MARINE ECOLOGY PROGRESS SERIES Vol. 135: 247-258,1996 Published May 17 Mar Ecol Prog Ser

Nutrients, and microbial heterotrophy in the southeastern Chukchi Sea: Arctic summer nutrient depletion and heterotrophy

G. F. Cotal.*, L. R. pomeroy2, W. G. ~arrison~,E. P. Jones3, F. Peters4, W. M. Sheldon, ~r~,T. R. Weingartner5

'Graduate Program in Ecology, University of Tennessee, Knoxville, Tennessee 37996-1610, USA 21nstitute of Ecology, University of Georgia, Athens, Georgia 30602-2202, USA 3Bedford Institute of Oceanography, Dartmouth, Nova Scotia, Canada B2Y 4A2 41nstitut de Ciencies del Mar (CSIC), Passeig Joan de Borbo, sln, E-08039 Barcelona, Catalunya, Spain 'Institute of Marine Science. University of Alaska. Fairbanks. Alaska 99775. USA

ABSTRACT: In August 1993, we measured , chlorophyll a, bacterial secondary produc- tion, microb~alcommunity respiratory rate, bacterial abundance, dissolved free armno acids, nitrate, phosphate, silicate, and dissolved in the eastern Chukchi Sea. Our crulse track was mostly in loose pack ice exceed~ng50% ice cover, with heavier ice cover near 7 5" N. We sclmpled over the conti- nental shelf and slope, in deep water in the Canadian Basin, and over the Chukchi Cap. Primary pro- duction was highest over the upper continental slope, averaging 748 mg C m-' d-' In deep water and heavier ice cover in the Canadian Basin, primary productivity averaged 123 mg C m-' d-l. However. microbial community respiratory rates averaged 840 mg C m ' d-l over the upper slope and 860 mg C m-2 d.' in the Canadian Basin. Nitrate was virtually depleted In the .upper m~xedlayer, suggesting some nutrient limitation and dependence on regenerated ammonium in late summer. This is supported by f-ratios ranging from 0.05 to 0.38. Estimates of annual prlmary production of organlc carbon, both from our 'v and 13<1assimilation measurements and from the supersaturation of dissolved oxygen in the upper mixed layer at all stations, suggest that significant primary production occurs well beyond the continental shelves out into the so-called perennial pack ice. Respiratory activity in the upper mixed layer exceeded primary productivity at the deep-water stations, as it often does in summer olig- otrophic conditions at lower latitudes. These observations suggest that rates of both autotrophic and heterotrophic biological activity in the upper mixed layer of the deep waters of the Arctic Ocean may be considerably higher than suspected and should be incorporated lnto models of polar proccsscs.

KEY WORDS: Arctic . Primary production - Microbial heterotrophy . Respiration Oxygen . Nutrients

INTRODUCTION have little influence on the concentrations of oxygen, phosphate, nitrate, and silicate in the water beyond the Previous investigations in the central basins of the continental shelves. Because direct measurements of Arctic Ocean, especially those done at ice camps (Eng- primary production have been limited almost entirely lish 1961), have tended to suggest very low rates of to the continental margins, most estimates of primary photosynthesis in the water column, leading some production for the Arctic basin as a whole have been investigators to conclude that biological processes indirect estimates of new production (e.g. Macdonald et al. 1987, Bjork 1990), sometimes with the stated

Ot In sltu 'Present address: Center for Coastal Physical Oceanography, aSSumptlonthat regeneration nutrients in Old Dominion Univers~ty,Norfolk, Virginia 23529, USA. water is insignificant (Jones & Anderson 1986). Our E-mail: [email protected] data suggest otherwise, and we show that microbial

