studies are accordingly considered of minor importance.
Light intensities at the bottom of the ice, where the majority of algae are located [15,38] are, apart from any seasonal variation in light, generally regulated by the sea ice and the snow cover, with its high albedo [50] and light attenuation coefficients [40]. It has been demonstrated that a decrease in snow cover thickness increased PP and photosynthetic performance [47,51] but other studies have not been able to establish any a clear relationship, e.g., [23] in northern BB. The role of snow in light transmittance was emphasized by [52], where the transition time from cold polar snow to melting snow increased transmittance and initiated an under-ice bloom. A sea ice algae spring bloom can also be inhibited by a sudden increase in under-ice light induced by manual snow clearing [15,37]. The present review showed no general correlations between the thickness of sea ice and snow relative to PP rates and biomasses. Study [53] discussed that the low PP rates in YS could be related to a thick (45.0 cm) snow cover, which might be the case here, though PP rates are still low at other GL sites with much lower (10.0 cm) snow thicknesses.
There were no specific patterns or relationships between the study locations and concentrations of nutrients, except for relatively high concentrations in below-ice water of both Si(OH)4 and (NO3 + NO2), whereas PO4 concentrations were on average higher in the ice than in the water. Accordingly, linkages between PP rates and nutrient concentrations can be complex. This is here illustrated by the very high (147 mg C m−2 d−1) average PP rates in RB and northern BB (97.1 mg C m−2 d−1), where low (0.05 µM L−1) and high (10.0 µM L−1) NO3 concentrations were measured in the water, respectively. In RB it was noted that “...NO3 concentrations were highly variable week to week, and obviously reflected the movement of different water masses…” [54]. A negative relationship between below-ice NO3 concentrations and bottom-ice Chl a biomass was found by [55], who related this to the uptake of nutrients by the algae. Stratification caused by the melting of sea ice can further reduce the flux of nutrients to the ice–ocean interface and reduce PP, as demonstrated for the central Arctic Ocean [56]. Due to stratification, it was suggested that nitrogen limitation was the main factor explaining the low concentrations of nitrogen in Dease Strait [47]. Nitrogen was also identified as the limiting nutrient in a study of algal growth in FB [46]. Across the entire dataset we found a significant (p < 0.05) correlation between average Si(OH)4 concentrations in the below-ice water and PP rates. This points towards Si(OH)4 as an important driver, which it has been shown to limit sea ice algae photosynthesis and blooms, especially at a later stage in a diatom-dominated bloom in FB [46].
There is a net flow of water from west to east through the CA Archipelago, driven by the higher sea levels in the Pacific Ocean, and these waters contain higher nutrient concentrations and especially Si(OH)4 compared to Atlantic waters [18]. Study [57] further showed a clear iron enrichment of the water column with the flow of water from the Pacific through the Barrow Strait, passing Resolute Bay and towards Baffin Bay. Iron was not measured in any of the present studies but as an important marine phytoplankton micronutrient [58,59], iron might have added to the high PP rates in RB and northern BB. Nonetheless, our compiled data showed that nutrient concentrations of Si(OH)4 and (NO3 + NO2) tended to be higher in the water below the ice at CA sites compared to GL sites, and especially for (NO3 + NO2) and PO4 in BB, although the differences were not statistically significant. A recent study in DS showed statistically significantly higher Chl a concentrations above a sill exposed to increased current speeds and mixing in a tidal strait [60]. The term “invisible polynyas’’ was applied to this phenomenon, as a reference to large-scale areas of open waters in the ice [61] which are often highly productive [62]. Accordingly, it is probable that the high RB PP rates are the combined result of the inflow of nutrient-rich water of Pacific origin [18] and the tidally generated mixing of the water masses above a sill in the Barrow Strait adjacent to Resolute Bay [18]. In comparison, northern BB locations were all located within the North Water Polynya, which one of the most productive of the Canadian polynyas [63,64]. This high production relies on the general circulation of nutrient-rich water masses of Pacific origin that flow into the northern Baffin Bay through the Nares Strait [65]. These water masses flow at relatively high current speeds of 0.20–0.35 m s−1 [66] and are also rich in Si(OH)4 and PO4 [65]. This strongly indicates that the very high northern BB PP rates are related to the flow of these nutrient-rich waters. Relatively high current speeds impede the development of a strong stratification below the sea ice, which inhibits the vertical flux of nutrients [56]. Sills are present at the entrances to NF and YS in GL, but apparently no tide generated the mixing of water and nutrients, while YS is additionally governed by the nutrient-depleted East Greenland Current [23,45]. The YS and the Kobberfjord and Kapisillit locations in NF are relatively small fjords with no through flow of nutrient-rich waters although nutrient concentrations in below-ice water are relatively high in NF [51].
