Greenland seas and shelves

Progress in Oceanography 114 (2013) 26–45

Contents lists available at SciVerse ScienceDirect

Progress in Oceanography journal homepage: www.elsevier.com/locate/pocean

Phytoplankton production and growth regulation in the Subarctic North Atlantic: A comparative study of the Labrador Sea-Labrador/Newfoundland shelves and Barents/Norwegian/Greenland seas and shelves W. Glen Harrison a, K. Yngve Børsheim b, William K.W. Li a,⇑, Gary L. Maillet c, Pierre Pepin c, Egil Sakshaug d, Morten D. Skogen b, Philip A. Yeats a a

Bedford Institute of Oceanography, Dartmouth, Nova Scotia, Canada Institute of Marine Research, Bergen, Norway c Northwest Atlantic Fisheries Centre, St. John’s, Newfoundland, Canada d University of Trondheim, Trondheim, Norway b

a r t i c l e

i n f o

Article history: Available online 9 May 2013

a b s t r a c t A study was made of phytoplankton (distribution, phenology, physiology, productivity and community composition) and environment properties that influence their growth (light and nutrients) comparing the western Subarctic Atlantic (Labrador Sea, Labrador/Newfoundland shelves) with the eastern Subarctic (Barents, Norwegian and Greenland Seas and shelves) and drawing on ship-based observations, satellite ocean colour data (SeaWiFS) and output from a 3D coupled ecosystem-ocean circulation model, covering the last 15–25 yrs. Similarities between regions were seen in geographic variability (e.g. latitudinal gradients), seasonal cycles and magnitude of phytoplankton biomass and productivity, and community composition. Regional differences were related to geographic location, presence/absence of ice, seasonal mixing, source waters (Arctic versus Atlantic) and nutrient supply, and response to atmospheric forcing. With regard to the latter, most of the observations considered in this study cover the recent period of rapid warming and the historical out-of-phase response (e.g. ice conditions, air and ocean temperatures, hydrography) of the western and eastern Subarctic Atlantic to atmospheric forcing is no longer apparent. Observations and modelling looking back over the last two decades suggest that the timing of the spring bloom and peak seasonal productivity are occurring progressively earlier in the year, particularly at high latitudes in both the western and eastern Subarctic. Climate change (ocean warming) is projected to increase overall phytoplankton productivity in the Subarctic Atlantic and will be manifest particularly in ice-influenced regions Labrador/Newfoundland Shelves, Barents/Greenland Seas and shelves and regions where Arctic outflow and Atlantic inflow influence phytoplankton dynamics. Northward movement of Atlantic waters as a result of climate change, manifest earliest in the eastern Subarctic (Norwegian/Barents Seas) will displace cold-water phytoplankton species with warm-water species and shift community transitions zones farther north in the coming decades. Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved.

1. Introduction Over the past two decades or so, data collected or generated from large-scale ocean surveys, satellites and coupled circulation models have provided an unprecedented perspective on the spatial and temporal dynamics of oceanographic processes at the ocean basin to global scale. One of the most striking of the global features is the pronounced seasonal growth cycle of phytoplankton from satellite ocean colour, the signal being strongest and most variable at the high, sub-polar latitudes. There is no place this is more evident

⇑ Corresponding author. E-mail address: [email protected] (W.K.W. Li).

than the North Atlantic. This is not only a region of high (and highly variable) biological production, but also one where ocean physics (convective mixing) and biology work in concert to form one of the principle oceanic ‘‘sinks’’ for atmospheric CO2 and a major focal point for ocean feedbacks to the climate system. Emerging interest in the continuing global decline in harvestable ocean living resources, the role their supporting ecosystems play and how climate change will influence these linkages were some of the principal questions underlying the NORCAN comparative ecosystem study. This paper represents an analysis of the distribution, seasonal cycles and environmental factors that control the distribution, growth and productivity of phytoplankton in the Northwest (Labrador Sea, Labrador and Newfoundland shelves) and Northeast (Barents, Greenland and Norwegian seas and shelves) Subarctic

0079-6611/$ - see front matter Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pocean.2013.05.003

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

Atlantic and how climate change might influence the ecological dynamics at the base of the sub-polar foodweb. Longhurst’s Ecological Geography of the Sea (Longhurst, 2007) partitions the global ocean based on the growth dynamics of phytoplankton as mediated primarily by physical processes. According to this classification, the NORCAN regions fall within the Atlantic Polar Biome (APB) where, at its northern boundaries, phytoplankton growth is largely irradiance-mediated, set primarily by freeze–thaw cycles of sea ice and the high-latitude extremes in the solar cycle. At its more southerly boundaries, ice and solar extremes have less influence, and seasonal wind and thermal cycles that determine mixing patterns, have a greater influence on phytoplankton growth with the consequence that both light and nutrients can limit productivity. The APB, with a complex geography including perpetually ice-covered waters, marginal ice zones (MIZs), polynyas and ice-free open waters, can be further sub-divided into three ecological provinces, the Boreal Polar Province (BPLR), the Atlantic Arctic Province (ARCT) and the Atlantic Subarctic Province (SARC). The ice-dominated BPLR includes the Arctic Ocean proper, adjacent MIZs and polynya areas; NORCAN regions in this province include the Barents Sea north of the polar front (polar domain influenced by Arctic waters) and the Labrador Shelf. The ARCT includes the two major North Atlantic cyclonic sub-polar gyres east and west of the southern tip of Greenland, and generally ice-free open water regions characterized by deep winter convective mixing; NORCAN regions in this province include the Labrador and Greenland Seas. The SARC is also generally ice-free with deep winter mixing (but deep mixing not to the extent of ARCT) and is dominated by northward flowing Atlantic waters: NORCAN regions in this province include the Norwegian Sea and Shelf and the Barents Sea south of the Polar Front (Atlantic domain influenced by Atlantic waters). The northern Newfoundland Shelf is actually not included in any of these provinces but due to the strong influence of sea ice in the region, it is included in this comparative analysis. Sakshaug (2004) has taken a slightly different approach by partitioning the high latitude seas based on geography, bathymetry and process. These include: the deep Arctic Ocean basin, polynyas, Arctic shelf seas (which includes the Barents Sea) and the so-called Atlantic Sector (which includes most of the NORCAN regions, i.e. the Greenland, Norwegian and Labrador Seas and their shelves). Again, the Newfoundland Shelf is not included but will be considered in this comparative analysis. Compared to the relatively limited information on phytoplankton in the Northwest Subarctic Atlantic, considerable research has been done in the eastern Subarctic (particularly in the Norwegian and Barents Seas) over the past several decades and much of this work has been summarized in a number of excellent reviews (e.g. Rey, 2004; Sakshaug and Walsh, 2000; Sakshaug, 2004). The general approach taken in these syntheses has been to describe the seasonal growth cycle of phytoplankton, emphasizing the influence of local environmental and biotic factors (light, nutrients, grazing) on their physiology, productivity and community structure. The seasonal cycle has been divided into the winter/early spring pre-bloom period, the spring bloom period, and the summer/fall post-bloom period. These studies have emphasized mean conditions and regional variability and provided only a limited description of inter-annual variability, but have included some discussion of anticipated future trends related to climate change (e.g. see Loeng et al., 2005). However, more recent work employing coupled circulation-biochemical models have investigated the influence of large-scale forcing (e.g. NAO, ice, water transport) on phytoplankton production and temporal trends in the North Atlantic (e.g. Skogen et al., 2007; Hensen et al., 2009). In this comparative analysis, we take a similar approach, employing observational data to establish mean phytoplankton

27

conditions for the NORCAN regions, describe temporal trends where possible and employ a coupled 3D physical–chemical–biological model to explore the influence of large-scale forcing on phytoplankton dynamics. Emphasis is placed on ‘‘bottom-up’’ environmental controls (light, nutrients); ‘‘top-down’’ (zooplankton grazing) controls are addressed in a companion paper (Head et al., 2013).

2. Observations and modelling Evaluation of the comparative growth and production dynamics of phytoplankton and their environmental co-variates for this study is based on field observations (both published and new data) and model results. Observational data on phytoplankton distribution, production and growth limitation in the eastern Subarctic are extensive and have been summarized in numerous papers and reviews, covering several decades (1960s to the present), as mentioned previously. In comparison, fewer phytoplankton studies have been made in the Labrador Sea and Labrador/Newfoundland Shelf regions and most observations have been made relatively recently (1990s to present). The subpolar Northwest (NW) and Northeast (NE) Atlantic basins (NORCAN regions) are strongly influenced by and linked through large-scale circulation of major water masses (principally, warm/salty Atlantic waters and cold/fresh Arctic waters) and these processes contribute to regionally distinct physical, chemical and biological cycles (Drinkwater et al., 2013). Phytoplankton growth dynamics are among those features that vary regionally. For our comparative analyses, we have selected a number of specific (relatively data-rich) study sites, ocean transects and weather stations (Fig. 1) with the view of capturing this regional variability and characterizing the regionally distinct phytoplankton cycles. In the NW Atlantic basin, for example, we have chosen sites to characterize the phytoplankton growth dynamics along the north– south axis of the Labrador–Newfoundland shelves that are strongly influenced by ice and Arctic waters, the Labrador Sea central basin that is influenced by Arctic and Atlantic waters and the narrow West Greenland Shelf that is influenced by Atlantic and Arctic (West Greenland Current) waters (Fig. 1a). Sites selected in the NE Atlantic basin characterize the ice, polar and Atlantic domains of the Barents Sea, the Greenland Sea that is influenced by ice and Arctic waters, and the Norwegian Sea central basin and shelf that are largely influenced by Atlantic waters (Fig. 1b). The Labrador Sea and Labrador–Newfoundland Shelves occupy an area approximately 1.2  106 km2 whereas the Norwegian and Barents Seas and Shelves occupy an area of 2.5  106 km2 (Drinkwater et al., 2013). In addition to conventional (ship-based) oceanographic data, satellite data (SeaWiFS 4 km – 8 day product, 1998–2006) have been extracted and used to characterize seasonal cycles of surface chlorophyll concentrations. Model results are derived from the NORWECOM coupled physical, chemical, and biological model system (Skogen et al., 2007), which has been implemented for the study of primary production, nutrient budgets, and particle dispersion. The ocean (physical) model component is based on the Regional Ocean Modelling System (ROMS) version 2.1. ROMS is a 3D baroclinic general ocean model, which uses a topography-following coordinate system in the vertical to permit enhanced resolution near the surface and bottom. Orthogonal curvilinear coordinates are used in the horizontal. A spline expansion is used for vertical discretization, which allows improved representation of the baroclinic pressure gradient. Ice dynamics are simulated using a dynamic-thermodynamic sea-ice module coupled to the ocean model and employs an elastic–viscous–plastic (EVP) rheology. The EVP scheme is based on a

28

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

Fig. 1a. NORCAN regions, NW subarctic Atlantic. Boxes: (1) Hudson Strait, (2) southern Labrador Shelf, (3) central Labrador basin, (4) West Greenland Shelf, (5) central Newfoundland Shelf. Transects (north to south): AR7/W (L3) line, Bonavista line, Flemish Cap line. Point: Ocean Weather Station ‘‘Bravo’’.