C Inter-Research 1996 Resale of fullarticle not perrn~tted Mar Ecol Prog Ser 135: 247-258, 1996

activity, both autotrophlc and heterotrophic, must be were collected with 10 l go-flo Niskin bottles for nutri- taken into account for a full explanation of seasonal ent concentrations [NO3, Si(OH)4and HPO,], chloro- changes in the vertical distribution of oxygen, nitrate, phyll a (chl a),particulate organic carbon and nitrogen, and phosphate in the upper mixed layer and the upper and a varlety of experiments Optical depths were esti- halocline. E~enless consideration has been given to mated with the Secchi disk and the upper 7 depths cor- microbial processes in the central basins of the Arctic responded to 100, 50, 30, 15, 5, 1, and 0.1 % of surface Ocean, although extensive investigations of microbial irradiance. The 0.1 'Yo light level averaged 37 + 13 m processes at high latitudes in Baffin Bay and the Cana- (n = 12) and ranged from 25 to 61 m throughout the dian archipelago have demonstrated their significance cruise. Samples from nonexperimental stations were (Harrison et al. 1985, 1987, Harrison 1986, Platt et al. collected at standard water depths. 1987). Inorganic nutrients. Duplicate unfiltered seawater The Arctic Ocean is a varied environment with samples taken for nutrient analyses were collected in definable subregions (e.g.Lyakhin & Rusanov 1980). A well-rinsed, acid-washed 30 m1 plastic bottles. Sam- general circulation and throughput of the upper water ples were frozen immediately and kept frozen until masses 1s now well recognized, but its time scale, while they were analyzed at the Bedford Institute of still controversial, is certainly long enough so that dis- Oceanography, about 3 mo later, with an AutoAna- tinctive physical, chemical, and biological processes lyzer uslng standard techniques (Pars0n.s et al. 1984). may result from regional and seasonal differences in Replicate analyses almost always agreed to within 5 %, ice cover, wind fields, and water movement. The and many agreed to within 1 %. Chukchi Sea varies from moderate, and in part sea- Chlorophyll. Chl a was determined fluorometrically sonal, ice cover in the south to extensive, multi-year ice (Holm-Hansen et al. 1965) by filtering 100 to 250 m1 toward the North Pole. The Anadyr Current brings seawater samples through 25 mm Whatman GF/F glass nutrient-rich water into the Chukchi Sea through the fiber filters. The filters were placed in vials on ice, soni- Bering Strait, making the southwestern Chukchi Sea cated in 90% acetone for 10 min, extracted for 20 min one of the most biologically productive regions in a more, and then analyzed immediately. Extracted fluo- largely oligotrophic body of water (McRoy 1993). Infor- rescence was measured before and after acidification mation on the Chukchi Sea north of the ice-free coastal (5 % HC1) with a Turner Designs model 10 fluorometer, region has been relatively scant. In August 1993, the calibrated with commercially purified chl a (Sigma). ANWAP (Arctic Nuclear Waste Assessment Program) Primary production and nutrient uptake. Primary program provided an opportunity to collect a range of productivity was measured by "'C (carbon) fixation biological and chemical data between the Alaskan with simulated in situ(SK) incubations. Isotope stocks shelf and 75" 22' N, aboard the icebreaker U.S. Coast were prepared according to the recommendations of Guard 'Polar Star'. We encountered late summer con- Fitzwater et al. (1982). Our SIS incubator had neutral ditions and measured primary productivity, bacterial density and/or blue plastic filters (CineMill) to simulate secondary productivity, inorganic nutrients, commu- in situirradiance spectra vertically over the euphotic nity respiratory rates, and dissolved oxygen. zone; it was cooled with flowing surface seawater. Two sets of samples from each of the 7 optical depths were placed in 280 m.1. polycarbonate bottles, inoculated METHODS with 370 kBq I4C-NaHC03,and one set was incubated for 6 to 8 h (morning to afternoon) and the other set for Sampling procedures. Nutrient and oxygen concen- 22 to 26 h (morning to morning). Total activity added trations were determined throughout the water col- and particulate adsorption were measured at time umn at 45 to 55 stations, while phytoplankton chloro- equals zero in parallel samples. Particulate material phyll biomass was measured only in the upper 150 m at was harvested on 25 mm Whatman GF/F filters and most stations. Carbon fixation, nitrogen uptake and rinsed with 5 to 10 m1 of 0.01 N HC1 in filtered seawa- bacterial productivity were measured in surface ter to remove inorganic carbon. Radioactivity was waters (<75 m) at selected morning stations. Note that assayed by liquid scintillation counting and corrected duplicate points on Fig 1 (e.g. El and E31 correspond for particulate adsorption at zero time, background, to sequential morning casts at the same nominal and counting efficiency. Short-term (6 to 8 h) values for alphanumeric station. Routine sampling at morning primary production were 1.75 times higher, on aver- productiv~tystations included continuous vertical pro- age, than day-long incubations. Water temperature in files of temperature, salinity, and fluorescence with a the incubator and incident photosynthetically active Sea-Cat CTD (conductivity, temperature, depth) pro- radiation (lo PAR = 400 to 700 nm) above the incubator filer, fluorometer, and Secchi disk followed by a second were measured continuously with a Licor model 1000- cast with a SBE-911 CTD and rosette. Discrete samples 15 thermistor and Licor model SA-190 cosine collector, Cota et al.. Arctic primary production, nutnent depletion and heterotrophy 249

