Potential catastrophic reduction of sea ice in the western Arctic Ocean

Global and Planetary Change 136 (2016) 1–17

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Review: Potential catastrophic reduction of sea ice in the western Arctic Ocean: Its impact on biogeochemical cycles and marine ecosystems Naomi Harada Research and Development Center for Global Change/Institute of Arctic Climate and Environment Research, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, 237-0061, Japan

a r t i c l e

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Article history: Received 4 August 2014 Received in revised form 13 November 2015 Accepted 13 November 2015 Available online 14 November 2015 Keywords: Arctic Ocean Productivity Biological pump Marine ecosystem Eddy

a b s t r a c t The reduction of sea ice in the Arctic Ocean, which has progressed more rapidly than previously predicted, has the potential to cause multiple environmental stresses, including warming, acidification, and strengthened stratification of the ocean. Observational studies have been undertaken to detect the impacts on biogeochemical cycles and marine ecosystems of these environmental stresses in the Arctic Ocean. Satellite analyses show that the reduction of sea ice has been especially great in the western Arctic Ocean. Observations and model simulations have both helped to clarify the impact of sea-ice reductions on the dynamics of ecosystem processes and biogeochemical cycles. In this review, I focus on the western Arctic Ocean, which has experienced the most rapid retreat of sea ice in the Arctic Ocean and, very importantly, has a higher rate of primary production than any other area of the Arctic Ocean owing to the supply of nutrient-rich Pacific water. I report the impact of the current reduction of sea ice on marine biogeochemical cycles in the western Arctic Ocean, including lower-trophic-level organisms, and identify the key mechanism of changes in the biogeochemical cycles, based on published observations and model simulations. The retreat of sea ice has enhanced primary production and has increased the frequency of appearance of mesoscale anticyclonic eddies. These eddies enhance the light environment and replenish nutrients, and they also represent a mechanism that can increase the rate of the biological pump in the Arctic Ocean. Various unresolved issues that require further investigation, such as biological responses to environmental stressors such as ocean acidification, are also discussed. © 2015 The Author. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . 2. Chukchi and Beaufort seas in the western Arctic Ocean . . . . 3. Primary production . . . . . . . . . . . . . . . . . . . . 4. Biological pump . . . . . . . . . . . . . . . . . . . . . 5. Mechanisms enhancing productivity and the biological pump . 6. Benthic community and higher-trophic-level organisms . . . 7. Perspectives on Arctic ecosystem research . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . .

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1. Introduction The exchange of carbon with the Pacific and Atlantic oceans and internal biogeochemical cycling dominate the carbon cycle of the Arctic Ocean basin. Dissolved inorganic carbon, the largest carbon inventory in the ocean, originates from air–sea exchange, river runoff, and, to a E-mail address: [email protected].

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lesser degree, dissolution of carbonate-containing minerals, decay of organic matter, and biological respiration. The carbon budget of the Arctic Ocean is thus influenced by river runoff and coastal sources of organic carbon (Anderson et al., 1998; Stein and Macdonald, 2004). However, the net Arctic Ocean air–sea flux appears to be relatively small, because of the relatively small size of the basin and because ice covers much of the sea surface. McGuire et al. (2009) have estimated the dissolved inorganic carbon stocks to be 310 petagrams (1 Pg = 1 × 1015 g) C and the

http://dx.doi.org/10.1016/j.gloplacha.2015.11.005 0921-8181/© 2015 The Author. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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dissolved organic carbon stocks to be 9 Pg C in the Arctic Ocean, including the shelf seas (Canada and Eurasian basins and Chukchi, East Siberian, Laptev, Kara, Barents, and Beaufort seas) but excluding the Nordic seas and the Bering Sea. The organic carbon stored in Arctic Ocean sediments (surface layer to 3 cm depth in the basins and to 10 cm depth on the shelves and slopes), mainly of the shelf seas, has been estimated to be 9.4 Pg C as particulate carbon (McGuire et al., 2009). Methane (CH4) is also stored in the Arctic Ocean sediments as hydrates, from 2 to 65 Pg C on the shelves and slopes and from 30 to 170 Pg C in the basins (McGuire et al., 2009). The Arctic area plays an important role in the dynamics of the global carbon cycle; in recent decades the Arctic has been a sink for atmospheric CO2 of 0–0.8 Pg C y−1, which corresponds to 0–25% of the global net land/ocean flux during the 1990s. Furthermore, the Arctic is a substantial source of CH4 to the atmosphere, the estimated flux being 32–112 teragrams (1 Tg = 1 × 1012 g) C y− 1 (McGuire et al., 2009). The fact that the Arctic is a sink for atmospheric CO2 has been attributed to large phytoplankton blooms in the spring, strong cooling in the winter, and the relatively high alkalinity of the Arctic Ocean (Takahashi et al., 2009). The Arctic climate, which modulates biogeochemical cycles in the Arctic region, was growing colder (− 0.22 °C ky− 1) during the 2000 years prior to the 20th century, owing to a reduction of insolation, but since then it has begun to warm (Kaufman et al., 2009). In the fourth assessment report by the Intergovernmental Panel on Climate Change (IPCC) the Arctic region was already identified as one of the areas of the world most vulnerable to global warming (IPCC, 2007). During the period 1979–2012, the annual mean Arctic sea-ice extent decreased at a rate that was very likely in the range of 3.5–4.1% per decade, and the rate of decrease of the summer sea-ice minimum (perennial sea ice) was very likely in the range of 9.4–13.6% per decade (IPCC, 2013). The magnitude of the rate of ice loss increased from 0.35 × 106 km2 per decade during the period 1979–1993 (Comiso, 2006) to 0.9 × 106 km2 per decade between 1993 and 2007 (Deser and Teng, 2008). According to Stroeve et al. (2012), the extent of sea-ice loss during the summer has recently become remarkable, and the area of open water in September has increased at an accelerating rate since 1999. These changes in Arctic sea-ice extent have been attributed to changes in large-scale atmospheric circulation as indicated by the status of the Arctic Dipole Anomaly (Wu et al., 2006; Overland et al., 2008), and to more variability in the phase of the winter Arctic Oscillation (Stroeve et al., 2012). A shift in the wind circulation pattern to a meridional flow that blows toward the central Arctic has caused the rate of sea-ice loss to accelerate since 2000 (Budikova, 2009, and references therein). Ocean forcing is another potential driver of the sea-ice retreat. Warming of Pacific Summer Water (PSW), which is a water mass that typically spreads out on the Chukchi Shelf, has been observed frequently since the late 1990s and is likely responsible for the rapid reductions of summer sea ice in the Chukchi and Beaufort seas of the western Arctic Ocean that have been observed since then (Shimada et al., 2006). The combined effect of these multiple processes is to warm the Arctic climate in all seasons, which leads to more open water in the summer, thereby enhancing the summer ice-albedo feedback effect. Warm ocean waters promote not only the expansion of areas that are ice free in the summer but also the further thinning of multi-year ice (Stroeve et al., 2012). Sea-ice reduction (melting) may adversely affect marine organisms. Ocean acidification, another effect, in addition to global warming, of increases of atmospheric carbon dioxide (CO2) concentrations, is likely to have a serious impact on organisms in the Arctic Ocean, because ocean acidification is expected to proceed most rapidly in polar regions (Orr et al., 2005). In the Canada Basin of the western Arctic Ocean, the area in which the saturation index of aragonite was less than 1 (Ω b 1), indicating undersaturation, expanded from 1997 to 2008 as a result of the dilution effect of sea-ice melting. Thus, sea-ice melting associated with warming can accelerate the impact of ocean acidification in the Arctic Ocean (Yamamoto-Kawai et al., 2009). In contrast, a reduction of sea ice will bring improved light conditions to the ocean surface and

might thereby enhance phytoplankton photosynthesis and the supply of food for higher trophic level organisms. In the western Canada Basin, diatom productivity was greater in 2004 than in 1994, the implication being that the biological pump was enhanced during 1994–2004 because of the reduction of sea ice (Nishino et al., 2009). This result suggests that the accelerated reduction of sea ice in the Arctic Ocean means that it will continue to be a sink for atmospheric carbon dioxide in the near future (Nishino et al., 2011a). For these reasons, the Arctic Ocean is set to undergo one of the most serious, potentially catastrophic changes in environmental status of any ecosystem in the world. Understanding the impact of warming, freshening, and increases of pCO2 in the water column associated with this rapid sea-ice reduction on the organisms in the Arctic region is an urgent issue. Predicting the changes in productivity at each trophic level and within pelagic and benthic food webs in the near future is important, not only for improving scientific knowledge but also for anticipating societal impacts, including impacts on local communities. A number of descriptive reviews have summarized important knowledge about primary production, the biological pump, and marine ecosystems in the Arctic Ocean and pan-Arctic region (e.g., Grebmeier et al., 2006; Carmack and Wassmann, 2006: Grebmeier, 2012; Arrigo, 2014). Carmack and Wassmann (2006), for example, have summarized existing knowledge about pan-Arctic marine food webs and have developed some unifying concepts. They have used semi-quantitative diagrams to show the relationship between the production and vertical export of biogenic matter during the productive season as a function of the physical–biological continuum. Their model is based primarily on data from the Barents Sea shelf collected at depths greater than 200 m. This paper complements these earlier reviews by summarizing recently published and otherwise available yearlong or nearly yearlong datasets for the fluxes of sinking particles and lower trophic level organisms, collected mainly in sediment traps on the Northwind Abyssal Plain and shelves along the margins of the Chukchi Sea, Canada Basin, and Beaufort Sea in the western Arctic Ocean. The aim is to improve our understanding of the physical processes that potentially control biogenic particle fluxes, the dynamics of production and the biological pump, and the response of the functionality of lower trophic level organisms to the dramatic environmental changes in the western Arctic Ocean associated with sea-ice reduction. I will also make some predictions based on a novel ecosystem model developed specifically for the Arctic Ocean. 2. Chukchi and Beaufort seas in the western Arctic Ocean In this paper, the western Arctic Ocean (Figs. 1a and b) refers to the area encompassing the Chukchi Sea, the northern Bering Strait, and the Beaufort Sea. The Chukchi Sea (area 620 × 103 km2), together with the northern Bering Strait and the Beaufort Sea (area 178 × 103 km2), occupies only 13% of the total shelf area and 9% of the total shelf volume of the Arctic Ocean (Jakobbson et al., 2004, 2008, 2012). Pacific-origin water comprises two water masses, each associated with a different season, PSW and Pacific Winter Water (PWW), which spread into the northern Bering Strait and the Chukchi Sea. Both PSW and PWW appear in the upper halocline of the western Arctic Ocean (depth b ~ 200 m); PSW is characterized by a temperature maximum and a salinity of 31–32 at less than ~80 m depth, and PWW is characterized by a temperature minimum and a salinity of ~33 at 100–150 m depth (Coachman and Barnes, 1961). The PSW is further divided into Eastern Chukchi Summer Water (ECSW), which originates from Alaskan Coastal Water and has a relatively high temperature and low salinity, and Western Chukchi Summer Water (WCSW), which originates from Bering Sea Water and has a relatively low temperature and high salinity (Shimada et al., 2001). ECSW flows into the Canada Basin via the Beaufort Gyre, where it forms a temperature maximum at a salinity of 31–32 east of the Chukchi Plateau, and WCSW flows across the Chukchi Abyssal Plain west of the Chukchi Plateau, where it forms a temperature maximum at a salinity of ~ 32.5 (Shimada et al., 2001; Steele et al.,

N. Harada / Global and Planetary Change 136 (2016) 1–17

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Fig. 1. Map of the Arctic Ocean a) with the sea ice condition acquired 13 September 2012 (http://earthobservatory.nasa.gov/IOTD/view.php?id=79256&eocn=image&eoci=related_ image); b) a red circled is the target region of the western Arctic described in this study.

2004). The lower halocline water beneath the PSW and PWW (salinity ~34.2, depth ~ 200 m) originates from the eastern Arctic Ocean shelves (Aagaard et al., 1981; Jones and Anderson, 1986) or the eastern Arctic basin (Rudels et al., 1996; Itoh et al., 2007). Below the lower halocline water is Atlantic water, which is characterized by a temperature maximum at depths of 300–500 m in the Canada Basin.

I focus on the western Arctic in this review because that is where the most rapid retreat of sea ice has been observed in the Arctic Ocean (Comiso, 2012). Analyses over a 32-year period, from 1979/1980 to 2010/2011, have shown that this region has experienced a delay of the sea-ice advance of 1.0–1.4 months, an earlier retreat of sea ice by 1.6–1.9 months, and a reduction of the duration of the ice season by 3

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months (Stammerjohn et al., 2012). The key factor responsible for the recent anomalous reduction of sea ice in the western Arctic Ocean is enhancement of the northward transport of PSW over the Northwind Ridge in mid-winter. The heat content of the PSW prevents sea-ice growth during the winter (Sumata and Shimada, 2007). Even considering the immense area and shallow average water depth of the Chukchi and Beaufort seas in the Arctic Ocean, their productivity is high and very important relative to that of other seas in the Arctic Ocean. The nutrient-rich Pacific water doesn't supply a significant proportion of the total supply of nutrient-rich water to the “deep” Arctic Ocean, that is about one-fifth that of nutrient-rich Atlantic water (Carmack and Wassmann, 2006). The high nutrient concentrations in the Pacific water that enters the Arctic Ocean via the northern Bering Sea reflect the high productivity throughout the food chain of the Bering Sea continental shelf ecosystem (Taniguchi, 1999; Grebmeier et al., 2006; Harada et al., 2012; Cooper et al., 2013) as well as the contribution of the Anadyr Current, which consists of Bering Slope Current water that has upwelled onto the Bering shelf (Kinder et al., 1975; Wang et al., 2009). Runoff from the Yukon River contributes a substantial flux of terrestrial dissolved organic carbon (DOC) derived from glaciers to the Gulf of Alaska; the DOC flux is 0.13 Tg y−1 (standard deviation 0.01 Tg y−1), of which 77% (~0.1 Tg) is highly labile (Hood et al., 2009). Currents from the Bering Sea shelves flow toward the Chukchi and Beaufort seas primarily through Barrow and Herald canyons (Codispoti et al., 2005; Grebmeier and Harvey, 2005; Weingartner et al., 2005) and the Central Channel of the Chukchi Shelf (Pickart et al., 2005). In addition to the current flow, episodic physical mechanisms such as eddies, filaments, jets, and downwelling in canyons and along the shelf break transport plankton, particulates, and nutrients offshore into the basin, or from the deep basin via upwelling onto the Chukchi Shelf (Ashjian et al., 2005; Codispoti et al., 2005). Biomass in the benthic boundary layer and suspended in the water column supplies large cumulative amounts of biogenic matter such as detrital organic matter and plankton originating from the Chukchi and Beaufort shelves along their slopes and through the major canyons to a rich benthic fauna. These seawater and particulate organic carbon (POC) exchanges between the Bering Sea and the western Arctic Ocean are critical for maintaining the thermohaline and ecosystem structure of the Arctic Ocean, and because of the high concentrations of nutrients and biomass in the seawater, the exchanges are key contributors to the Arctic Ocean's organic carbon budget (Grebmeier et al., 2006). However, few zooplankton that originate from the Pacific (e.g. planktic foraminifera) have been taken by plankton tows in the Chukchi Sea or in time-series sediment traps at the Northwind Abyssal Plain site (St. NAP: 75°N, 162°W), which is located on the western side of the Canada Basin (K. Kimoto, Japan Agency for Marine-Earth Science and Technology [JAMSTEC], personal communication). The amount of zooplankton supplied from the Pacific Ocean through the Bering Strait and over the Chukchi shelf is limited because of the shallowness of the water column. Therefore, zooplankton grazing and the microbial loop play less important roles in these nutrient-rich waters (Carmack and Wassmann, 2006). Grebmeier et al. (2006) have described the lower trophic levels of the ecosystem in the northern Bering and Chukchi seas, which are shallow Arctic regions with high water column production and strong spatial linkages between water column organic carbon production and the benthos. These linkages have created a robust benthic–pelagic ecosystem that supports a high biomass of long-lived benthic fauna. The Beaufort Sea is characterized by high freshwater and dissolved organic carbon inputs from streams and numerous rivers, including the Mackenzie River (Emmerton et al., 2008). Those inputs have produced an environment that is decidedly estuarine in character, especially during the late spring and summer months. Coastal erosion and river discharges are largely responsible for introducing high concentrations of suspended sediment from upland regions into the nearshore zone, and sediment is often trapped in nearshore lagoons (Carmack and Wassmann, 2006).