Fig. 1b. NORCAN regions, NE subarctic Atlantic. Boxes: (6) Barents Sea – arctic waters, (7) Barents Sea – Atlantic waters, (8) Greenland Sea, (9) Norwegian Sea – basin, (10) Norwegian Sea – coastal. Transects (north to south): Greenland Sea (75 N) section, Fugløya–Bjørnøya section, Svinoy section. Point: Ocean Weather Station ‘‘Mike’’.

time-splitting approach whereby short elastic time-steps are used to regularize the solution when the ice exhibits nearly rigid behaviour. Because the time discretization uses explicit time-stepping, the ice dynamics are readily parallelizable, so computationally efficient. Employing linearization of viscosities about ice velocities at every elastic (short) time-step maintains the ice internal stress state on or in the plastic yield curve. The EVP ice dynamics also provide a good transient response to rapidly varying winds as well as to inertial and tidal dynamics, particularly in the marginal ice zone. The ice thermodynamics employ two ice layers and a single snow layer. The snow layer possesses no heat content, but is, in effect, an insulating layer. Surface melt ponds are included in the ice

thermodynamics. A molecular sub-layer separates the bottom of the ice cover from the upper ocean. The inclusion of the molecular sub-layer produces more realistic freezing and melting rates than if the ice-ocean heat flux is based purely on the temperature difference between the ice bottom and the upper layer of the ocean. The chemical–biological module is coupled to the physical model through the subsurface light, the hydrography, and the horizontal and vertical movement of the water masses. The prognostic variables are dissolved inorganic nitrogen, phosphorus, and silicate, two different types of phytoplankton (diatoms and flagellates), detritus (dead organic matter), diatom skeletals (biogenic silica), inorganic suspended particulate matter, and oxygen. The

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

processes include primary production, respiration, algal death, remineralization of inorganic nutrients from dead organic matter, self-shading, turbidity, sedimentation, resuspension, sediment burial, and denitrification. Phytoplankton mortality is given as a constant fraction (10% d 1), and is assumed to account also for zooplankton grazing which, in this context, is included as a forcing function. Particulate matter has a sinking speed, relative to the water, and may accumulate on the bottom if the bottom stress is below a certain threshold value; resuspension takes place if the bottom stress is above a prescribed limit. Remineralization takes place in both the water column and the sediments. Parameterization of the biochemical processes and the exchange between the water column and sediment are from the literature based on experiments in laboratories and mesocosms, or deduced from field measurements. Skogen et al. (2007) provide details of the model set-up, forcing and initialization. For this study, the model domain covers the North Atlantic (from 20°S) and includes the Arctic. In the region of the Labrador–Newfoundland waters and the Barents/Greenland/Norwegian Seas, the horizontal resolution is 20 km. There are 30 generalized s-coordinate(s) vertical levels, stretched to increase vertical resolution near the surface and the seabed. No tides were included in the simulation. The model simulation is started from 1 August 1980, initialized by fields from that date from a coarse resolution (50 km grid size) simulation of the North Atlantic and Arctic oceans for the period 1948–2002, as described by Budgell (2005). A time-step of 900 s is used for both the ocean internal mode and ice thermodynamics. A ratio of 30 is used between the ocean internal and external mode time-steps, and one of 60 is used between ice thermodynamic and dynamic time-steps. The physical model is run initially whereas the biochemical model is run in offline mode, using 3D mean physical fields. The time-step of the biochemical model is 1 h. For the biochemical model, incident irradiation was derived from the formulation of Skartveit and Olseth (1986, 1987), using data for global daily downward short-wave radiation from the NCEP/NCAR reanalysis data set. The nutrient fields are re-initialized every 1 January using typical values for winter nutrients of Atlantic Water in the Norwegian Sea, 12.0, 5.5, and 0.8 mmol m 3 of inorganic nitrogen, silicate, and phosphate, respectively. Such a re-initialization avoids any drift in the nutrient fields, and has a minor effect on the results because the annual variations in winter nutrient concentration are no greater than 10% (Rey, 2004). The model is initialized with small amounts of algae (0.10 mgN m 3) for both diatoms and flagellates. Inorganic nitrogen is added to the system from the atmosphere (200 mgN m 2 yr 1); there are no river nutrient inputs. Model output (mixed-layer depths, nutrient fields, phytoplankton biomass and productivity) are summarized for the same areas as observational data (Fig. 1) for consistency and to facilitate within and among-region comparisons. 2.1. Light, ice and hydrography Light for photosynthesis is a fundamental environmental factor that influences the growth cycle, overall productivity and community structure of phytoplankton in the global ocean but particularly so in high latitude waters such as the NORCAN regions (Longhurst, 2007). Irradiance at the sea surface is dependent on the annual solar cycle, atmospheric conditions (e.g. clouds, fog) and the presence of sea ice. Light available for phytoplankton growth also depends on the nature of upper ocean mixing and attenuation with depth due to light absorbing and scattering properties of the water mass. 2.1.1. Solar cycle The daily and annual solar cycle varies dramatically by latitude from the equator to the poles. Since the NORCAN regions span al-

29

most 40° in latitude (Fig. 1), regional differences in the solar cycle will be significant (Fig. 2a). For example, the day-length on the Newfoundland Shelf (45°N) varies from 9 h in December to 15 h in June. In contrast, in the northern Barents Sea (80°N) there are >2 months of continuous darkness in winter and >2 months of continuous light in summer. In addition, because of the progressive lower sun angle northward (solar elevation <40° at the North Pole at the summer solstice) and thus higher scatter and reflection at the sea surface, there is proportionally less penetration into the ocean with increasing latitude. Therefore, the geography and solar cycle alone can account for differences in annual mean light budgets among the NORCAN regions of as much as a factor of 2 or more, e.g. between the northern Barents Sea and the southern Newfoundland Shelf. 2.1.2. Atmosphere Clouds and sea fog are prominent atmospheric features in all NORCAN regions. Measurements of incident solar radiation compared to clear-sky levels at both Canadian and Norwegian landbased meteorological sites (Figs. 2a–2c) indicate that average cloud cover is a significant attenuator (e.g. cloud cover alone averages 75% annually at St. John’s, Newfoundland, 47°N) and can reduce surface irradiance by >50%. Indeed, at all Canadian coastal sites, observed surface irradiances average 40–50% of clear sky levels. Moreover, at-sea observations of incident radiation (Labrador Sea, 55°–60°N) over a 10-yr period are consistent with the landbased results and indicate that surface irradiances in spring to fall are 50% of clear sky levels. The >50 yr cloud-cover record in Newfoundland (Fig. 2c) shows distinct interannual variability with decade-scale trends, i.e. cloud cover was relatively less during the decades of the 1960s and 1970s compared with the 1980s and 1990s (Fig. 2c). There is also a suggestion from other Canadian stations that interannual variability of incident radiation may increase with latitude. 2.1.3. Ice Ice and its accompanying snow cover both attenuate and reflect light and are important contributors to the growth dynamics of phytoplankton. Typical sea ice can attenuate light reaching the underlying water from 1% to 5% (I-yr ice) to <0.5% incident (multi-year ice); snow cover will substantially decrease these levels as well. Of the NORCAN regions considered, ice is an important consideration for the polar domain of the Barents Sea, the eastern and western Greenland Sea and Labrador and Newfoundland Shelf waters (Fig. 3a). There is a strong season cycle of ice coverage in all of these regions (Figs. 3a and 3b), however, the Labrador/Newfoundland shelves are ice free for 2–4 months per year whereas some fraction of the polar domain of the Barents Sea and northeast Greenland Shelf can have ice present year-round (see also Drinkwater et al., 2013). Over the past 50 yrs, the extent of ice cover in the northern hemisphere has been steadily decreasing, from 10  106 km2 in the late 1960s to 8  106 km2 at present. Although variable year-to-year, an overall downward trend over the past 25 yrs is apparent from modelled ice conditions in the NORCAN regions, showing decreases of 5600, 3000 and 1500 km2 yr 1 in the Barents, Greenland and Labrador Seas, respectively (Fig. 3c). 2.1.4. Mixed layer and stratification Mixing of near surface waters and stratification (resistance to mixing) are features of ocean physics that have an influence on both the light environment and nutrient availability for phytoplankton growth. Deep winter (convective) mixing, which is a distinctive characteristic of many of the NORCAN regions, principally in the central basins of the Labrador and Greenland/Norwegian Sea (Fig. 4a), occurs well before (January–March) seasonal light

30

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

Fig. 2a. Seasonal average monthly irradiance (RF1-Global Solar Radiation) from measurements (1965-present) made at Environment Canada land stations along the east coast of Canada and the eastern Canadian Arctic, 44–84°N.

Fig. 2c. Time-series of annual average percent cloud cover at St. John’s, Newfoundland (47.5°N), Environment Canada land station.

Fig. 2b. Predicted (clear-sky) and measured (partial and full cloud cover) daily incident irradiance cycle in June, Norwegian coastal station (74°N).

conditions favour phytoplankton growth starting in spring. However, the extent of vertical mixing will determine the levels of nutrient reserves in surface waters before the growth season and these nutrient reserves set the lower limit on the magnitude and duration of the spring bloom. As incident radiation increases in spring, both ice melt and/or surface water warming establish a stratified mixed layer that provides the (light) conditions needed to initiate the spring phytoplankton bloom. In the NORCAN regions, ice retreat precedes surface water warming (Labrador/

Newfoundland Shelf waters, NE Greenland and Barents Seas) and therefore in those regions, density stratification may result in spring blooms that precede those in ice-free waters where thermal stratification dominates the MLD dynamics (Labrador Sea, Norwegian Sea). Climatologies of the seasonal development of the MLD in the NORCAN regions (Fig. 4b) show the deep (P500 m) winter convective mixing zones in the Labrador and Greenland/Norwegian basins. In the other regions, winter mixing is generally <200 m and mixed-layers shallow to minimum depths (<20 m) in late summer. Due to the spatial and temporal averaging required to produce these monthly climatologies, however, MLDs tend to be underestimated (e.g. Harrison and Li, 2007). Climatologies of the seasonal development of the stratification in the NORCAN regions (Fig. 4b) show the early, ice-melt driven, density stratification zones on the Labrador and Newfoundland Shelves and in the polar domain of the Barents Sea. Note also the early stratification in the permanently ice-free Norwegian coastal

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

Fig. 3a. Monthly ice extent in the NORCAN regions during the 1980 ‘‘heavy’’ and 2006 ‘‘light’’ ice years, NSIDC (http://nsidc.org/data/gis/data.html).

Fig. 3b. Maximum and minimum seasonal ice extent (1972–1994) in the Labrador and Barents Seas, NSIDC (http://nsidc.org/data/gis/data.html).

31

32

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

2.1.5. Other attenuators Light attenuation due to other constituents of the water certainly affects light availability to phytoplankton. This is largely attributed to particles and mostly to the phytoplankton themselves. Euphotic depths, for example, can vary from 50 m when chlorophyll concentrations are 1 mg m 3 to as shallow as 15 m with 10 mg chlorophyll m 3 in the water column. In coastal-inshore and shallow waters, non-living particulates (detritus, sediments) and coloured dissolved organic matter (CDOM) also attenuate light. The latter is known to be a significant contributor to the optical properties of seawater along the Norwegian Coast (Børsheim and Myklestad, 1997) and may compromise the interpretation of satellite ocean colour data with regard to phytoplankton concentration (to be discussed later). Fig. 3c. Modelled March ice extent (concentration >15%) in the Labrador (45–80°N, 70–45°W), Greenland (69–80°N, 30°W–16°E) and Barents Seas (70–80°N, 15–55°E) for the simulation period, 1981–2006.

