Trophic structure and pathways of biogenic carbon flow in the eastern North Water Polynya

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Trophic structure and pathways of biogenic carbon flow inthe eastern North Water Polynya

Jean-Eric Tremblay a,*, Hiroshi Hattori b, Christine Michel c, Marc Ringuette a,Zhi-Ping Mei d, Connie Lovejoy a, Louis Fortier a, Keith A. Hobson e,

David Amiel f, Kirk Cochran f

a Departement de Biologie, Universite Laval, Pavillon Vachon, Cite Universitaire, Que., Canada G1K 7P4b Hokkaido Tokai University, Sapporo 005-8601, Japan

c Freshwater Institute, Fisheries and Oceans Canada, 501 University Crescent, Winnipeg, Manitoba, Canada 53T 2N6d Institut des sciences de la mer (ISMER), Universite du Quebec a Rimouski, 310 allee des Ursulines, Rimouski, Que., Canada G5L 3A1

e Prairie and Northern Wildlife Research Center, Canadian Wildlife Service, Saskatoon, Saskatchewan, Canada S7N OX4f Marine Sciences Research Center, State University of New York, 11794-5000 Stony Brook, USA

Abstract

In the eastern North Water, most of the estimated annual new and net production of carbon (C) occurred during themain diatom bloom in 1998. During the bloom, at least 30% of total and new phytoplankton production occurred as dis-solved organic carbon (DOC) and was unavailable for short-term assimilation into the herbivorous food web or sinkingexport. Based on particle interceptor traps and 234Th deficits, 27% of the particulate primary production (PP) sank out ofthe upper 50 m, with only 7% and 1% of PP reaching the benthos at shallow (�200 m) and deep (�500 m) sites, respec-tively. Mass balance calculations and grazing estimates agree that �79% of PP was ingested by pelagic consumers betweenApril and July. During this period, the vertical flux of biogenic silica (BioSi) at 50 m was equivalent to the total BioSi pro-duced, indicating that all of the diatom production was removed from the euphotic zone as intact cells (direct sinking) orempty frustules (grazing or lysis). The estimated flux of empty frustules was consistent with rates of herbivory by the large,dominant copepods and appendicularians during incubations. Since the carbon demand of the dominant planktivorousbird, Alle alle, amounted to �2% of the biomass synthesized by its main prey, the large copepod Calanus hyperboreus, mostof the secondary carbon production was available to pelagic carnivores. Stable isotopes indicated that the biomass of pred-atory amphipods, polar cod and marine mammals was derived from these herbivores, but corresponding carbon fluxeswere not quantified. Our analysis shows that a large fraction of PP in the eastern North Water was ingested by consumersin the upper 50 m, leading to substantial carbon respiration and DOC accumulation in surface waters. An increasinglyearly and prolonged opening of the Artic Ocean is likely to promote the productivity of the herbivorous food web, butnot the short-term efficiency of the particulate, biological CO2 pump.� 2006 Elsevier Ltd. All rights reserved.

Keywords: Polynya; Primary production; Dissolved organic carbon; Carbon fluxes; Sinking; Grazing; Food web; Bacterial respiration

0079-6611/$ - see front matter � 2006 Elsevier Ltd. All rights reserved.

doi:10.1016/j.pocean.2006.10.006

* Corresponding author. Tel.: +1 418 656 5917; fax: +1 418 656 2339.E-mail address: [email protected] (Jean-Eric Tremblay).

Progress in Oceanography 71 (2006) 402–425

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Progress inOceanography

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1. Introduction

Fluxes of biogenic carbon (C) in the Arctic Ocean are believed to be tightly linked to ice dynamics and thecoupling between primary and secondary production (Michel et al., 1996; Fortier et al., 2002). When epipe-lagic grazers are scarce, or when the release of ice algae is sudden or when pelagic blooms sink abruptly, thenvertical export of particulate organic matter may efficiently deliver organic carbon to the benthos, especiallyover the extensive and shallow continental shelves that characterize the Arctic. This sinking pathway shouldfavour the storage of carbon in the sediment or deep waters, thereby contributing to the biological CO2 pump(Volk and Hoffert, 1985; Feely et al., 2001). The biological pump is thought to be efficient in the Arctic due tothe relatively high growth efficiencies of bacteria at low temperature (Rivkin and Legendre, 2001). Althoughherbivory can also lead to vertical carbon export when large, fast-sinking feces and housing material arereleased (Fortier et al., 1994), it primarily channels carbon toward harvestable pelagic resources and apex con-sumers such as birds and marine mammals. That trophic pathway promotes respiration and leakage of dis-solved organic carbon (DOC) into surface waters, thus limiting the short-term efficiency of the biologicalCO2 pump. The relative importance of the different pathways of carbon flux has not been quantified at theseasonal scale.

In the effort to understand how the herbivorous food webs and the biogeochemical cycling of carbonrespond to inter-annual variability and climate change in the Arctic Ocean, much can be learned from polyn-yas. The North Water, located in northern Baffin Bay, is a large polynya (5–8 · 104 km2) where open watersappear early in April. By contrast, the onset of ice melt in adjacent seasonally ice-covered waters of the Cana-dian Archipelago occurs between mid-July and mid-August, depending on radiative forcing and precipitation(Fortier et al., 2002). Early opening of the North Water is caused by northerly winds and currents that carryice away from an ice arch (Barber et al., 2001), with a contribution of sensible heat from the West GreenlandCurrent and upwelling in the east (Melling et al., 2001). In 1998, the North Water sustained an intense diatombloom that began as early as the end of April (Mei et al., 2002; Klein et al., 2002). Satellite imagery (Belanger,2001) and opportunistic measurements (Lewis et al., 1996) suggest that early blooms are recurrent in the poly-nya. This peculiar timing is likely to become more common with the decreasing extent and thickness of sea iceand earlier dates of seasonal melt (ACIA, 2005).

The long-standing Inuit communities and rich megafauna associated with the North Water led Dunbar(1981) to hypothesize a causal link with locally enhanced primary production. Such coupling is not entirelyintuitive, however, because precocious blooms are potentially unavailable to herbivores that remain in deepwaters (diapause) or whose eggs hatch later during summer in response to increased water temperatures (Rin-guette et al., 2002). This decoupling presumably favors the sinking of ungrazed algae to deep waters and, whilepromoting the biological CO2 pump, would sustain benthic food webs rather than the epipelagic biota. Analternative hypothesis to Dunbar’s is that large pelagic consumers exploit the polynya for physical rather thanbiological reasons. The unique combination of open water, drifting ice floes and fast ice facilitates breathingand reproduction for marine mammals, access to prey for birds and bears, and foraging for visual predators ofplankton.

We synthesize here new and published information on the North Water in order to establish the dominantpathways of carbon flux and to test rigorously the hypothesis that primary production transits primarilythrough pelagic heterotrophs and does not sink directly to deep waters or the benthos. Due to the difficultiesinherent to experimental determinations of ingestion by heterotrophs and to meaningful assessment of theerrors attached to various estimates of carbon stocks and fluxes, the fate of phytoplankton was assessed fromdifferent angles. This approach successfully reconciled estimates of carbon fluxes based on mesoscale changesin the different pools of carbon and nitrogen (i.e. mass balance), on stable isotopes, on vertical sinking and ondiscrete estimates of primary production and ingestion. Using this quantitative analysis as a foundation, weconstructed a flow chart of the herbivorous food web in the Greenland sector of the North Water.

2. Material and methods

Roughly half of the data were transformed and re-analyzed from previously published manuscripts. A largesubset of the other data can be accessed at http://www.quebec-ocean.ulaval.ca/now/. The methods used for

J.-E. Tremblay et al. / Progress in Oceanography 71 (2006) 402–425 403

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sampling, analyses and calculations are reviewed briefly. Details can be found in the original manuscripts.Unless stated otherwise our synthesis will cover the comprehensive sampling campaign of 1998, when theCCGS Pierre Esprit Radisson occupied the North Water from April to July.