3. Primary production The most important organisms associated with sea ice are microalgae, and the most abundant microalgal taxa in the Arctic sea ice are diatoms (Arrigo, 2014). Sea-ice algae are one of the most ubiquitous primary producers in the sea-ice ecosystem in the cryopelagic region of both Arctic and Antarctic waters. In the Arctic Ocean, the productivity of ice algae shows regional heterogeneity, with up to half of total primary productivity occurring in the central Arctic, and relatively less occurring in the seasonal sea-ice area (Gosselin et al., 1997; Gradinger, 2009; Onodera et al., 2015a). The ice algal community, which is composed mainly of diatoms, accounts for 87% of the water mass carbon-specific biomass of phytoplankton in the under-ice bloom in the Chukchi Sea (Laney and Sosik, 2014). A total of 30–40 different species of sea-ice-related diatoms have been identified (Melnikov et al., 2003; Riaux-Gobin et al., 2003; Werner et al., 2007) from among the more than 550 diatom species in the Arctic Ocean (Il'iash and Zhitina, 2009), and diatoms are the most dominant of Arctic phytoplankton species (Bluhm et al., 2011). The most common diatoms are pennates (e.g., Nitzschia, Fragilariopsis, Entomoneis, and Navicula), which can survive in bottom ice (Fiala et al. 2006), in land-fast ice (Ratkova and Wassmann, 2005), in surface ice (Whitaker and Richardson, 1980; Lizotte and Sullivan, 1992; Ryan et al., 2006), and within sea-ice-infiltration communities (Garrison, 1991). Fragilaria, Cylindrotheca and Achnanthes are relatively common genera of unicellular diatoms in the Arctic. In the western Arctic, they survive at the seaice bottom/water interface, and they prefer the weak light conditions (clear ice transmits light) associated with moderately thick (2–4 m) sea ice in the melting season (Horner, 1985). The maximum densities of ice algae are usually restricted to relatively thin layers because of the high light attenuation by ice and self-shading by high concentrations of algal pigments in both the Arctic (Arrigo et al., 1991) and Antarctic (Lazzara et al., 2007). Generally, sea-ice algal blooms start in coastal seasonal sea-ice areas in mid-March, when light becomes sufficient for their photosynthesis (Bluhm et al., 2011); in the western Arctic Ocean, Fragilariopsis (oceanica and cylindrus) gradually increases from April (Onodera et al., 2015a). Both in situ and satellite observations are used to estimate primary production. In situ observations are useful because they directly estimate primary production throughout the water column, from surface to subsurface, but they have the disadvantage, compared with satellite observations, of being restricted to very small areas. The primary production rates in the western Arctic Ocean (Table 1, Fig. 2), measured before the catastrophic reduction of sea ice in ~2005, were 20–50, 30–50 (Sakshaug, 2004), and 25–40 g C m− 2 y−1 (Petrova et al., 2004; Sakshaug, 2004) in the Fram Strait (80°N, 11°W), Kara Sea (74°N, 80°W), and East Siberian Sea, respectively. At the Lomonosov Ridge (81°5′N, 138°54′E) in the central Arctic Ocean, the primary production rate, estimated from the flux of POC collected in sediment traps, was 18 g C m−2 y− 1 from September 1995 to August 1996 (Boetius and Damm, 1998; Fahl and Nöthig, 2007). At the edge of the Canada Basin, annual primary production was estimated from ship-based measurements to be 20 g C m−2 y− 1, with a summertime peak of 0.32 g C m−2 d−1 (Hill and Cota, 2005). In contrast, Hill et al. (2013) reported that annual vertically-integrated primary production is relatively high throughout the Bering, Barents, and Nordic seas than in other areas of the Arctic Ocean. Primary production rates in the Chukchi Sea, northern Bering Sea, and Beaufort Sea are higher than those in other areas of the Arctic Ocean (Table 1, Fig. 2). Estimated primary production rates in the northern Bering Sea and Chukchi Sea are particularly high, 250–470 g C m− 2 y− 1 (Fukuchi et al., 1993; Springer and McRoy, 1993; Springer et al., 1996) and 70–840 g C m− 2 y− 1 (Springer and McRoy, 1993; Springer et al., 1996; Wassmann et al., 2004; Hill and Cota, 2005; Moran et al., 2005), respectively, except on the slope in the Northern Chukchi Sea, where quite low values of b 50 g C m−2 y−1 have been reported (Sakshaug, 2004; Wassmann et al., 2004; Moran

N. Harada / Global and Planetary Change 136 (2016) 1–17

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Table 1 Primary production at various locations in the Arctic Ocean. Area

Location (average)

Northern Bering Sea

62°–65°N, 165°W–180°, Eastern Bering Sea shelf slope Southern Anadyr and Shpanberg Chukchi Sea Strait to 70°N Northern 70.5°–73°N, 153–166°W Chukchi Sea shelf Northern 71°–74°N, 152–160°W Chukchi Sea slope Western 69.9°N, 138.5°W Beaufort Sea Southeast Cape Bathurst Polynya Beaufort (70.5–72°N, 122–128°W) Sea Southeast 70°–76°N, 123–138°W Beaufort Sea Arctic Basin – (Nansen Basin) Central Arctic 81°5'N, 138°54'E Ocean East Siberian – Sea Fram Strait 80°N, 11°W

Observation period

Primary Reference production

(m)

(g C m−2 y−1)

Water sampler (Niskin bottle)

30–80

175–470

Springer and McRoy, 1993; Springer et al., 1996

1985–1989, 1992–1993 2002

Water sampler (Niskin bottle), Sediment trap

50–100

80–840

Water sampler (Niskin bottle)

50–200

70–430

Springer and McRoy, 1993; Springer et al., 1996; Wassmann et al., 2004 Hill and Cota, 2005; Moran et al., 2005

Sediment trap, Water sampler (Niskin bottle), model estimation from 14C or nitrate measurement Sediment trap, Water sampler (Niskin bottle), model estimation from 14C or nitrate measurement Satellite, Water sampler (Niskin bottle)

200–2000 b50

Wassmann et al., 2004; Sakshaug, 2004; Moran et al., 2005

50–2000

30–70

Wassmann et al., 2004; Sakshaug, 2004; Hill and Cota, 2005

0–250

12–175

2003–2004

Sediment trap

90–130

3–129a

Arrigo and van Dijken, 2004; Carmack et al. 2004; Tremblay et al. 2008 Sampei et al., 2011

1994

Model estimation from 14C or nitrate measurement

N2000

b11

Sakshaug, 2004

–

Sediment trap

–

18

–

Model estimation from 14C or nitrate measurement Model estimation from 14C or nitrate measurement Model estimation from 14C or nitrate measurement – –

30

25–40

Boetius and Damm, 1998; Fahl and Nöthig, 2007 Sakshaug, 2004; Petrova et al., 2004

–

20–50

Sakshaug, 2004

–

30–50

Sakshaug, 2004

– –

2–40 0.2–4b

Arrigo et al., 2010; Arrigo, 2014 Arrigo et al. 1997, 1998, 2010; Rysgaard et al. 2001

2002

2002

1998–2002, 2003–2004

–

74°N, 80°W

–

Arctic Ocean Arctic Ocean

Area averaged Area averaged

– –

b

Depth

1985–1989

Kara Sea

a

Platform

Diatomaceous new production. Ice algae.

et al., 2005). The primary production rate in the western Beaufort Sea at 69.9°N, 138.5°W has been estimated to be 30–70 g C m−2 y−1 (Table 1,

Fig. 2), which is higher than the estimated rates in the Fram Strait, in the Kara Sea (Sakshaug, 2004), and above the Lomonosov Ridge (Boetius

Fig. 2. Primary production (g C m−2 y−1) estimated by in-situ observation, sediment trap mooring systems, satellite, and model simulation at various locations in the Arctic Ocean (Northern Bering Sea: Springer and McRoy, 1993; Springer et al., 1996; Southern Chukchi Sea: Springer and McRoy, 1993; Springer et al., 1996; Wassmann et al., 2004; Northern Chukuchi Sea shelf: Hill and Cota, 2005; Moran et al., 2005; Northern Chukuchi Sea slope: Wassmann et al., 2004; Sakshaug, 2004; Cooper et al., 2005; Moran et al., 2005; Western Beaufort Sea: Wassmann et al., 2004; Sakshaug, 2004; Hill and Cota, 2005; Southeast Beaufort Sea: Arrigo and van Dijken, 2004; Carmack et al. 2004; Tremblay et al. 2008; Sampei et al., 2011; Arctic Basin (Nansen Basin): Sakshaug, 2004; Central Arctic Ocean: Boetius and Damm, 1998; Fahl and Nöthig, 2007; East Siberian Sea: Sakshaug, 2004; Petrova et al., 2004; Fram Strait: Sakshaug, 2004).

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and Damm, 1998; Fahl and Nöthig, 2007). In the southeast Beaufort Sea, new production and total primary production rates of 12–175 g C m− 2 y−1 have been estimated (Arrigo and van Dijken, 2004; Carmack et al., 2004; Tremblay et al., 2008), and new production rates associated with diatoms range from 2.8 to 128.7 g C m− 2 y− 1 (Sampei et al., 2011). A few studies have indicated on the basis of in situ incubations involving 14C uptake that annual primary production in the Arctic is in the range of 2–15 g C m−2 y−1, and that the maximum value of annual primary production in the Arctic Ocean is almost half that in the Antarctic (Arrigo et al., 2010). Satellite-based estimation of primary production is an indirect method based on sensor measurements of chlorophyll a (Chl. a). Although satellite-based observations have the advantage, compared with in situ observations, of much better spatial coverage, they have a disadvantage in that under-ice production is assumed to be zero. Satellite Chl. a data provided by NASA and monthly Chl. a-based primary production anomalies from the monthly climatological average (April– September) from 1998 to 2014, are shown in Fig. 3 (E. Siswanto unpublished). Satellite observations of Chl. a indicate that surface primary production in the Arctic Ocean is relatively high in coastal regions such as the Chukchi Sea as well as in the Laptev, East Siberian, and Kara seas (Matrai et al., 2013). According to Arrigo (2014), even in the most productive sea-ice habitats, annual primary production is b40 g C m−2 y−1, which is lower than primary production in the oligotrophic central gyres of the open ocean (e.g., 180 g C m−2 y−1 at station ALOHA; http://hahana.soest.hawaii.edu/hot/hot_jgofs.html). The productivity of ice algae in most areas of the Arctic Ocean is even lower than this value and accounts for approximately 1% of annual primary production in pelagic environments of the polar regions (Arrigo et al., 1997, 1998, 2010; Rysgaard et al., 2001). However, consumption of dissolved inorganic carbon and nitrate in surface waters beneath the sea ice, observed during a field campaign in the Chukchi Sea, yielded a high production value of ~ 70 g C m−2 during an under-ice bloom from 4 to 8 July 2011. Moreover, this production value is consistent with daily net primary production, estimated from 14C uptake measurements, of the under-ice bloom (1.2–4.8 g C m−2 d−1) (Arrigo et al., 2014). This result suggests that the contribution of primary production of under-ice blooms is higher than previous observations have indicated. Based on a synthesis of (1) surface primary production rates estimated from in situ incubations involving uptake of 14C, (2) primary production of satellite-based estimates of Chl. a, and (3) remotely sensed

primary production in various regions of the Arctic Ocean, the average primary production rate in the Arctic Ocean over the past 50 years (1957–2007) has been 70 and 21 mg C m−3 day−1 in spring and summer, respectively (Matrai et al., 2013). The daily primary production rate depends on which of the above three methods is used for the estimate, because of differences in data availability and coverage (Matrai et al., 2013). The annual surface primary production estimated with the three methods agrees to within a median difference of ±400 mg C m−3 y−1 (Matrai et al., 2013). Pabi et al. (2008) estimated primary production in the Arctic Ocean by remote sensing to be 419 ± 33 Tg C y−1 from 1998 to 2006. Interannual variation was high (26%); primary production increased during 1998–2001, then decreased until 2003, and increased again to the maximum value of 483 Tg C y−1 in 2006 (Pabi et al., 2008). The vertically integrated primary production rate for the Arctic Ocean was estimated from in situ incubations and satellite Chl. a data for 1957 to 2007 to be a minimum of 466 ± 94 Tg C y−1 and a maximum of 993 ± 94 Tg C y−1 (Hill et al., 2013). Full coupling of a global physical model with an open-ocean pelagic ecosystem model that includes an ice algal ecosystem model is rare, because the ice algal community is considered to make a relatively minor contribution to the total primary production compared with the open-ocean pelagic community. However, Jin et al. (2012) have reported the mean seasonal cycle of ice algal production from March to May and subsequent ocean production from May to September in the Arctic Ocean. In their simulation result, mean open-ocean primary production in the upper 100 m of the Arctic Ocean was 413 ± 88 Tg C y−1 in 1998–2006. Recently, an Arctic version of a coupled sea ice–ocean circulation marine ecosystem model with a 5-km mesh that incorporates sea-ice-related algal activity has been used to explore the mechanism of year-to-year changes in ice algal production (Watanabe et al., 2015). According to moored sediment trap time-series experiments at St. NAP, the flux of sea-icerelated algal assemblages was high in August 2011, whereas a high flux of sea-ice-related algal assemblages was not observed in August 2012 (Onodera et al., 2015a). This interannual difference in summertime sea-ice-related algal activity between 2011 and 2012 is attributable to different wind patterns: In 2011, easterly winds in the southern part of a distinct Beaufort High supplied nutrient rich water to surface water in the St. NAP region via Ekman transport of Chukchi shelf water and vertical turbulent mixing with underlying nutricline water. In contrast, in 2012, northwesterly winds in the northern part of an extended Siberian High promoted the flow of an oligotrophic

Fig. 3. a) Satellite Chl. a (g Chl. a m−2 month−1) provided by NASA and b) Chl. a based primary production (mg C m−2 month−1) which are monthly anomaly from the average of monthly climatological data (April–September) from 1998 to 2014 (E. Siswanto unpublished). The Chl. a based primary production is estimated by using Arctic/subarctic local algorithm proposed by Cota et al. (2004). The red contour line denotes zero trend line. White area indicates insignificant trends (p N 0.05).