Fig. 4a. Monthly mixed-layer depth (MLD) climatologies from NODC and WOCE databases (1941–2002), mapped on 2°  2° global grid (http://www.loceanipsl.upmc.fr/~cdblod/mld.html) showing maximum winter mixing in the North Atlantic.

waters. Stratification in the polar Barents Sea is a case of meltinfluenced Arctic water whereas the density-driven stratification in Norwegian Coastal water is related to the less salty Norwegian Coastal Current. Those regions marked by early onset of stratification are also those where late summer/early fall peak stratification are greatest (i.e. the Labrador and Newfoundland shelves, the polar domain of the Barents Sea and coastal Norwegian Sea waters). Another physical feature of the waters of the NORCAN regions that not only influences the density structure and mixing of the water column but can also directly affect phytoplankton physiology is surface temperature. Climatological seasonal cycles reveal similarities in pattern among the NORCAN regions but distinctly different ranges and magnitudes (Fig. 4c). The seasonal range of temperatures and overall magnitude decrease with increasing latitude (and increasing influence of Arctic waters) in both the western and eastern Subarctic zones and this is most evident in the eastern regions where annual average surface temperature differ by as much as 8–10 °C (see also Drinkwater et al., 2013). Noteworthy also is the range in temperatures seen at the southern-most Newfoundland Shelf where seasonal extremes exceed 10 °C.

2.2. Nutrients Nutrients play a significant role in the growth dynamics of phytoplankton in Subarctic waters. Although light is thought to be the principal control on the timing of growth, nutrients, and especially winter reserves in surface waters, set a lower limit for biomass accumulation during the annual spring-to-summer bloom, and will influence the duration of the bloom, i.e. nutrient depletion due to biological consumption is considered a major factor in the decline of blooms. In addition, physically-mediated vertical mixing of nutrients and biological remineralization fuel phytoplankton productivity in summer and fall. Nutrients also play an important role in determining phytoplankton community structure. While all phytoplankton require nitrogen (principally nitrate and ammonium) and phosphorus (phosphate) for growth, specific groups (diatoms, silicoflagellates) require silicon (silicate) for their skeletal integrity. Moreover, diatoms represent a major component (both in abundance and biomass) of Subarctic waters. Nutrient ratios in surface and source waters, therefore, may be an important consideration in studies of large scale spatial patterns in phytoplankton community structure as well as small scale temporal (seasonal) evolution of species groups. Note that there is near universal acceptance of the opinion that phosphate is in excess of phytoplankton growth requirements year-round in much of the global ocean, including the Subarctic North Atlantic, and for that reason subsequent discussion of nutrients in this analysis will focus principally on growth-limiting nitrogen and silicon. Both the NW and NE Subarctic Atlantic are influenced by Arctic and Atlantic waters through similar large scale circulation patterns, i.e. southerly Arctic flow on the western boundaries of the Labrador and Greenland/Norwegian Seas and northerly Atlantic flow on the eastern boundaries (see Drinkwater et al., 2013). Arctic and Atlantic source waters (below the upper biological production zone) have distinctive nutrient characteristics, i.e. Arctic waters are rich in silicate (and phosphate) and Atlantic waters rich in nitrate relative to the other (Fig. 5a). The difference in the relative reserves of nitrate and silicate between Arctic and Atlantic waters is more apparent when the difference in concentrations in surface waters is plotted (Fig. 5b). Phytoplankton (diatoms) generally consume nitrate and silicate in approximately equivalent molar proportions so this difference indicator provides a general view of zones of ‘‘surplus’’ silicate (positive numbers), and potential for nitrogen limitation (e.g. Labrador/Newfoundland shelves), or ‘‘surplus’’ nitrate (negative numbers), and potential for silicate limitation (e.g. Norwegian Sea), of phytoplankton growth. No evidence of silicate ‘‘deficit’’ is apparent along the western boundary of the Greenland Sea, as seen in the Labrador Sea, which might suggest more mixing of Arctic and Atlantic waters in the eastern Subarctic seas. However, these plots based on coarse spatial (1  1°) and temporal (monthly means) gridded climatologies will not capture well the smaller spatial and temporal scale variability in this index.

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

33

Fig. 4b. Seasonal mixed-layer and stratification cycles in NORCAN regions, based on NODC 1°  1° monthly climatologies (http://www.nodc.noaa.gov/OC5/WOA94/mix.html and http://www.nodc.noaa.gov/OC5/WOA05/woa05data.html). See Fig. 1 for NORCAN region numbers.

Fig. 4c. Seasonal surface temperature cycle in NORCAN regions, based on NODC 1°  1° monthly climatologies (http://www.nodc.noaa.gov/OC5/WOA05/woa05data.html). See Fig. 1 for NORCAN region numbers.

A more detailed inspection of spring/summer nitrate (minus) silicate levels along selected transects in the NORCAN regions show similar patterns with clear zones of silicate deficit penetrating to 150 m on the Labrador Shelf and extending well offshore (upper 50 m) off the northern and southern Newfoundland Shelf (Fig. 6). In contrast, zones of silicate deficit are much less evident along transects across the western entrance to the Barents Sea, across

the northwestern Greenland Sea and southeastern Norwegian Shelf, as expected. In general, therefore, spatial patterns of the contribution of Arctic and Atlantic waters to the NORCAN regions and their influence on the inventory and supply of nitrate and silicate may help explain regional organization of phytoplankton community composition, in particular, areas where the scope for growth of diatoms is favoured or disfavoured.

34

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

Fig. 5a. Annual average source water (200 m) silicate and nitrate concentrations (mmol m OC5/WOA05/woa05data.html).

Fig. 5b. Nitrate minus silicate (mmol m 3) index in surface waters of the North Atlantic, annual average based on NODC climatologies (http://www.nodc.noaa.gov/ OC5/WOA05/woa05data.html).

Seasonal inventories of nutrients in surface waters show similar cycles in the Labrador/Newfoundland region and Barents/Norwegian/Greenland Seas (Fig. 7). Although there are gaps in the NW Atlantic data, nitrate concentrations vary from maximum levels

3

) in the North Atlantic, based on NODC climatologies (http://www.nodc.noaa.gov/

of 4–16 mmol m 3 in winter to <1 mmol m 3 in summer/fall. Highest winter concentrations are seen in the Labrador Sea basin where convective mixing is greatest (see Fig. 4b). Silicate concentrations range from 9–10 mmol m 3 in winter to 1–2 mmol m 3 in summer/fall. Plots of nitrate versus silicate (Fig. 7 insets) indicate that concentrations fall on or slightly above the 1:1 line in shelf waters indicating Arctic origin but below the line in the Labrador basin, suggesting the presence of Atlantic water. Seasonal nutrient data are much more complete in the NE Atlantic; winter nitrate levels peak at 12 mmol m 3 and decrease to 1–2 mmol m 3 in summer/fall. Silicate levels are only about half those in the Labrador/ Newfoundland regions, ranging from 5–6 mmol m 3 in winter to <1 mmol m 3 in summer/fall. Nitrate versus silicate plots all fall below the 1:1 line indicating the influence of Atlantic waters, as expected. Although the nitrate versus silicate plots in these examples intersect the silicate axis slightly above the origin (indicating nitrate depletion before silicate), there have been a number of reported instances in near surface waters in summer where silicate is exhausted before nitrate in both the Labrador Sea (Harrison and Li, 2007) and Norwegian Sea (Rey, 2004). Over the past decade or so, temperature and salinity trends (warmer/saltier) in the Labrador Sea central basin (Yashayaev et al., 2003) have suggested that the contribution of Atlantic water is increasing; this has been reflected in slightly increasing nitrate and decreasing silicate concentrations in source waters (60–200 m). Similarly, silicate concentrations in

Fig. 6. Nitrate minus silicate index along NORCAN transects (see Figs. 1a and 1b).

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

Fig. 7. Season cycles of surface (avg: 0–20 m) nitrate concentrations (mmol m concentrations with 1:1 and linear regression lines indicated.

35

3

) in NORCAN regions. Inset plots: scatterplots of monthly average nitrate versus silicate

source waters of the Norwegian Sea have been decreasing relative to nitrate, suggesting an increasing contribution of Atlantic water. Winter to summer nitrate depletion based on these seasonal cycles can be used to make minimum estimates of ‘‘new’’ primary production (Dugdale and Goering, 1967); these estimates will be discussed later in the context of observed and modelled total and new primary production. 2.3. Phytoplankton Published accounts of the distribution, seasonal growth cycles, physiology and community structure of phytoplankton in the eastern Subarctic seas are extensive (e.g. Dale et al., 1999; Rey, 1991, 2004; Rey and Loeng, 1985; Rey et al., 2000; Sakshaug, 2004; Sakshaug and Skjoldal, 1989; Sakshaug and Slagstad, 1991; Sakshaug and Walsh, 2000). This wealth of information has been a valuable underpinning for more recent investigations of basin scale variability of phytoplankton productivity derived from regional coupled physical–biochemical models (Skogen et al., 2007). Far fewer publications (and most of those available are in the grey literature) have dealt with phytoplankton dynamics in the NW subpolar Atlantic and these have dealt primarily with the distribution of phytoplankton biomass with only limited information on physiology, productivity and community structure (e.g. Irwin, 1990; Harrison and Cota, 1991; Head et al., 2000; Stuart et al., 2000; Li et al., 2006a,b; Fuentes-Yaco et al., 2007; Harrison and Li, 2007; Wu et al., 2007, 2008). These earlier studies in the NORCAN regions provide the background for and complement our comparative analysis which focuses principally on satellite ocean colour data and model output. 2.3.1. Biomass distribution and seasonal cycles The dynamics of phytoplankton growth from seasonal to interannual time scales in the NORCAN regions can be visualized from satellite-based ocean colour data (=surface chlorophyll concentrations) (Fig. 8). Apparent from this representation is the general south-to-north progression in the timing of the spring bloom, i.e. growth starts early in the year, March–April, at southern limits (e.g. Newfoundland Shelf, Norwegian coastal waters), and starts late, June–July at northern limits (e.g. northern Labrador Shelf, central Labrador Sea and polar domain of the Barents Sea). An exception to this pattern is the relatively early bloom development (late April) off the West Greenland Shelf. Other features include areas where the spring blooms are particularly intense (e.g. West Greenland Shelf, Atlantic domain of the Barents Sea, Greenland Sea) and where spring blooms are followed by less intense fall blooms (e.g. Labrador and Newfoundland shelves, Norwegian Sea basin). The timing of some blooms is persistent year-to-year (e.g. West Greenland Shelf, Atlantic domain of the Barents Sea) and others show significant interannual variability in timing (e.g. Labrador and