respectively. Both variables were recorded at 5 min Three such subsamples were collected from each intervals with a Licor model LI-1000 data logger Niskin sampler. The vials were placed in a freezer and Parallel SIS Incubations with the same morning \yere returned without thawing to our home laboratory water samples were used in experiments to measure for analysis by high performance liquid chromatogra- the simultaneous uptake rates of "N-NO3, lSN-NFI,, phy following the general precolumn derivatization and '.'C-HCO.,. Heavy isotope-enriched (95 to 9Y':l;) procedure of Lindroth & Mopper (1978) and Mopper & solutions of H1*O3, K%03 or ("'NH4)2SC?,, were Lindroth (1982). We followed the specific procedures added to 535 m1 polycarbonate bottles at concentra- of Henrichs & Williams (1985), except that samples tions of -0.05 to 0.1 pM (NO3, NH,) and -0.2 mM (CO,) were thawed at 4°C. 2 m1 subsamples were deriva- and were incubated for 6 to 8 h. Samples were then fil- tized, and 300 1-11 were injected. Derivatized primary tered onto precombusted Whatman GF/F glass fiber amino acids were separated in a 250 X 4.6 mm car- filters and dried at 60% C for later analyses of "N and tridge-style column (Alltech) packed with Spherisorb ''C enrichment of particles and for concentrations of ODS-l, 5 pm (Phase Separation) and detected using a particulate organic carbon (POC) and particulate Kratos FS970 Spectrofluoromonitor. The amino acids organic nitrogen (PON) using a Tracermass Stable Iso- quantified were: aspartic acid, glutamic acid, serine, tope Analyzer (Europa Scientific). Nitrogen and car- histidine + threonine + glycine (CO-eluted),alanine, bon uptake rates were determined using equations tyrosine, arginine, methionine, valine, phenylalanine, described in Dugdale & Goering (1967) for "N and isoleucine, leucine, and lysine. Hama et al. (1983) for "C. Bacterial secondary production. Because samples f-ratios. Two approaches were used to estimate f- were being collected by other investigators to measure ratios. In the first, uptake of "NO, was converted to the naturally occurring tritium during the ANWAP cruise, Redfield ratio carbon equivalent and compared with the use of tracer concentrations of tritiated compounds primary production measurements made at the same was not a compatible activity. Instead, we estimated time. In the second, an assumed ammonium concentra- bacterial secondary production from the uptake of ''C- tion of 0.1 prY1 was used to compute NO3 uptake/N03 + l-leucine. On a previous cruise we had compared NH, uptake Results from the 2 approaches are sub- uptake of ',C- and 3H-leucine and found no significant stantially in agreement. difference, except that the sensitivity was lower with Community respiratory rates. Multiple 125 m1 Win- the carbon label because of its lower specific activity kler bottles were filled from the bottom and over- (data not shown). Triplicate sets of 10 m1 seawater sam- flowed for more than 1 volume of the bottle. Six bottles ples were pulsed with 10 nM I4C-leucine (1.1 kBq) for were fixed for Winkler initially and additional periods of 1, 3, and 6 h at sea temperature in a water sets of 6 bottles were placed immediately in dark bath, and protein was extracted with 5 'Yotrichloracetic refrigerators kept at sea temperature (usually -1.4"C). acid at 95OC for 30 mm. Precipitated protein was col- Temperature in the refrigerators was monitored con- lected on a 0.2 pm cellulose butyrate membrane filter, tinuously with electronic max-min thermometers. Sets and the filter was dried and stored in a desiccator for of bottles were fixed and titrated at approximately 24 later liquid scintillation counting. and 48 h intervals. Titration was performed with a Leucine uptake rates were converted to bacterial Mettler DL-21 titrator, using a potentiometric end carbon production according to Simon & Azam (1989), point. This 3-point analysis permitted us to inspect the correcting for internal pool dilution by a factor of 2. data for departures from linearity which might result While, with one exception, external leucine pool con- from the growth or death of microbial populations dur- centrations were