N. Harada / Global and Planetary Change 136 (2016) 1–17

water mass within the Beaufort Gyre circulation toward St. NAP (Watanabe et al., 2015). The mean sea-ice algal production in the Northern Hemisphere has been estimated to be 21.3 Tg C y−1 from 1992 to 2007 using a 3-D global ice–ocean ecosystem model (Jin et al., 2012), a value within the range of multiple estimates (9–73 Tg C y−1) based on in situ measurements (Legendre et al., 1992). Net community production, the difference between gross primary production and autotrophic and heterotrophic respiration, has been estimated from the availability of nitrate, nitrite, and phosphate to be ~ 1000 Tg C y− 1 (Codispoti et al., 2013); this value is similar to the vertically integrated primary production (Hill et al., 2013). The reduction in the extent of sea ice during the summer has become remarkable recently, and the downward trend in September has accelerated since 1999 (Stroeve et al. (2012) or 2000 (Budikova, 2009). To investigate the impact of the sea-ice retreat on primary production, Pabi et al. (2008) compared annual primary production before and after the catastrophic reduction of sea ice from 1998 to 2006, based on surface Chl. a concentrations estimated from 8-day Sea-viewing Wide Field-of-view Sensor (SeaWiFS) data. They found an increasing trend of surface Chl. a only in the East Siberian Sea, and no clear trend in the Chukchi, Kara, Baffin, Greenland, Barents, or Laptev seas (Pabi et al., 2008). Only in the Beaufort Sea did annual production actually decrease from 1998 to 2006, the rate of decline being 1.5 Tg C y−1 (Pabi et al., 2008). However, this decreasing trend was not statistically significant, and it was driven primarily by large decreases in production during the first 2 years, 1998 and 1999 (Pabi et al., 2008). Hirawake et al. (2012) compared primary production rates in the western Arctic Ocean before and after the catastrophic sea ice reduction in 2005 during 2002–2010, different from but overlapping the observation period (1998–2006) of Pabi et al. (2008). They based their comparison on estimates derived from remote sensing algorithms that ignored the influences of colored dissolved organic matter and non-algal particles (Hirawake et al., 2012). They found an increasing trend of summer (August and September) primary production, and suggested that warming sea surface temperatures led to this increased production. Arrigo et al. (2008) estimated open ocean primary production during 2003–2007, excluding that by the ice algal community, with a model that utilized remote sensing data from the Arctic Ocean. They found that open ocean primary production increased by 24%, from about 410 to 510 Tg C y−1, as a result of the increased area of open water, the increased temperature, and the longer duration of the growth season (Arrigo et al., 2008). For comparison, Jin et al. (2012) estimated primary production with a coupled sea-ice physical and open-ocean pelagic ecosystem model that included an ice algal ecosystem component and found that although primary production fell within a narrow range during 2003–2007, it increased by 15%, from 480 to 550 Tg C y−1, during that time period. 4. Biological pump The biological pump is the mechanism by which carbon-containing compounds are exported via biological processes from the surface to the deep ocean (Sarmiento and Gruber, 2006). The export flux of soft and hard tissues that originate from organisms and fecal pellets is called the passive flux, and the export flux mediated by the vertical migration of zooplankton is called the active flux. Longhurst and Harrison (1988) have shown that the active flux associated with the vertical migration of common migrant zooplankton such as copepods and euphausiids makes an important contribution to the total vertical flux. In fact, the contribution to the vertical flux of the common migrant zooplankton is almost equal to the passive flux (Le Borgne and Rodier, 1997; Steinberg et al., 2000; Honjo et al., 2008). Recent time-series sediment trap observations from the Amundsen Gulf in the southeastern Beaufort Sea have indicated that sinking dead copepods also contribute substantially to the passive flux during the winter season (Sampei et al., 2011). Sampei et al. (2009, 2011) estimated the contribution of passively

7

sinking copepods to the overall copepod flux in the Beaufort Sea on the basis of sediment trap data from September 2002 to August 2003 and reported that passively sinking Calanus hyperboreus and Paraeuchaeta glacialis accounted for less than 6% of the overall flux of copepods, whereas passively sinking C. glacialis accounted for 42% and 100% of the total copepod flux during November–December 2002 and July 2003, respectively (Sampei et al., 2009). Passively sinking copepods of these three species, which accounted for 36% of the overall POC flux, are potentially an important food resource for pelagic and benthic organisms (Sampei et al., 2009, 2011). Annual mean POC fluxes determined by moored sediment trap experiments and by determining 234Th/238U disequilibria (Coale and Bruland, 1985) of large-volume water samples (including drifting sediment trap samples) at various locations in the Arctic Ocean are summarized in Fig. 4 and Table 2; in the table the observation periods are also given in chronological order. From 1997 to 1998, that is, before the catastrophic sea-ice reduction (1999/2000), maximum POC fluxes of 13.8 g C m−2 y−1 were observed in a sediment trap experiment in a polynya in Baffin Bay (Sampei et al., 2004), and in August 1994, a maximum POC flux of 166 g C m−2 y−1 was estimated in the Chukchi Sea and on its shelf on the basis of 234Th/238U disequilibria (Moran et al., 1997). The second-highest POC fluxes before 1999 of 5.8 and 32 g C m−2 y−1 were recorded by sediment traps along the Mackenzie Shelf edge in the Beaufort Sea (Table 2 and Fig. 4; O'Brien et al., 2006) and, also in the Beaufort Sea, by using 234Th/238U disequilibria, respectively (Table 2; Moran and Smith, 2000). The annual mean POC fluxes estimated by using 234Th/238U disequilibria tend to be larger than those estimated by moored sediment trap experiments (Table 2) because they were calculated using data from only spring to summer, when primary production is largest (Table 2), and because the efficiency with which settling particles are trapped is frequently not 100% (Lalande et al., 2007). The POC export flux in the Chukchi Sea, estimated from Ice-Ocean Environmental Buoy (IOEB) data during 1997–1998, was 0.59 g C m− 2 y− 1 (Honjo et al., 2010). This POC export flux is lower than the fluxes of 1.0–2.7 g C m−2 y−1 in the northeast water polynya in the Fram Strait (Bauerfeind et al., 1997), 1.6 g C m−2 y−1 on the Greenland continental shelf (Bauerfeind et al., 2005), and 1.0–1.5 g C m− 2 y−1 in the Laptev Sea estimated by sediment trap mooring system (Zernova et al., 2000; Fahl and Nöthig, 2007). The minimum POC flux in the cryopelagic Arctic Ocean, 0.08 g C m−2 y−1, was recorded in the Canada Basin in a moored sediment trap experiment (Honjo et al., 2010). After the catastrophic sea-ice reduction in 1999/2000, a maximum POC flux of 12.9 g C m−2 y− 1 was observed in sediment traps in the southeastern Beaufort Sea (Sampei et al., 2011), and a maximum flux of 301 g C m−2 y−1 was estimated from 234Th/238U disequilibria in the Chukchi Sea (Lalande et al., 2007). The POC flux of 9.8 g C m−2 y−1 recorded in the Kara Sea was also relatively high (Gaye et al., 2007). In contrast, relatively low POC fluxes were recorded in the Fram Strait (1.0 g C m−2 y−1; Bauerfeind, 2004), on the Mackenzie Shelf slope in the Beaufort Sea (1.0–1.7 g C m−2 y−1; Forest et al., 2007), and at the Canadian Ice Island (0.07 g C m−2 y−1; Hargrave, 2004). The POC flux of 0.17 g C m−2 y−1 in the Canada Basin obtained during 2004–2005 by a time-series sediment trap experiment is still low, although it is higher than the flux of 0.08 g C m− 2 y− 1 observed there during 1996–1997 by the IOEB (Table 2 and Fig. 4). Honjo et al. (2010) have summarized the biological pump and mineral material fluxes in the cryopelagic Canada Basin. POC collected by moored sediment trap systems at 3067 m depth from 2004 to 2005 did not show clear seasonal changes and consisted of old carbon with an average age of approximately 1900 years (Hwang et al., 2008). POC export fluxes ranged from 0.08 to 0.12 g C m− 2 y−1 and were 2–3 orders of magnitude smaller than the POC fluxes recorded at equivalent depths in lower latitude oceans, the Southern Ocean, and the Okhotsk Sea, although the estimated annual primary production in the Canada Basin is comparable to the annual primary production in some low-latitude seasonal sea

8

N. Harada / Global and Planetary Change 136 (2016) 1–17

Fig. 4. The POC fluxes (g C m−2 y−1) estimated by sediment trap mooring systems in the Arctic Ocean (Canadian Archipelago: Hargrave et al., 1994; North-East Water Polynya, Fram Strait: Bauerfeind et al., 1997; Amundsen Bay, Laptev Sea: Zernova et al., 2000; Canadian Ice Island: Hargrave, 2004; North Water Polynya, Baffin Bay: Sampei et al., 2004; Greenland Continental Shelf: Bauerfeind et al., 2005; Mackenzie Shelf Edges, Beaufort Sea: O'Brien et al., 2006; Lomonosov Ridge, Laptev Sea: Fahl and Nothing, 2007; Mackenzie Shelf Slope, Beaufort Sea: Forest et al., 2007; Kara Sea: Gaye et al., 2007; Chukchi Rise, Chukchi Sea: Honjo et al., 2010; South Eastern Beaufort Sea: Sampei et al., 2011).

ice oceans (Honjo et al., 2010). The extremely low POC export flux in the Canada Basin may be due to the small amount of biogenic ballast (e.g., diatom frustules, coccoliths, and lithogenic particles) in the sinking particles and the inactivity of secondary producers in the water column, as indicated by the lack of a fecal pellet export. Honjo et al. (2010) hypothesized that the biological pump does not function effectively in the cryospheric Arctic Ocean because of a lack of ballast particles required to export the POC into deep water. A recent (October 2010–September 2011) assessment of export fluxes of POC and the seasonal changes of plankton assemblages, carried out by using moored sediment traps at St. NAP, has estimated export POC fluxes of 0.31 and 0.26 g C m− 2 y−1 at water depths of 180 m and 1300 m, respectively (Watanabe et al., 2014). These POC fluxes accounted for 5–20% of the total mass flux (TMF), and lithogenic materials accounted for 60–80% of the TMF (Watanabe et al., 2014). The characteristics of the exported particles differed in two ways between St. NAP and the cryopelagic Canada Basin site (Honjo et al., 2010): 1) the flux of 0.31 g C m−2 y−1 at St. NAP at 180 m depth was four times the flux of 0.08 g C m−2 y−1 at the IOEB at 200 m depth; and 2) remarkable seasonal changes in the biogenic export fluxes at St. NAP were associated with the high biodiversity of the planktic community, which consisted of phytoplankton (mainly diatoms), micro-zooplankton, and meso-zooplankton (Watanabe et al., 2014). The maximum TMF and POC flux were observed at St. NAP during November and December, when the sea-ice-cover season was just beginning, in both 2010 and 2011. High fluxes were also observed in July, August, and September 2011, but no high fluxes were observed during summer 2012 (Watanabe et al., 2014). During the high-POC flux seasons in 2010 and 2011, diatoms were the dominant component of the phytoplankton, and the diatom assemblage was mainly planktic. The contribution of sea-ice-related algae was minor (Onodera et al., 2015a). The predominant diatom assemblage was completely different between the November–December, 2010 and 2011 and summertime high-flux seasons. During the summer, 2011, the major diatom taxa were Fossula arctica and Fragilariopsis oceanica (Onodera et al., 2015a), which are common diatom species in the Arctic Ocean and other cold waters; their presence suggests that active primary production takes place in the water column during the summer. During November–December

(the start of the sea-ice-cover season), 2010 and 2011, the major taxa were Chaetoceros resting spores; centric diatoms, which are abundant on the Chukchi Sea shelf; and Thalassionema nitzschioides, which is a common diatom species in the Canada Basin (Onodera et al., 2015a). The micro-zooplankton consisted of planktic foraminifera, ostracodes, coastal bivalvia, and pteropods with carbonate tests (K. Kimoto, JAMSTEC, unpublished data). Fluxes and assemblages of microzooplankton, including planktic juveniles of coastal bivalvia, showed clear seasonality; the highest fluxes were observed in August– September and October–November. This seasonality is similar to the seasonal pattern of diatom (Watanabe et al., 2014), silicoflagellate, ebridian, and dinoflagellate fluxes (Onodera et al., 2015b). The bivalve larvae originate mainly from the Bering Strait to the east of the Chukchi shelf, but they rarely appear in the Canada Basin (K. Kimoto, JAMSTEC, unpublished data). The fluxes of zooplankton swimmers ranged from 5 to 44 individuals m−2 day−1; these fluxes were greatest in July–October and they were not as high in November–December (Matsuno et al., 2013). The zooplankton swimmers were dominantly copepods, which accounted for 18–94% of swimmer fluxes (Matsuno et al., 2013). The copepod assemblage changed dramatically in February–April, when C. hyperboreus increased drastically (Matsuno et al., 2013). It seems likely that seasonal changes in vertical migration related to changes in the day–night cycle in February–April led to this increase in the C. hyperboreus flux (Matsuno et al., 2013). Although seasonal changes in the copepod assemblage are thought to be affected by changes in the sea-ice concentration, temperature, and salinity (Makabe et al., 2010), an internal body timer may also be an important factor in the timing of their seasonal upward migration (Miller and Grigg, 1991; Miller et al., 1991) that leads to an increase of C. hyperboreus production during winter. In addition to the Arctic copepod C. hyperboreus, the Pacific copepod Neocalanus cristatus was present during August– September at St. NAP (Matsuno et al., 2013). Furthermore, fresh organisms, including diatoms, micro-zooplankton, and copepods with soft tissues, were captured; fresh organisms are ones that were alive until shortly before their capture in the sediment traps (Matsuno et al., 2013; Watanabe et al., 2014). The increasing biodiversity and export fluxes since the observations of 1996–1997 suggest that the Canada Basin may have recently become more productive. Further

N. Harada / Global and Planetary Change 136 (2016) 1–17

9

Table 2 Annual particulate organic carbon (POC) fluxes at various locations in the Arctic Ocean. Area

Mackenzie Shelf Edges, Beaufort Sea Canadian Archipelago North-East Water Polynya, Fram Strait Chukchi Sea, Chukchi shelf

Location (average)

Canada Abbysal Plain Canadian Ice Island Kara Sea Northwind Abbysal Plain, Canada Basin Northwind Abbysal Plain, Canada Basin a b

POC flux (g C m−2 y−1)

Reference

Mooring

125

1.7–5.8

O'Brien et al. (2006)

79°N, 102°W

1989–1990

Mooring

130

0.2

80°N, 11°W

1992–1993

Mooring

130

1.0–2.7

August–September, 1994 1994–1995

234

10–300

166b

Hargrave et al. (1994) Bauerfeind et al. (1997) Moran et al. (1997)

245

1.6

69.9°–73.0°N, 136.9.8°–145.4°W Amundsen Basin, Laptev Sea 81°N, 138°E Lomonosov Ridge, Laptev 81°N, 138°54'W Sea Lomonosov Ridge, Laptev 81°N, 138°54'W Sea Canada Basin 79.1°–76.7°N, 132.2°–131.8°Wa Chukchi Rise, Chukchi Sea 75.2°–80.0°N, 142.2°–155.9°Ea North Water Polynya Buffin 75°N, 75°W Bay Canada Basin 75.1°N, 161.6°W Chukchi Sea 71.7°–73.3°N, 153.9°–155.1°W Canada Basin 73.8°–75.2°N, 149.9°–152.9°W Chukchi Sea 79.1°–76.7°N, 132.2°–131.8°W Chukchi Sea, Chukchi shelf 67°–75°N, 155°–169.7°W

Chukchi Sea

Depth (m)

1987–1988

Beaufort Sea

South eastern Beaufort Sea Mackenzie Shelf Slope, Beaufort Sea Chukchi shelf

Platform or method

70°N, 132°W

67.8°–76.6°N, 168.8°–173.3°W Greenland Continental Shelf 75°N, 13°W

Canada Basin

Observation period

71.3°–80.2°N, 146.7°–171.9°W 71°N, 126°W 71°N, 133°W 70°–73.9°N, 152.1°–160.7°W Barrow Canyon and East Hanna Shoal 75°N, 150°W 81°N, 96°W 74°N, 80°E 75°N, 162°W 75°N, 162°W