Newfoundland shelves, polar domain of the Barents and Greenland Seas). There are some limitations, however, in the interpretation of ocean colour data with regard to phytoplankton, particularly in coastal waters where detrital and sedimentary particulates and CDOM dominate the ocean optics. This may account for the apparent extended (into summer/fall) spring bloom in Norwegian coastal waters (Fig. 8). There is some evidence from field observations, however, that a significant amount of chlorophyll remains in surface waters well beyond the spring peak, e.g. at Ocean Weather Station ‘‘Mike’’ (Dale et al., 1999; Rey, 2004). Climatologies (1998–2006) constructed from the satellite data provide another means of investigating similarities and differences in phytoplankton growth cycles among the NORCAN regions (Figs. 9 and 10, upper panels). Although the satellite climatologies show considerable seasonal variability, early peaks in biomass (March–May) are evident on the Newfoundland and West Greenland shelves in the NW Atlantic and Norwegian coastal waters and Atlantic domain of the Barents Sea in the NE Atlantic. Late peaks in biomass (June–July) are seen for the northern Labrador Shelf (Hudson Strait) and the polar domain of the Barents Sea. Blooms at other sites fall in between these limits. Peak biomass (chlorophyll) levels average 2.6 mg m 3 in the Labrador/Newfoundland region and 2.3 mg m 3 in the Barents/Greenland/Norwegian Seas. The strongest blooms are seen on the West Greenland Shelf (>5 mg m 3) and in the Atlantic domain of the Barents Sea (4 mg m 3). Peak chlorophyll levels from field studies rarely exceed 4 mg m 3 in the Norwegian Sea (Rey, 2004) or 10 mg m 3 in the Barents Sea (Sakshaug and Walsh, 2000) but are often seen at or well above those levels in spring on the Labrador Shelf and, particularly, the West Greenland Shelf where concentrations exceeding 20 mg m 3 are not uncommon. Seasonal climatologies constructed from the 3D coupled model output (Fig. 9, lower panels) show less variable, more well-defined blooms but similar patterns to the satellite data, e.g. an early and strong bloom on the West Greenland Shelf and late blooms on the northern Labrador Shelf and polar domain of the Barents Sea. Peak spring–summer chlorophyll levels from satellite and model data, overall, are similar; however, the apparent persistence of chlorophyll in the late summer and fall seen in the satellite data is not seen in the model data. Hensen et al. (2009) observed similar coherence between their model-satellite comparisons in spring with deviations in the fall. The northward progression of the timing of the bloom is more evident in the model output; peak bloom conditions vary from late May at the southern bounds of the Newfoundland Shelf and Norwegian Sea to early July on the northern Labrador Shelf and Barents Sea, some 30–40 days difference. An exception to this general northward progression of blooms, as mentioned previously, is the atypically early bloom seen in the eastern Labrador Sea (West Greenland Shelf), occurring as much as a month or more earlier (April–May) than in adjacent waters

36

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

Fig. 8. Contour plots (month versus year) of surface chlorophyll concentrations (mg m data, 9-km/8-day product. See Fig. 1 for NORCAN region numbers.

3

), log transformed) in NORCAN regions. Derived from satellite (SeaWiFS) ocean colour

Fig. 9. Seasonal cycles of surface chlorophyll concentrations (mg m 3) in NORCAN regions; upper panels = average (1998–2006) from SeaWiFS satellite data, lower panels = average (1981–2006) from 3D coupled model output. See Fig. 1 for NORCAN region numbers.

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

37

Barents Sea (Rey and Loeng, 1985; Sakshaug and Skjoldal, 1989), i.e. a northward progression of the timing of the blooms and later blooms in heavy ice years. Interestingly, under heavy winter ice conditions where the ice edge penetrates into the Atlantic domain of the Barents Sea, the warm Atlantic waters melt the ice in spring stabilizing the upper water column and triggering an earlier than usual bloom in that region, by some 4–6 weeks in the extreme (Sakshaug, 2004). An assessment was made of the satellite (1998–2006) and model (1981–2006) data for interannual variability in mean biomass levels, timing and magnitude of the blooms. No statistically significant trends were seen in mean biomass or bloom magnitude in any of the NORCAN regions. There is some indication that spring chlorophyll levels from field data on the Labrador Shelf and central basin have been declining over the past decade, however, the changes have been small (10–20% decade 1) and only marginally significant. In contrast, the timing of the bloom has apparently changed in some regions in both the NW and NE Atlantic with greatest changes occurring at highest latitudes (Fig. 10, lower panel). In the Hudson Strait and the Arctic waters of the Barents Sea, for example, the blooms have been progressively earlier (>3 days yr 1) over the 8 yrs (1998–2006) of SeaWiFS observations. In some locations (Central Newfoundland Shelf, Norwegian Sea Basin), however, the timing of the bloom has been somewhat later in recent years.

Fig. 10. Trends in timing of the spring phytoplankton bloom in the NORCAN regions from SeaWiFS data. Upper panel: Climatological (1998–2006) mean timing of the onset of the bloom (chlorophyll >1 mg m 3). Bloom onset estimated as the year day, YD (numbers inside graph) when surface chlorophyll levels exceed 1 mg m 3. Lower panel: temporal trends in bloom timing. Trends derived from linear regression of timing versus year. Numbers inside graph represent bloom timing (YD) at the start (1998) and end (2006) of the time series. See Fig. 1 for NORCAN region numbers.

of similar latitude (June–July). Shallow winter mixed-layers and early seasonal onset of density-driven stratification, due to the low salinity transport off the West Greenland Shelf is thought to drive the early bloom in that region (Frajka-Williams and Rhines, 2010). More generally, Hensen et al. (2009) observed a strong negative correlation between chlorophyll and MLD in subpolar waters of their model study of the North Atlantic, supporting the argument that light limitation is a dominant factor for phytoplankton growth in the NORCAN regions. Fuentes-Yaco et al. (2007) studied the spring bloom dynamics along the Labrador/Newfoundland Shelf system in detail and concluded that the bloom progresses northward at a pace of 1 week/ deg latitude or a 10 week difference between 50°N and 60°N. The spring bloom along the Labrador Shelf has also been linked to ice dynamics, i.e. early spring ice retreat has been associated with early and more prolonged blooms (Wu et al., 2007). On the southern Labrador Shelf, for example, ice coverage in the spring of 2006, a ‘‘light’’ ice year, was 10% of that seen during the ‘‘heavy’’ ice year of 2002. In 2006, the bloom was 2 months earlier (May) than during 2002 (July) and reached a peak chlorophyll level of >4 mg m 3 compared with 2 mg m 3 in 2002. Drinkwater and Harding (2001) attribute the prolonged late summer/fall phytoplankton production on the northern Labrador Shelf to a continuous supply of nutrients from Hudson Strait. Bloom dynamics in the Barents Sea have also been linked with ice conditions in the

2.3.2. Community structure The phytoplankton communities of the Subarctic Atlantic are comprised of a mixture of the major taxonomic groups common to boreal (Arctic) and temperate (Atlantic) waters, including predominantly nano (2–20 lm) and microplantonic (>20 lm) diatoms, chrysophytes, dinoflagellates, prymnesiophytes, and flagellates (Sakshaug, 2004). The smaller, less abundant picoplankton (<2 mm) are found principally along the southern boundaries of the region. Diatoms are dominated by centric forms of the genera Chaetoceros and Thalassiosira and pennates such as Fragilariosis, Navicula and Pseudo-Nitzschia. Common dinoflagellates include the genus Ceratium and the heterotrophic genus Protoperidinium. Primnesiophytes are also important and include the genus Phaeocystis and the coccolithophorids (e.g. Emiliania huxleyi). The major bloom-formers in the Subarctic Atlantic are the centric diatoms and the prymnesiophytes, primarily Phaeocystis. Flagellates (chrysophytes) and dinoflagellates are more common under post spring bloom conditions. Taxonomic analysis has been a common element of phytoplankton studies in NE Atlantic Subarctic seas and much of the general knowledge of phytoplankton community structure and species succession in Subarctic seas has come from those studies (e.g. Rey, 2004). In the Norwegian Sea, for example, flagellates dominate the phytoplankton community in the winter pre-bloom period, followed by the spring bloom that is dominated by centric diatoms (Thalassiosira, Chaetoceros, Rhizosolenia, Skeletonema). Immediately after the spring bloom there is a transition from a few diatom species to a diverse assemblage of (small) flagellates; the species diversity peaks during this post-bloom period. In late summer/early fall there may be a small secondary bloom, generally comprised of dinoflagellates. Frequently also, widespread (Norwegian, coastal waters, Greenland and Barents Seas) prymnesiophyte blooms occur, generally after the spring diatom bloom (see Fig. 11). However, both Phaeocystis and coccolithophore blooms have been observed preceding or coincident with the spring diatom bloom (Dale et al., 1999; Rey et al., 2000). Information on phytoplankton community structure in the Labrador/Newfoundland region was limited to microscopic analysis in early work, but has extended in recent years to analyses of

38

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

photosynthetic pigments by chromatographic separation and of bio-optical characteristics by flow cytometry. At Station Bravo, observations over an entire annual cycle led Holmes (1956) to conclude that the phytoplankton community is a mix of organisms from several biogeographic provinces reflecting the various water masses in the area. Although diatoms and dinoflagellates bloom in the spring and autumn, Holmes noted that the smaller phytoplankton species (nanoplankton) constituted a substantial portion of the total assemblage. Continuous Plankton Recorder (CPR) surveys on the southern Labrador and Newfoundland shelves since the mid-1960s indicate that the larger microplankton are dominated in spring by diatoms (principally Chaetoceros sp.) with dinoflagellates becoming more prevalent in fall/winter (mostly Ceratium species). Over the 40 yr CPR time series, diatom abundance has stayed relatively stable while dinoflagellate abundance has increased. The few taxonomic analyses done across the Labrador Sea suggest that diatoms dominate the phytoplankton community in spring, particularly on the Labrador Shelf but that prymnesiophytes (Phaeocystis) are common in areas of high chlorophyll in the central basin and on the eastern (West Greenland Shelf) side (Head et al., 2000; Stuart et al., 2000). Pigment analyses (Stuart et al., 2000) have also been used to differentiate major phytoplankton community types (e.g. diatoms and prymnesiophytes) in the Labrador Sea. Diatoms dominate the chlorophyll biomass (40%) throughout the region in spring while the contribution of prymnesiophytes increases from nil on the Labrador Shelf to >5% of the chlorophyll on the West Greenland Shelf. Moreover, a decade of analysis indicates that the contribution of diatoms to the total phytoplankton biomass has been decreasing throughout the region over time while the contribution of prymnesiophytes has been increasing, principally in the central Labrador basin and on the West Greenland Shelf (Li, unpubl.). Although microphytoplankton account for a large proportion of photosynthetic biomass, they do not constitute the numerical dominants of the photosynthetic community. Picoplankton comprising picoeukaryotic algae and Synechococcus cyanobacteria (Fig. 12D) and nanoplankton (Fig. 12E) generally outnumber dia-

toms and dinoflagellates (Fig. 12F). Community composition is evidently related to the different hydrographic (Fig. 12A) and nutrient (Fig. 12B and 12C) regimes of the Labrador shelf and slope, the central Labrador Basin, and the western Greenland Shelf. This is most clear for Synechcoccus which are distributed in the same manner as temperature, salinity and nitrate (Fig. 12), indicating a strong affinity with Atlantic source water. The numerical dominant in the entire NORCAN region appears to be the picoeukaryotic prasinophyte Micromonas, which is thought to form the baseline community that persists throughout all seasons (Not et al., 2005; Lovejoy et al., 2007). At pan-Arctic concentrations of 1000 to 10000 cells per milliliter (Tremblay and Gagnon, 2009), picoeukaryotes represent a large gene pool undergoing evolutionary change under natural selection. Under the current climate condition, Arctic picoeukaryotes are already increasing at a rate of 10% per year (Li et al., 2009). 2.3.3. Physiology Investigations of the physiological response of phytoplankton communities at high latitudes to their environment, not surprisingly, have focused principally on light. Photosynthesis–irradiance (P–E curve) experiments have been carried out under a wide range of environmental conditions in both the Labrador/Newfoundland region and Barents/Greenland/Norwegian Seas. Despite the considerable variability (3–4 orders of magnitude) in phytoplankton biomass over this large geographic domain, the main parameters of the P–E curve, i.e. maximum photosynthetic rate (Pmax) at saturating light and the photosynthetic efficiency at low light (a), fall within a much more restricted range. Approximately 75% of Pmax and a estimates for pelagic communities fall within the 1– 5 mgC mgCHL 1 h 1 and 0.03–0.15 mgC mgCHL 1 (W m 2) 1 range, respectively, in the Subarctic North Atlantic. A smaller number of estimates fall outside that range; notably, low values of Pmax (and high values of a) are seen in low-light adapted communities, e.g. at base of the euphotic zone or ice-algal communities (Cota, 1985; but see Irwin, 1990), and high values, mainly Pmax, are seen under high light (surface waters) bloom conditions. [Note: a per

Fig. 11. Coccolithophore bloom in the Barents Sea, MODIS-Terra image from 1 August, 2007. The visible portion of the bloom was estimated to cover 150,000 km2 (http:// oceancolor.gsfc.nasa.gov/cgi/image_archive.cgi?c=CHLOROPHYLL).