Figure 3 shows a conceptual model of the main drivers of ice algae PP at the ice–water interface in the CA–GL Arctic region, where most of the ice algae are located [38]. The quantity of light that reaches the bottom of the sea ice for photosynthesis is controlled mainly by the thickness of the snow cover, its water content and age [52], and comparatively less by the physical properties of the ice itself [67]. Nutrients are taken up from the water column, where the horizontal supply of these is controlled by the advection of water masses, and the vertical supply is governed by the stratification of the water below the sea ice. Expulsion of the highly saline brine can also inhibit and reduce the photosynthetic performance of the sea ice algae [68]. This review pointed out that the high ice algae PP rates in parts of CA were related to the inflow of nutrient-rich water of Pacific origin, as compared to the very low production rates in East Greenland waters, where production rates are governed by the nutrient-low East Greenland Current arriving from the Arctic Ocean [45]. A second parameter is the vertical flux of nutrients to the bottom of the ice when a stratification of the water column is established by the melting of the ice, or an inflow of water with a lower density, which strongly inhibits the vertical mixing and thereby the flux of the nutrients towards the bottom of the sea ice [69]. Specifically, the weaker stratification enhances the vertical transport of nutrients towards ice algae, as observed in RB, where the mixing was promoted by sills [18]. The grazing by copepods and amphipods is a third parameter that can severely reduce ice algae biomasses [70], however, photosynthesis is not a factor.

4. Conclusions

There were some significant differences in the spatial distribution of the PP rates and biomasses of sea ice algae, as seen in RB and northern BB in CA, with their very high PP rates and biomasses. PP rates outside of RB and BB were similar in CA and GL, but the average Chl a beyond the two was higher in CA compared to GL. The RB and BB sites are the exceptions, and this review showed that the high PP rates and biomasses of sea ice algae were related to the large-scale, driven inflow and mixing of nutrient-rich waters of Pacific origin. Waters were mixed by stronger currents above sills and in straits that generated a high flux of nutrients towards the bottom of the sea ice, which sustained the high PP rates. In spite of the general focus on light as a driver of sea ice algae PP, we conclude that advection and mixing of nutrient-rich water masses are also important drivers.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jmse11112063/s1, Table S1: Geographical area, reference, location, sampling period, method, ice type, ice thickness, snow depth, primary production, and Chl a. Table S2: Geographical area, samplig period, SiO2, PO4, NO3 + NO2, NH4, N:P, reference. Table S3: Pearson correlation coefficients linking physico-chemical parameters to primary production (PP) and chlorophyll a concentration (Chl a). Table S4: Dominant ice algal species as reported in the primary production studies. References [71,72,73,74,75,76,77,78,79] are citied in the Supplementary Materials.

Author Contributions

L.C.L.-H. and L.M.G., conceptualization; writing—original draft preparation; B.S. and D.H.S., writing—review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This paper was conceived and developed in the framework of the project FACE-IT (The Future of Arctic Coastal Ecosystems—Identifying Transitions in Fjords and Adjacent Coastal Areas). FACE-IT has received funding from the European Union’s Horizon 2020 research and innovation program under grant agreement No. 869154. This is a contribution to the Arctic Science Partnership (ASP) asp-net.org.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

No new data were created in this study, and data sharing is not applicable to this article.

Conflicts of Interest

All authors declare that they have no conflicts of interest.

References

  1. Wratten, E.E.; Cooley, S.W.; Mann, P.J.; Whalen, D.; Fraser, P.; Lim, M. Physiographic controls on landfast ice variability from 20 years of maximum extents across the Northwest Canadian Arctic. MDPI Open Access J. 2022, 14, 2175. [Google Scholar] [CrossRef]
  2. Karami, M.P.; Myers, P.G.; de Vernal, A.; Tremblay, L.B.; Hu, X. The role of Arctic gateways on sea ice and circulation in the Arctic and North Atlantic Oceans: A sensitivity study with an ocean-sea-ice model. Clim. Dyn. 2021, 57, 2129–2151. [Google Scholar] [CrossRef]
  3. Francis, J.A.; Wu, B. Why has no new record-minimum Arctic sea-ice extent occurred since September 2012? Environ. Res. Lett. 2020, 15, 114034. [Google Scholar] [CrossRef]
  4. Parkinson, C.L. Spatially mapped reductions in the length of the Arctic sea ice season. Geophys. Res. Lett. 2014, 41, 4316–4322. [Google Scholar] [CrossRef] [PubMed]
  5. Jeong, H.; Park, H.; Stuecker, M.F.; Yeh, S. Record low Arctic sea ice extent in 2012 linked to two-year La Niña-driven sea surface temperature pattern. Geophys. Res. Lett. 2022, 49, e2022GL098385. [Google Scholar] [CrossRef]
  6. Steiner, N.S.; Bowman, J.; Campbell, K.; Chierici, M.; Eronen-Rasimus, E.; Falardeau, M.; Flores, H.; Fransson, A.; Herr, H.; Insley, S.J.; et al. Climate change impacts on sea-ice ecosystems and associated ecosystem services. Elem. Sci. Anthr. 2021, 9, 00007. [Google Scholar] [CrossRef]
  7. Jahn, A.; Kay, J.E.; Holland, M.M.; Hall, D.M. How predictable is the timing of a summer ice-free Arctic? Geophys. Res. Lett. 2016, 43, 9113–9120. [Google Scholar] [CrossRef]
  8. Lund-Hansen, L.C.; Søgaard, D.H.; Sorrell, B.K.; Gradinger, R.; Meiners, K.M. Arctic Sea Ice Ecology; Springer: Berlin, Germany, 2020; p. 178. Available online: https://link.springer.com/book/10.1007/978-3-030-37472-3 (accessed on 28 October 2023).