2.1. Spatial focus

In 1998, the timing and magnitude of biogenic carbon fluxes differed greatly among the two main sectors ofthe North Water (Fig. 1). The Baffin Land Current continuously supplied nutrient-rich water to the westernside of the polynya (Tremblay et al., 2002b). This region was characterized by strong and variable southwardadvection of surface waters (mean of 23 km d�1; Melling et al., 2001), so that much of the primary productionwas exported horizontally across the southern edge of the polynya. The various estimates of carbon flux canhardly be compared in this context. In the east, however, surface Baffin Bay Water (BBW) entered from thesouth at a low velocity (mean northward component of 3.0 km d�1 from April to June; Melling et al., 2001),implying a residence time of P100 days in the polynya. Synoptic images from SeaWiFs showed that the devel-opment and demise of the bloom was simultaneous throughout the core of this water mass (Belanger, 2001).Free-drifting traps deployed in BBW travelled only short distances, hence the vertical coherence of sinkingfluxes at 50, 100 and 150 m (Michel et al., 2002a). For these reasons, the present analysis focuses on the coreof BBW, where the various estimates of carbon flux were spatially coherent. These sites were identified using aquasi-conservative tracer of water masses (Tremblay et al., 2002a) and include Stns. 18, 27, 38, 40, 49 and 54 inApril, Stn. 18, 38, 40, 52 and 54 in May, Stns. 18, 40, 49, 50, 52 and 54 in June, and Stns. 40, 54 and 58 in July.Although additional sampling was performed during late summer in 1997 and 1999, the data were notincluded in the time series because inter-annual variability in the timing of the bloom was noted (Belanger,2001), and advection must play an important, but poorly constrained role at time scales of >3 months.

2.2. Physical and chemical properties

Temperature, salinity and in vivo fluorescence were recorded using a Rosette sampler equipped with a CTDand a fluorometer. Samples for nutrients and DIC were obtained from vertical profiles using 10-l bottlesattached to the Rosette (details in Tremblay et al., 2002b and Miller et al., 2002). Concentrations ofNO�3 þNO�2 and NO�2 were determined automatically by colorimetry (Koroleff, 1976). During the samplingperiod NO�2 accounted for <1% of NO�3 þNO�2 , which is hereafter referred to as NO�3 . Concentrations ofNHþ4 and urea were determined manually within 2 h of collection using the indophenol-blue (Koroleff,1976) and diacetylmonoxine (Aminot and Kerouel, 1982) methods, respectively. Total DIC was determinedby continuous gas extraction and coulometric titration (Miller et al., 2002). All values were normalized toa salinity of 34.2 pss. The depletions of NO�3 and DIC (apparent) at each station were estimated by differencefrom end member inventories established by conservative salinity-property relationships at Stn. A27 (used forStns. 18, 38 and 40) and A54 (used for Stns. 49, 50, 52 and 54). The mean biological consumption over theregion was obtained by linear regression of the apparent deficit against time and dividing by the appropriatenumber of days. Corrections of the apparent DIC deficit for the air-sea flux of CO2 are discussed below.

2.3. Primary production, nitrogen uptake and particulate standing stocks

Primary production was estimated using the simulated in situ 14C method (details in Klein et al., 2002) Atthe end of 24-h incubations, a small subsample was taken for the determination of total production (PT, thesum of 14C incorporated into POC and released as DOC, cf. Lewis and Smith, 1983) following the protocol ofGosselin et al. (1997). Remaining contents of the incubation bottles were filtered gently onto 0.4 lm and 5 lmNuclepore filters for the determination of total (PP) and >5 lm (PPL) particulate production, respectively. A

posteriori corrections for ice cover were performed by Mei et al. (2002). The production of DOC (PDOC) andthe particulate production of small phytoplankton (PPS) were obtained by difference. Net uptake rates ofNO�3 , NHþ4 and urea were estimated using the 15N-labeling method (details in Tremblay et al., 2006). Ureauptake was estimated at a subset of stations. Uptake rates (qN) were not corrected for isotopic dilutionnor ice cover (for justification see Tremblay et al., 2006). For the subset of stations where urea uptake was

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estimated, the regression slope of total nitrogen uptake against the combined uptake of inorganic nitrogen was1.14 (R2 = 0.98, p < 0.0001). This factor was used to estimate total nitrogen uptake at other stations. Concen-trations of POC were obtained in parallel with the mass spectrometric determination of isotope ratios. Chlo-rophyll-containing phytoplankton were counted and sized with light microscopy. Biovolumes were calculatedusing appropriate geometric shapes, and carbon content was estimated from volumetric conversion factors(details in Lovejoy et al., 2002a).

Fig. 1. Maps of the Arctic Ocean showing the large-scale margin of sea ice (hatched line) and the schematic extent of pack and land-fastice (hatched areas) in the North Water region during early May. Black dots mark sampling stations in Baffin Bay Water (Greenlandsector). The dashed line indicates the mean boundary between the two main water masses (see text). This figure was produced with theOcean-Data-View Software (R. Schlitzer; http://www.awi-bremerhaven.de/GEO/ODV).


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2.4. Bacterial production and respiration

Bacterial abundance and net production (NBP) for July 1998 were reported by Middelboe et al. (2002).Extrapolation of their NBP estimates to previous sampling months can be justified by the broad spectrumof conditions in July, which ranged from full bloom and low DOC at cold stations in the northwest (notshown) to post-bloom and high DOC at warm, BBW sites (e.g. Stn. 54). The association between relativelyhigh NBP and post-bloom communities is a recurrent feature in the Arctic Ocean (e.g., Nielsen and Hansen,1995). Accordingly, vertically integrated NBP estimates in the upper 50 and 150 m were inversely related to theminimum concentration of PO3�

4 in the upper mixed layer (e.g. NBP50 ¼ 0:121e�4:229½PO4�; r2 = 0.97; n = 8). Therationale for using PO3�

4 is that it was in excess and continued to decrease slightly after NO�3 was exhausted,thus providing the best available indicator of seasonal ecosystem maturity. Regression parameters were usedto estimate NBP for previous sampling months. The latter was converted into gross production (GBP = NBP/BGE) and respiration (BR = GBP � NBP) assuming a growth efficiency (BGE) of 0.25 for consistency withthe Arctic literature (Middelboe et al., 1992).

2.5. Heterotrophic biomass and ingestion

The biomass of copepods was assessed by microscopic counts and length-carbon conversions on animalscollected during vertical net tows through the upper water column (see details in Ringuette et al., 2002; Saun-ders et al., 2003). Direct estimates of herbivory were obtained during shipboard experiments at a limited num-ber of stations. Females and late copepodite stages of C. hyperboreus, C. glacialis and M. longa were incubatedin filtered sea-water. Animals were collected sequentially to follow changes in gut content over time. Signifi-cant relationships (species and stage specific) between gut content and chla inventories in the upper 50 m wereused in combination with monthly averaged gut turnover rates to estimate ingestion at other stations whereonly chla and copepod biomass were measured. Grazing was estimated by assuming 30% degradation of chla

in the digestive tract and a C:chl a ratio of 50 (Mei et al., 2003). In the absence of experimental determinationsfor other life stages and species, estimates of carbon ingestion were obtained indirectly. Production(lg C l�1 d�1) was estimated using biomass (B) and mean temperature (T) in the upper 50 m in the relation-ship of Huntley and Lopez (1992) and in keeping with published studies in nearby regions (e.g. Madsen et al.,2001):

P ¼ B � 0:045eð0:111�T Þ: ð1Þ

Carbon ingestion (I) was estimated using a gross growth efficiency (GGE) of 0.3 (Straile, 1997):

I ¼ P=GGE ð2Þ

This method assumes that ingestion is not resource-limited. Rates of herbivory by appendicularians wereassessed from gut content and throughput dynamics during July only (Acuna et al., 2002). Since these esti-mates covered a wide-range of chla concentrations and temperature, we applied their mean grazing rate of35.8 mg C m�2 d�1 to the whole sampling period.