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

39

Fig. 12. Spring conditions in the Labrador Sea along the AR7W transect over the Labrador Shelf and Slope (LS), the central Labrador Basin (LB), and the western Greenland Shelf (GS) whose nominal geographic boundaries are indicated by vertical dashed lines. (A) Temperature (°C) and salinity (psu) averaged over the upper 100 m. (B) Nitrate (mmol m 3) and silicate (mmol m 3) averaged over the upper 100 m. (C) Difference between concentrations of nitrate and silicate (mmol m 3) in the upper 100 m. (D) Picophytoplankton abundance (log cells ml 1) averaged over the upper 100 m: picoeukaryotes and Synechococcus. (E) Nanophytoplankton abundance (log cells ml-1) averaged over the upper 100 m: small cells (2–10 lm) and large cells (10–20 lm). (F) Microphytoplankton abundance (log cells ml 1) at 10 m: diatoms and dinoflagellates. All physical, chemical and biological data are averaged over 15 years (1994-2008) except for microphytoplankton abundance which were recorded only in 1997.

chlorophyll is often lower in shade-acclimated communities because of the strong packaging effect in pigment-rich cells (Sakshaug et al., 1997).] Temperature also has an effect on Pmax. On the Newfoundland Shelf and in the Labrador Sea, for example, Pmax has been observed to increase by a factor of 1.5–2 over a 10 °C temperature range ( 1 °C to 9 °C). A similar response has been seen in the Barents Sea populations (Rey, 1991). Harrison and Li (2007) compared seasonal variations in light available (in the upper mixed layer) for phytoplankton growth in the Labrador Sea with the derived P–E parameter EK (Pmax/a, W m 2) that defines the threshold for light-dependent growth and concluded that light limitation can occur in near surface phytoplankton populations even during the peak growth months in summer when the solar cycle is at its maximum. 2.3.4. Primary productivity Primary productivity measurements are far less numerous than chlorophyll, however, long-term monitoring programs, regularly repeated ocean surveys and transects, and weather stations in both the Labrador/Newfoundland region and Barents/Greenland/Norwegian Seas have provided sufficient field data to compile annual estimates of primary production for all the NORCAN regions (Table 1). Annual production estimates for the Newfoundland Shelf (>400 gC m 2) are considerably higher than seen in any of the other NORCAN regions and heavily weighted by productivity levels averaging 3 gC m 2 d 1 during the spring bloom and >1 gC m 2 d 1 during the secondary late summer peak. Further north on the Labrador Shelf and through the central basin and West Greenland Shelf, spring/summer peak productivities range from 1 to 1.5 gC m 2 d 1 with annual estimates of 90–170 gC m 2. Highest annual production in the eastern Subarctic seas is seen in the

Atlantic domain of the Barents Sea where peak spring productivities may reach 2 gC m 2 d 1 and annual production is on the order of 60–200 gC m 2 (Sakshaug, 2004); annual production is lower (90 gC m 2) in the polar domain of the Barents Sea. Productivities are also high in the Norwegian Sea during the spring bloom (1–1.5 gC m 2 d 1) with annual production from 80 to 120 gC m 2 and highest levels observed in the coastal current (Rey, 2004). Peak spring productivities in the Greenland Sea are <1 gC m 2 d 1 with annual production 70 gC m 2 (Rey et al., 2000). Overall, annual primary production is somewhat higher (130 gC m 2) in the Labrador/Newfoundland region (excluding the Newfoundland Shelf) than in the Barents/Greenland/Norwegian Seas (100 gC m 2). Primary production estimates from our 3D coupled model are somewhat lower than field observations, however, they are consistent overall, showing highest levels on the West Greenland Shelf, Atlantic domain of the Barents Sea and coastal Norwegian Sea (Table 1). The Newfoundland Shelf is an exception where observations greatly exceeded model estimates. Time-series of annual production for the model-run period, 1981–2006, provide yet another perspective on primary production in the NORCAN regions (Fig. 13, upper panels). In Canadian waters, productivities aggregate into two groups: with relatively low annual production (50 gC m 2) and high interannual variability on the northern Labrador Shelf and higher production (100 gC m 2) with lower interannual variability at the remaining sites. In the eastern Subarctic seas as well, production falls into two groups. However in this case, three areas fall within the low production/high variability zone (Polar domain of the Barents Sea, Greenland Sea and Norwegian Basin) and the remaining two in the high production/low variability zone. Differences in production in the NW Atlantic are likely linked to the influence of ice. In the NE Atlantic, differences may

40

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

Table 1 Total and ‘‘New’’ (nitrate-based) primary production in NORCAN regions. Nitrate-depletion estimates of new production derived from difference in March and August surface nutrient concentrations, integrated to 50 m and converted to carbon using the Redfield Ratio. Incubation estimates of new production derived from 15NO3 tracer uptake experiments. Region

Total Prim Prod (gC m Observed

Barents Sea Arctic Barents Sea Atlantic Greenland Sea Norwegian Sea Basin Norwegian Sea Coastal N Labrador Shelf S Labrador Shelf Labrador Basin W Greenland Shelf Newfoundland Shelf a b

b

90 60–200b 70b 80b 90–120b 85 120 143 172 420

2

yr

1

)

‘‘New’’ Prim Prod (gC m Model

NO3 depl

2

yr

<40 70–110b 36–55b 39–48b 32–85b 34 59 42 34

)

Incubation

b

50 92 58 62 113 49 93 82 107 87

1

71 70 88

Modela 37 66 45 45 72 35 69 57 65 59

Model run for year 2006. Literature values.

Fig. 13. Time-series (1981–2006) of: (upper panels) annual primary production (gC m regions from 3D coupled model output. See Fig. 1 for NORCAN region numbers.

be attributed to a more complex interaction of ice and the (relative) influence of Arctic and Atlantic waters. Overall, modelled annual primary production in the Labrador/Newfoundland region is slightly higher (84 gC m 2) than in the Barents/Norwegian/ Greenland Seas (75 gC m 2) but covers similar ranges and was not statistically different. Temporal trends (1994–2006) in the productivity data from available field observations (Newfoundland and Labrador shelves, Labrador basin and West Greenland Shelf) were absent. For the longer time series model results (Fig. 13, upper panels), however,

2

yr

1

) and (lower panels) timing (Year Day, YD) of maximum production, in NORCAN

there appears to be a slight (although not statistically significant) increase over time in primary production at the northern-most sites (northern Labrador Shelf, polar domain of the Barents Sea) and a decrease in the Norwegian coastal waters and Atlantic domain of the Barents sea: no temporal trends are apparent at the other sites. Overall, there is a slight negative trend in annual primary production for both Canadian waters and the eastern Subarctic seas. Although highly variable from year-to-year, particularly at the northern sites, primary production (Fig. 13, lower panels) in both Canadian and eastern Subarctic waters has peaked

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

progressively earlier over the 25 yr time model series, by 2 weeks on average. This is consistent with the earlier timing of the spring bloom as discussed previously. It is the ‘‘new’’ primary production, fuelled by external nutrient sources (principally nitrate) and the portion of total production available for transfer up the foodweb (Eppley, 1981), that is of most interest to ocean ecologists. New production estimates based on tracer (15N) incubations and nitrate depletion in surface waters (observations and model output) have been compiled for the NORCAN regions (Table 1). Field estimates range from 30–50 gC m 2 yr 1 in the Labrador/Newfoundland region to 40–110 gC m 2 yr 1 in the Barents/Greenland/Norwegian Seas. Model estimates were similar and in the range of 40–70 gC m 2 yr 1 in both the NW and NE Atlantic. Overall, these estimates suggest that new production represents a large fraction of total primary production (40– 60% observations; 60–80% model) in the Subarctic North Atlantic, a point that has been made previously for high latitude environments in general (Codispoti et al., 1991). Indeed, Kristiansen et al. (1994) showed from 15NO3 tracers measurements that new production in the marginal-ice zone of the Barents Sea accounts for >90% of the total production in winter–spring, >40% in summer and 20% in fall. 2.3.5. Polynyas, marginal ice zones (MIZs) and ice algae To the extent that the NORCAN regions are influenced by ice, ice algae and the epontic and pelagic phytoplankton associated with the ice edge, polynyas, marginal ice zones and under-ice communities will be an important consideration in any description of the comparative dynamics of phytoplankton in the Subarctic North Atlantic. The two major polynyas in the NORCAN domain are the Northeast Water Polynya off the northeast coast of Greenland and the Northwater Polynya in northern Baffin Bay. Phytoplankton production within these two systems occurs mainly between May and August and generates annual estimates of from 20– 50 gC m 2 yr 1 (Northeast Water Polynya) to 150 gC m 2 yr 1 (Northwater Polynya) of which >60% at both sites is new production (Sakshaug, 2004). Under-ice communities and those at ice edges are also an important part of the base of the foodweb in the NORCAN regions and more specifically on Labrador and Newfoundland shelves, and in the northern Greenland and Barents Seas. Phytoplankton production at the marginal ice zone has not been investigated in Canadian waters but has been studied in eastern Subarctic seas (e.g. Smith, 1987). The general picture developed for these regions (Sakshaug and Skjoldal, 1989) is the appearance of strong phytoplankton blooms, comprised of mixed populations of large diatoms (e.g., Fragilariopsis, Thalassiosira, Chaetoceros, Pseudo-Nitzschia), in the melt water adjacent to the ice edge that tracts the northward retreat of the ice during the summer melt period. Smith et al. (1987) and Smith and Kattner (1989), for example, observed primary productivity in the MIZ of Fram Strait of >400 mgC m 2 d 1 of which 60% was new production. Interannual variability in ice conditions and the associated MIZ phytoplankton populations, however, may exceed the large seasonal ice-retreat cycle (Falk-Petersen et al., 2000). Ice algae studies over the past 20 yrs have been extensive in both the north and south polar regions (Horner et al., 1992; Legendre et al., 1992); in the northern hemisphere these have been concentrated in Hudson Bay and the eastern Canadian Arctic archipelago (Barrow Strait) and northern Greenland and Barents Seas. From a compilation of these studies, Legendre and co-workers estimate that primary production within sea ice (north of 65°N) represents 5–25% of the total regional production. However, Gosselin et al. (1997) estimate that ice algae account for >50% of the total (ice + water column) primary production in the central Arctic basin and 3% in surrounding Subarctic waters (includes the NORCAN regions). Coupled snow-ice-ice algae models (e.g. Lavoie et al., 2005) simulate field observations

41

well and suggest that snow cover and bottom ice melt rate (and their effects on light and nutrient availability) determine the duration, maximum biomass accumulation and termination of ice algal blooms.