  9. Kohlbach, D.; Schaafsma, F.L.; Graeve, M.; Lebreton, B.; Lange, B.A.; David, C.; Vortkamp, M.; Flores, H. Strong linkage of polar cod (Boreogadus saida) to sea ice algae-produced carbon: Evidence from stomach content, fatty acid and stable isotope analyses. Prog. Oceanogr. 2017, 152, 62–74. [Google Scholar] [CrossRef]
  10. Kaartokallio, H.; Søgaard, D.; Norman, L.; Rysgaard, S.; Tison, J.L.; Delille, B.; Thomas, D.N. Short-term variability in bacterial abundance, cell properties, and incorporation of leucine and thymidine in subarctic sea ice. Aquat. Microb. Ecol. 2013, 71, 57–73. [Google Scholar] [CrossRef]
  11. Luthanen, A.; E-Rasimus, E.; Oksanen, H.A.; Tison, J.-L.; Delille, B.; Dieckmann, G.; Rintala, J.-M.; Bamford, D.H. The first known virus isolates from Antarctic sea ice have complex infection patterns. FEMS Microbiol. Ecol. 2017, 94, 2018. [Google Scholar] [CrossRef]
  12. Hassett, B.T.; Ducluzeau, A.L.L.; Collins, R.E.; Gradinger, R. Spatial distribution of aquatic marine fungi across the western Arctic and sub-arctic. Environ. Microbiol. 2017, 19, 475–484. [Google Scholar] [CrossRef]
  13. Bluhm, B.A.; Swadling, K.M.; Gradinger, R. Sea Ice, 3rd ed.; Thomas, D.N., Ed.; Wiley Blackwell: Oxford, UK, 2017; 652p. [Google Scholar]
  14. Horner, R.; Schrader, G. Relative contributions of ice algae, phytoplankton, and benthic microalgae to primary production in nearshore regions of the Beaufort Sea. ARCTIC 1982, 35, 485–503. [Google Scholar] [CrossRef]
  15. Lund-Hansen, L.C.; Hawes, I.; Hancke, K.; Salmansen, N.; Nielsen, J.R.; Balslev, L.; Sorrell, B.K. Effects of increased irradiance on biomass, photobiology, nutritional quality, and pigment composition of Arctic sea ice algae. Mar. Ecol. Prog. Ser. 2020, 648, 95–110. [Google Scholar] [CrossRef]
  16. Arrigo, K. Sea ice as a habitat for primary producers. In Sea Ice, 3rd ed.; Thomas, D.N., Ed.; Wiley Blackwell: Oxford, UK, 2017; 652p. [Google Scholar]
  17. Michel, C.; Nielsen, T.G.; Nozais, C.; Gosselin, M. Significance of sedimentation and grazing by ice micro- and meiofauna for carbon cycling in annual sea ice (northern Baffin Bay). Aquat. Microb. Ecol. 2002, 30, 57–68. [Google Scholar] [CrossRef]
  18. Michel, C.; Ingram, R.; Harris, L. Variability in oceanographic and ecological processes in the Canadian Arctic Archipelago. Prog. Oceanogr. 2006, 71, 379–401. [Google Scholar] [CrossRef]
  19. Michel, C.; Legendre, L.; Therriault, J.-C.; Demers, S.; Vandevelde, T. Springtime coupling between ice algal and phytoplankton assemblages in southeastern Hudson Bay, Canadian Arctic. Polar Biol. 1993, 13, 441–449. [Google Scholar] [CrossRef]
  20. Olsen, L.M.; Laney, S.R.; Duarte, P.; Kauko, H.M.; Fernández-Méndez, M.; Mundy, C.J.; Rösel, A.; Meyer, A.; Itkin, P.; Cohen, L.; et al. The seeding of ice algal blooms in Arctic pack ice: The multiyear ice seed repository hypothesis. J. Geophys. Res. Biogeosciences 2017, 122, 1529–1548. [Google Scholar] [CrossRef]
  21. Boetius, A.; Albrecht, S.; Bakker, K.; Bienhold, C.; Felden, J.; Fernández-Méndez, M.; Hendricks, S.; Katlein, C.; Lalande, C.; Krumpen, T.; et al. Export of Algal Biomass from the Melting Arctic Sea Ice. Science 2013, 339, 1430–1432. [Google Scholar] [CrossRef]
  22. Smith, R.E.H.; Anning, J.; Pierre Clement Cota, G. Abundance and production of ice algae in Resolute Passage, Canadian Arctic. Mar. Ecol. Prog. 1988, 48, 251–263. [Google Scholar] [CrossRef]