The abundance of heterotrophic ciliates and dinoflagellates was determined by a combination of fluores-cence and Nomarski optics, and their individual carbon content was assessed by volumetric conversion usingappropriate geometric shapes (see Lovejoy et al., 2002b for details on methodology and species diversity). Atsites where samples were collected at two depths in the euphotic zone (Stn. 40, 49 and 54 in April, Stn. 18, 40and 54 in May, Stn. 40, 49, 50 and 54 in June, Stn. 40, 54 and 58 in July), the production of microheterotrophswas estimated with the empirical relationships of Levinsen et al. (1999) established at 1.4 �C for nearby DiskoBay, and converted to ingestion rates using Eq. (2), with a fixed GGE of 0.33 for dinoflagellates and a GGEranging from 0.33 to 0.55 for ciliates, depending on the concentration of POC in the water column (see Straile,1997). Ingestion rates were corrected for temperature using a Q10 of 2.8 (Levinsen et al., 1999).

The partitioning of ingested carbon was assessed using physiological constraints binding ingestion (I) torespiration (RE), growth (g) and egestion (e) in aquatic protozoan and metazoan zooplankton:


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RE ¼ I � ðAE�GGEÞ ð3Þg ¼ I �GGE ð4Þe ¼ I � ð1�AEÞ ð5Þ

where AE is the mean assimilation efficiency of consumers. We assumed an AE value of 0.8 based on exper-imental measurements with C. glacialis and C. hyperboreus in the Northeast Water Polynya (Daly, 1997). Anexhaustive review of diverse protozoan and metazoan zooplankton showed that a mean GGE of �0.33 overthe range of POC concentrations observed during our study is a reasonable assumption (Straile, 1997). Forconsistency with published studies on the fate of grazed carbon in other systems we assumed a GGE of0.33 (e.g. Pesant et al., 2000).

2.6. Sinking fluxes

Sinking fluxes of C, pigments, intact diatom cells and biogenic silica (BioSi) were estimated using free-drift-ing sediment traps (FST) deployed at 50, 100 and 150 m for 12–24 h (details in Caron et al., 2004). For C,vertical fluxes were also estimated using the 234Th/238U disequilibrium approach (Amiel et al., 2002). Thefluxes estimated by the two methods agreed well (Th-derived carbon flux = 0.68 + 1.05 FST flux; n = 13;r2 = 0.89; p < 0.001, see Amiel et al., 2002 for all data) at the BBW sites considered in the present analysis(eastern Stns. S2, S4, E1, E2 and D2).

2.7. Stable isotopic analyses

Water-column samples (P20 l) were collected away from ice at 5 m using Niskin bottles. Ice-bottom sam-ples were taken with an ice auger and melted slowly in filtered seawater (Details in Michel et al., 2002b). Sam-ples were filtered onto 62-mm GF/F filters using an Amicon stirred cell unit with gentle pressure. Filters weresoaked in 0.1 N HCl to remove inorganic carbon and dried. Zooplankton were obtained from net tows, frozenwhole and dried prior to analysis. Sampling procedures for larger organisms are described in Hobson et al.(2002). Following combustion of 1-mg homogenates at 1800 �C, isotopic analyses were performed with aEuropa 20/20 mass spectrometer (details in Hobson et al., 2002). Stable isotopic abundance is reported asa deviation (d in &) from known standards.

2.8. Scaling

Most of the data were grouped in depth intervals based on mixed layer dynamics, light penetration, andbiological imperatives. The thickest upper mixed layer in BBW was 56-m deep (mean of five casts) at Stn.18 in May. Averages for the depth of the euphotic zone (defined here as the 1% light level) rose from 51 min April to �20 m in May and June, and then declined to 33 m in July. Based on incubations, nearly 100%of the cumulative photosynthesis and nitrogen uptake occurred above 50 m (Tremblay et al., 2002b). There-fore the FST deployed at 50 m systematically intercepted material exported from the euphotic zone and theupper mixed layer. We also assumed that visual predators were not able to feed below 50 m and that feedingby micro and mesozooplankton occurred primarily above this depth. Hereafter we will refer to the 50 m layeras the euphotic zone. The deepest drifting traps were at 150 m, which corresponds to the depth where no deple-tion of nutrient occurred during the bloom and is close to the bottom at the shallowest sampling sites (e.g.,Stn. 18). We will refer to the 50–150 m layer as the subsurface zone. Examinations of in vivo fluorescence pro-files and CTD records indicated that discrete bottle sampling did not entirely resolve vertical structures (e.g.,thickness of the chlorophyll maximum). In order to compensate for this, relationships were establishedbetween salinity and chemical measurements, and between fluorescence and the concentrations of POC forindividual stations or for groups of similar and closely related sites. The highly significant regression param-eters were used to interpolate POC data between bottle sampling depths. Flux data were integrated temporallyin order to provide cumulative fluxes. Mean, weighted rates can be retrieved by dividing the cumulative valueby the appropriate number of days. Unless stated otherwise, all quantities are given in molar units for consis-tency and to ease comparisons among stocks and fluxes.


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3. Results and discussion

3.1. Net changes in standing stocks and inventories

Starting on 23 April the inventory of POC increased in concert with the progressive depletion of NO�3 andDIC until the bloom’s apogee on June 12 (Fig. 2a–c). DIC decreased a little more over the next week, whereasNO�3 and recycled nitrogen ðureaþNHþ4 Þ increased. POC declined abruptly between 12 June and 1 July,thereafter hovering above pre-bloom levels while DOC inventories reached maximum values (Fig. 2d). Largefluctuations in POC were mediated primarily by centric diatoms >5 lm (Fig. 2e). Chl-containing flagellatesand coccolithophores made a negligible contribution to autotrophic carbon (Lovejoy et al., 2002). The bio-

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Fig. 2. Changes in the different pools of carbon and dissolved nitrogen in the upper 50 m (open symbols) and 150 m (closed symbols) ofthe water column during 1998 in the BBW sector of the North Water: (a) Apparent deficit of DIC, (b) NO�3 deficit (circles) and combinedinventory of NHþ4 and urea (crosses), (c) POC inventory, (d) DOC inventory, and the biomass of (e) diatoms, (f) heterotrophic ciliates(circles and solid lines) and dinoflagellates (squares and dashed lines), (g) large herbivorous copepods, and (h) small copepods. All units aremol C m�2, except for panel b (mol N m�2). Note the logarithmic scale of the y-axis in panels f–h.


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mass of heterotrophic dinoflagellates showed three peaks, a small one at the beginning of the sampling period(peridiniales) and larger ones in early June (peridiniales) and mid-July (gymnodiniales) (Fig. 2f). Heterotro-phic ciliates peaked only once (Tintinids) during late June. Large herbivorous copepods (mostly C. hyperbo-

reus, with a secondary contribution by C. glacialis) peaked in early June (Fig. 2g). At this time, most of thebiomass was in the large copepodites (CVI and CV) and females (not shown). The biomass of small copepods(dominated by Oithona similis), generally considered to be omnivorous, was two orders of magnitude lower(Fig. 2h), with a distribution that mirrored that of the heterotrophic dinoflagellates (Fig. 2f). The biomassof heterotrophic flagellates and mixotrophic protists amounted to less than 5% of the combined biomass ofcopepods and heterotrophic ciliates and dinoflagellates.

Based on the patterns shown in Fig. 2a–d, net changes in DIC, nitrogen, POC and DOC were calculated forthree periods, each starting on 23 April and extending to 12 June (build-up of the bloom), July 1st (build-upand collapse) or 21 July (entire sampling period). Detailed results are given in Appendices 1 and 2. For eachperiod, the net change in DIC and dissolved nitrogen was obtained by fitting a linear regression to the data inFig. 2 and multiplying the slope by the appropriate number of days. An exponential regression model wasused for DOC. Since the resulting estimates were obtained by pooling different stations, most of whichrepeated in time, the error on the slope encompasses spatial variability and minor advective effects at the edgesof the sampling grid. Net changes in POC were calculated using the linear regression method (first two peri-ods) or by subtracting initial values on April 23 from the July average (entire sampling period). For the latter,the error is simply the standard deviation of the average.