3. Critical links to climate variability and change It is well established from both large-scale models and regional observations that the changing climate is having a demonstrable effect on the environment and ecosystems of the oceans, particularly at high latitudes (ACIA, 2005). Several studies dating back over a decade have described changes already occurring or predicted to occur in phytoplankton distribution, productivity and community structure at high latitudes (e.g. Legendre et al., 1992; Sakshaug and Walsh, 2000;, Drinkwater et al., 2003; Macdonald et al., 2004; Loeng et al., 2005; Arrigo et al., 2008). Among the most obvious of the environment links with climate variability and change is through large-scale atmosphere processes. The North Atlantic Oscillation (NAO) is the dominant mode of recurrent atmosphere variability in the North Atlantic and can influence phytoplankton dynamics in a variety of ways either by its effect on air-sea fluxes (heat balance, mixing-stratification) or effects on circulation (advection). Exploring the relationship between observed changes in phytoplankton abundance in the North Atlantic (from CPR surveys) and phases of the NAO, Drinkwater et al. (2003) showed that positive NAOs result in stronger NW winds over Labrador Sea (cold air, cooler waters, more ice, more mixing) and stronger SW winds over the Barents Sea (warmer air masses, warmer waters, reduce ice, increased inflow of Atlantic waters, reduced mixing); negative NAOs result in the opposite, i.e. milder conditions in the Labrador Sea (less ice and mixing) and more harsh conditions (more ice and mixing) in the Barents Sea. These environmental conditions, in turn, influence the timing and duration of blooms, overall abundance and shifts in community composition (through changes in stratification onset and intensity, vertical mixing of nutrients and advective changes in water masses). Drinkwater et al. (2003) emphasized, however, that phytoplankton response to large scale environmental forcing can be a complex balance between the sometimes opposing effects of mixing-stratification on light and nutrient availability that both limit primary production in Subarctic waters. NAO conditions during the time period of this comparative study have been variable with strong positive anomalies during the early 1980s and early 1990s and neutral or slightly negative anomalies during the 2000s; the overall trend has been decreasing NAO (and Arctic Oscillation, AO) anomalies since the late 1980s/early 1990s (Fig. 14, see also Drinkwater et al., 2013). Skogen et al. (2007) investigated the relationship between NAO and primary production in an earlier 3D couple model analysis of the eastern Subarctic seas. They found that the NAO index is positively correlated with primary production in the Iceland Sea but negatively correlated in the Barents Sea. They attributed these differences to the fact that during the positive phase of the NAO, storms take a more northerly track, enhancing mixing and destabilizing the upper water column in the eastern regions (Barents Sea) resulting in reduced primary production. In the southwestern regions (Iceland Sea), conditions are milder with less mixing that is more favourable for primary production. In the present study, primary production is positively correlated with NAO on the east Greenland and Newfoundland shelves, and the Norwegian Sea. The underlying processes that link NAO and primary production in these geographically separated areas, however, is not immediately clear. Oschlies (2001) demonstrated with a coupled ecosystem-circulation model of the North Atlantic that the phase of the NAO can be linked to vertical mixing, advection and nutrient

42

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

Fig. 14. Time-series (1950–2006) of North Atlantic Oscillation (NAO) and Arctic Oscillation (AO) indices (anomalies), period of observed and modelled phytoplankton dynamics discussed in this report shown.

supply to the surface ocean. However, the influence on primary production in the subpolar gyre was concluded to be minimal due to the counteracting influence of mixing on the light environment and its limitation of phytoplankton growth at high latitudes. It is tempting to speculate that the overall trend in the NAO over the past 25 yrs (strongly positive to slightly negative anomalies) is manifest in a similar way at the base of the foodweb in both the NW and NE Subarctic Atlantic, i.e. the trends (albeit weak) in annual primary production (decreasing over time) and timing of the production peak (earlier over time). Hensen et al. (2009) noted no discernible trends in phytoplankton growth characteristics (bloom magnitude, timing) in their modelling study in the sub-polar North Atlantic over their run period (1959–2004), however, they did observed distinct decadal-scale periodicity in bloom timing correlated with the phase of the NAO, i.e. positive phases generated deep mixed layers and delayed blooms (by as much as 2– 3 weeks). Another clear climate-environment link at high latitudes that influences phytoplankton dynamics is ice. Our 3D model simulations show that ice extent has decreased significantly in all NORCAN regions (Barents, Greenland and Labrador Seas, Fig. 3c) and that ice conditions are negatively correlated with primary production in the Greenland Sea and polar domain of the Barents Sea but, surprisingly, not with the Labrador Shelf production. There is also a positive correlation between Barents Sea ice and primary production in the Atlantic domain of the Barents Sea which may be an indication that some of the production moves northward when there is less ice. Interestingly, there is a positive correlation between East Greenland Shelf production and ice conditions in the Labrador Sea and Newfoundland Shelf production and ice in the Greenland and Barents Seas, however, a cause-effect of such remote connections is not immediately obvious. Sakshaug and Walsh (2000), Macdonald et al. (2004) and Sakshaug (2004) discuss in some detail the implications for primary production of a warming arctic climate, where ice extent, thickness and albedo decrease. Under the now well-documented evidence that sea-ice is rapidly disappearing at high latitudes, including the NORCAN regions (see Fig. 3), the most immediate affect will be on the under-ice (epontic) communities. Less extensive ice will mean less epontic production, however, the effects will be greatest in the high arctic where most of the epontic production occurs (see Section 2.3.5). Simulation modelling of ice algal dynamics (Lavoie et al., 2005) further reinforces the idea that under a warming Arctic, reduced snow cover and earlier snow and ice melt will result in a substantially shorter production season and lower overall epontic production. Reduced sea ice will have similar effects on primary production in the marginal ice zone (MIZ); production of both the epontic and pelagic components will decrease. The prevalence of and contribution to overall primary production of polynyas, on

the other hand, may increase in a warmer ocean (Legendre et al., 1992). While ice-associated primary production will generally decrease with climate warming, it may increase in the ice-free pelagic domain. For example, Sakshaug and Walsh (2000) have observed that primary production in the polar domain of the Barents Sea is 30% higher during warm (relatively low ice) years. Indeed, Sakshaug (2004) suggests that the disappearance of ice in the Barents Sea north of the polar front could lengthen substantially the phytoplankton growing season and increase primary productivity from <40 gC m 2 yr 1 to 100–150 gC m 2 yr 1, a > 3.5-fold increase. Concomitant longer exposure to wind mixing at the surface of ice-free waters could provide more nutrients for production and more new production (Macdonald et al., 2004), however, if the wind fields are too strong and the mixing is too deep (e.g. >60 m), phytoplankton community changes might occur, favouring slow-growing, low-light adapted species such as prymnesiophytes or nanoflagellates rather than the more typical mixed diatom populations. On the other hand, increased freshwater input and winter stratification may serve to retard or ‘‘cap’’ the very deep convective mixing characteristic of the NORCAN regions which could influence (decrease) winter nutrient reserves. An apparent shift from larger to smaller phytoplankton and bacteria is already occurring in the Arctic as a likely consequence of surface warming and freshening and decreased mixing and nutrient supply (Li et al., 2009). In addition to local effects, community structure may be altered by large-scale circulation changes as, for example, the recent re-appearance (last record was 0.8–1.4 million yrs ago) of a Pacific diatom, Neodenticula seminae, in the Northwest Atlantic (Reid et al., 2007). Beaugrand et al. (2008) and Beaugrand (2009) have shown through spatio-temporal analysis of historical plankton and oceanographic data in the North Atlantic that large-scale changes (geographic distributions, size structure and composition, trophic linkages) in plankton communities are occurring now and will continue to change as the surface ocean warms. They have suggested that a critical thermal boundary (9–10 °C) delineating significant shifts in plankton community attributes (e.g. displacing cold-water species with warm-water species) exists and will migrate northward as the climate warms over the next several decades, penetrating first into the Norwegian/Barents Seas and later into the Labrador–Newfoundland region (see also Head et al., 2013). Aside from climate effects on the water column production, it is expected that there will be significant changes in vertical material flux and coupling to the benthos (Legendre et al., 1992; MacDonald et al., 2004) in a warmer ocean. Behrenfeld et al. (2006) have documented a progressive global decline in satellite ocean colour (and computed net primary production, NPP) since the late 1990s as SST has been increasing, however, the emphasis in their paper was on the tropics to mid-latitudes. A closer inspection of their results shows that ocean colour has, in fact, been increasing over recent years at higher (subpolar) latitudes. Doney (2006), in a commentary on the Behrenfeld et al. results, speculates that stronger surface stratification in a warmer ocean will decrease (nutrient-limited) productivity at mid-to-low latitudes because of reduced vertical mixing and availability of nutrients but will increase (light-limited) productivity at high latitudes because stratification will provide more favourable light conditions for phytoplankton growth. Coupled ecosystem-circulation models (e.g. Sarmiento et al., 2004; Schmittner et al., 2008) have predicted that primary production will indeed increase at high latitudes (including the NORCAN regions) as the ocean warms. Hensen et al. (2009), on the other hand, suggest that climate warming may result in increasingly positive NAO conditions, increased mixing and hence weaker and later phytoplankton blooms in the subpolar North Atlantic. It has also been predicted that calcifiers may play an increasingly important role in sub-polar

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

waters due to CO2 enrichment (Schmittner et al., 2008; see also Signorini and McClain, 2009), however, the negative impacts of ocean acidification on these forms, particularly at high latitudes where the corrosive effects will be manifest earliest (Orr et al., 2005; Fabry et al., 2008), have not been considered in these modelling studies. Based on the foregoing discussion, therefore, climate change and a warming ocean will have both direct and indirect effects on phytoplankton dynamics in Subarctic seas. Direct effects will include, for example, altered metabolic rates (see Section 2.3.3) and changes in community composition due to increasing ocean temperatures and freshening. Indirect effects will include: (1) reduction in sea ice that will result in altered growth cycles and production of epontic and pelagic phytoplankton communities (less epontic, more pelagic), (2) changes in upper ocean mixing (shallower MLDs, stronger stratification) that will alter growth cycles and production (enhanced under light-limited conditions, reduced under nutrient-limited conditions), (3) changes in largescale circulation that will alter growth cycles and community composition. For the NORCAN regions in specific, warmer waters will mean: (1) less ice/longer open water seasons on the Labrador/ Newfoundland shelves, NE Greenland Sea and polar domain of the Barents Sea, (2) shallower MLDs, stronger stratification and reduced winter convective mixing (Labrador, Greenland and Norwegian Seas basins) and (3) changes in large scale-circulation, i.e. contributions of Arctic and Atlantic waters. In the northern and/ or ice-influenced and light-limited NORCAN regions, it is anticipated that there will be, proportionally more pelagic productivity, longer growing seasons and overall higher annual production. For the more southerly, nutrient-limited NORCAN regions, it is anticipated that the pelagic production cycle may start earlier, be of lower magnitude and shorter in duration, there may be less summer production, smaller fall blooms and consequently less new production and material export. Changes in Arctic (down western side)

43

and Atlantic (up eastern side) inflows into the NORCAN regions will influence local ice and mixing dynamics, nutrient availability and phytoplankton production cycles and community composition in complex ways that are difficult to predict. Moreover, the degree to which regional species and community assemblages will adapt/ adjust to a changing environment over the next decades is a major unknown.