  23. Nozais, C.; Gosselin, M.; Michel, C.; Tita, G. Abundance, biomass, composition and grazing impact of the sea-ice meiofauna in the North Water, northern Baffin Bay. Mar. Ecol. Prog. Ser. 2001, 217, 235–250. [Google Scholar] [CrossRef]
  24. Rysgaard, S.; Nielsen, T.G.; Hansen, B.W. Seasonal variation in nutrients, pelagic primary production and grazing in a high-Arctic coastal marine ecosystem, Young Sound, Northeast Greenland. Mar. Ecol. Prog. Ser. 1999, 179, 13–25. [Google Scholar] [CrossRef]
  25. Smith, R.E.H.; Herman, A.W. Productivity of sea ice algae: In situ vs. incubator methods. J. Mar. Syst. 1991, 2, 97–110. [Google Scholar] [CrossRef]
  26. Lund-Hansen, L.C.; Petersen, C.M.; Søgaard, D.H.; Sorrell, B.K. A Comparison of Decimeter Scale Variations of Physical and Photobiological Parameters in a Late Winter First-Year Sea Ice in Southwest Greenland. J. Mar. Sci. Eng. 2021, 9, 60. [Google Scholar] [CrossRef]
  27. Gosselin, M.; Levasseur, M.; Wheeler, P.A.; Horner, R.A.; Booth, B.C. New measurements of phytoplankton and ice algal production in the Arctic Ocean. Deep. Sea Res. Part II Top. Stud. Oceanogr. 1997, 44, 1623–1644. [Google Scholar] [CrossRef]
  28. Booth, J. The epontic algal community of the ice edge zone and its significance to the Davis Strait ecosystem. ARCTIC 1984, 37, 234–243. [Google Scholar] [CrossRef]
  29. Dupont, F. Impact of sea-ice biology on overall primary production in a biophysical model of the pan-Arctic Ocean. J. Geophys. Res. Oceans 2012, 117, COOD17. [Google Scholar] [CrossRef]
  30. Fernández-Méndez, M.; Katlein, C.; Rabe, B.; Nicolaus, M.; Peeken, I.; Bakker, K.; Flores, H.; Boetius, A. Photosynthetic production in the central Arctic Ocean during the record sea-ice minimum in 2012. Biogeosciences 2015, 12, 3525–3549. [Google Scholar] [CrossRef]
  31. Gradinger, R. Sea-ice algae: Major contributors to primary production and algal biomass in the Chukchi and Beaufort Seas during May/June 2002. Deep. Sea Res. Part II Top. Stud. Oceanogr. 2009, 56, 1201–1212. [Google Scholar] [CrossRef]
  32. Haecky, P.; Andersson, A. Primary and bacterial production in sea ice in the northern Baltic Sea. Aquat. Microb. Ecol. 1999, 20, 107–118. [Google Scholar] [CrossRef]
  33. Horner, R.; Ackley, S.F.; Dieckmann, G.S.; Gulliksen, B.; Hoshiai, T.; Legendre, L.; Melnikov, I.A.; Reeburgh, W.S.; Spindler, M.; Sullivan, C.W. Ecology of sea ice biota. Polar Biol. 1992, 12, 417–427. [Google Scholar] [CrossRef]
  34. Mock, T.; Gradinger, R.R. Determination of Arctic ice algal production with a new in situ incubation technique. Mar. Ecol. Prog. Ser. 1999, 177, 15–26. [Google Scholar] [CrossRef]
  35. Mundy, C.J.; Gosselin, M.; Gratton, Y.; Brown, K.; Galindo, V.; Campbell, K.; Levasseur, M.; Barber, D.; Papakyriakou, T.; Bélanger, S. Role of environmental factors on phytoplankton bloom initiation under landfast sea ice in Resolute Passage, Canada. Mar. Ecol. Prog. Ser. 2014, 497, 39–49. [Google Scholar] [CrossRef]
  36. Mikkelsen, D.M.; Rysgaard, S.; Glud, R.N. Microalgal composition and primary production in Arctic sea ice: A seasonal study from Kobbefjord (Kangerluarsunnguaq), West Greenland. Mar. Ecol. Prog. Ser. 2008, 368, 65–74. [Google Scholar] [CrossRef]
  37. Lund-Hansen, L.C.; Hawes, I.; Sorrell, B.K.; Nielsen, M.H. Removal of snow cover inhibits spring growth of Arctic ice algae through physiological and behavioral effects. Polar Biol. 2014, 37, 471–481. [Google Scholar] [CrossRef]