3.2. Renewal of NO�3 and DIC during the bloom

Comparison of the two vertical strata implies that about half of the NO�3 consumed by 12 June originatedin the subsurface layer (Fig. 2b and Appendix 1). Only a minute fraction of this subsurface deficit could havebeen produced in situ since nearly the entire cumulative NO�3 uptake during incubations occurred above the1% isolume, which rose from 45 to 22 m between 26 April and 15 May (Tremblay et al., 2006). The mesope-lagic deficit was thus produced by partial, episodic mixing of nutrient-rich intermediate waters and depletedsurface waters during storms. These storms occurred until late May when atmospheric warming established aresilient density gradient in the upper 20 m (see Tremblay et al., 2002b). Assuming that DNO�3 was drivenmostly by biological uptake in the upper 50 m prior to 12 June, the cumulative biological drawdown (DDICb)of DIC on that day was:

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DNO�3 50

ð6Þ

The rationale is that in the absence of atmospheric supply the subsurface DIC inventory would be dilutedalong with NO�3 during mixing events. However, the subsurface DIC deficit is relatively small (Appendix 2)and implies that waters entrained from the surface were enriched with atmospheric DIC. Wind-driven dis-ruption of the pycnocline did not occur after June 12, and further changes in DIC reflected mostly bio-logical processes. Accordingly, the difference (4.59 ± 1.73 mol C m�2) between DDICb and the apparentdeficit at the bloom’s apogee was added to the apparent deficit on 1 July and 21 July. An alternate cor-rection (2.47 ± 1.65 mol m�2; Miller et al., 2002) based on wind velocities and the Schmidt number, over-laps statistically with the one obtained with Eq. (6). Since Miller et al. (2002) considered their correctionto be conservative due to the prescribed gas transfer velocities, our estimates of DDICb should be reason-ably accurate.

3.3. Bacterial production, primary production and nitrogen uptake

During July, volumetric rates of NBP ranged from 3.8 to 16 mg C m�3 d�1 in the surface waters of BBW,with corresponding depth-integrated values of 270–450 mg C m�2 d�1 (not shown; see Middelboe et al., 2002).These rates are higher than those reported for unproductive waters of the central Arctic in summer (0.1–4.1 mg C m�3 d�1; Sherr and Sherr, 2003; Rich et al., 1997), but similar to those in more productive areas


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of the Greenland, Bering and Chukchi Seas (1.0–10 mg C m�3 d�1). Shipboard experiments indicated thatbacterial production was, at some stations, stimulated by glucose addition during incubations (Middelboeet al., 2002). This artificial stimulation suggests that a large portion of the DOC that accumulated was notreadily labile or of lesser nutritive value than glucose. Otherwise it should have been more than sufficientto fuel GBP. This finding is consistent with previous observations that only 33% of the DOC produced byphytoplankton is readily labile (Sondergaard et al., 2000). The cumulative NBP and GBP obtained from directmeasurements (July) and the regression parameters described in Section 2 (April–June) are given in Appendix3.

Most of the particulate and dissolved primary production occurred between mid-May and mid-June(Fig. 3a), corresponding to the period of net POC accumulation. On 21 July, small and large phytoplanktonhad mediated �13% and 54% of the cumulative PT, respectively, with the rest (33%) being released as DOC.The uptake of NO�3 increased rapidly during May and June, whereas NHþ4 uptake increased throughout thesampling period (Fig. 3b). The daily f-ratio (based on NHþ4 and NO�3 uptake) at individual stations was ini-tially high and decreased after the collapse of the bloom in June (Fig. 3c). The cumulative f-ratio (calculatedfrom the cumulative uptake of the different nitrogen sources up to each time point) remained high (�0.80) andnearly constant until late May, decreasing to an overall value of 0.58 by the end of the sampling period. Totaland particulate new production at individual stations were estimated by multiplying f-ratios by PT and PP,respectively. Cumulative values are shown in Appendix 3. Particulate new production was nearly equivalentto particulate production by phytoplankton >5 lm (PPL), augmenting the geographical range of the relation-ship proposed for subarctic regions (Dauchez et al., 1996).

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Fig. 3. Temporal changes in the (a) DOC production by total phytoplankton (triangles) and the particulate production of phytoplankton<5 lm (squares) and >5 lm (circles), (b) the uptake of nitrate (circles) and NHþ4 (squares), and (c) the daily (circles) and cumulative(dashed line) f-ratios.


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The exportable fraction of PT, i.e. that which can sink out of the euphotic zone or be stored into the bio-mass of consumers without compromising the integrity of the ecosystem, was estimated as the ratio of netcommunity (DDICb) to total (PT) production (hereafter termed ‘‘c-ratio’’) using data in Appendices 2 and3. The crucial difference between the c-ratio and the f-ratio is that PT includes DOC production, whereasnitrogen uptake rates account only for net assimilation into PON (Bronk et al., 1994). During the NorthWater bloom, however, the accumulation of ammonium and urea in the euphotic zone was negligible, anda mass balance exercise showed that the release of non-urea DON, if any, was at most 7% of the cumulativeNO�3 uptake (Tremblay et al., 2006). In this context, the close agreement between the cumulative f- andc-ratios on 21 July confirmed that �58% of PDOC was new and potentially exportable production.

Net community production (i.e. DDICb) was nearly equivalent to total new production (f · PT) until July 1(Fig. 4). It follows that for the first two periods at least, C production from regenerated nutrients was roughlyequivalent to the combined respiration of all consumers. Otherwise, DDICb would have been much lower thantotal new production. This is also supported by the inventories of recycled nitrogen sources. Because the con-centrations of NHþ4 and urea were at detection limit prior to the bloom and did not increase substantially until1 July, the sustained use of recycled nitrogen by phytoplankton (Fig. 3b) must have been balanced with therelease of reduced nitrogen (e.g. excretion) by heterotrophs. Note that the relationship between net communityproduction and cumulative new production is expected to break down as the season progresses further andorganic carbon is respired back to DIC.

3.4. Carbon budget

A carbon budget for the upper 150 m was established by comparing estimates of new and net communityproduction with cumulative sinking fluxes and net changes in POC and DOC inventories. The 150 m layer waschosen because it represents the depth above which no changes in nutrients and DIC were observed, andbecause DOC release and respiration by vertically migrating animals can occur below feeding depth. Cumu-lative POC sinking fluxes obtained from free-drifting sediment traps are given in Table 2. At the peak of thebloom (June 12), up to 88% of the missing DIC was accounted for, with POC representing the major reservoir(Fig. 4). On July 1, only 68% of the missing DIC was accounted for, with DOC now representing the dominantcarbon pool. By July 21, the majority of new production or missing DIC was recovered in DOC. This resultimplies that some of the POC had been temporarily stored in the biomass of large consumers (i.e. not as partof the POC pool), but that an equivalent amount of carbon was subsequently released as DOC.

3.5. Vertical distribution of sinking fluxes and inferred diatom mortality

On a cumulative basis, the POC flux decreased exponentially with depth when compared with PP in theeuphotic zone (Fig. 5). The cumulative carbon supply to the deepest traps at 500 m (long-term sequential traps

Cum

ulat

ive

C fl

ux (

mol

m-2

)

12 June 1 July 21 July0

2

4

6

8

10

12

14

Fig. 4. Estimates of DDICb (net community production; gray bars), cumulative new production (open bars) and the sum of cumulativesinking (dashed bars), DPOC (solid bars) and DDOC (dotted bars) since 23 April.


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moored near Stn. 54; Hargrave et al., 2002) was consistent with the estimated demand of benthic organisms(Grant et al., 2002) and burial in underlying sediments (Hamel et al., 2002). It is noteworthy that the esti-mated, annual vertical flux at 500 m amounted to only 1% of the cumulative PP by July 21. By contrast,the BioSi flux showed little vertical attenuation in the upper 150 m. Vertical fluxes at 50 and 100 m were nearlyequivalent to the total amount of BioSi produced in the euphotic zone (estimated by multiplying PPL by aBioSi:POC build-up ratio of 0.12; see Tremblay et al., 2002b), consistent with low silica dissolution in the coldsurface waters of the polynya (Michel et al., 2002a). The observed pattern of BioSi sinking indicates thatnearly all the diatom frustules synthesized by 21 July were exported vertically and locally, confirming that hor-izontal advection was a minor loss term.