Table 1. Total dissolved free amino acids (XDFAA) and leucine concentration, uptake and turnover at selected stations in the Chukchi Sea, August 1993

Stn Latitude Longitude Total Sample tDFAA Leucine Leucine Leucine N W depth depth (nM) concentration uptake turnover (m) (m) (nM) (PMh-') (h1

E12 72O29.9' 159O48.4' 40 4 69 2.2 5.36 410 E12 16 173 5.4 8.43 65 1 E6 73'05.3' 158O45.1' 1450 6 34 11 2.04 539 E6 2 1 5 2 2 1 1.84 1141 E6 4 5 33 17 1.44 1181 E 5 73" 3.2.4' 158" 28.4' 1880 5 88 14 6.77 207 E5 19 1473 192.5 4.05 42778 G6 71°24.3' 157'28.1' 113 10 34 1.4 1.01 1386 G6 30 191 6.3 1.05 600 G6 50 147 2.8 0.92 305 B1 72" 00.4' 1.4 36 1.3 6.68 195 B1 14 135 3.7 5.19 713 B1 30 29 0.6 5.70 105

RESULTS SSE across the continental shelf to 72ON. The G section runs NE along the inner continental shelf past Point The E section is the most detailed of the ANWAP Barrow, Alaska, and down the Barrow Canyon to a cruise, running NNE from a point near 72.5'N on the depth of 1660 m. continental shelf north of Icy Cape, across the conti- Beneath the melting pack ice, a surface mixed layer nental slope to a depth exceeding 3800 m in the Cana- of water of reduced salinity was 15 to 20 m in thick- dian Basin. (Fig. l). Most of this section was in 50% or ness, followed by the halocline-nutricline, extending greater cover of mixed first-year and multi-year ice. down to 150 m (Fig. 2). Nitrate was nearly depleted in The less detailed D section then runs m7 across the the upper 10 to 20 m at most stations over the conti- Chukchi Cap to 75.5ON in depths of 1000 to 2000 m. nental shelf and varied from 10.1 to 0.4 pM in the Percent ice cover and ice floe thickness increased upper 20 to 25 m offshore. Nitrate exceeded 0.5 pM in northward along this section, with multi-year ice near surface waters only at Stns E5 and E6. increasing in relative abundance to the north. The C section runs SW up the continental slope to the shelf break, while the B section, partly in open water, runs Chlorophyll and photosynthesis

There was always a subsurface chlorophyll maxi- mum which exceeded 1 mg m-3 over the continental shelf, dropping below 1 approximately at the shelf break. Over the continental slope, the chlorophyll maximum was at the top of the cold halocline at a depth of 30 to 40 m, with maximum concentrations ranging from 1 m.g m-"ear the shelf break to 0.1 mg m-" over deep water in the Canadian Basin (Figs. 1 & 2). Stations over the upper continental slope having high chlorophyll or high photosynthesis were C6, E5 and G13; these same stations also showed high nitrate concentrations relatively near the surface. The general distributions of chlorophyll and nitrate suggest a post-

1 TO 'W 160 'W 150 "W bloom condition, but with some kind of vertical advec- tion having taken place recently on the upper conti- Longitude nental slope near Stns E5 and E6. Mean profiles through the euphotic zone showed that Fig. 1. Cruise track for U.S. Coast Guard 'Polar Star' from 29 July to 15 August 1993. Sampling sequence was E, D, C, B, G. the maxima for daily (22 to 26 h incubations) primary See Tables 1 and 2 for experimental station locations and depths productivity and biomass-specif~cproductivity were Cota et al.:Arctic primary production, nutnent depletion and heterotrophy 25 1