  38. Leu, E.; Mundy, C.; Assmy, P.; Campbell, K.; Gabrielsen, T.; Gosselin, M.; Juul-Pedersen, T.; Gradinger, R. Arctic spring awakening–Steering principles behind the phenology of vernal ice algal blooms. Prog. Oceanogr. 2015, 139, 151–170. [Google Scholar] [CrossRef]
  39. Nielsen, E.S. The use of radio-active carbon (14C) for measuring organic production in the sea. ICES J. Mar. Sci. 1952, 18, 117–140. [Google Scholar] [CrossRef]
  40. Lund-Hansen, L.C.; Hawes, I.; Nielsen, M.H.; Dahllöf, I.; Sorrell, B.K. Summer meltwater and spring sea ice primary production, light climate and nutrients in an Arctic estuary, Kangerlussuaq, west Greenland. Arctic Antarct. Alp. Res. 2018, 50, S100025. [Google Scholar] [CrossRef]
  41. Matthes, L.; Ehn, J.; Dalman, L.; Babb, D.; Peeken, I.; Harasyn, M.; Kirillov, S.; Lee, J.; Bélanger, S.; Tremblay, J.; et al. Environmental drivers of spring primary production in Hudson Bay. Elementa Sci. Anthr. 2021, 9, 00160. [Google Scholar] [CrossRef]
  42. Sanz-Martín, M.; Vernet, M.; Cape, M.R.; Mesa, E.; Delgado-Huertas, A.; Reigstad, M.; Wassmann, P.; Duarte, C.M. Relationship Between Carbon- and Oxygen-Based Primary Productivity in the Arctic Ocean, Svalbard Archipelago. Front. Mar. Sci. 2019, 6, 468. [Google Scholar] [CrossRef]
  43. Bergmann, M.; Welch, H.; Butler-Walker, J.; Siferd, T. Ice algal photosynthesis at Resolute and Saqvaqjuac in the Canadian Arctic. J. Mar. Syst. 1991, 2, 43–52. [Google Scholar] [CrossRef]
  44. Hsiao, S. Spatial and seasonal variations in primary production of sea ice microalgae and phytoplankton in Frobisher Bay, Arctic Canada. Mar. Ecol. Prog. Ser. 1988, 44, 275–285. [Google Scholar] [CrossRef]
  45. Rysgaard, S.; Kühl, M.; Glud, R.N.; Hansen, J.W. Biomass, production and horizontal patchiness of sea ice algae in a high-Arctic fjord (Young Sound, NE Greenland). Mar. Ecol. Prog. Ser. 2001, 223, 15–26. [Google Scholar] [CrossRef]
  46. Riedel, A.; Michel, C.; Gosselin, M.; LeBlanc, B. Winter–spring dynamics in sea-ice carbon cycling in the coastal Arctic Ocean. J. Mar. Syst. 2008, 74, 918–932. [Google Scholar] [CrossRef]
  47. Campbell, K.; Mundy, C.; Landy, J.; Delaforge, A.; Michel, C.; Rysgaard, S. Community dynamics of bottom-ice algae in Dease Strait of the Canadian Arctic. Prog. Oceanogr. 2016, 149, 27–39. [Google Scholar] [CrossRef]
  48. Rysgaard, S.; Glud, R.N.; Sejr, M.K.; Blicher, M.E.; Stahl, H.J. Denitrification activity and oxygen dynamics in Arctic sea ice. Polar Biol. 2007, 31, 527–537. [Google Scholar] [CrossRef]
  49. Glud, R.N.; Rysgaard, S.; Kühl, M. A laboratory study on O2 dynamics and photosynthesis in ice algal communities: Quantification by microsensors, O2 exchange rates, 14C incubations and a PAM fluorometer. Aquat. Microb. Ecol. 2002, 27, 301–311. [Google Scholar] [CrossRef]
  50. Perovich, D.; Cota, G.; Maykut, G.; Grenfell, T. Bio-optical observations of first-year Arctic sea ice. Geophys. Res. Lett. 1993, 20, 1059–1062. [Google Scholar] [CrossRef]
  51. Søgaard, D.H.; Kristensen, M.; Rysgaard, S.; Glud, R.N.; Hansen, P.J.; Hilligsøe, K.M. Autotrophic and heterotrophic activity in Arctic first-year sea ice: Seasonal study from Malene Bight, SW Greenland. Mar. Ecol. Prog. Ser. 2010, 419, 31–45. [Google Scholar] [CrossRef]
  52. Hancke, K.; Lund-Hansen, L.C.; Lamare, M.L.; Pedersen, S.H.; King, M.D.; Andersen, P.; Sorrell, B.K. Extreme low light requirement for algae growth underneath sea ice: A case study from Station Nord, NE Greenland. J. Geophys. Res. Oceans 2018, 123, 985–1000. [Google Scholar] [CrossRef]