At 50 m, the time series of vertical POC flux was a sequence of near-Gaussian shape with maximum valuesimmediately following the peak of the bloom (Fig. 6a). Microscopic examination of FST material showed rel-atively high numbers of large, intact diatoms prior to July. Nearly 100% of the chlorophyll flux was associatedwith particles retained on 5 lm filters (Caron et al., 2004), suggesting that sinking cells were mostly large dia-toms or aggregates. The chlorophyll flux peaked at the same time as the total POC flux, but decreased muchmore abruptly during the second and third weeks of June (Fig. 6b). The flux of phaeopigments remained rel-atively high during that time, suggesting an increased fraction of grazed material in the flux. The change insedimenting material was reflected in the fluxes of intact diatom cells vs. total biogenic silica, the latter main-taining relatively high values during the second half of June (Fig. 6c).

The time series presented in Fig. 6 can be used to back-calculate diatom mortality in the upper 50 m. TheBioSi flux is particularly useful in this respect, because heterotrophs do not digest frustules (Tande and Slags-tad, 1985) and BioSi was well preserved during descent in the North Water (see Fig. 5). Division of the BioSiflux at 50 m by the BioSi:POC ratio of 0.12 gives the total loss of diatom-synthesized POC (sum of mortalitywithin the euphotic zone and direct sinking of intact cells). The cumulative loss amounted to 68%, 73% and92% of cumulative PPL (mostly diatoms) on 12 June, 1 July and 21 July, respectively.

POC flux (mol m-2)

0 2 4 6 8 10 12

Dep

th (

m)

0

100

200

300

400

500

BioSi flux (mol m-2)

0.0 0.2 0.4 0.6 0.8 1.0 1.2

?

Fig. 5. Comparison of cumulative particulate primary production (PP; open square) and BioSi production (open circle) in the euphoticzone on 21 July with the cumulative sinking fluxes of POC (closed squares) and BioSi (closed circles) obtained from free-drifting sedimenttraps (50, 100 and 150 m), and the sinking flux of POC obtained from long-term sequential traps (closed triangles; Hargrave et al., 2002)moored at 200 and 500 m near Stn. 54. The sequential trap data at 200 m (question mark) are considered anomalous and were not includedin calculations.


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The portion of total diatom carbon loss due to direct sinking of intact cells was estimated by converting thevolume of intact diatoms in trap material into carbon and also by multiplication of the chla flux by a POC:Chlratio of 36 (see Caron et al., 2004). Changes in the carbon loss via direct sinking are shown in Fig. 6d andcumulative values are provided in Table 2. The volumetric and chl-based approaches produced very similarresults, indicating that diatoms mediated nearly all the vertical flux of autotrophic matter. Subtracting the fluxof intact diatoms from the BioSi-derived carbon loss gives an estimate of mortality within the euphotic zone,which could be caused by grazing or viral lysis. Although the quantitative impact of lysis has not been assessedin polar regions, there is evidence that viral infection may be rare in cryophilic diatoms and other walled,

a

Tot

al P

OC

(mm

ol C

m-2

d-1

)0

20

40

60

80

100

b

Chl

a

(mg

m-2

d-1

)

0

4

8

12

16

20

24

Phaeopigm

ents (m

g m-2 d

-1)

0

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c

Bio

Si

(mm

ol S

i m-2

d-1

)

0

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Intact cells

(x108 cells m

-2 d-1)

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40

d

Car

bon

loss

(mm

ol C

m-2

d-1

)

0

30

60

90

120

150

180

May June July

Fig. 6. Temporal changes in the vertical fluxes of (a) POC, (b) chla (closed circles and solid line) and phaeopigments (open squares anddashed line), (c) BioSi (closed circles and solid line) and intact diatom cells (open squares and dashed line) at 50 m, and the inferred, (d)total loss of diatom carbon (sum of mortality within the upper 50 m and the sinking of intact cells across 50 m) and sinking of carbon fromintact diatoms (open triangles and dashed line) and intact phytoplankton (open squares).


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eukaryotic microalgae (Gowing, 2003). Diatoms can also retain viability for at least 2 weeks following nitro-gen deprivation (Berges and Falkowski, 1998). In this context, we surmise that the BioSi-derived estimates ofmortality primarily reflected ingestion, whose temporal variability and cumulative values are shown in Fig. 6dand Table 3, respectively. Note that beyond the end of June the formation and sinking of silicon-rich restingspores of Chaetoceros socialis probably caused the BioSi approach to overestimate mortality (Michel et al.,2002a). This process may contribute significantly to the second peak in Fig. 5d and would explain why thecumulative BioSi-derived estimate of grazing on July 21 is somewhat higher than other estimates of ingestion(Table 3).

3.6. Vertical dilution

In addition to sinking, a portion of the biomass synthesized during the bloom was subjected to vertical dilu-tion, consistent with the observation that 26% of the POC (1.17 mol m�2) and PON at the bloom’s apogee waslocated in the subsurface layer (Appendices 1 and 2; calculated by difference between the two strata). Massbalance confirms that half of the accumulation was due to mixing supply (Mmin) and not sinking (S), since:

DPOC50–150 � S50 þ S150 ¼ Mmin ¼ 0:59 mol m�2 ð7Þwould otherwise be 60 (see Table 2 for S values). Note that this estimate is a minimum since it does not ac-count for respiration or solubilization of POC within the subsurface layer (e.g. Huston and Deming, 2002).The mixing supply was thus at least 6% of PP. Note that this loss affects small and large phytoplankton inproportion to their relative contribution to total PP and DPOC. Incidentally, �6% of the fresh DOC releasedfrom phytoplankton and other sources was also diluted into the subsurface.

3.7. Direct and indirect estimates of grazing

The isotopic signature of a mixture composed of small copepods generally considered to be omnivorousclearly indicated that their trophic level was similar to that of the large herbivorous copepods (Fig. 7). Trophicenrichment of nitrogen isotopes is generally 3–4& per trophic level (Michener and Schell, 1994). Clearly, allcopepods had a relatively low trophic level (i.e. TL = 2) when compared to strict carnivores (e.g. the plank-tivorous bird, the Dovkie, Alle alle, and the large predatory copepod Euchaeta glacialis). The highly negatived13C of copepods also shows that ice algae were not a major item in their diet (Tremblay et al., 2006). More-over, the similar isotopic composition of planktonic POM (mostly diatoms) and the material intercepted by

δ13Corg (‰)

-24 -22 -20 -18 -16 -14 -12

δ15N

org

(‰)

6

7

8

9

10

11

12

PlanktonTraps

Bottom ice

C. hyperboreus

Small copepods

C. glacialis

E. glacialis

Alle alle

Fig. 7. Average d15N and d13C of planktonic (closed circle) and bottom-ice (closed square) POM, sinking material (inverted triangle),different copepods (open circles) and carnivorous animals (open squares) during May and June.


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drifting traps in May and June suggests that the fecal material released by the dominant zooplankton wasderived primarily from phytoplankton. Grazing experiments are summarized in Appendices 4 and 5. Resultsfor female C. hyperboreus were consistent with previous investigations in the Arctic, both in terms of gut con-tent (range 0–375 ng chla ind�1; Nielsen and Hansen, 1995) and evacuation rates (range 0.015–0.032 min�1;see Hansen et al., 1990). Temporal variations in the rates of herbivory (not shown) closely followed changesin copepod biomass (Fig. 2g). Cumulative herbivory by the CIV, CV and females of C. hyperboreus and C.

glacialis was 3.77, 5.10 and 5.17 mol C m�2 by 12 June, 1 July and 21 July, respectively (Table 1). Additionalcarbon ingestion (estimated from the production model of Huntley and Lopez, 1992) by smaller stages of thesetwo copepods and all stages of the other six species was relatively small. Using the mean experimental rateprovided by Acuna et al. (2002), appendicularians ingested �0.31 mol m�2 of autotrophic carbon duringthe entire sampling period. The main food items ingested by Oikopleura in the North Water in July were dia-toms, especially C. socialis (Acuna et al., 2002). The estimated carbon ingestion by heterotrophic ciliates wasmoderate. By 21 July, heterotrophic dinoflagellates mediated �36% of the total carbon ingestion.