Th (large-volume water sampling)

10–200

3.1–32

Mooring Mooring

150 150

1.0–1.5 1.5

1995–1996

Mooring

1550

1.05

1996–1997

IOEB

200

0.08

Bauerfeind et al. (2005) Moran and Smith (2000) Zernova et al. (2000) Fahl and Nöthig (2007) Fahl and Nöthig (2007) Honjo et al. (2010)

1997–1998

IOEB

120

0.59

Honjo et al. (2010)

1997–1998

Mooring

198–257 1.0–13.8

August, 1999 Summer, 2000

234

Summer, 2000 Spring–Summer, 2002 July–September, 2003 July–September, 2003 2003–2004 2003–2004

August–September, 1995 1995–1996 1995–1996

Spring–Summer, 2004 Spring–Summer, 2004 2004–2005

Mooring 234

Th (large-volume water sampling)

b

Sampei et al. (2004)

b

Th (large-volume water sampling) Th (large-volume water sampling)

0, 50 50

234

Th (large-volume water sampling)

50

234

Th (large-volume water sampling)

50

234

Th (large-volume water sampling)

40

4.4–27 Chen et al. (2003) 18.4–250b Trimble and Baskaran (2005) 6 Trimble and Baskaran (2005) 0.4–171b Trimble and Baskaran (2005) 0.13–3.9b Zhang et al. (2015)

234

Th (large-volume water sampling)

40–100

0.04–3.2b

Zhang et al. (2015)

Mooring Mooring

90–128 200

2.2–12.9 1.0–1.7

Sampei et al. (2011) Forest et al. (2007)

234

50

2.9–301b

Lepore et al. (2007)

234

Th (large-volume water sampling)

234

b

10–100

2.2–290

Lalande et al. (2007)

2010–2011

Th (large-volume water sampling and drifting sediment trap) Mooring Mooring Mooring Mooring

3067 100 36 180

0.17 0.07 9.8 0.31

2010–2011

Mooring

1300

0.26

Honjo et al. (2010) Hargrave (2004) Gaye et al. (2007) Watanabe et al. (2014) Watanabe et al. (2014)

From the location that trap bottle opened firstly to the location that trap bottle closed finally of Ice-Ocean Environmental Buoy (IOEB). Annual average of POC flux was estimated by the 234Th/238U disequilibria from limited seasonal data (spring and summer).

investigations are needed to determine whether the efficiency of the biological pump has increased or decreased; the size distribution of the phytoplankton community has been shifting toward smaller sizes based on observations made during the last 5 years (Li et al., 2009). The POC fluxes in the Beaufort Sea and Chukchi Sea also seem to have been higher after 2000 than during the 1980s and 1990s (Table 2). In the Amundsen Gulf in the southeastern Beaufort Sea, sinking dead copepods accounted for 87–91% of the export flux during the winter (January–February), 2003–2004, when the large copepods C. hyperboreus and P. glacialis were present (Sampei et al., 2009, 2012). The spawning of C. hyperboreus generally peaks at some point during the winter; as a result, the senescence and mortality of most adult stages occurs in winter. Thus, sinking dead copepods in winter may contribute importantly to the annual TMF (Sampei et al., 2012). The development time of copepods from egg to hatching is such that the relatively high abundance of copepod nauplii collected in March

would reflect the eggs laid between December and March (Sampei et al., 2012). 5. Mechanisms enhancing productivity and the biological pump A remarkable enhancement of biological productivity and the biological pump has been associated with the retreat of sea ice in the Arctic, presumably owing to an increase of irradiance in the water column (Frey et al., 2011; Lee and Whitledge, 2005), wind-induced mixing that replenishes sea surface nutrients (Carmack et al., 2006), and the combined effects of light enhancement and nutrient replenishment (Nishino et al., 2009). In the vicinity of the Chukchi Sea, Canada Basin, and Beaufort Sea, physical processes such as eddies, filaments, jets, and downwelling in canyons and along the shelf break are crucial mechanisms that promote the transport of materials (plankton, particles, and nutrients) offshore into the basin, or from the deep basin via upwelling

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onto the shelf. Anti-cyclonic eddies appear occasionally in the Canada Basin (Manley and Hunkins, 1985) and along the Chukchi shelf break (Spall et al., 2008), and cold eddies in particular are thought to be important transporters of plankton, biogenic particles, and nutrients in Pacific water (Mathis et al., 2007; Kadko et al., 2008). Lateral transport of resuspended biogenic particles from the ocean floor in association with eddy activity has also been suggested to play an important role in the oceanic carbon pump, as indicated by time-series sediment trap measurements in off-shelf regions of the western Arctic (O'Brien et al., 2013), in the deep Canada Basin (Honjo et al., 2010), above Canadian Beaufort shelves (Forest, et al., 2007, 2011; O'Brien et al., 2006, 2011; Sampei et al., 2011), in the northern Laptev Sea (Fahl and Nöthig, 2007), and in the Nordic seas (Wassmann et al., 2004). Nevertheless, the role of eddies, except in the lateral transport of particles, is not fully understood. Nishino et al. (2011b) investigated the physical, chemical, and biological properties of a large, warm eddy with an approximate diameter of 100 km in the vicinity of the Northwind Abyssal Plain in the western Arctic Ocean in September 2010. The temperature at the center of eddy was 7 °C, concentrations of nutrients (ammonium) that originated on the shelf slope were high in the eddy, and the abundance of small phytopankton such as dinoflagelates was higher inside the warm eddy than in the surrounding water (Nishino et al., 2011b, their Fig. 4a). This snapshot of the eddy characteristics suggests that the eddy's warm core may serve not only as transporter of heat and particles toward the cryopelagic Arctic Ocean but also as an incubator of lower-trophic-level organisms. A moored sediment trap experiment carried out from September 2010 to October 2011 at St. NAP in near the area of the eddy studied by Nishino et al. (2011b) revealed high bimodal flux peaks during the summer (July–September) and at the beginning of the polar night season (November–December) of POC (Watanabe et al., 2014), diatoms (Onodera et al., 2015a), silicoflagellates, ebridians, and dinoflagellates (Onodera et al., 2015b), micro-zooplankton with carbonate tests (K. Kimoto, JAMSTEC, unpublished data), and zooplankton swimmers (Matsuno et al., 2013). Furthermore, some of the micro-zooplankton and copepods captured in the sediment trap during the high-flux period at the beginning of the polar night were fresh, even though photosynthesis is expected to be nil at the beginning of the polar night because of the paucity of insolation. A marine ecosystem model might help to reveal the influence of physical processes such as coastal currents, eddy activity, and upwelling on the marine ecosystem, and thus help to elucidate the mechanism(s) responsible for the active production of lowertrophic-level organisms at the beginning of the polar night in the western Arctic Ocean. An eddy-resolving coupled sea ice–ocean model (COCO3.4) that included a bioenergetics model coupled with a threedimensional lower-tropic-level ecosystem model has been developed to describe the ecosystem in the subarctic North Pacific (NEMURO; Kishi et al., 2007). Recently, simulations performed with this panArctic physical ocean circulation model with a 5-km mesh resolution have explained the movement of nutrients from the Chukchi shelf break toward the cryopelagic Arctic basin (Watanabe, 2011). This model successfully captured the major spatial and temporal features of the phytoplankton bloom following the summertime sea-ice retreat on the shallow Chukchi shelf and in Barrow Canyon (Watanabe et al., 2012). The model simulation results also support the observation that mesoscale eddies positively influence primary production in the western Arctic Ocean (Watanabe et al., 2012). The Arctic version of the coupled sea ice–ocean circulation marine ecosystem model has also reproduced active vertical convection occurring inside mesoscale eddies; this convection effectively transports nutrient- and particlerich (biogenic and mineral) subsurface water masses toward the surface (Watanabe et al., 2014), which allows zooplankton to be actively incubated inside the eddies, where they graze on the particles derived from active convection. Subsequently, these zooplankton are transported from the shelf break area of the Canada Basin to St. NAP in the Northwind Abyssal Plain by the anti-cyclonic Beaufort Gyre

(Watanabe et al., 2014). Anti-cyclonic mesoscale eddies are thus important both as transporters of trace minerals and phytoplankton from coastal to more oceanic waters (Johnson et al., 2005; Batten and Crawford, 2005) and, because they enhance the supply of nutrients to the mixed layer, as incubators of lower-trophic-level organisms. These roles of anti-cyclonic mesoscale eddies have previously been discussed with respect to the northwestern and northeastern subarctic Pacific Ocean (Kusakabe et al., 2002; Ueno et al., 2010; Peterson and Harrison, 2012). Mesoscale eddies, which have been detected in multiple shelf–basin boundary regions of the Arctic Ocean (Plueddemann et al., 1998; Woodgate et al., 2001; Dmitrenko et al., 2008), may play an important role by enhancing the biological pump via biogeochemical cycling as the sea ice retreats in the near future (Fig. 5). 6. Benthic community and higher-trophic-level organisms The enhancement of primary productivity in the surface resulting from the increase of POC flux also affects the benthic community on the seafloor because the POC flux is a direct source of food for the benthos (Clark, 2003; Bluhm et al., 2011). The pelagic–benthic coupling system is an important component of the food-web system of the Arctic Ocean. Although the benthic community includes some benthic diatoms as primary producers, the most abundant and widespread benthic species are brittle stars, amphipods, bivalves, and polychaetes (Bluhm et al., 2011). Bluhm et al. (2011) calculated the Arctic benthic species richness to be on the order of ~4600. The species richness is considered to exhibit a unimodal depth species diversity gradient (DSDG) with a peak at about 100–200 m depth in the Arctic Ocean (Clark, 2003), which is much shallower than the peak in other oceans, which is typically at 1000–2000 m depth (Rex and Etter, 2010). The species diversity of deep-sea prosobranch gastropods is negatively correlated with latitude in the North Atlantic and the Norwegian Sea; that is, species richness decreases as latitude increases (Clark, 2003); this latitudinal pattern is a fundamental feature of the world's biota (Willing et al., 2003; Rex and Etter, 2010). In contrast, a modeling study showed a deep unimodal DSDG in benthic foraminifera with a peak at depths on the order of 1000 m along with a unimodal latitudinal species diversity gradient (LSDG) with a peak at about 82–83°N; benthic ostracodes, however, showed the typical Arctic unimodal DSDG with a peak at 100 m depth and a negative LSDG (Yasuhara et al., 2012). Yasuhara et al. (2012) also suggested that the underlying mechanisms of these depth and latitudinal species diversity patterns are complex; moreover, the relative importance of the various environmental parameters, including seaice cover, temperature, salinity, primary productivity, and the seasonality of productivity, that determine DSDGs and LSDGs, might be different for different taxa. These environmental parameters, together with the POC flux, probably also affect the latitudinal and depth gradients of benthic species and the benthic–pelagic coupling system in the Arctic Ocean. Marine ecosystem diversity of higher-trophic-level organisms in the Arctic Ocean is controlled mainly by geographic characteristics (broad continental shelves and many riverine mouths), water-mass interactions between Pacific and Atlantic inflows, sea ice, and light and temperature conditions. Michel et al. (2012) reviewed the basic structure and diversity of the Arctic marine ecosystem and the predictable impacts of drastic environmental changes in the Arctic Ocean on the marine ecosystem. They indicated that Atlantic-origin species such as shrimp (Pandalus borealis, although this species also lives in Pacific Ocean), herring (Clupea harengus), Atlantic cod (Gadus morhua), and capelin (Mallotus villosus) associated with Atlantic water mass inflow inhabit middle and deep layer in the Barents, Norwegian, and Greenland seas. Pacific benthic species are found in the Chukchi Sea (Dunton, 1992; Bluhm et al., 2009), having passed through the Bering Strait, but otherwise Pacific influence on benthic fauna seems to be limited to the Beaufort and East Siberian seas (Grebmeier et al., 2006). Arctic zooplankton are predominantly of Atlantic origin; zooplankton of Pacific origin do

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Fig. 5. Conceptual diagram of the lateral transport and export flux of particles at St. NAP a) before and b) after the recent catastrophic sea-ice reduction in the Arctic Ocean. a) Lateral transport of lithogenic and old organic particles were the predominant mechanism from the shelf break into more oceanic waters before the recent catastrophic sea-ice reduction; b) fresh biological particles, which were incubated inside the eddy, have been added to the lithogenic and old organic particles, and such an eddy introduced biogenic particles that contributed to enhancement of the biological pump in the Arctic Ocean.

not occur in the Arctic Ocean, because the vertical distribution of the zooplankton assemblage is strongly related to water mass and zooplankton living in deep Pacific would not pass through the shallow Bering strait (Michel et al., 2012). Maximum zooplankton diversity, which occurs in subsurface to deep layers (300–2000 m), is associated with the Atlantic inflow. The presence of sea ice is fundamental to the maintenance of the ecosystem structure in the Arctic Ocean. As reviewed by Michel et al. (2012), the distribution and survival of C. glacialis, which is a key zooplankton species in the Arctic, depends on the timing and amount of ice algal production; in turn, zooplankton species and sea-ice-related amphipods are important food resources for Arctic cod, Boreogadus saida, and polar cod, A. glacialis, which are food resources for seabirds (fulmars, murres, guillemots, and kittiwakes) and mammals (ringed seals, narwals, and belugas). The top predator of the food web, the polar bear, uses sea ice for ice-based hunting of prey such as ringed seals. The loss of sea ice is expected to affect the ability of polar bears to maintain their body condition, and their ability to survive, because they cannot satisfy their nutritional requirements with terrestrial food sources, owing to insufficient quantities and competition with brown bears (Rode et al., 2015). Except for some diatom species, which can survive both just above the sediment and in sea ice, sea-ice reduction is likely to have a cascading negative effect throughout the pelagic– benthic food web of the Arctic Ocean. Temperature and light are important factors controlling the timing of blooms and the reproductive, metabolic, and growth rates of individual organisms. Seasonal temperature changes are relatively large above the continental shelves, compared with in the open ocean, and highamplitude seasonal temperature changes promote the diversity of the marine ecosystem in the Arctic Ocean (Michel et al., 2012). The maximum near-future temperature rise is expected to occur in the Earth's polar regions (IPCC, 2013), and the temperature change is expect to be accompanied by changes in oxygen concentrations, pH, and productivity, which are environmental stressors for marine organisms. During the Coupled Model Intercomparison Project Phase 5 (CMIP5), the cumulative stress of multiple stressors (changes in temperature, oxygen concentration, pH, and productivity) in 2100 was analyzed, and the results indicated that, among global marine habitats, the most negative impact would be in continental shelf areas and in shallow seas.