Fig. 2. (a) Temperature, (b) salinity, (c) nitrate, (d) dis- solved oxygen, (e) chloro- phyll, and (f)primary produc- tivity (based on 22 to 26 h in- cubation~)In the upper water colun~nalong the E section from the outer continental shelf (40m) to the Canadian Basin (>3800m). The approxi- mate depth of 10OCKtsaturation for dissolved oxygen is shown by the broken line at 385 PM and lncludes a small bolus of water centered around 85 m at Stn E5 D~stance(km) Dislance(km) above the chlorophyll biomass maximum (Fig. 3), how- ever there were regional differences. At 4 stations over Chlorophyll (rng Chl the continental slope (c200 m), maximum photosyn- thetic rates usually occurred well above the chlorophyll maximum. A subsurface photosynthetic maximum was found between 4 and 22 m, while the chlorophyll maxi- mum was between 31 and 58 m, usually at light intensi- ties of 0.1 to 0.001 % Io. The photosynthetic maximum was just above the chlorophyll maximum, and the top of the nutricline was observed over the upper slope. At 2 of 3 stations over the lower slope, with total depths >2000 m, the photosynthetic maximum was below the chlorophyllmaxirnum, and at 1 of the 3 it was above the chlorophyll maximum. In all 3, the photosynthetic max- imum was in the top of the nutricline.

Fiq. 3 Vertical distributions of chl a, primary production and biomass-specific production during August, 1993 at expen- mental stations (n = 12) in the Chukchi Sea. Production esti- mates were based on 22 to 26 h incubations. Values shown Primary Production P (rng C h-') are means r 1 SE Specific Production pB [rng C (rng ~hl).'h-'] Mar Ecol Prog Ser 135: 247-258, 1996

Table 2. Euphotic zone integrations of primary production (6 to 8 h incubations), microbial community respiration (comm. resp.) and bacterial (bact.) production, and standing stocks of particulate organic carbon [POC] in the Chukchi Sea. P/R is "C produc- tion versus respiration. New production is based on '^C and lSN;f-ratio assumes an ammonium concentration of 0.1 vM. Euphotic depth = 0.1 % lo

Stn Latitude Longitude Total Primary prod. Comm. resp. Euphotic P/R Bact. prod. POC % New f-ratio 1\' W depth (mg C m-' d-I) (mg C m-* depth (mg C m-' (g C prod. (m) ^c IT d-I) (ml d-I) m2)

Rates of vertically integrated primary production in bon (Simon & Azam 1989) for shelf waters was 29.3  the euphotic zone were not significantly correlated 4.8 ng C 1'h' (mean  1 SE; n = 14); for upper slope with integrated concentrations of inorganic nutrients samples it was 9,7  2.3; for stations >2000 m it was [No3, Si(OHL or PO.,] or cumulative incident irradi- 6.1  1.6. Bacterial production did not necessarily ance over the incubation periods. By contrast, areal decrease with depth within the mixed layer, but sam- chlorophyll biomass explained almost half of the vari- ples taken below 50 m had a mean of 1.8  0.8 (n = 3). ance in '"C primary productivity, but only 21 % of the Since our assumption that uptake was saturated by variability in the "C values. Nevertheless, there was 10 nM leucine may not be correct, the above rates may generally good agreement between our estimates of underestimate bacterial secondary production. At '"C and 13C productivity (Table 2). Stn E7 on the outer continental shelf we ran 1 enrich- The integrated mean photosynthetic rate over the ment experiment of the kind reported by Pomeroy et cruise track was 295  81 mg C m-2 d-' (mean  1 SE; al. (1995). No limiting substance for bacterial produc- n = 12) based on 22 to 26 h incubations. However, tion and respiration, organic or inorganic, was identi- regional differences in photosynthesis along the cruise fied. Likewise, no stimulation of primary production track were marked, especially in the deeper waters, was detected for any treatment in parallel enrichment Photosynthesis over the continental shelf was 102 to experiments with surface phytoplankton populations 486 mg C m-' d"' (mean = 336; n = 41, but photosynthe- held at 100% incident irradiance for 48 h. sis was highest over the upper continental slope, in Microbial community respiratory rates in the upper water depths from 200 to 2000 m, ranging from 45 to mixed layer did not vary systematically with distance 950 mg C m2dl (mean = 394; n = 5). Photosynthesis in from shore or total depth (Table 2). Respiratory rates the Canadian Basin at depths >2000 m, and with were never higher in the chlorophyll maximum than in >50% ice cover, ranged from 47 to 120 mg C m"* d-I the water above it. The mean rate for the upper 50 m (mean = 74; n = 3). Note primary production values in over the cruise track was 576  151 mg C m" d"' Table 2 are short-term not daily values. Microbial community respiratory rates were not higher at the stations near the shelf break that had the highest photosynthetic rates. Rates over the shelf and upper Heterotrophic activity slope were almost always measurable, while rates in the upper 50 m at stations having water depths Rates of bacterial assimilation of '"C-leucine into >2000 m in the Canadian Basin and over the Chukchi protein were >3 pM leucine 1'h-I over the continental Cap (in relatively thick ice) sometimes were below our shelf generally, with rates up to 26 pM leucine 1" h" at limit of resolution, even in the upper mixed layer and Stn E8 (Table 1).Rates then decreased beyond E5 and halocline. The limit of resolution depends on the vari- were around 1 pM leucine I"' h" in the Canadian ance within each set of replicate samples, and is Basin stations. The mean production of bacterial car- approximately 0.03 pM 0, h-' or 7 mg C m-3 d-' (Pom- Cota et al.: Arctic primary production, nutrient depletion and heterotrophy 253