3.8. Non-sinking loss of phytoplankton: a mass balance approach

Mass balance calculations are based on the observation that intact chla < 5 lm did not contribute signif-icantly to sinking flux (Caron et al., 2004) and assumes that sloppy feeding was restricted to mesozooplanktonforaging on phytoplankton >5 lm. The ingestion of phytoplankton <5 lm (IS) is

IS ¼ 0:94PPS � DPOCp; ð8Þand the ingestion of phytoplankton >5 lm is

IL ¼0:94PPL � ðDPOCp þ SpÞ

1þ yð9Þ

where the factor 0.94 corrects for vertical dilution (see Section 3.6), Sp is the sinking flux of intact diatomsacross 50 m (Table 2) and y is the ratio of carbon loss by sloppy feeding to ingested C, which typically rangesfrom 0.10 to 0.29 (Anderson and le B. Williams, 1998). For consistency we used the intermediate y of 0.23proposed by Anderson and le B. Williams (1998), despite a recent report of extremely high y (0.96) for Arcticcopepods in culture (Møller et al., 2003). The estimated cumulative ingestion of phytoplankton >5 lm by het-erotrophs was 2.77, 5.74 and 5.78 mol C m�2 on 12 June, 1 July and 21 July, respectively. Corresponding esti-mates for small phytoplankton were 1.78, 2.05, and 2.27.

3.9. Similarity and differences between the various estimates of ingestion

Estimates of ingestion are summarized and compared in Table 3. Recall that these estimates were obtainedusing an incomplete, albeit extensive, data set and that some calculations required several assumptions that arehardly verifiable. Nevertheless we used care to insure that the assumptions were coherent with extensive liter-ature reviews and previous investigations of Arctic systems. It is also difficult to provide a meaningful estimateof the error attached to several of the estimates.

The agreement among the potential ingestion of diatoms (the BioSi approach in Section 3.5), the experi-mental rates of herbivory by large metazoan zooplankton (see Section 3.7), and the potential grazing loss

Table 1Cumulative estimates of herbivory by the large herbivorous copepods (females, CV and CIV of C. hyperboreus and C. glacialis), the totalcopepod assemblage and appendicularians, and of ingestion by heterotrophic ciliates and dinoflagellates

Large copepods All copepods Appendicularians Ciliates Dinoflagellates

June 12 3.77 3.88 0.19 0.43 2.08July 1 5.10 5.29 0.25 0.82 2.47July 20 5.17 5.68 0.31 1.36 4.11

The calculation period started on 23 April for each time point. All units are mol C m�2.


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of phytoplankton > 5 lm (the mass balance approach in Section 3.8) is good. We interpret this convergence assolid evidence that the herbivorous food web is the major pathway of biogenic carbon flux in the North Water.In addition, the agreement suggests that the assumptions made regarding the degradation of chla during gutpassage are approximately correct. It is noteworthy that the above grazing estimates are much higher thanthose obtained by chlorophyll disappearance in incubation bottles (Saunders et al., 2003). The discrepancyis possibly caused by bottle effects, e.g. copepods may have been feeding much less actively in the bottles(see Mauchline, 1998 for a review of potential artifacts). The estimated carbon ingestion by heterotrophic cil-iates and dinoflagellates is of the same order as herbivory by large metazoans, a phenomenon observed in thenearby coastal waters of Disko Bay (Levinsen and Nielsen, 2002). While it is possible that the heterotrophicprotists ingested some of the phytoplankton >5 lm, their main prey are small phytoplankton and bacteria inpolar waters (Anderson and Rivkin, 2001). Carbon ingestion by protists was reasonably close to the sum ofNBP and PP <5 lm on 12 June and 1 July, but substantially higher afterward. The discrepancy could occur ifdetritus became a significant part of their diet.

Additional evidence for the grazing pathway is provided by the match between regenerated carbon produc-tion (driven by nitrogen recycling) and combined heterotrophic respiration discussed in Section 3.3. In thiscontext, carbon production from regenerated nutrients (Appendix 3) can be used to estimate ingestion usingEq. (3) and the values of AE and GGE justified in Section 2. The predicted ingestion (Table 3) was slightly

Table 2Cumulative sinking fluxes of POC across 150 and 50 m (obtained from free-drifting sediment traps), with different estimates of thecontribution of phytoplankton and diatom-derived material at 50 m

C flux (mol m�2)

12 June 1 July 21 July

Total POC at 150 m 1.07 1.80 2.12Total POC at 50 m 1.64 2.68 3.08Intact cells (Sc in Eq. (3))a 1.11 1.50 1.64Chlab 1.21 1.69 1.81Phaeopigmentsb 0.46 0.81 1.06Potential flux from BioSic 5.36 6.65 8.55

The calculation period started on 23 April for each time point.a Estimated by volumetric conversion of intact cells into POC.b Estimated by multiplying pigment flux by 36.c Estimated by dividing the cumulative BioSi flux by a BioSi:POC ratio of 0.12 in the euphotic zone (see Tremblay et al., 2002b).

Table 3Compared estimates of cumulative mortality and heterotrophy in the euphotic zone

Cumulative carbon flux (mol C m�2)


Diatom mortality from BioSi fluxa 4.25 5.15 6.91Non-sinking loss of phyto >5 lm (mass balance) 2.77 5.74 5.78Non-sinking loss of phyto <5 lm (mass balance) 1.78 2.05 2.27Total herbivory by copepods and appendicularians 4.07 5.54 5.99Ingestion by het. ciliates and dinoflagellates 2.51 3.29 5.47Non-sinking loss of phyto <5 lm + NBP 2.24 3.03 3.56Total non-sinking loss 4.72 8.55 9.18Total ingestion 6.60 8.85 11.5Total ingestion predicted from PREG 7.20 10.9 12.2

The calculation period started on 23 April for each time point.a Estimated by subtracting the C flux associated with intact cells from the potential carbon flux associated with the sinking of BioSi (data

in Table 2).


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higher than the estimated total ingestion, which is expected since the latter does not take bacterial respirationinto account.

3.10. Fate of primary production in the eastern North Water

On 21 July, cumulative PP was compared to the sum of direct sinking (Sp), dilution, DPOCp and total inges-tion (combined carbon ingestion by copepods, appendicularians and heterotrophic protists minus NBP)(Fig. 8). Roughly 79% of PP was processed by heterotrophs, with only 15% sinking as intact cells (mostlyat the peak of the bloom). It is noteworthy that vertical dilution of the bloom by mixing transported halfas much carbon to the subsurface. Given the good agreement observed between Th- and FST-derived esti-mates of sinking flux in the eastern North Water (using the subset of stations identified in Section 2; see alsoAmiel et al., 2002), the exponential decrease in vertical flux (Fig. 6) can be used to calculate a cumulative e-ratio (POC sinking across 100 m: PP = 0.22) for consistency with the calculations of Ducklow et al. (2001).Even if we based the calculation on the 50-m FST data (i.e. close to the bottom of the euphotic zone), theresulting e-ratios would only be 0.17, 0.24 and 0.27 on 12 June, 1 July and 21 July, respectively. These esti-mates are lower than the values predicted by Wassmann (1990) for productive boreal systems. Bulk e-ratioscan be compared with the export efficiency of the carbon processed through heterotrophs by computing theratio of exported detritus (i.e. S50 � SP) to total ingestion in Tables 2 and 3. This calculation yields valuesof 0.08, 0.13 and 0.13 for the three periods and suggests that intense grazing dragged the e-ratio downwardin the eastern North Water. Note that as the season continued and the ice eventually formed again, it is likelythat the cumulative export of carbon (either as POC or animal carcasses) continued to increase, closing thegap with cumulative new production.