Moreover, subpolar and polar regions and lower-trophic-level oceanic species (euphausiids, cetaceans, squids, and pinnipeds) would be among the global biological hot spots (Mora et al., 2013). However, Mora et al. (2013) also suggested that productivity in the future Arctic Ocean might rise, overcoming the negative impact of ocean acidification. 7. Perspectives on Arctic ecosystem research The recent retreat of sea ice during the Arctic summer was especially dramatic in 2007 and 2012. The summer sea surface temperature in the Chukchi Sea is normally 4–6 °C, but it reached 12 °C in 2007 (Vanin, 2010; Matsuno et al., 2012). The retreat of sea ice in early summer 2007 (Markus et al., 2009) and enhanced solar heating (Mizobata et al., 2010; Vanin, 2010), among other factors, contributed to this anomalously high temperature. A change in the Pacific Water inflow through the Bering Strait is another possible cause of high SST in the Chukchi Sea, and a significant volumetric input of cold PWW (salinity up to 33.8) has not been apparent since 2003 (Itoh et al., 2012). It means that the inflowing water from Pacific is less cold and saline than before. Instead, subsurface warming on the Chukchi Shelf may have promoted the warming of the intermediate layer in the southern Canada Basin (Itoh et al., 2012). Shimada et al. (2006) have also reported that warming of the upper layer in the Canada Basin began in the late 1990s, and Steele et al. (2008) indicated that the heat content of the upper layer of the Chukchi Sea also increased during the 2000s. Nevertheless, Honjo et al. (2010) have suggested that an increase in productivity and enhancement of the biological pump in the Arctic Basin is unlikely in the near future, because high atmospheric pressure conditions are expected to suppress the physical mechanisms that bring nutrients to the surface in the newly ice-free area. However, the average area of summer sea ice in the Arctic Ocean was 6.9 × 106 km2 during the 1990s and declined to 3.9 × 106 km2 after the 2000s, and this reduction of sea ice facilitated an 84% volumetric increase of eddies in the western Arctic Ocean, as estimated by a pan-Arctic sea ice–ocean physics model (Watanabe et al., 2014). The model results also indicated that the increased occurrence of eddies in the Arctic Ocean would lead to particulate organic nitrogen fluxes during the 2000s that were approximately twice as high as those

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Fig. 6. Model estimated sea ice covering on October 1 in the (yellow) 2010 M, (pink) Ice2.0, and (blue) Ice0.5 cases. Black contours represent 1000 m isobaths. The location of St. NAP is shown by a yellow cone. The inset profile shows the vertical profile of November mean particulate organic nitrogen (PON) flux in each case (μmol-N m−2 d−1). The average region is the southwestern Canada Basin, which is outlined by a blue contour (modified from Watanabe et al., 2014).

during the 1990s (Watanabe et al., 2014; Fig. 6). The explanation is that eddies promote active vertical mixing between subsurface and surface waters, and the increased occurrence of eddies directly contributes to enhancement of primary production. Therefore, it seems likely that the sea-ice retreat will promote further enhancement of the biological pump by facilitating the occurrence of eddies in the Arctic Ocean in the near future. Pacific copepods, including resting individuals, were observed in the intermediate water layer throughout the year from October 2010 to September 2011 (Matsuno et al., 2013). During 2007, the numbers of large Pacific copepods increased remarkably south of Cape Lisburne (Matsuno et al., 2011), although a comparison of zooplankton numbers in 1991, 1992, 2007, and 2008 shows that interannual variability of the zooplankton community has not been large (Matsuno et al., 2012). In 2011, substantial numbers of Neocalanus cristataus, a copepod indigenous to the Pacific, were detected in sediment trap samples during August–September at St. NAP (Matsuno et al., 2015). These findings imply that Pacific copepods will be able to invade the Arctic Ocean and survive there under a shortened duration of sea-ice cover in the near future. Simultaneously, ocean acidification, which has seriously progressed in the Arctic Ocean (Rysgaard et al., 2007; Mathis et al., 2011), may have a negative impact on the survival of organisms there. In 1997, the Canada Basin surface water was oversaturated (Ω N 1) with respect to aragonite, but in 2008 it was undersaturated (Ω b 1) (YamamotoKawai et al., 2009). This undersaturation was caused by sea-ice meltwater, which greatly diluted the total alkalinity and dissolved inorganic carbon concentration (Yamamoto-Kawai et al., 2009). Subsurface waters at depths of 100–200 m in the Canada Basin in 2008 were also undersaturated with respect to aragonite owing to the influence of carbonate-corrosive PWW at those depths (Yamamoto-Kawai et al.,

2009). Calcifiers with aragonite tests, especially pteropods, will have difficulty producing their tests in such undersaturated waters, which will threaten their survival in the Arctic Ocean (Bates and Mathis, 2009; Fabry et al., 2009). However, the response of calcifiers to ocean acidification is not simple. For example, the calcification rate of Emiliania huxleyi (Lohmann), a pelagic coccolithophorid species, has been reported to decrease under high-CO2 conditions (Riebesell et al., 2000; Zondervan et al., 2001; Sciandra et al., 2003; Delille et al., 2005), but Iglesias-Rodriguez et al. (2008) found that a different strain of E. huxleyi increased its rate of coccolith production under high-CO2 conditions. Irie et al. (2010) used an optimality model to predict the evolutionary response of coccolithophorids to high-CO2 conditions under the assumption that the coccolith serves to reduce the instantaneous mortality rate; from the results, they concluded that natural selection favors a more heavily calcified exoskeleton when acidification-driven costs increase. If all calcifiers were excluded from the marine ecosystem, not only food chains but also global biogeochemical cycles would be negatively affected, because although coccolithophorids account for no more than 20% of total carbon fixation (Poulton et al., 2007), the global planktic foraminiferal flux to the ocean floor of 0.36–0.88 gigatons C y−1 accounts for 32–80% of the total deep marine calcite budget (Schiebel, 2002). The current methodology used to evaluate the impacts of ocean acidification is semi-quantitative and involves, for example, microscopic examination of carbonate tests and measurement of their weight (e.g., Bednaršek et al., 2012). The development of new quantification methodologies for accurate estimation of the physiological impacts of acidification on plankton are necessary to evaluate the impact of ocean acidification on organisms and marine ecosystems. One example is the Micro-focus X-ray Computing Tomography (MXCT) technique for measuring the X-ray attenuation of an object (calcifier), which is

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linearly related to its density (Iwasaki et al., 2015). The MXCT technique has the potential to be a robust method for quantifying the response of marine organisms to ocean acidification. Recent physiological experiments have succeeded in isolating and cloning E. huxleyi from the waters of the northern Bering Sea and Chukchi Sea (M. Satoh, University of Tsukuba, personal communication). Future culture experiments with strains of E. huxleyi isolated from the Arctic Ocean are expected to clarify whether this species will be able to invade the Arctic Ocean (because of warming effects), or not (because of ocean acidification). In addition, the response of E. huxleyi to freshening and iron depletion in the Arctic Ocean needs to be analyzed. Quantification of the impact on marine organisms of ocean acidification and other stressors such as warming and freshening will contribute to the improvement of coupled sea-ice physical and marine ecosystem (lower trophic level) models and should allow future conditions to be predicted with greater accuracy. In particular, a 3-D coupled sea-ice physical and marine ecosystem model with a resolution finer than 5 km (so that it can resolve eddies) is needed. The impact of global warming on higher-trophic-level organisms such as commercially valuable fish has been investigated in the sub-Arctic North Pacific (Welch et al., 1988; Kishi et al., 2010). Welch et al. (1988) compared the predicted distributions of sockeye salmon in winter (7 °C) and summer (12 °C), which are suitable temperature for living, based on the atmospheric CO2 concentration at the end of the 1980s (the Mauna Loa atmospheric CO2 concentration passed 350 ppmv in October 1989) with their distributions under a doubling of atmospheric CO2 to 700 ppmv as predicted by the Canadian Climate Center's group ocean–atmosphere general climate model (Boer et al., 1992; McFarlane et al., 1992). The results indicated that in the North Pacific, the area of acceptable thermal habitat would decrease to zero in summer and would be sharply lower during the winter. Only the Okhotsk Sea and the northern half of the Bering Sea would have acceptable habitat in winter with 700 ppmv of atmospheric CO2 (Welch et al., 1988). Kishi et al. (2010) investigated the impact of global warming on the distribution of Japanese chum salmon by using the marine ecosystem model NEMURO and the IPCC SRES-A1B scenario (SRES-A1B: special report of emissions scenarios and A1 scenario groups are distinguished by their technological emphasis and A1B is a balance across all sources of fossil and non-fossil energies where balanced is defined as not relying too heavily on one particular energy source). The NEMURO model predicted that only the Bering Sea and the northwestern part of the Okhotsk Sea would have an acceptable thermal habitat (8–12 °C) for Japanese chum salmon by midsummer 2050 (Kishi et al., 2010), and by summer 2095, no optimal temperature area for Japanese chum salmon would exist in the North Pacific. Instead, the thermally habitable area was predicted to shift to the Arctic Ocean (Kishi et al., 2010). Although these model studies by Welch et al. (1988) and Kishi et al. (2010) focused on global warming only, fishes have already begun to shift toward higher latitudes. For example, bluefin tuna, Thunnus thynnus (Linnaeus 1758), were captured in a single net-haul in 9–11 °C waters east of Greenland (65°N) in August 2012 during exploratory fishing for Atlantic mackerel, Scomber scombrus (Linnaeus 1758). Atlantic mackerel is a preferred prey species of bluefin tuna and itself a new immigrant to the area (B. R. MacKenzie, Technical Univ. of Denmark, unpublished data). Regional temperatures in August 2012 were historically high, as a consequence of a warming trend that began in 1985, and bluefin tuna were likely present in this region in part because the water temperature had reached warmer, physiologically more tolerable temperatures and in part because an important prey species (Atlantic mackerel) had immigrated into the region (B. R. MacKenzie, Technical Univ. of Denmark, personal communication). However, ocean acidification will be an additional stressor for some fish species in the near future (e.g., Arctic cod B. saida; D. Storch, Alfred Wegener Institute for Polar and Marine Research, unpublished data). Yoon et al. (2015), in the western Arctic Ocean, estimated the potential habitat of chum salmon, defined as an area where the growth rate of

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chum salmon was positive, by using a 3-D lower trophic ecosystem model and evaluated the habitat responses to monthly changes of water temperature between 2005 and 2095 under the IPCC SRES-A1B global warming scenario. The results predicted an expansion of the potential habitat of chum salmon under modern climate conditions because of rising water temperature and zooplankton density. However, under the climate condition in 2095, the area of potential habitat south of 71°N would shrink during summer owing to a temperature increase beyond the optimal range (4–12 °C) for chum salmon. A fish resources variability model to evaluate the effects of multiple environmental stressors of fishes (such as the NEMURO.FISH model; Kishi et al., 2011) needs to be developed for the Arctic Ocean; the results reported by Yoon et al. (2015) are based on predicted temperature changes only. Hopefully, an Arctic Ocean version of a fish resources variability model will make it possible to predict how the distribution and migration routes of higher-trophic-level organisms will be modified by warming, freshening, and acidification of the Arctic, and by changes in the community of grazing organisms such as zooplankton.

Acknowledgments NH is grateful to Drs. E. Siswanto, and E. Watanabe for providing the original figures (Figs. 3 and 6), used in this manuscript. I thank Dr. Thomas M. Cronin, Editor, and two anonymous reviewers for their fruitful comments that improved the manuscript. This work was supported by the Japan Agency for Marine-Earth Science and Technology, Arctic Challenge for Sustainability Project and the Japan Society for the Promotion of Science, KAKENHI (S) No. 22221003 and KAKENHI (S) No. 15H05712.

References Aagaard, K., Coachman, L.K., Carmack, E., 1981. On the halocline of the Arctic Ocean. DeepSea Res. 28, 529–545. Anderson, L.G., Olsson, K., Chierici, M., 1998. A carbon budget for the Arctic Ocean. Glob. Biogeochem. Cycles 12, 455–465. Arrigo, K.R., 2014. Sea ice ecosystems. Ann. Rev. Mar. Sci. 6, 439–467. http://dx.doi.org/10. 1146/annurev-marine-010213-135103. Arrigo, K.R., Perovich, D.K., Pickart, R.S., Brown, Z.W., van Dijken, G.L., Lowry, K.E., Mills, M.M., Palmer, M.A., Balch, W.M., Bates, N.R., Benitez-Nelson, C.R., Brownlee, E., Frey, K.E., Laney, S.R., Mathis, J., Matsuoka, A., Mitchell, B.G., Moore, G.W.K., Reynolds, R.A., Sosik, H.M., Swift, J.H., 2014. Phytoplankton blooms beneath the sea ice in the Chukchi Sea. Deep-Sea Research II 105, 1–16http://dx.doi.org/10.1016/j.dsr2.2014. 03.018. Arrigo, K.R., van Dijken, G.L., 2004. Annual cycles of sea ice and phytoplankton in Cape Bathurst polynya, southeastern Beaufort Sea, Canadian Arctic. Geophys. Res. Lett. 31, L08304. http://dx.doi.org/10.1029/2003GL018978. Arrigo, K.R., van Dijken, G., Pabi, S., 2008. Impact of a shrinking Arctic ice cover on marine primary production. Geophys. Res. Lett. 35, L19603. http://dx.doi.org/10.1029/ 2008GL035028. Arrigo, K.R., Lizotte, M.P., Mock, T., 2010. Primary producers and sea ice. In: Thomas, D.N., Dieckmann, G.S. (Eds.), Sea Ice, 2nd edition Wiley-Blackwell, Oxford, UK, pp. 283–326. Arrigo, K.R., Lizotte, M.P., Worthen, D.L., Dixon, P., Dieckmann, G., 1997. Primary production in Antarctic sea ice. Science 276, 394–397. Arrigo, K.R., Sullivan, C.W., Kremer, J.N., 1991. A bio-optical model of Antarctic sea ice. J. Geophys. Res. 96, 10581–10592. Arrigo, K.R., Worthen, D.L., Dixon, P., Lizotte, M.P., 1998. Primary productivity of near surface communities within Antarctic pack ice. In: Lizotte, M.P., Arrigo, K.R. (Eds.), Antarctic Sea Ice: Biological Processes, Interactions, and VariabilityAntarctic Research Series 73. American Geophysical Union, Washington D.C., pp. 23–43. Ashjian, C.J., Gallager, S.M., Plourde, S., 2005. Transport of plankton and particles between the Chukchi and Beaufort Seas during summer 2002, described using a Video Plankton Recorder. Deep-Sea Res. II 52, 3259–3280. Bates, N.R., Mathis, J.T., 2009. The Arctic Ocean marine carbon cycle: evaluation of air–sea CO2 exchanges, ocean acidification impacts and potential feedbacks. Biogeosciences 6, 2433–2459. Batten, S.D., Crawford, W.R., 2005. The influence of coastal origin eddies on oceanic plankton distributions in the eastern Gulf of Alaska. Deep-Sea Res. II 52 (7–8), 991–1010. Bauerfeind, E., 2004. North east water polynya. In: Stein, R., Macdonald, R.W. (Eds.), The Organic Carbon Cycle in the Arctic Ocean. Springer, Berlin, pp. 106–109. Bauerfeind, E., Garrity, C., Krumbholz, M., Ramseier, R.O., Voss, M., 1997. Seasonal variability of sediment trap collections in the Northeast Water Polynya. Part 2. Biochemical and microscopic composition sedimenting matter. J. Mar. Syst. 10 (1–4), 371–389.