  53. Glud, R.N.; Rysgaard, S.; Kühl, M.; Hansen, J.W. The sea ice in Young Sound: Implications for carbon cycling. Carbon cycling in Arctic marine ecosystems: Case study Young Sound. Meddr. Grønland 2007, 58, 62–85. [Google Scholar]
  54. Welch, H.E.; Bergmann, M.A. Seasonal development of ice algae and its prediction from environmental factors near Resolute, NWT, Canada. Can. J. Fish. Aquat. Sci. 1989, 46, 1793–1804. [Google Scholar] [CrossRef]
  55. Rózanska, M.; Gosselin, M.; Poulin, M.; Wiktor, J.M.; Michel, C. Influence of environmental factors on the development of bottom ice protist communities during the winter–spring transition. Mar. Ecol. Prog. Ser. 2009, 386, 43–59. [Google Scholar] [CrossRef]
  56. Lund-Hansen, L.C.; Bendtsen, J.; Stratmann, T.; Tonboe, R.; Olsen, S.M.; Markager, S.; Sorrell, B.K. Will low primary production rates in the Amundsen Basin (Arctic Ocean) remain low in a future ice-free setting, and what governs this production? J. Mar. Syst. 2020, 205, 103287. [Google Scholar] [CrossRef]
  57. Colombo, M.; Jackson, S.L.; Cullen, J.T.; Orians, K.J. Dissolved iron and manganese in the Canadian Arctic Ocean: On the biogeochemical processes controlling their distributions. Geochim. et Cosmochim. Acta 2020, 277, 150–174. [Google Scholar] [CrossRef]
  58. Kanna, N.; Toyota, T.; Nishioka, J. Iron and macro-nutrient concentrations in sea ice and their impact on the nutritional status of surface waters in the southern Okhotsk Sea. Prog. Oceanogr. 2014, 126, 44–57. [Google Scholar] [CrossRef]
  59. Yoshida, K.; Seger, A.; Karsh, K.; Corkill, M.; Heil, P.; McMinn, A.; Suzuki, K. 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. Front. Mar. Sci. 2021, 8, 221. [Google Scholar] [CrossRef]
  60. Dalman, L.A.; Else, B.G.T.; Barber, D.; Carmack, E.; Williams, W.J.; Campbell, K.; Duke, P.J.; Kirillov, S.; Mundy, C.J.; Tremblay, J.-É. Enhanced bottom-ice algal biomass across a tidal strait in the Kitikmeot Sea of the Canadian Arctic. Elementa Sci. Anthr. 2019, 7, 22. [Google Scholar] [CrossRef]
  61. Hannah, C.G.; Dupont, F.; Dunphy, M. Polynyas and tidal currents in the Canadian Arctic Archipelago. ARCTIC 2009, 62, 83–95. [Google Scholar] [CrossRef]
  62. Smith, W.O., Jr.; Barber, D. (Eds.) Polynyas: Windows to the World; Elsevier Oceanography Series; Elsevier: Amsterdam, The Netherlands, 2007; Volume 74, p. 474. [Google Scholar]
  63. Stirling, I. The importance of polynyas, ice edges, and leads to marine mammals and birds. J. Mar. Syst. 1997, 10, 9–21. [Google Scholar] [CrossRef]
  64. Klein, B.; LeBlanc, B.; Mei, Z.-P.; Beret, R.; Michaud, J.; Mundy, C.-J.; von Quillfeldt, C.H.; Garneau, M.-È.; Roy, S.; Gratton, Y.; et al. Phytoplankton biomass, production and potential export in the North Water. Deep. Sea Res. Part II Top. Stud. Oceanogr. 2002, 49, 4983–5002. [Google Scholar] [CrossRef]
  65. Tremblay, J.; Gratton, Y.; Carmack, E.C.; Payne, C.D.; Price, N.M. Impact of the large-scale Arctic circulation and the North Water Polynya on nutrient inventories in Baffin Bay. J. Geophys. Res. Ocean. 2002, 107, 26-21–26-14. [Google Scholar] [CrossRef]
  66. Ingram, R.G.; Bâcle, J.; Barber, D.G.; Gratton, Y.; Melling, H. An overview of physical processes in the North Water. Deep. Sea Res. Part II Top. Stud. Oceanogr. 2002, 49, 4893–4906. [Google Scholar] [CrossRef]
  67. Perovich, D.K. Sea ice and sunlight. In Sea Ice, 3rd ed.; Thomas, D.N., Ed.; Wiley Blackwell: Oxford, UK, 2017; pp. 110–137, 652. [Google Scholar] [CrossRef]