The modest short-term efficiency of vertical POC export in the eastern North Water departs from thenotion that polar ecosystems characterized by a pulsed diatom bloom display relatively high e-ratios (e.g.Buesseler, 1998), presumably due to rapid sedimentation of intact diatoms and relatively high bacterial growthefficiency (Rivkin and Legendre, 2001). Our observation is not isolated; a low e-ratio of 0.20 was reported forthe Antarctic Polar Front, where elevated biomass and diatom dominance persist seasonally (Tremblay et al.,2002c). Thus it appears that conditions that favor prolonged diatom blooms may also lead to low sinkingexport efficiency. The high e-ratio reported for the Northeast Water Polynya (Buesseler, 1998) may be relatedto a short window of observation at or near the peak sedimentation, when decreasing rates of daily primaryproduction are compared with a time-integrative measure of flux. A similar result can be obtained for theNorth Water by comparing daily primary production and sinking fluxes on 12 June, but comparisons atthe daily time scale are not relevant to carbon cycling and ecosystem function in a seasonally pulsed system.

Direct sinking15%

Dilution 5%

Accumulation1%

Ingestion 79%

Fig. 8. Partitioning of cumulative particulate primary production (PP) into ingestion, sinking, vertical dilution and POC accumulation by21 July.


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One explanation for the low e-ratios observed in the eastern North Water and at the Antarctic Polar Frontwould be the slow sinking velocities of diatoms during spring and summer (Caron et al., 2004; Mei et al.,2003). The highest intrinsic growth rate (calculated from nitrogen uptake and PON inventories) during thebloom was 0.4 d�1 on May 3, which is low but close to the maximum rate of 0.5 d�1 for diatoms growingat subzero temperatures under saturating irradiance and nutrient concentrations (Eppley, 1972). Mean sinkingrates in the North Water were only 0.35 and 1.09 m d�1 based respectively on SETCOL estimates (Mei et al.,2003) and particle interceptor traps at 50 m (Caron et al., 2004). The prolonged residence times of the diatomsin surface water allows the grazers to consume a relatively high portion of their production, thus raising DOCrelease, respiration and nutrient recycling in surface waters. In the North Water, the added replenishment ofnitrate during the bloom permitted the realization of very high biomasses, which probably drove the peak inthe sedimentation of intact cells and aggregates during the first half of June. The near-Gaussian pattern of thetime-series of vertical flux of POC and intact cells (estimated from floating sediment traps; FST), with max-imum values matching the peak of the bloom, is consistent with a critical concentration threshold for coag-ulation and the increased stickiness of diatoms in an ageing bloom (Fig. 5A). Combined with theincreasing stratification and exhaustion of nitrate from the upper mixed layer, heterotrophs were able to con-sume the remaining portion of the bloom after rates of primary production began to decline.

The situation was different at the polynya’s margin, where land-fast ice persisted during the development ofthe adjacent open water bloom. Ice algae contributed the bulk of primary production and sinking flux fromApril to June (Michel et al., 2002b). Meiofaunal grazing was minimal, and nearly all of the ice-algal produc-tion was exported into the water column, presumably sinking to the benthos inside the 50 m isobath. Thiswould explain the high 13C-enrichment of benthic organisms observed by Hobson et al. (2002). However,ice-algal primary production and the cumulative sinking export from the ice (0.11 mol C m�2) were negligiblecompared to the primary production and vertical flux (3.08 mol C m�2 at 50 m) associated with the pelagicbloom. It thus appears that open-water conditions favored vertical POC export, not because the early accu-mulation of diatoms led to a higher efficiency of export (e-ratio), but mostly because sinking fluxes scaled withoverall productivity.

3.11. Probable structure of the pelagic food web in the eastern North Water

We have assembled a synthesis of the food web structure in the eastern North Water (Fig. 9). The proposedlinkages are by no means definitive; the intent is to provide a plausible scenario that reconciles the analysis ofcarbon fluxes presented in the previous sections, with trophic ranking based on stable isotopes, stomach con-tents and the temporal co-incidence of peaks and troughs in the abundance of the different organisms. Thearrows in Fig. 9 depict important sources of carbon for a given consumer, but contain no information onthe actual magnitude of the flux. The latter would require estimates of population sizes and ingestion rates,which are available only for the dominant copepods and avian predators (Dovekie; Alle alle). The carbon syn-thesized by heterotrophs feeding on phytoplankton and protists can be consumed by avian and planktonicpredators. In most studies, the amount of mesozooplankton carbon transferred toward higher trophic levelsis difficult to assess given the lack of abundance data and ingestion rate estimates for carnivorous macroplank-ton and fish. In addition, the mobile nature of avian and large pelagic consumers makes it difficult to deter-mine how much of their carbon requirement is fulfilled in a given sampling region.

The bell-shaped time sequence of biomass estimates for the large copepods (Fig. 2G) suggests substantialpredation pressure during June. Energetic budgets and gut content analyses for dovekies allowed for a roughestimation of their carbon demand (Karnovsky and Hunt, 2002). Based on stable isotopes, the trophic level ofthese birds was 3.2 (Hobson et al., 2002; Fig. 7), which is consistent with the strong dominance in their gutcontents of female C. hyperboreus from May to July and a switch to Themisto libellula and cod larvae after-ward (Karnovsky and Hunt, 2002; Nina Karnovsky, unpublished data). By 21 July, C. hyperboreus ingested�5.2 mol C m�2, which corresponds to a biomass production of 1.7 mol C m�2 based on a GGE of 0.33. Theestimated carbon demand of birds up to that point was �0.034 mol C m�2 (estimated using data in Fig. 3 ofKarnovsky and Hunt, 2002), or 2% of the production of C. hyperboreus over the sampling grid.

This rough calculation implies that most of the biomass synthesized by copepods was available to pelagicpredators. Young-of-the-year (YOY) polar cod (Boreogadus saida) were very small in the North Water,


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suggesting that adult C. hyperboreus were too large to be ingested to a great extent. The trophic level of YOYwas relatively low (2.7), consistent with an omnivorous diet and the presence of large diatoms, abundant C.

hyperboreus nauplii and copepodites (CI and CII) and small adult copepods (O. similis and Oncaea borealis) intheir stomachs (Marc Ringuette, unpublished data). It is likely that the larger 1+ juveniles switched to largeadult calanoids, but this cannot be confirmed. However, the inferred trophic level of adult cod (3.6) clearlyconfirmed an ontogenic shift to carnivory on larger prey. On the basis of stable isotopes and previous studiesof stomach contents (Lowry and Frost, 1981), an important prey of adult cod is T. libellula (trophic

1

2

3

4

5

Large diatoms > 5 μm Phytoplankton < 5 μm

C. glacialis

C. hyperboreus

Small copepods

Protozoa

Themisto libellula

Polar Bear

Adult cod

Cod larvae

Oikopleura

Ringed sealBeluga, Narwal

Bowhead

E. glacialis

Glaucus gull

Other birds

Alle alle

MeanTrophic level

Fig. 9. Proposed structure of the pelagic food web in the North Water Polynya, based on carbon budgets, stable isotopes, analyses of gutcontents and the literature (see text). Numbers in the margin indicate the trophic level inferred from stable isotopes. The size of arrowsreflects the relative importance of a food item for a given consumer, not the magnitude of the carbon flux.


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level = 2.5). Themisto is a voracious predator, known to feed on a variety of copepods in open waters, includ-ing C. hyperboreus and C. glacialis (Auel and Werner, 2003). Themisto were not very abundant in vertical nettows, with only 0.11 individuals per m3, on average. Its inferred trophic level is consistent with a mixed diet ofphytoplankton (juvenile stages) and calanoid copepods. Other probable consumers of the large copepods areE. glacialis and mysids, although their abundance was negligible in the North Water. The importance of chae-tognaths and pteropods was not assessed.

Concerning larger animals, ringed seal was the most abundant pinniped in the North Water, occupying atrophic level of 5.5 that is consistent with a nearly exclusive diet of Polar cod for adults and a significant role ofT. libellula for juveniles (Holst et al., 2001). The trophic level of belugas was on par with that of seals, con-sistent with a diet of large carnivorous zooplankton and cod (Hobson et al., 2002). However, many belugasprobably migrate to adjacent bays in summer and probably feed extensively outside of the North Water(Koski et al., 2002). Several tagged belugas that overwinter in the North Water move south and west duringsummer to feed in seasonally open waters (Richard et al., 2001). Walruses, narwhals and bowhead whales pre-sumably follow a similar pattern (Richard et al., 1998), which suggests that marine mammals use the polynyaas a shelter against ice entrapment during winter months. The extent to which they feed in the polynya duringspring is not known. Finally, Polar bear (Ursus maritimus) had the highest trophic level, suggesting a quasi-exclusive diet of ringed seals (Hobson et al., 2002).