14

N. Harada / Global and Planetary Change 136 (2016) 1–17

Bauerfeind, E., Leipe, T., Ramseier, R.O., 2005. Sedimentation at the permanently icecovered Greenland continental shelf (74°57.7′N/12°58.7′W): significance of biogenic and lithogenic particles in particulate matter flux. J. Mar. Syst. 56 (1–2), 151–166. Bednaršek, N., Tarling, G.A., Bakker, D.C.E., Fielding, S., Jones, E.M., Venables, H.J., Ward, P., Kuzirian, A., Lézé, B., Feely, R.A., Murphy, E.J., 2012. Extensive dissolution of live pteropods in the Southern Ocean. Nat. Geosci. 5. http://dx.doi.org/10.1038/NGEO1635. Bluhm, B.A., Gebruk, A.V., Gradinger, R., Hopcroft, R.R., Huettmann, F., Kosobokova, K.N., Sirenko, B.I., Weslawski, J.M., 2011. Arctic marine biodiversity: an update of species richness and examples of biodiversity change. Oceanography 24, 232–248. Bluhm, B.A., Iken, K., Mincks, S.I., Sirenko, B.I., Holladay, B.A., 2009. Community structure of epibenthic megafauna in the Chukchi Sea. Aquatic Biology 7, 269–293http://dx.doi. org/10.3354/ab00198. Boer, G.J., McFarlane, N.A., Lazare, M., 1992. Greenhouse gas-induced climate change simulated with the CCC second-generation general circulation model. J. Clim. 5, 1045–1077. Boetius, A., Damm, E., 1998. Benthic oxygen uptake, hydrolytic potentials and microbial biomass at the Arctic continental slope. Deep Sea Res. I 45 (2–3), 239–275. http:// dx.doi.org/10.1016/S0967-0637(97)00052-6. Budikova, D., 2009. Role of Arctic sea ice in global atmospheric circulation: a review. Global Planetary Change 68, 149–163. http://dx.doi.org/10.1016/j.gloplacha.2009. 04.001. Carmack, E.C., Macdonald, R.W., Jasper, S., 2004. Phytoplankton productivity on the Canadian Shelf of the Beaufort Sea. Mar. Ecol. Prog. Ser. 277, 37–50. Carmack, E., Barber, D., Christensen, J., Macdonald, R., Rudels, B., Sakshaug, E., 2006. Climate variability and physical forcing of the food webs and the carbon budget on pan-Arctic shelves. Prog. Oceanogr. 71, 145–181. Carmack, E., Wassmann, P., 2006. Food webs and physical–biological coupling on panArctic shelves: unifying concepts and comprehensive perspectives. Prog. Oceanogr. 71, 446–477. Chen, M., Huang, Y.P., Cai, P.G., Guo, L.D., 2003. Particulate organic carbon export fluxes in the Canada Basin and Bering Sea as derived from 234T/238U disequilibria. Arctic 58, 32–44. Clark, A., 2003. The polar deep seas. In: Tyler, P.A. (Ed.), Ecosystems of the Deep Oceans. Elsevier, Amsterdam pp, pp. 239–260. Coachman, L.K., Barnes, C.A., 1961. The contribution of Bering Sea water to the Arctic Ocean. Arctic 14, 147–161. Coale, K.H., Bruland, K.W., 1985. 234Th:238U disequilibria within the California Current. Limnol. Oceanogr. 30 (1), 22–33. Codispoti, L.A., Flagg, C., Kelly, V., Swift, J.H., 2005. Hydrographic conditions during the 2002 SBI process experiments. Deep-Sea Res. II 52, 3199–3226. Codispoti, L.A., Kelly, V., Thessen, A., Matrai, P., Suttles, S., Hill, V.J., Steele, M., Light, B., 2013. Synthesis of primary production in the Arctic Ocean: III. Nitrate and phosphate based estimates of net community production. Prog. Oceanogr. 110, 126–150. http:// dx.doi.org/10.1016/j.pocean.2012.11.006. Comiso, J.C., 2006. Abrupt decline in the Arctic winter sea ice cover. Geophys. Res. Lett. 33. http://dx.doi.org/10.1029/2006GL027341. Comiso, J.C., 2012. Large decadal decline of the Arctic multiyear ice cover. J. Clim. 25, 1176–1193. Cooper, L.W., Sexson, M.G., Grebmeier, J.M., Gradinger, R., Mordy, C.W., Lovvorn, J.R., 2013. Linkages between sea-ice coverage, pelagic–benthic coupling, and the distribution of spectacled eiders: observations in March 2008, 2009 and 2010, northern Bering Sea. Deep-Sea Res. II 94, 31–43. http://dx.doi.org/10.1016/j.dsr2.2013.03.009. Cota, G.F., Wang, J., Comiso, J.C., 2004. Transformation of global satellite chlorophyll retrievals with a regionally tuned algorithm. Remote Sens. Environ. 90, 373–377. Delille, B., Harlay, J., Zondervan, I., Jacquet, S., Chou, L., Wollast, R., Bellerby, R.G., Frankignoulle, M., Borges, A.V., Riebesell, U., Gattuso, J.-P., 2005. Response of primary production and calcification to changes of pCO2 during experimental blooms of the coccolithophorid Emiliania huxleyi. Glob. Biogeochem. Cycles 19, GB2023. http://dx. doi.org/10.1029/2004GB002318. Deser, C., Teng, H., 2008. Evolution of Arctic sea ice concentration trends and the role of atmospheric circulation forcing, 1979–2007. Geophys. Res. Lett. 35, L02504. http:// dx.doi.org/10.1029/2007GL032023. Dmitrenko, I.A., Kirillov, S.A., Ivanov, V.V., Woodgate, R.A., 2008. Mesoscale Atlantic water eddy off the Laptev Sea continental slope carries the signature of upstream interaction. J. Geophys. Res. 113, C07005. http://dx.doi.org/10.1029/2007JC004491. Dunton, K., 1992. Arctic biogeography: the paradox of the marine benthic fauna and flora. Trends in Ecology and Evolution 7, 183–189. Emmerton, C.A., Lesack, L.F.W., Vincent, W.F., 2008. Mackenzie River nutrient delivery to the Arctic Ocean and effects of the Mackenzie Delta during open water conditions. Glob. Biogeochem. Cycles 22, GB1024. http://dx.doi.org/10.1029/2006GB002856. Fabry, V.J., McClintock, J.B., Mathis, J.T., Grebmeier, J.M., 2009. Ocean acidification at high latitudes: the bellwether. Oceanography 22 (4), 160–171. Fahl, K., Nöthig, E.-M., 2007. Lithogenic and biogenic particle fluxes on the Lomonosov Ridge (central Arctic Ocean) and their relevance for sediment accumulation: vertical vs. lateral transport. Deep-Sea Res. I 54, 1256–1272. http://dx.doi.org/10.1016/j.dsr. 2007.04.014. Fiala, M., Kuosa, H., Kopczynska, E.E., Oriol, L., Delille, D., 2006. Spatial and seasonal heterogeneity of sea ice microbial communities in the first-year ice of Terre Adélie area (Antarctica). Aquat. Microb. Ecol. 43, 95–106. Forest, A., Sampei, M., Hattori, H., Makabe, R., Sasaki, H., Fukuchi, M., Wassmann, P., Fortier, L., 2007. Particulate organic carbon fluxes on the slope of the Mackenzie Shelf (Beaufort Sea): physical and biological forcing of shelf-basin exchanges. Journal of Marine System 68, 39–54. Forest, A., Galindo, V., Darnis, G., Lalande, C., Pineault, S., Tremblay, J.E., Fortier, L., 2011. Carbon biomass, elemental ratios (C:N) and stable isotopic composition (δ13C,

δ15N) of dominant calanoid copepods during the winter-to-summer transition in the Amundsen Gulf (Arctic Ocean). J. Plankton Res. 33, 161–178. Frey, K.E., Perovich, D.K., Light, B., 2011. The spatial distribution of solar radiation under a melting Arctic sea ice cover. Geophys. Res. Lett. 38, L22501. http://dx.doi.org/10. 1029/2011GL049421. Fukuchi, M., Sasaki, H., Hattori, H., Matsuda, O., Tanimura, A., Handa, N., McRoy, C.P., 1993. Temporal variability of particulate flux in the northern Bering Sea. Cont. Shelf Res. 13, 693–704. Garrison, D.L., 1991. Antarctic sea ice biota. Integrative and Comparative Biology, American Society of Zoologists 31, 17–34. http://dx.doi.org/10.1093/icb/31.1.17. Gaye, B., Fahl, K., Kodina, L.A., Lahajnar, N., Nagel, B., Unger, D., Gebhardt, A.C., 2007. Particulate matter fluxes in the southern and central Kara Sea compared to sediments: bulk fluxes, amino acids, stable carbon and nitrogen isotopes, sterols and fatty acids. Cont. Shelf Res. 27, 2570–2594. Gosselin, M., Levasseur, M., Wheeler, P.A., Horner, R.A., Booth, B.C., 1997. New measurements of phytoplankton and ice algal production in the Arctic Ocean. Deep Sea Res. II 44, 1623–1644. Gradinger, R., 2009. Sea-ice algae: Major contributors to primary production and algal biomass in the Chukchi and Beaufort Seas during May/June 2002. Deep Sea Res. II 56, 1201–1212. http://dx.doi.org/10.1016/j.dsr2.2008.10.016. Grebmeier, J.M., 2012. Biological community shifts in Pacific Arctic and sub-Arctic seas. Annual Review Marine Science 4, 63–78. 10.114/annurev-marine-120710-100926. Grebmeier, J.M., Cooper, L.W., Feder, H.M., Sirenko, B.I., 2006. Ecosystem dynamics of the Pacific influenced Northern Bering and Chukchi Seas. Prog. Oceanogr. 71, 331–361. Grebmeier, J.M., Harvey, H.R., 2005. The Western Arctic Shelf-Basin Interactions (SBI) Project: an overview. Deep-Sea Res. II 52, 3109–3115. Harada, N., Sato, M., Oguri, K., Hagino, K., Okazaki, Y., Katsuki, K., Tsuji, Y., Shin, K.-H., Tadai, O., Saitoh, S.-I., Narita, H., Konno, K., Jordan, R.W., Shiraiwa, Y., Grebmeier, J., 2012. Enhancement of coccolithophorid blooms in the Bering Sea by recent environmental changes. Glob. Biogeochem. Cycles 26, GB2036. http://dx.doi.org/10.1029/ 2011GB004177. Hargrave, B., 2004. North water polynya. In: Stein, R., Macdonald, R.W. (Eds.), The Organic Carbon Cycle in the Arctic Ocean. Springer, Berlin, pp. 103–106. Hargrave, B.T., Bodungen, B., Stoffyn-Egli, P., Mudie, J., 1994. Seasonal variability in particle sedimentation under permanent ice cover in the Arctic Ocean. Cont. Shelf Res. 14 (2–3), 279–293. Hill, V., Cota, G., 2005. Spatial patterns of primary production on the shelf, slope and basin of the Western Arctic in 2002. Deep Sea Res. II 52, 3344–3354. Hill, V.J., Matrai, P.A., Olson, E., Suttles, S., Steele, M., Codispoti, L.A., Zimmerman, R.C., 2013. Synthesis of integrated primary production in the Arctic Ocean: II. In situ and remotely sensed estimates. Prog. Oceanogr. 110, 107–125. http://dx.doi.org/10. 1016/j.pocean.2012.11.005. Hirawake, T., Shinmyo, K., Fujiwara, A., Saitoh, S., 2012. Satellite remote sensing of primary productivity in the Bering and Chukchi Seas using and absorption-based approach. ICES J. Mar. Sci. 69 (7), 1194–1204. http://dx.doi.org/10.1093/icesjms/fss111. Honjo, S., Manganini, S.J., Krishfield, R.A., Francois, R., 2008. Particulate organic carbon fluxes to the ocean interior and factors controlling the biological pump: a synthesis of global sediment trap programs since 1983. Prog. Oceanogr. 76, 217–285. Honjo, S., Krishfield, R.A., Eglinton, T.I., Manganini, S.J., Kemp, J.N., Doherty, K., Hwang, J., McKee, T.K., Takizawa, T., 2010. Biological pump processes in the cryopelagic and hemipelagic Arctic Ocean: Canada Basin and Chukchi Rise. Prog. Oceanogr. 85, 137–170. Hood, E., Fellman, J., Spencer, R.G.M., Hernes, P.J., Edwards, R., D'Amore, D., Scott, D., 2009. Glaciers as a source of ancient and labile organic matter to the marine environment. Nature 462. http://dx.doi.org/10.1038/nature08580. Horner, R.A., 1985. Sea-Ice Biota. CRC Press, Boca Raton, p. 215 ISBN 0-8493-6578-3. Hwang, J., Eglinton, T.I., Krishfield, R.A., Manganini, S.J., Honjo, S., 2008. Lateral organic carbon supply to the deep Canada basin. Geophys. Res. Lett. 35, L11607. http://dx. doi.org/10.1029/2008GL034271. Iglesias-Rodriguez, M.D., Halloran, P.R., Rickaby, R.E.M., Hall, I.R., Colmenero-Hidalgo, E., Gittins, J.R., Green, R.H., Tyrrell, T., Gibbs, S.J., von Dassow, P., Rehm, E., Armbrust, E.V., Boessenkool, K.P., 2008. Phytoplankton calcification in a high-CO2 world. Science 320, 336–340. Il'iash, L.V., Zhitina, L.S., 2009. Comparative analysis of sea-ice diatom species composition in the seas of Russian Arctic. Zhurnal Obshchei Biologii (Journal of General Biology) 70, 143–154 Russian with English abstract. Intergovernmental Panel on Climate Change (IPCC), 2007. Climate change 2007. In: Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L. (Eds.), The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA. Intergovernmental Panel on Climate Change (IPCC), 2013. Climate change 2013. In: Stocker, T.F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S.K., Boschung, J., Nauels, A., Xia, Y., Bex, V., Midgley, P.M. (Eds.), The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA. Irie, T., Bessho, K., Findley, H.S., Calosi, P., 2010. Increasing costs due to ocean acidification drives phytoplankton to be more heavily calcified: optimal growth strategy of coccolithophores. PLoS One 5 (10), e13436. Itoh, M., Carmack, E., Shimada, K., McLaughlin, F., Nishino, S., Zimmermann, S., 2007. Formation and spreading of Eurasian source oxygen-rich halocline water into the Canadian Basin in the Arctic Ocean. Geophys. Res. Lett. 34, L08603. http://dx.doi.org/10. 1029/2007GL029482. Itoh, M., Shimada, K., Kamoshida, T., McLaughlin, F., Carmack, E., Nishino, S., 2012. Interannual variability of Pacific Winter Water inflow through Barrow Canyon from