  68. Yoshida, K.; Seger, A.; Kennedy, F.; McMinn, A.; Suzuki, K. Freezing, melting, and light stress on the photophysiology of ice algae ex situ incubation of the ice algae diatom Fragilariaopsis cylindrus (Bacillariophyceae) using an ice tank. J. Phycol. 2020, 56, 1323–1338. [Google Scholar] [CrossRef]
  69. Randelhoff, A.; Fer, I.; Sundfjord, A.; Tremblay, J.-E.; Reigstad, M. Vertical fluxes of nitrate in the seasonal nitracline of the Atlantic Sector of the Arctic Ocean. J. Geophys. Res. Oceans 2016, 121, 5282–5295. [Google Scholar] [CrossRef]
  70. Sampei, M.; Fortier, L.; Raimbault, P.; Matsuno, K.; Vet, Y.; Quéguiner LaFond, A.; Babin, M.; Hirawake, T. An esti-mation of the quantitative impacts of copepod grazing on an under sea-ice spring phytoplabnkton bloom in western Baffin Bay, Canadian Arctic. Elem. Sci. Anthr. 2021, 9, 00092. [Google Scholar] [CrossRef]
  71. Dunbar, M.J.; Acreman, J.C. Standing crops and species composition of diatoms in sea ice From Robeson Channel to the Gulf of St. Lawrence. Ophelia 1980, 19, 61–72. [Google Scholar] [CrossRef]
  72. Pineault, S.; Tremblay, J.E.; Gosselin, M.; Thomas, H.; Shadwick, E. The isotopic signature of particulate factors and applications for tracing the fate of ice-algae in the Arctic Ocean. J. Geophys. Res. Oceans 2013, 118, 287–300. [Google Scholar] [CrossRef]
  73. Søgaard, D.H.; Sorrell, B.K.; Sejr, M.K.; Andersen, P.; Rysgaard, S.; Hansen, P.J.; Skyttä, A.; Lemcke, S.; Lund-Hansen, L.C. An under-ice bloom of mixotrophic haptophytes in low nutrient and freshwater-influenced Arctic waters. Sci. Rep. 2021, 11, 2915. [Google Scholar] [CrossRef]
  74. Søgaard, D.H.; Thomas, D.N.; Rysgaard, S.; Glud, R.N.; Norman, L.; Kaartokallio, H.; Juul-Pedersen, T.; Geilfus, N.-X. The relative contributions of biological and abiotic processes to carbon dynamics in subarctic sea ice. Polar Biol. 2013, 36, 1761–1777. [Google Scholar] [CrossRef]
  75. Andersen, O.G.N. Primary production associated with sea ice at Godhavn, Disko, West Greenland. Ophelia 1977, 16, 205–220. [Google Scholar] [CrossRef]
  76. Gosselin, M.; Legendre, L.; Therriault, J.C.; Demers, S. Light and nutrient limitation of sea-ice microalgae (Hudson Bay, Canadian Arctic). J. Phycol. 1990, 26, 220–232. [Google Scholar] [CrossRef]
  77. Gosselin, M.; Legendre, L.; Demers, S.; Ingram, R. Responses of sea-ice microalgae to climatic and fortnightly tidal energy inputs (Manitounuk Sound, Hudson Bay). Can. J. Fish. Aquat. Sci. 1985, 42, 999–1006. [Google Scholar] [CrossRef]
  78. Lehmann, N.; Kienast, M.; Granger, J.; Bourbonnais, A.; Altabet, M.A.; Tremblay, J. Remote Western Arctic nutrients fuel remineralization in Deep Baffin Bay. Glob. Biogeochem. Cycles 2019, 33, 649–667. [Google Scholar] [CrossRef]
  79. Lewis, E.L.; Ponton, D.; Legendre, L.; Leblanc, B. Springtime sensible heat, nutrients and phytoplankton in the Northwater Polynya, Canadian Arctic. Cont. Shelf Res. 1996, 16, 1775–1792. [Google Scholar] [CrossRef]
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Figure 1. Study sites (red circles) and names of locations, which are abbreviated in the text as: Franklin Bay (FB), Dease Strait (DS), Resolute Bay (RB), Northern Baffin Bay (BB), Robeson Channel (RC), Hudson Bay (HB), Frobisher Bay (FO), Disko Island (Di), Kangerlussuaq (KL), and Young Sound (YS). Nuuk Fjord (NF) comprises Malene Bight, Kapisillit, and Kobberfjord.