4. Summary: Similarities and differences between the NW and NE Subarctic Atlantic Drinkwater et al. (2013) looked at the large-scale atmospheric forcing and ocean circulation in the North Atlantic as a starting point for understanding the observed similarities and differences in the hydrographic conditions in the NORCAN regions. Both the Labrador and Norwegian Seas and Shelves are part of the Subarctic domain with the Barents Sea the largest of the Arctic marginal seas. Both the NW and NE Atlantic are highly advective systems with the Labrador more strongly influenced by the southward flowing cold Arctic water and the Norwegian–Barents Seas by the northward flowing warm Atlantic water. Still, both regions receive significant inputs from the Atlantic (south) and the Arctic (north). Common also to both regions is the latitudinal gradient in mean air temperature, heat flux, zonal winds and sea surface temperature (air and ocean temperatures and winds decrease and annual heat loss increases northward). Winds, however, are typically stronger in the Labrador region than in the Norwegian– Barents region. The historical data records (back to the 1950s) show linked quasi-decadal variability in atmospheric and ocean variability in both regions. Low (high) NAO conditions in the NW Atlantic have been associated with weaker (stronger) northwesterly winds, warmer (colder) air and ocean temperatures and less (more) ice whereas opposite (out-of-phase) conditions have been

Table 2 Phytoplankton production and growth dynamics: similarities and differences between the NW (Labrador–Newfoundland) and NE (Barents–Greenland–Norwegian Seas) Subarctic Atlantic, NORCAN Regions. Similarities Deep basins and shelves 1. Fall principally within Longhurst’s Atlantic Polar Biome where the phytoplankton production cycle is irradiance-mediated (his Case 1 model), except at southern boundaries where production cycle may be nutrient-limited in summer (his Case 2 model) 2. Respond to large-scale meteorological forcing (NAO/AO) 3. Exhibit extremes in solar cycle and strong surface light attenuation due to clouds and fog 4. Influenced by sea-ice at least part of the year NOTE: principally shelves 5. Exhibit deep winter convective mixing (basins) 6. Influenced by (cold/fresh) Arctic and (warm/salty) Atlantic waters 7. Exhibit a relatively diverse mix of boreal to temperate species: prominence of diatoms (spring bloom) and prymnesiophytes (e.g. Phaeocystis) in summer 8. Exhibit similar features of phytoplankton growth cycles (e.g. latitudinal gradients in timing) and comparable magnitude of phytoplankton biomass and production 9. Timing of phytoplankton blooms and peak seasonal production have occurred progressively earlier over the past two decades, trend increasing with latitude; temporal trends in the magnitude of blooms and annual primary production less apparent 10. Climate change (warming) will alter atmospheric and oceanographic conditions (melt ice, change mixing and circulation patterns) with large-scale consequences for phytoplankton growth cycles, productivity and community composition Differences Deep basins 1. Greenland–Barents Seas extend to higher latitudes than the Labrador Sea thus less available light, on a seasonal basis, for phytoplankton production 2. Greenland–Barents Seas are partially ice-covered in winter/spring whereas the Labrador Sea is ice-free year-round contributing to differences in timing of phytoplankton growth and community composition 3. Relatively stronger influence of Atlantic waters in the eastern Subarctic waters compared to Canadian waters results in a perceived ‘‘deficit’’ of silicate in the east and ‘‘surplus’’ in the west that may have consequences for phytoplankton community composition, particularly diatoms Shelves 4. Labrador–Newfoundland Shelf extends to lower latitudes than the Norwegian Shelf thus more light available, on a seasonal basis, for phytoplankton production 5. Labrador–Newfoundland Shelf is ice covered in winter/spring whereas the Norwegian Shelf is ice-free year-round contributing to differences in timing of phytoplankton growth and community composition 6. Labrador–Newfoundland Shelf is heavily influenced by cold/fresh Arctic waters whereas the Norwegian Shelf is influenced principally by warm/salty Atlantic waters with consequences for nutrients, phytoplankton growth cycles and species composition 7. Climate change (warming) will alter southward arctic outflow and northward Atlantic inflow with differential effects on phytoplankton, e.g. earlier and greater penetration of Atlantic waters into the Norwegian–Barents Seas than Labrador–Newfoundland

44

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45

observed in the NE Atlantic. More recently (since the mid 1990s), however, this relationship has broken down due to changes in the spatial structure of atmospheric pressure patterns: air and ocean temperatures have risen rapidly and ice has decreased significantly in both regions. Most of the phytoplankton observations and modelling discussed here have been made during this latter warming period (see Fig. 14) in which atmospheric and hydrographic conditions have been changing in similar ways in the NORCAN regions. The NORCAN regions (NW and NE Subarctic Atlantic) share a number of common characteristics with regard to their phytoplankton dynamics and environmental controls (Table 2). The Subarctic North Atlantic falls within the Polar Biome (Longhurst, 2007) where phytoplankton growth cycle is mediated principally by light availability although at its southern limits, nutrient limitation may occur in summer. Mixing plays an important role in determining light and nutrient availability for phytoplankton and is strongly influenced by large-scale meteorological forcing. Ice is an important light attenuator and substrate for phytoplankton growth. Large-scale circulation patterns including the interplay of cold/ fresh southward flowing Arctic water and warm/salty northward flowing Atlantic water influence the productivity, phenology and community structure of phytoplankton resulting in similarities in phytoplankton growth cycles and community structure. Decadal changes in meteorological and oceanographic conditions can be linked to observed trends in phytoplankton growth cycles and, to a lesser extent, to productivity. Ocean warming due to climate change is projected to accelerate these temporal shifts in phytoplankton phenology and production over the entire Subarctic Atlantic and overall increase regional productivity. There are, however, some distinct differences between the NW and NE Subarctic Atlantic. The Greenland–Barents Seas extend to higher latitudes and Labrador–Newfoundland basins to lower latitudes than their regional counterparts resulting in differences in the relative importance of light availability (NE Atlantic) and nutrient limitation (NW Atlantic) for phytoplankton growth. For example, ice plays a critical role in the seasonal phytoplankton growth cycle in the Barents and Greenland Seas and on the Labrador–Newfoundland shelves while their counterparts, the central Labrador Sea and the Norwegian shelf are ice free year-round; pelagic blooms in the ice-free regions generally precede those in the icecovered regions by weeks whereas distinct epontic communities contribute to the phytoplankton growth and production cycle only in ice-covered regions. The interplay of Arctic and Atlantic waters results in a ‘‘deficit’’ of silicate in the NE and ‘‘surplus’’ in the NW which may have consequences for phytoplankton community succession, i.e. the relative importance of diatoms in the annual growth cycle, particularly at the southern limits of the Subarctic where nutrient exhaustion in surface waters is observed in summer. Lastly, while climate-related changes in atmospheric and ocean conditions will be large-scale, alterations in southward arctic outflow and northward Atlantic inflow with have differential effects in the NW and NE NORCAN regions. For example, the penetration of warmer Atlantic waters into the sub-artic, with concomitant changes in phytoplankton growth and shifts in community composition, are predicted to occur earlier and penetrate further north in the NE (Norwegian–Barents Seas) than in the NW Atlantic over the coming decades. Acknowledgements Financial and other support for the NORway-CANada Comparison of Marine Ecosystems (NORCAN) project were provided by the Department of Fisheries and Oceans, Canada, the Institute of Marine Research, Bergen, the University of Trondheim, Trondheim, and by the Research Council of Norway (RCN) as part of the Bilateral

Research Cooperation Program between Norway and North America. References ACIA, 2005. Arctic Climate Impact Assessment Scientific Report. Cambridge University Press, 1042pp. Arrigo, K.R., van Dijken, G., Pabi, S., 2008. Impact of a shrinking Arctic ice cover on marine primary production. Geophysical Research Letters 35, L19603. http:// dx.doi.org/10.1029/2008GL035028. Beaugrand, G., 2009. Decadal changes in climate and ecosystems in the North Atlantic Ocean and adjacent seas. Deep-Sea Research II 56, 656–673. Beaugrand, G., Edwards, M., Brander, K., Luczak, C., Ibañez, F., 2008. Causes and projections of abrupt climate-driven ecosystem shifts in the North Atlantic. Ecology Letters 11, 1157–1168. Behrenfeld, M.J., O’Malley, R.T., Siegel, D.A., McClain, C.R., Sarmiento, J.L., Feldman, G.C., Milligan, A.J., Falkowski, P.G., Letelier, R.M., Boss, E.S., 2006. Climate-driven trends in contemporary ocean productivity. Nature 444, 752–755. Børsheim, K.Y., Myklestad, S., 1997. Dynamics of DOC in the Norwegian Sea inferred from monthly profiles collected during three years at 66°N, 2°E. Deep-Sea Research 44, 593–601. Budgell, W.P., 2005. Numerical simulation of ice-ocean variability in the Barents Sea region: towards dynamical downscaling. Ocean Dynamics 55, 370–387. Codispoti, L.A., Friederich, G.E., Sakamoto, C.M., Gordon, L.I., 1991. Nutrient cycling and primary production in the marine systems of the Arctic and Antarctic. Journal of Marine Systems 2, 359–384. Cota, G.F., 1985. Photoadaptation of high arctic algae. Nature 315, 219–222. Dale, T., Rey, F., Heimdal, B.R., 1999. Seasonal development of phytoplankton at a high latitude oceanic site. Sarsia 84, 419–435. Doney, S.C., 2006. Oceanography: plankton in a warmer world. Nature 444, 695– 696. Drinkwater, K.F., Harding, G.C., 2001. Effects of the Hudson Strait outflow on the biology of the Labrador Shelf. Canadian Journal of Fisheries and Aquatic Sciences 58, 171–184. Drinkwater, K.F., Belgrano, A., Borja, A., Conversi, A., Edwards, M., Greene, C.H., Ottersen, G., Pershing, A.J., Walker, H., 2003. The response of marine ecosystems to climate variability associated with the North Atlantic Oscillation. In: Hurrell, J., Kushnir, Y., Ottersen, G., Visbeck, M. (Eds.), The North Atlantic Oscillation. Climatic Significance and Environmental Impact. Geophysical Monograph Series 134. AGU Press, pp. 211–234. Drinkwater, K.F., Colbourne, E., Loeng, H., Sundby, S., Kristiansen, T., 2013. Comparison of the atmospheric forcing and oceanographic responses between the Labrador and Newfoundland Shelves and the Norwegian and Barents Seas. Progress in Oceanography 114, 11–25. Dugdale, R.C., Goering, J.J., 1967. Uptake of new and regenerated forms of nitrogen in primary productivity. Limnology and Oceanography 12, 196–206. Eppley, R.W., 1981. Autotrophic production of particulate matter. In: Longhurst, A.R. (Ed.), Analysis of Marine Ecosystems. Academic Press, London, pp. 343–361. Fabry, V.J., Seibel, B.A., Feely, R.A., Orr, J.C., 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science 65, 414– 432. Falk-Petersen, S., Hop, H., Budgell, W.P., Hegseth, E.N., Korsnes, R., Løyning, T.B., Ørbæk, J.B., Kawamura, T., Shirasawa, K., 2000. Physical and ecological processes in the marginal ice zone of the northern Barents Sea during the summer melt period. Journal of Marine Systems 27, 131–159. Frajka-Williams, E., Rhines, P.B., 2010. Physical controls and interannual variability of the Labrador Sea spring phytoplankton bloom in distinct regions. Deep-Sea Research I 57, 541–552. Fuentes-Yaco, C., Koeller, P.A., Sathyendranath, S., Platt, T., 2007. Shrimp (Pandalus borealis) growth and timing of the spring phytoplankton bloom on the Newfoundland–Labrador Shelf. Fisheries Oceanography 16, 116–129. 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 Research 44, 1623–1644. Harrison, W.G., Cota, G.F., 1991. Primary production in polar waters: relation to nutrient availability. Polar Research 10, 87–104. Harrison, W.G., Li, W.K.W., 2007. Phytoplankton growth and regulation in the Labrador Sea: light and nutrient limitation. Journal of the Northwest Atlantic Fishery Science 39, 71–81. Head, E.J.H., Harris, L.R., Campbell, R.W., 2000. Investigations on the ecology of Calanus spp. in the Labrador Sea. I. Relationship between the phytoplankton bloom and reproduction and development of Calanus finmarchicus in spring. Marine Ecology Progress Series 193, 53–73. Head, E.J.H., Melle, W., Pepin, P., Bagøien, E., Broms, C., 2013. A comparative study of the ecology of Calanus finmarchicus in the Labrador and Norwegian Seas. Progress in Oceanography 114, 46–63. Hensen, S.A., Dunne, J.P., Sarmiento, J.L., 2009. Decadal variability in North Atlantic phytoplankton blooms. Journal of Geophysical Research 114, C04013. http:// dx.doi.org/10.1029/2008JC005139. Holmes, R.W., 1956. The annual cycle of phytoplankton in the Labrador Sea, 1950– 51. Bull. Bingham Oceanographic Collection 16, 1–74. Horner, R., Ackley, S.F., Dieckmann, G.S., Guiliksen, B., Hoshiai, T., Legendre, L., Melnikov, I.A., Reeburgh, W.S., Spindler, M., Sullivan, C.W., 1992. Ecology of sea ice biota 1. Habitat, terminology, and methodology. Polar Biology 12, 417–427.