Unfortunately, the paucity of data on abundance and foraging (either from the NOW program or othersources) does not allow us to quantify carbon fluxes through marine mammals or determine whether theirfitness can be linked to the high local productivity. Some evidence exists for ringed seal, whose femalesreach sexual maturity earlier in Quanaaq (eastern North Water) than in the western North Water orthe Canadian Archipelago, where phytoplankton bloom much later in the season (Holst and Stirling,2002).

4. Summary and implications

Several comparisons indicate that the North Water is among the most productive ecosystems north of thepolar circle (e.g. Klein et al., 2002). This high productivity is supported by the substantial inventories of nitrateprior to the bloom and augmented by the moderate stirring effect of episodic storms during May (Tremblayet al., 2002b). Despite the high maximum biomass attained by the diatoms early in the season (up to19 lg chla l�1; Klein et al., 2002), mass sinking of intact cells did not occur. The large copepod C. hyperboreus

and to a lesser extent C. glacialis were able to exploit the thriving diatoms. Data from the North Water con-firmed that the annual recruitment of this dominant Arctic copepod is synchronized with diatom bloomsacross the Canadian Archipelago and the Barents and Greenland Seas (Ringuette et al., 2002). The successof C. hyperboreus is believed to be due to its spawning and overwintering strategies (Hirche, 1997); the femalesrelease their eggs throughout the winter and some eggs obviously ascend early enough to mature into CIcopepodites and exploit the bloom. Since this species has a multi-year life cycle, larger copepodites (CIVand CV) and females also ascend to feed during spring and, in fact, are responsible for most of the grazing.Thus, there is cause to believe that the vanishing multi-year ice and advancing dates of seasonal melt wouldnot directly threaten the base of the pelagic herbivorous food web.

Our synthesis demonstrates that most of the new and net primary production in the eastern North Waterwas consumed or retained in surface waters during the productive season. Vertical POC export was a modestcomponent of carbon fluxes due to the low sinking velocities of diatoms, intense grazing and the production ofDOC by phytoplankton. As the season continued and ice eventually formed, it is likely that the cumulativeexport of detritus and animal carcasses continued to increase, closing the gap with cumulative new production.By the end of summer, however, some of the accumulated DOC would have been advected out of the region.Although the ultimate fate of that DOC (e.g. respiration or vertical transport) is unknown, it implies a netexport of carbon from the North Water. Finally, our analysis shows that an increasingly early opening ofthe Artic Ocean is unlikely to increase the short-term efficiency of the particulate, biological CO2 pump,but may promote the productivity of the pelagic herbivorous food web and those apex predators that arenot affected adversely by the loss of ice.


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Acknowledgments

We thank the chief scientists, captains, and crews of the CCGS Pierre Esprit Radisson (Canadian CoastGuard) for invaluable support in the field. We thank three anonymous reviewers for constructive commentsand suggestions. The field work was funded by the Natural Sciences and Engineering Research Council(NSERC) of Canada and is a contribution to the NOW Research Network (International North Water Poly-nya Study), the scientific program of Quebec Ocean (strategic research group funded by the Fonds Quebecoisde la recherche sur la nature et les technologies) and the Canada Research Chair on the Response of ArcticMarine Ecosystems to Climate Warming. The final synthesis work was supported by the Canadian NetworkCenter of Excellence (NCE) ArcticNet.

Appendix 1

Net changes in the inventories of NO�3 and recycled N in the upper 50 and 150 m of the water column ± onestandard error on the slope (e.g. Fig. 1). See text for description of the different variables. The calculation per-iod started on 23 April for each time point. All values are expressed as mol C m�2

Layer 12 June 1 July 21 July

0–50 m DNO�3 �0.47 ± 0.10 �0.40 ± 0.09 �0.35 ± 0.11D½ureaþNHþ4 � 0.015 0.022 0.031

0–150 m DNO�3 �0.92 ± 0.12 �0.74 ± 0.16 �0.55 ± 0.21D½ureaþNHþ4 � 0.015 0.031 0.098

Appendix 2

Net changes in DIC (apparent and corrected for air-sea flux, DDICb), total POC, phytoplankton carbon(POCp) for the small and large size fractions and DOC in the upper 50 and 150 m of the water column.See text for description of the different variables. Values for POCp were obtained using a C:chl ratio of 50.The calculation period started on 23 April for each time point. All values are expressed as mol C m�2

Layer 12 June 1 July 21 July

0–50 m Apparent DDIC �3.51 ± 0.80 �4.27 ± 0.89 �4.09 ± 1.36DPOC 3.33 ± 0.31 0.61 ± 0.11 0.61 ± 0.11DPOCp < 5 lm 0.18 ± 0.06 0.08 ± 0.04 0.08 ± 0.04DPOCp > 5 lm 2.85 ± 0.37 0.09 ± 0.06 0.09 ± 0.06DDOC 1.64 ± 1.03 2.09 ± 1.31 2.62 ± 1.64

0–150 m Apparent DDIC �4.85 ± 0.67 �5.72 ± 0.78 �5.53 ± 1.52DDICb �9.44 ± 2.40 �10.31 ± 2.51 �10.12 ± 3.25DPOC 4.49 ± 0.48 0.45 ± 0.04 0.45 ± 0.04DPOCp < 5 lm 0.30 ± 0.10 0.11 ± 0.05 0.11 ± 0.05DPOCp > 5 lm 3.45 ± 0.54 0.12 ± 0.05 0.12 ± 0.05DDOC 1.68 ± 1.97 3.47 ± 1.43 6.87 ± 3.32

Appendix 3

Net, cumulative uptake of inorganic nitrogen (q), f-ratio, particulate primary production for total phyto-plankton (PP) and the small (PPS) and large (PPL) size fractions, dissolved primary production (PDOC), the


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c-ratio, new production (PNEW; calculated by multiplying the f-ratio by particulate or total primary produc-tion separately for each depth and station prior to temporal integration), total regenerated production (PREG;estimated by subtraction of PNEW from PT) and the estimated respiration (BR) and net production (NBP) ofbacteria in the upper 150 m. The calculation period started on 23 April for each time point. All values aregiven in mol C m�2, except nitrogen uptake rates (mol N m�2) and the f- and c-ratios (no unit)


qNHþ4 0.40 0.68 0.85qNO�3 0.89 1.06 1.18qDIN 1.29 1.74 2.03f-ratio 0.69 0.60 0.58PP 9.62 11.2 11.6PPS 1.78 2.05 2.27PPL 7.84 9.16 9.28PDOC 3.98 5.30 5.78c-ratio 0.69 0.62 0.58Particulate PNEW 7.15 7.81 7.88Total PNEW 10.2 11.4 11.6Total PREG 3.40 5.11 5.73NBP 0.60 1.25 1.61BR 1.79 3.74 4.83

Appendix 4

Experimental gut evacuation rates in dominant herbivores

Evacuation rate (min�1)

20 April–6 June 6 June–19 June 19 June –21 July

C. hyperboreus Female 0.015 0.034 0.018CV 0.013a 0.026 0.013

C. glacialis Female 0.029 0.052 0.062CV 0.020a 0.037 0.020

a Not determined, July value assumed.

Appendix 5

Significant regressions (p < 0.01) between gut content (ng chl ind�1) and chlorophyll a inventory (mg m�2)in the upper 50 m for the copepods that comprised most of the herbivorous zooplankton biomass. N is thenumber of experiments

n Equation r2

C. hyperboreus Female 15 0.71chl + 24.75 0.63CV 21 0.41chl � 5.39 0.76

C. glacialis Female 14 0.22chl + 15.4 0.38CV 22 0.15chl � 1.84 0.67


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Trophic structure and pathways of biogenic carbon flow in the eastern North Water Polynya

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