Figure 1. Study sites (red circles) and names of locations, which are abbreviated in the text as: Franklin Bay (FB), Dease Strait (DS), Resolute Bay (RB), Northern Baffin Bay (BB), Robeson Channel (RC), Hudson Bay (HB), Frobisher Bay (FO), Disko Island (Di), Kangerlussuaq (KL), and Young Sound (YS). Nuuk Fjord (NF) comprises Malene Bight, Kapisillit, and Kobberfjord.
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Figure 2. Data compiled from the literature, with data given in Tables S1 and S2. Average ± s.d. sea ice thickness (a), snow thickness (b), primary production (c), Chl a (d), Si(OH)4 in ice (e), Si(OH)4 in water (f), PO4 in ice (g), PO4 in water (h), (NO3 + NO2) in ice (i), and (NO3 + NO2) in water (j) at locations with abbreviations as in Figure 1. In water means that water was sampled 1–2 m below the sea ice. Note that numbers for Nuuk Fjord (NF) are averages comprising the three locations—Kapisillit, Malene Bight, and Kobberfjord. Data for each of these three locations are given in Tables S1 and S2. The * signifies that the parameter or component was not measured at that specific location.
Figure 2. Data compiled from the literature, with data given in Tables S1 and S2. Average ± s.d. sea ice thickness (a), snow thickness (b), primary production (c), Chl a (d), Si(OH)4 in ice (e), Si(OH)4 in water (f), PO4 in ice (g), PO4 in water (h), (NO3 + NO2) in ice (i), and (NO3 + NO2) in water (j) at locations with abbreviations as in Figure 1. In water means that water was sampled 1–2 m below the sea ice. Note that numbers for Nuuk Fjord (NF) are averages comprising the three locations—Kapisillit, Malene Bight, and Kobberfjord. Data for each of these three locations are given in Tables S1 and S2. The * signifies that the parameter or component was not measured at that specific location.
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Figure 3. Conceptual model of the main drivers of the primary production of sea ice algae at the sea ice–water interface.
Figure 3. Conceptual model of the main drivers of the primary production of sea ice algae at the sea ice–water interface.
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Table 1. Ranges of primary production of sea ice algae from RB (Resolute Bay) and northern BB (Baffin Bay), and other Arctic locations.
Table 1. Ranges of primary production of sea ice algae from RB (Resolute Bay) and northern BB (Baffin Bay), and other Arctic locations.
LocationProduction Rate (mg C m−2 d−1)Reference
Davis Strait0.003–2.3[28]
Pan Arctic PP model60–1[29]
Arctic Ocean5.8[30]
Arctic Ocean0.5–310[27]
Chukchi Sea20–30[31]
Beaufort Sea4–9[31]
Baltic Sea1.0–2.4[32]
Beaufort Sea2.8–11.2[33]
Greenland Sea0.25–1.71[34]
Resolute Bay (RB)20.6–469[25]
Northern Baffin Bay (BB)26.3–317[23]
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García, L.M.; Sorrell, B.; Søgaard, D.H.; Lund-Hansen, L.C. Spatial Variability in the Primary Production Rates and Biomasses (Chl a) of Sea Ice Algae in the Canadian Arctic–Greenland Region: A Review. J. Mar. Sci. Eng. 2023, 11, 2063. https://doi.org/10.3390/jmse11112063

AMA Style

García LM, Sorrell B, Søgaard DH, Lund-Hansen LC. Spatial Variability in the Primary Production Rates and Biomasses (Chl a) of Sea Ice Algae in the Canadian Arctic–Greenland Region: A Review. Journal of Marine Science and Engineering. 2023; 11(11):2063. https://doi.org/10.3390/jmse11112063

Chicago/Turabian Style

García, Laura Martín, Brian Sorrell, Dorte Haubjerg Søgaard, and Lars Chresten Lund-Hansen. 2023. "Spatial Variability in the Primary Production Rates and Biomasses (Chl a) of Sea Ice Algae in the Canadian Arctic–Greenland Region: A Review" Journal of Marine Science and Engineering 11, no. 11: 2063. https://doi.org/10.3390/jmse11112063

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