N. Harada / Global and Planetary Change 136 (2016) 1–17 2000 to 2006. J. Oceanogr. 68, 575–592. http://dx.doi.org/10.1007/s10872-012-01201. Iwasaki, S., Kimoto, K., Sasaki, O., Kano, H., Honda, M.C., Okazaki, Y., 2015. Observation of the dissolution process of Globigerina bulloides tests (planktic foraminifera) by X-ray micro-computed tomography. Paleoceanography 30, 317–331. http://dx.doi.org/10. 1002/2014PA002639. Jakobbson, M., Grantz, A., Kristoffersen, Y., Macnab, R., 2004. The Arctic Ocean: boundary conditions and background information. In: Stein, R., Macdonald, R.W. (Eds.), The Organic Carbon Cycle in the Arctic Ocean. Springer, New York, pp. 1–5. Jakobbson, M., Macnab, R., Mayer, L., Anderson, R., Edwards, M., Hatzky, J., Schenke, H.W., Johnson, P., 2008. An improved bathymetric portrayal of the Arctic Ocean: implications for ocean modeling and geological, geophysical and oceanographic analyses. Geophys. Res. Lett. 35, L07602. http://dx.doi.org/10.1029/2008GL033520. Jakobbson, M., Mayer, L., Coakley, B., Dowdeswell, J.A., Forbes, S., Fridman, B., Hodnesdal, H., Noormets, R., Pedersen, R., Rebesco, M., Scheneke, H.W., Zarayskaya, Y., Accettella, D., Armstrong, A., Anderson, R.M., Bienhoff, P., Camerlenghi, A., Church, I., Edwards, M., Gardner, J.V., Hall, J.K., Hell, B., Hestvik, O., Kristoffersen, Y., Marcussen, C., Mohammad, R., Mosher, D., Nghiem, S.V., Pedrosa, M.T., Travaglini, P.G., Weatherall, P., 2012. The international bathymetric chart of the Arctic Ocean (IBCAO) version 3.0. 39 p. L12609. http://dx.doi.org/10.1029/2012GL052219. Jin, M., Deal, C., Lee, S.H., Elliott, S., Hunke, E., Maltrud, M., Jeffery, N., 2012. Investigation of Arctic sea ice and ocean primary production for the period 1992–2007 using a 3-D global ice-ocean ecosystem model. Deep Sea Res. II 81–84, 28–35. http://dx.doi.org/ 10.1016/j.dsr2.2011.06.003. Johnson, W.K., Wong, C.S., Miller, L.A., Sutherland, N., Whitney, F.A., Chierici, M., 2005. Iron distribution and transport by Haida eddies. Deep Sea Res. II 52 (7–8), 933–954. Jones, E.P., Anderson, L.G., 1986. On the origin of the chemical properties of the Arctic Ocean halocline. J. Geophys. Res. 91, 10,759–10,767. Kadko, D., Pickart, R.S., Mathis, J., 2008. Age characteristics of a shelfbreak eddy in the western Arctic and implications for shelf–basin exchange. J. Geophys. Res. 113, C02018. http://dx.doi.org/10.1029/2007JC004429. Kaufman, D.S., Schneider, D.P., McKay, N.P., Ammann, C.M., Bradley, R.S., Briffa, K.R., Miller, G.H., Otto-Bliesner, B.L., Overpeck, J.T., Vinther, B.M., Arctic Lakes 2k Project Members, 2009. Recent warming reveres long-term Arctic cooling. Science 325, 1236–1239. http://dx.doi.org/10.1126/science.1173983. Kinder, T.H., Coachman, L.K., Galt, J.A., 1975. The Bering slope current system. J. Phys. Oceanogr. 5, 231–244. Kishi, M.J., Kashiwai, M., Ware, D.M., Megrey, B.A., Eslinger, D.L., Werner, F.E., NoguchiAita, M., Azumaya, T., Fujii, M., Hashimoto, S., Huang, D., Izumi, H., Ishida, Y., Kang, S., Kantakov, G.A., Kim, H.-C., Komatsu, K., Navrotsky, V.V., Lan Smith, S., Tadokoro, K., Tsuda, A., Yamamura, O., Yamanaka, Y., Yokouchi, K., Yoshie, N., Zhang, J., Zuenko, Y.I., Zvalinsky, V.I., 2007. NEMURO — a lower trophic level model for the North Pacific marine ecosystem. Ecological Modeling 202, 12–25. Kishi, M.J., Kaeriyama, M., Ueno, H., Kamezawa, Y., 2010. The effect of climate change on the growth of Japanese chum salmon (Oncorhynchus keta) using a bioenergetics model coupled with a three-dimensional lower tropic ecosystem model (NEMURO). Deep-Sea Res. II 57, 1257–1265. Kishi, M.J., Ito, S., Megrey, B.A., Rose, K.A., Werner, F.E., 2011. A review of the NEMURO and NEMURO.FISH models and their application to marine ecosystem investigations. J. Oceanogr. 67, 3–16. Kusakabe, M., Andreev, A., Lobanov, V., Zhabin, I., Kumamoto, Y., Murata, A., 2002. Effects of the anticyclonic eddies on water masses, chemical parameters and chlorophyll distributions in the Oyashio Current Region. J. Oceanogr. 58, 691–701. Lalande, C., Kepore, K., Cooper, L.W., Grebmeier, J.M., Moran, S.B., 2007. Export fluxes of particulate organic carbon in the Chukchi Sea: a comparative study using 234 Th/238U disequilibria and drifting sediment traps. Mar. Chem. 103, 185–196. Laney, S.R., Sosik, H.M., 2014. Phytoplankton assemblage structure in and around a massive under-ice bloom in the Chukchi Sea. Deep-Sea Research II 105, 30–41. http://dx. doi.org/10.1016/j.dsr2.2014.03.012. Lazzara, L., Nardello, I., Ermanni, C., Mangoni, O., Saggiomo, V., 2007. Light environment and seasonal dynamics of microalgae in the annual sea ice at Terra Nova Bay, Ross Sea, Antarctica. Antarct. Sci. 19, 83–92. Le Borgne, R., Rodier, M., 1997. Net zooplankton and the biological pump: a comparison between the oligotrophic and mesotrophic equatorial Pacific. Deep-Sea Research I 44, 2003–2023. Lee, S.H., Whitledge, T.E., 2005. Primary and new production in the deep Canada Basin during summer 2002. Polar Biol. 28, 190–197. Legendre, L., Ackley, S.F., Dieckmann, G.S., Gullicksen, B., Horner, R., Hoshiai, T., Melnikov, I.A., Reeburgh, W.S., Spindler, M., Sullivan, C.W., 1992. Ecology of sea ice biota — part 2: global significance. Polar Biol. 12, 429–444. Lepore, K., Moran, S.B., Grebmeier, J.M., Cooper, L.W., Lalande, C., Maslowski, W., Hill, V., Bates, N.R., Hansell, D.A., Mathis, J.T., Kelly, R.P., 2007. Seasonal and interannual changes in particulate organic carbon export and deposition in the Chukchi Sea. J. Geophys. Res. 112, C10024. http://dx.doi.org/10.1029/2006JC003555. Li, W.K.W., McLaughlin, F.A., Lovejoy, C., Carmack, E.C., 2009. Smallest algae thrive as the Arctic Ocean freshens. Science 326, 539. Lizotte, M.P., Sullivan, C.W., 1992. Biochemical composition and photosynthate distribution in sea ice microalgae of McMurdo Sound, Antarctica: evidence for nutrient stress during the spring bloom. Antarct. Sci. 4, 23–30. Longhurst, A.R., Harrison, W.G., 1988. Vertical nitrogen flux from the oceanic photic zone by diel migrant zooplankton and nekton. Deep-Sea Res. 35, 881–889. Makabe, R., Hattori, H., Sampei, M., Ota, Y., Fukuchi, M., Fortier, L., Sasaki, H., 2010. Regional and seasonal variability of zooplankton collected using sediment trap in the southeastern Beaufort Sea, Canadian Arctic. Polar Biol. 33, 257–270.

15

Manley, T.O., Hunkins, K., 1985. Mesoscale eddies of the Arctic Ocean. J. Geophys. Res. 90, 4911–4930. Markus, T., Stroeve, J.C., Miller, J., 2009. Recent changes in Arctic sea ice melt onset, freezeup, and melt season length. J. Geophys. Res. 114, C12024. http://dx.doi.org/ 10.1029/2009JC005436. Mathis, J.T., Cross, J.N., Bates, N.R., 2011. The role of ocean acidification in systematic carbonate mineral suppression in the Bering sea. Geophys. Res. Lett. 38, L19602. Mathis, J.T., Pickart, R.S., Hansell, D.A., Kadko, D., Bates, N.R., 2007. Eddy transport of organic carbon and nutrients from the Chukchi shelf: impact on the upper halocline of the western Arctic Ocean. J. Geophys. Res. 112, C05011. http://dx.doi.org/10. 1029/2006JC003899. Matrai, P.A., Olson, E., Suttles, S., Hill, V., Codispoti, L.A., Light, B., Steele, M., 2013. Synthesis of primary production in the Arctic Ocean: I. Surface waters, 1954–2007. Prog. Oceanogr. 110, 93–106. http://dx.doi.org/10.1016/j.pocean.2012.11.004. Matsuno, K., Yamaguchi, A., Fujiwara, A., Onodera, J., Watanabe, E., Harada, N., Kikuchi, T., 2015. Seasonal changes in the population structure of dominant planktonic copepods collected using a sediment trap moored in the western Arctic Ocean. J. Nat. Hist. 49, 2711–2726. http://dx.doi.org/10.1080/00222933.2015.1022613. Matsuno, K., Yamaguchi, A., Fujiwara, A., Onodera, J., Watanabe, E., Imai, I., Chiba, S., Harada, N., Kikuchi, T., 2013. Seasonal changes in mesozooplankton swimmers collected by sediment trap moored in the western Arctic Ocean. J. Plankton Res. 36, 490–502. http://dx.doi.org/10.1093/plankt/fbt092. Matsuno, K., Yamaguchi, A., Hirawake, T., Imai, I., 2011. Year-to-year changes of the mesozooplankton community in the Chukchi Sea during summers of 1991, 1992 and 2007, 2008. Polar Biol. 34, 1349–1360. Matsuno, K., Yamaguchi, A., Imai, I., 2012. Biomass size spectra of mesozooplankton in the Chukchi Sea during the summers of 1991/1992 and 2007/2008: an analysis using optical plankton counter data. ICES J. Mar. Sci. 69 (7), 1205–1217. http://dx.doi.org/10. 1093/icesjms/fss119. McFarlane, N.A., Boer, G.J., Blanchet, J.-P., Lazare, M., 1992. The Canadian Climate Center second-generation general circulation model and its equilibrium climate. J. Clim. 5, 1013–1044. McGuire, A.D., Anderson, L.G., Christensen, T.R., Dallimore, S., Guo, L., Hayes, D.J., Heimann, M., Lorenson, T.D., Macdonald, R.W., Roulet, N., 2009. Sensitivity of the carbon cycle in the Arctic to climate change. Ecol. Monogr. 79 (4), 523–555. Melnikov, I.A., Korneeva, G.A., Zhitina, L.S., Shanin, S.S., 2003. Dynamics of ecologicalbiochemical characteristics of sea ice in coastal waters of the White Sea. Biol. Bull. 30, 164–170. Michel, C., Bluhm, B., Gallucci, V., Gaston, A.J., Gordillo, F.J.L., Gradinger, R., Hopcroft, R., Jensen, N., Mustonen, T., Niemi, A., Nielsen, T.G., 2012. Biodiversity of Arctic marine ecosystems and responses to climate change. Biodiversity 13, 200–214, doi.org/ http://dx.doi.org/10.1080/14888386.2012.724048. Miller, C.B., Cowles, T.J., Wiebe, P.H., Copley, N.J., Grigg, H., 1991. Phenology in Calanus finmarchicus: hypotheses about control mechanisms. Mar. Ecol. Prog. Ser. 72, 79–91. Miller, C.B., Grigg, H., 1991. An experimental study of the resting phase in Calanus finmarchicus (Gunnerus). Bulletin of the Plankton Society of Japan Special 177, 479–493. Mizobata, K., Shimada, K., Woodgate, R., Saitoh, S.-I., Wang, J., 2010. Estimation of heat flux through the eastern Bering Strait. J. Oceanogr. 66, 405–424. Mora, C., Wei, C.-L., Rollo, A., Amaro, T., Baco, A.R., Billett, D., Bopp, L., Chen, Q., Collier, M., Danovaro, R., Gooday, A.J., Grupe, B.M., Halloran, P.R., Ingels, J., Jones, D.O.B., Levin, L.A., Nakano, H., Norling, K., Ramirez-Llodra, E., Rex, M., Ruhl, H.A., Smith, C.R., Sweetman, A.K., Thurber, A.R., Tjiputa, J.F., Usseglio, P., Watling, L., Wu, T., Yasuhara, M., 2013. Biotic and human vulnerability to projected changes in ocean biogeochemistry over the 21st century. PLoS Biol. 11, e1001682. Moran, S.B., Smith, J.N., 2000. 234Th as a tracer of scavenging and particle export in the Beaufort Sea. Cont. Shelf Res. 20, 153–167. http://dx.doi.org/10.1016/S0278-4343 (99)00065-5. Moran, S.B., Ellis, K.M., Smith, J.N., 1997. 234Th/238U disequilibria in the central Arctic Ocean: implications for particulate organic carbon export. Deep-Sea Res. II 44, 1593–1606. Moran, S.B., Kelly, R.P., Hagstrom, K., Smith, J.N., Grebmeier, J.M., Cooper, L.W., Cota, G.F., Walsh, J.J., Bates, N.R., Hansell, D.A., Maslowski, W., Nelson, R.P., Mulsow, S., 2005. Seasonal changes in POC export flux in the Chukchi Sea and implications for water column-benthic coupling in Arctic shelves. Deep-Sea Res. II 52, 3427–3451. Nishino, S., Kikuchi, T., Yamamoto-Kawai, M., Kawaguchi, Y., Hirawake, T., Itoh, M., 2011a. Enhancement/reduction of biological pump depends on ocean circulation in the seaice reduction regions of the Arctic Ocean. J. Oceanogr. 67, 305–314. http://dx.doi.org/ 10.1007/s10872-011-0030-7. Nishino, S., Itoh, M., Kawaguchi, Y., Kikuchi, T., Aoyama, M., 2011b. Impact of an unusually large warm-core eddy on distributions of nutrients and phytoplankton in the southern Canada Basin during late summer/early fall 2010. Geophys. Res. Lett. 38, L16602. http://dx.doi.org/10.1029/2011GL047885. Nishino, S., Shimada, K., Itoh, M., Chiba, S., 2009. Vertical double silicate maxima in the sea-ice reduction region of the western Arctic Ocean: implications for an enhanced biological pump due to sea-ice reduction. J. Oceanogr. 60, 871–883. O'Brien, M.C., MacDonald, R.W., Melling, H., Iseki, K., 2006. Particle fluxes and geochemistry on the Canadian Beaufort Shelf: implications for sediment transport and deposition. Cont. Shelf Res. 26, 41–81. O'Brien, M.C., Melling, H., Pedersen, T.F., Macdonald, R.W., 2011. The role of eddies and energetic ocean phenomena in the transport of sediment from shelf to basin in the Arctic. J. Geophys. Res. 116, C08001. O'Brien, M.C., Melling, H., Pedersen, T.F., Macdonald, R.W., 2013. The role of eddies on particle flux in the Canada Basin of the Arctic Ocean. Deep-Sea Res. I 71, 1–20.