W. Glen Harrison et al. / Progress in Oceanography 114 (2013) 26–45 Irwin, B.D., 1990. Primary production of ice algae on a seasonally-ice-covered continental shelf. Polar Biology 10, 247–254. Kristiansen, S., Farbrot, T., Wheeler, P.A., 1994. Nitrogen cycling in the Barents Sea – seasonal dynamics of new and regenerated production in the marginal ice zone. Limnology and Oceanography 39, 1630–1642. Lavoie, D., Denman, K., Michel, C., 2005. Modeling ice algal growth and decline in a seasonally ice-covered region of the Arctic (Resolute Passage, Canadian Archipelago). Journal of Geophysical Research 110, 1–17. Legendre, L., Ackley, S.F., Dieckmann, G.S., Guiliksen, B., Horner, R., Hoshiai, T., Melnikov, I.A., Reeburgh, W.S., Spindler, M., Sullivan, C.W., 1992. Ecology of sea ice biota 2. Global significance. Polar Biology 12, 429–444. Li, W.K.W., Harrison, W.G., Head, E.J.H., 2006a. Coherent sign switching in multiyear trends of microbial plankton. Science 311, 1157–1160. Li, W.K.W., Harrison, W.G., Head, E.J.H., 2006b. Coherent assembly of phytoplankton communities in diverse temperate ocean ecosystems. Proceedings of the Royal Society Series B 273, 1953–1960. Li, W.K.W., McLaughlin, F.A., Lovejoy, C., Carmack, E.C., 2009. Smallest algae thrive as the Arctic Ocean freshens. Science 326, 539. Loeng, H., Brander, K., Carmack, E., Denisenko, S., Drinkwater, K., Hansen, B., Kovacs, K., Livingston, P., McLaughlin, F., Sakshaug, E., 2005. Marine systems. In: Arctic Climate Impact Assessment (ACIA). Cambridge Univ. Press, Cambridge, pp. 453– 538 (Chapter 9). Longhurst, A., 2007. Ecological Geography of the Sea, second ed. Elsevier, pp. 542. Lovejoy, C., Vincent, W.F., Bonilla, S., Roy, S., Martineau, M.J., Terrado, R., Potvin, M., Massana, R., Pedros-Alio, C., 2007. Distribution, phylogeny, and growth of cold-adapted picoprasinophytes in arctic seas. Journal of Phycology 43, 78–89. Macdonald, R.W., Sakshaug, E., Stein, R., 2004. The Arctic Ocean: modern status and recent climate change. In: Stein, R., MacDonald, R.W. (Eds.), The Organic Carbon Cycle in the Arctic Ocean. Springer, pp. 6–21 (Chapter 1.2). Not, F., Massana, R., Latasa, M., Marie, D., Colson, C., Eikrem, W., Pedros-Alio, C., Vaulot, D., Simon, N., 2005. Late summer community composition and abundance of photosynthetic picoeukaryotes in Norwegian and Barents Seas. Limnology and Oceanography. 50, 1677–1686. 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. Oschlies, A., 2001. NAO-induced long-term changes in nutrient supply to the surface waters of the North Atlantic. Geophysical Research Letters 28, 1751–1754. Reid, P.C., Johns, D.G., Edwards, M., Starr, M., Poulin, M., Snoeijs, P., 2007. A biological consequence of reducing Arctic ice cover: arrival of the Pacific diatom Neodenticula seminae in the North Atlantic for the first time in 800,000 years. Global Change Biology 13, 1910–1921. Rey, F., 1991. Photosynthesis–irradiance relationships in natural phytoplankton populations of the Barents Sea. Polar Research 10, 105–116. Rey, F., 2004. Phytoplankton: the grass of the sea. In: Skjoldal, H.R., Saetre, E., Faerno, A., Misund, O.A., Rottingen, I. (Eds.), The Norwegian Sea Ecosystem. Tapir Academic Press, Trondhiem, Norway, pp. 97–136 (Chapter 5). Rey, F., Loeng, H., 1985. The influence of ice and hydrographic conditions on the development of phytoplankton in the Barents Sea. In: Gray, J.S., Christiansen, M.E. (Eds.), Marine Biology of Polar Regions and Effects of Stress on Marine Organisms. John Wiley & Sons Ltd., pp. 49–63. Rey, F., Noji, T.T., Miller, L.A., 2000. Seasonal phytoplankton development and new production in the central Greenland Sea. Sarsia 85, 329–344.

45

Sakshaug, E., 2004. Primary and secondary production in the Arctic seas. In: Stein, R., MacDonald, R.W. (Eds.), The Organic Carbon Cycle in the Arctic Ocean. Springer, pp. 57–81 (Chapter 3). Sakshaug, E., Skjoldal, H.R., 1989. Life at the ice edge. Ambio 18, 61–67. Sakshaug, E., Slagstad, D., 1991. Light and productivity of phytoplankton in polar marine ecosystems: a physiological view. Polar Research 10, 69–85. Sakshaug, E., Walsh, J., 2000. Marine biology: biomass, productivity distributions and their variability in the Barents and Bering Seas. In: Nuttall, M., Callaghan, T.V. (Eds.), The Arctic: Environment, People, Policy. Harwood, Amsterdam, pp. 163–196 (Chapter 7). Sakshaug, E., Bricaud, A., Dandonneau, Y., Falkowski, P.G., Kiefer, D.A., Legendre, L., Morel, A., Parslow, J., Takahashi, M., 1997. Parameters of photosynthesis: definitions, theory and interpretation of results. Journal of Plankton Research 19, 1637–1670. Sarmiento, J.L., Slater, R., Barber, R., Bopp, L., Doney, S.C., Hirst, A.C., Kleypas, J., Matear, R., Mikolajewicz, U., Monfray, P., Soldatov, V., Spall, S.A., Stouffer, R., 2004. Response of ocean ecosystems to climate warming. Global Biogeochemical Cycles 18 (GB3033), 1–23. Schmittner, A., Oschlies, A., Matthews, D., Galbraith, E.D., 2008. Future changes in climate, ocean circulation, ecosystems, and biogeochemical cycling simulated for a business-as-usual CO2 emission scenario until year 4000 AD. Global Biogeochemical Cycles 22 (GB1013), 1–21. Signorini, S.R., McClain, C.R., 2009. Environmental factors controlling the Barents Sea spring–summer phytoplankton bloom. Geophysical Research Letters 36, L10604. Skartveit, A., Olseth, J.A., 1986. Modeling slope irradiance at high latitudes. Solar Energy 36, 333–344. Skartveit, A., Olseth, J.A., 1987. A model for the diffuse fraction of hourly global radiation. Solar Energy 37, 271–274. Skogen, M.D., Budgell, W.P., Rey, F., 2007. Interannual variability in Nordic seas primary production. ICES Journal of Marines Science 64, 889–898. Smith Jr., W.O., 1987. Phytoplankton dynamics in marginal ice zones. Oceanography and Marine Biology Annual Reviews 25, 11–38. Smith Jr., W.O., Kattner, G., 1989. Inorganic nitrogen uptake by phytoplankton in the marginal ice zone of the Fram Strait. Rapports et Procès-Verbaux des Rèunions du Conseil International pour l’Exploration de la Mer 188, 90–97. Smith Jr., W.O., Baumann, M.E.M., Wilson, D.L., Aletsee, L., 1987. Phytoplankton biomass and productivity in the marginal ice zone of the Fram Strait during summer 1984. Journal of Geophysical Research 92, 6777–6786. Stuart, V., Sathyendranath, S., Head, E.J.H., Platt, T., Irwin, B., Maass, H., 2000. Biooptical characteristics of diatom and prymnesiophyte populations in the Labrador Sea. Marine Ecology Progress Series 201, 91–106. Tremblay, J.-E., Gagnon, J., 2009. The effects of irradiance and nutrient supply on the productivity of Arctic waters: a perspective on climate change. In: Nihoul, J.C.J., Kostianoy, A.G. (Eds.), Influence of climate change on the changing Arctic and sub-Arctic conditions. Springer, Dordrecht, pp. 73–92. Wu, Y., Peterson, I.K., Tang, C.L., Platt, T., Sathyendranath, S., Fuentes-Yaco, C., 2007. The impact of sea ice on the initiation of the spring bloom on the Newfoundland and Labrador Shelves. Journal of Plankton Research 29, 509–514. Wu, Y., Platt, T., Tang, C.L., Sathyendranath, S., 2008. Regional differences in the timing of the spring bloom in the Labrador Sea. Marine Ecology Progress Series 355, 9–20. Yashayaev, I., Lazier, J.R.N., Clarke, R.A., 2003. Temperature and salinity in the central Labrador Sea during the 1990s and in the context of the longer-term change. ICES Marine Science Symposium 219, 32–39.