16

N. Harada / Global and Planetary Change 136 (2016) 1–17

Onodera, J., Watanabe, E., Harada, N., Honda, M., 2015a. Diatom flux reflects water- mass conditions on the southern Northwind Abyssal Plain, Arctic Ocean. Biogeosciences 12, 1373–1385. http://dx.doi.org/10.5194/bg-12-1373-2015. Onodera, J., Watanabe, E., Nishino, S., Harada, N., 2015b. Distribution and vertical fluxes of silicoflagellates, ebridians, and the endoskeletal dinoflagellate Actiniscus in the western Arctic Ocean. Polar Biology doi:10/1007/s00300-015-1784-y. Orr, J.C., Fabry, V.J., Aumont, O., Bopp, L., Doney, S.C., Feely, R.A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key, R.M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R.G., Plattner, G.-K., Rodgers, K.B., Sabine, C.L., Sarmiento, J.L., Schlitzer, R., Slater, R.D., Totterdell, I.J., Weirig, M.-F., Yamanaka, Y., Yool, A., 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686. Overland, J.E., Wang, M., Salo, S., 2008. The recent Arctic warm period. Tellus 60A, 589–597. Pabi, S., van Dijken, G.L., Arrigo, K.R., 2008. Primary production in the Arctic Ocean, 1998–2006. J. Geophys. Res. 113, C08005. http://dx.doi.org/10.1029/2007JC004578. Peterson, T.D., Harrison, P.J., 2012. Diatom dynamics in a long-lived mesoscale eddy in the northeast subarctic Pacific Ocean. Deep-Sea Res. I 65, 157–170. Petrova, V.I., Batorva, G.I., Zinchenko, A.G., Kursheva, A.V., Narkevskiy, E.V., 2004. The East Siberian Sea: distribution, sources and burial of organic carbon. In: Stein, R., Macdonald, R.W. (Eds.), The Organic Carbon Cycle in the Arctic Ocean. SpringerVerlag, New York, pp. 204–212. Pickart, R.S., Weingartner, T.J., Pratt, L.J., Zimmermann, S., Torres, D.J., 2005. Flow of winter-transformed Pacific water into the Western Arctic. Deep-Sea Res. II 52, 3175–3198. http://dx.doi.org/10.1016/j.dsr2.2005.10.009. Plueddemann, A.J., Krishfield, R., Takizawa, T., Hatakeyama, K., Honjo, S., 1998. Upper ocean velocities in the Beaufort Gyre. Geophys. Res. Lett. 25, 183–186. Poulton, A.J., Adey, T.R., Balch, W.M., Holligan, P.M., 2007. Relating coccolithophore calcification rates to phytoplankton community dynamics: regional differences and implications for carbon export. Deep-Sea Res. II 54, 538–557. Ratkova, T.N., Wassmann, P., 2005. Sea ice algae in the White and Barents seas: composition and origin. Polar Res. 24, 95–110. Rex, M.A., Etter, R.J., 2010. Deep-sea Biodiversity: Pattern and Scale. Harvard University Press, Cambridge, MA, p. 368. Riaux-Gobin, C., Poulin, M., Prodon, R., Treguer, P., 2003. Land-fast ice microalgal and phytoplanktonic communities (Adélie Land, Antarctica) in relation to environmental factors during ice break-up. Antarct. Sci. 15, 353–364. Riebesell, U., Zondervan, I., Rost, B., Tortell, P.D., Zeebe, R.E., Morel, F.M.M., 2000. Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407, 364–367. Rode, K.D., Robbins, C.T., Nelson, L., Amstrup, S.C., 2015. Can polar bears use terrestrial foods to offset lost ice-based hunting opportunities? Front. Ecol. Environ. 13, 138–145. http://dx.doi.org/10.1890/140202. Rudels, B., Anderson, L.G., Jones, E.P., 1996. Formation and evolution of the surface mixed layer and halocline of the Arctic Ocean. J. Geophys. Res. 101, 8807–8821. Ryan, K.G., Hegseth, E.N., Martin, A., Davy, S.K., O'Toole, R., Ralph, P.J., Mcminn, A., Thorn, C.J., 2006. Comparison of the micro algal community within fast ice at two sites along the Ross Sea coast, Antarctica. Antarct. Sci. 18, 583–594. http://dx.doi.org/10.1017/ S0954102006000629. Rysgaard, S., Glud, R.N., Sejr, M.K., Bendtsen, J., Christensen, P.B., 2007. Inorganic carbon transport during sea ice growth and decay: a carbon pump in polar seas. J. Geophys. Res. 112, C03016. Rysgaard, S., Kuhl, M., Glud, R.N., Hansen, J.W., 2001. Biomass, production and horizontal patchiness of sea ice algae in a high-Arctic fjord (Young Sound, NE Greenland). Mar. Ecol. Prog. Ser. 223, 15–26. Sakshaug, E., 2004. Primary and secondary production in the Arctic ocean. In: Stein, R., Macdonald, R.W. (Eds.), The Organic Carbon Cycle in the Arctic Ocean. Springer, Berlin, pp. 57–81. Sampei, M., Sasaki, H., Forest, A., Fortier, L., 2012. A substantial export flux of particulate organic carbon linked to sinking dead copepods during winter 2007–2008 in the Amundsen Gulf (southeastern Beaufort Sea, Arctic Ocean). Limnol. Oceanogr. 57, 90–96. http://dx.doi.org/10.4319/lo.2012.57.1.0090. Sampei, M., Sasaki, H., Hattori, H., Forest, A., Fortier, L., 2009. Significant contribution of passively sinking copepods to the downward export flux in Arctic waters. Limnol. Oceanogr. 54, 1894–1900. http://dx.doi.org/10.4319/lo.2009.54.6.1894. Sampei, M., Sasaki, H., Hattori, H., Fukuchi, M., Hargrave, B.T., 2004. Fate of sinking particles, especially fecal pellets, within the epipelagic zone in the North Water (NOW) polynya of northern Baffin Bay. Mar. Ecol. Prog. Ser. 278, 17–25. Sampei, M., Sasaki, H., Makabe, R., Forest, A., Hattori, H., Tremblay, J.-É., Gratton, Y., Fukuchi, M., Fortier, L., 2011. Production and retention of biogenic matter in the southeast Beaufort Sea during 2003–2004: insights from annual vertical particle fluxes of organic carbon and biogenic silica. Polar Biol. 34, 501–511. http://dx.doi. org/10.1007/s00300-010-0904-y. Sarmiento, J.L., Gruber, N., 2006. Ocean Biogeochemical Dynamics. Princeton University Press, Princeton, NJ, USA, p. 503. Schiebel, R., 2002. Planktic foraminiferal sedimentation and the marine calcite budget. Glob. Biogeochem. Cycles 16 (4), 1065. http://dx.doi.org/10.1029/2001GB001459. Sciandra, A., Harlay, J., Lefèvre, D., Lemée, R., Rimmelin, P., Denis, M., Gattuso, J.-P., 2003. Response of coccolithophorid Emiliania huxleyi to elevated partial pressure of CO2 under nitrogen limitation. Mar. Ecol. Prog. Ser. 261, 111–122. Shimada, K., Carmack, E.C., Hatakeyama, K., Takizawa, T., 2001. Varieties of shallow temperature maximum waters in the western Canada Basin of the Arctic Ocean. Geophys. Res. Lett. 28, 3441–3444. Shimada, K., Kamoshida, T., Itoh, M., Nishino, S., Carmack, E., McLaughlin, F., Zimmermann, S., Proshutinsky, A., 2006. Pacific Ocean inflow: influence on

catastrophic reduction of sea ice cover in the Arctic Ocean. Geophys. Res. Lett. 33, L08605. http://dx.doi.org/10.1029/2005GL025624. Spall, M.A., Pickart, R.S., Fratantoni, P.S., Plueddemann, A.J., 2008. Western Arctic shelfbreak eddies: formation and transport. J. Phys. Oceanogr. 38, 1644–1668. Springer, A.M., McRoy, C.P., 1993. The paradox of pelagic food webs in the northern Bering Sea-III. Patterns of primary productivity. Cont. Shelf Res. 13, 575–599. Springer, A.M., McRoy, C.P., Flint, M.V., 1996. The Bering Sea green belt: shelf-edge processes and ecosystem production. Fish. Oceanogr. 5, 205–223. Stammerjohn, S., Massom, R., Rind, D., Martinson, D., 2012. Regions of rapid sea ice change: an inter-hemispheric seasonal comparison. Geophys. Res. Lett. 39, L06501. http://dx.doi.org/10.1029/2012GL050874. Steele, M., Morison, J., Ermold, W., Rigor, I., Ortmeyer, M., Shimada, K., 2004. Circulation of summer Pacific halocline water in the Arctic Ocean. J. Geophys. Res. 109, C02027. http://dx.doi.org/10.1029/2003JC002009. Steele, M., Ermold, W., Zhang, J., 2008. Arctic Ocean surface warming trends over the past 100 years. Geophys. Res. Lett. L02614. http://dx.doi.org/10.1029/2007GL031651. Stein, R., Macdonald, R.W., 2004. Arctic Ocean organic carbon accumulation and its global significance. In: Stein, R., Macdonald, R.W. (Eds.), The Organic Carbon Cycle in the Arctic Ocean. Springer, Berlin, Germany, pp. 315–322. Steinberg, D.K., Carlson, C.A., Bates, N.R., Goldthwait, S.A., Madin, L.P., Michaels, A.F., 2000. Zooplankton vertical migration and the active transport of dissolved organic and inorganic carbon in the Sargasso Sea. Deep-Sea Res. I 47, 137–158. Stroeve, J.C., Serreze, M.C., Holland, M.M., Kay, J.E., Malanik, J., Barrett, A.P., 2012. The Arctic's rapidly shrinking sea ice cover: a research synthesis. Clim. Chang. 110, 1005–1027. http://dx.doi.org/10.1007/s10584-011-0101-1. Sumata, H., Shimada, K., 2007. Northward transport of Pacific summer water along the Northwind Ridge in the western Arctic Ocean. J. Oceanogr. 63, 363–378. Takahashi, T., Sutherland, S.C., Wanninkhof, R., Sweeney, C., Feely, R.A., Chipman, D.W., Hales, B., Friederich, G., Chavez, F., Sabine, C., Watson, A., Bakker, D.C.E., Schuster, U., Metzl, N., Yoshikawa-Inoue, H., Ishii, M., Midorikawa, T., Nojiri, Y., Kortzinger, A., Steinhoff, T., Hoppema, M., Olafsson, J., Arnarson, T.S., Tilbrook, B., Johannessen, T., Olsen, A., Bellerby, R., Wong, C.S., Delille, B., Bates, N.R., de Baar, H.J.W., 2009. Climatological mean and decadal change in surface ocean pCO2, and net sea–air CO2 flux over the global oceans. Deep-Sea Res. II 56, 554–577. http://dx.doi.org/10.1016/j. dsr2.2008.12.009. Taniguchi, A., 1999. Differences in the structure of the lower trophic levels of pelagic ecosystems in the eastern and western subarctic Pacific. Prog. Oceanogr. 43, 289–315. Tremblay, J.-E., Simpson, K., Martin, J., Miller, L., Gratton, Y., Barber, D., Price, N.M., 2008. Vertical stability and the annual dynamics of nutrients and chlorophyll fluorescence in the coastal, southeast Beaufort Sea. Journal of Geophysical Research 113, C07S90. http://dx.doi.org/10.1029/2007JC004547. Trimble, S.M., Baskaran, M., 2005. The role of suspended particulate matter in 234Th scavenging and 234Th-derived export fluxes of POC in the Canada Basin of the Arctic Ocean. Mar. Chem. 96, 1–19. Ueno, H., Crawford, W.R., Onishi, H., 2010. Impact of Alaskan Stream eddies on chlorophyll distribution in the North Pacific. J. Oceanogr. 66, 319–328. Vanin, N.S., 2010. Thermohaline water structure on the southwestern Chukchi Sea shelf under conditions of opposite regimes of atmospheric circulation in summer periods of 2003 and 2007. Russ. Meteorol. Hydrol. 35, 468–475. Wang, J., Hu, H., Mizobata, K., Saitoh, S., 2009. Seasonal variations of sea ice and ocean circulation in the Bering Sea: a model-data fusion study. J. Geophys. Res. 14, C02011. Wassmann, P., Bauerfeind, E., Fortier, M., Fukuchi, M., Hargrave, B., Honjo, S., Moran, B., Noji, T., Nöthig, E.M., Peinert, R., 2004. Particulate organic carbon flux to the Arctic Ocean sea floor. In: Stein, R., Macdonald, R.W. (Eds.), The Organic Carbon Cycle in the Arctic Ocean. Springer, Berlin, pp. 101–138. Watanabe, E., 2011. Beaufort shelf break eddies and shelf–basin exchange of Pacific summer water in the western Arctic Ocean detected by satellite and modeling analyses. J. Geophys. Res. 116, C08034. http://dx.doi.org/10.1029/2010JC006259. Watanabe, E., Kishi, M.J., Ishida, A., Noguchi-Aita, M., 2012. Western Arctic primary productivity regulated by shelf-break warm eddies. J. Oceanogr. 68, 703–718. http://dx. doi.org/10.1007/s10872-012-0128-6. Watanabe, E., Onodera, J., Harada, N., Aita, M.N., Ishida, A., Kishi, J., 2015. Wind-driven interannual variability of sea ice algal production in the western Arctic Chukchi Borderland. Biogeosciences 12, 1–22. http://dx.doi.org/10.519/bg-12-1-2015. Watanabe, E., Onodera, J., Harada, N., Honda, M., Kimoto, K., Kikuchi, T., Nishino, S., Matsuno, K., Yamaguchi, A., Ishida, A., Kishi, J.M., 2014. Enhanced role of eddies in the Arctic marine biological pump. Nat. Commun. http://dx.doi.org/10.1038/ ncomms4950. Weingartner, T., Aagaard, K., Woodgate, R., Danielson, S., Sasaki, Y., Cavalieri, D., 2005. Circulation on the North Central Chukchi Sea shelf. Deep-Sea Res. II 52, 3150–3174. Welch, D.W., Ishida, Y., Nagasawa, K., 1988. Thermal limits and ocean migrations of sockeye salmon (Oncorhynchus nerka): long-term consequences of global warming. Can. J. Fish. Aquat. Sci. 55, 937–948. Werner, I., Ikavalko, J., Schunemann, H., 2007. Sea-ice algae in Arctic pack ice during late winter. Polar Biol. 30, 1493–1504. Willing, M.R., Kaufman, D.M., Stevents, R.D., 2003. Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annual Reviews of Ecology, Evolution, and Systematics 34, 273–309. Whitaker, T.M., Richardson, M.G., 1980. Morphology and chemical composition of a natural population of an ice-associated Antarctic diatom Navicula glaciei. J. Phycol. 16, 250–257. Woodgate, R.A., Aagaard, K., Muench, R.D., Gunn, J., Björk, G., Rudels, B., Roach, A.T., Schauer, U., 2001. The Arctic Ocean Boundary Current along the Eurasian slope and the adjacent Lomonosov Ridge: water mass properties, transports and transformations from moored instruments. Deep-Sea Res. I 48, 1757–1792.

N. Harada / Global and Planetary Change 136 (2016) 1–17 Wu, B., Wang, J., Walsh, J.E., 2006. Dipole anomaly in the winter Arctic atmosphere and its association with sea ice motion. J. Clim. 19, 210–225. Yamamoto-Kawai, M., McLaughlin, F.A., Carmack, E.C., Nishino, S., Shimada, K., 2009. Aragonite undersaturation in the Arctic Ocean: effects of ocean acidification and sea ice melt. Science 326, 1098–1100. http://dx.doi.org/10.1126/science.1174190. Yasuhara, M., Hunt, G., van Dijken, G., Arrigo, K.R., Cronin, T.M., Wollenburg, J.E., 2012. Patterns and controlling factors of species diversity in the Arctic Ocean. J. Biogeogr. 39, 2081–2088. http://dx.doi.org/10.1111/j.1365-2699.2012.02758.x. Yoon, S., Watanabe, E., Ueno, H., Kishi, M.J., 2015. Potential habitat for chum salmon (Oncorhynchus keta) in the Western Arctic based on a bioenergetics model coupled with a three-dimensional lower trophic ecosystem model. Prog. Oceanogr. 131, 146–158. http://dx.doi.org/10.1016/j.pocean.2014.12.009.

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Zhang, R., Chen, M., Ma, Q., Cao, J., Qiu, Y., 2015. Insights into the coupling of upper oceanbenthic carbon dynamics in the western Arctic Ocean from an isotopic (13C, 234Th) perspective. Acta Oceanol. Sin. 34, 26–33. http://dx.doi.org/10.1007/s13131-0150684-x. Zernova, V.V., Nothig, E.M., Shevchenko, V.P., 2000. Vertical microalgae flux in the Northern Laptev Sea (from the data collected by the yearlong sediment trap). Oceanology c/c of Okeanologiia 40 (6), 801–808. Zondervan, I., Zeebe, R.E., Rost, B., Riebesell, U., 2001. Decreasing marine biogenic calcification: a negative feedback on rising atmospheric pCO2. Glob. Biogeochem. Cycles 15, 507–516.