eroy et al. 1994). When photosynthesis and respiratory usually measurable in near surface waters, is well rates are integrated to the depth of 0.1% of surface below the saturation concentration for uptake by large light intensity, P/R (I4C production vs respiration) is phytoplankton (Smith & Harrison 1991). At most sta- seen to be

Table 3. Annual photosynthesis (g C m2) in the Chukchi Sea nutrient availability and species succession seasonally. estimated from excess dissolved oxygen in August 1993. Oxy- A pronounced phytoplankton bloom earlier in the sea- gen above saturat~onis converted, mole:rnole, to equivalent son with higher daily photosynthetic rates may be organic carbon more typical. For example, recent evidence indicates that Phaeocystis can have elevated photosynthetic El, D1, Stns E2 Stns D3 rates and be a major early producer elsewhere in the Excess oxygen 18 Arctic (Smith et al. 1991, Cota et al. 1994). Additional Flux to atmosphere 9 contributions by 11.lelosira and other ice algae also Summer respiration 4 would increase annual primary productivity. Much less Total estimated photosynthesis 31 is known about Melosira and ice algae in the pack ice. While our estimates based on excess oxygen and nutri- ent depletion are very crude and probably minimal, summer 1993, the excess dissolved oxygen in the they suggest that there is a band of significant primary upper 30 m of the Canadian Basin is equivalent to production extending well beyond the continental annual carbon fixation of 3.8 g C m-*. Corrected for shelves into the perennial pack ice over deep waters, losses to the atmosphere (Penta & Walsh 1995), it cor- at least 300 km from the Alaskan shore. Photoauto- responds to annual photosynthetic carbon fixation of trophic activities must diminish considerably where 27 to 36 g C m-' Adding 30 d of heterotrophic respira- multi-year ice in excess of 2 m in thickness normally tion (assumed to be 50% of community respiration), covers most of the water's surface, because light levels the annual primary production is 31 to 40 g C m-' will be below compensation intensities for net primary (Table 3). In these calculations we assumed the photo- production. synthetic quotient (PQ) to be 1.2. The estimate that However, the idea that the Arctic Ocean is a biologi- includes only supersaturation and diffusive losses cal desert because of its 'permanent' ice cover can be should be a minimal estimate of new production. very misleading. The ice cover is rarely continuous New production can also be estimated from the even in winter, and there can be significant amounts of observed late summer nutrient depletion. We assume open water anywhere in the pack ice zone during sum- that winter equilibrium concentrations of nitrate are mer. Almost a decade of passive-microwave observa- about 10 pM similar to the values at 50 m. Nitrate tions suggests that by August ice cover concentrations levels in the upper 20 m averaged

Heterotrophic processes land, situated in very thick ice on the outer continental

shelf north of Ellef Rlngness Island, POC was 1.2 1-19 1-I Est~matingannual community respiration in the Arc- in June and 8.5 in late August (Hargrave et al. 1989). tic Ocean IS problematic The relatlve uniformity of Thesc values can be compared with a mean of 117 ? commun~ty iesp~ratoly rates over our entire cruise 4 pg 1-' (n = 19) from our basln stations El and D3, and track and the lack of coherence of community respira- 270 ? 14 (n = 40) for our shelf stations E8,E12, B1, and tion 1~1thphotosynthetic rates suggest a large compo- B7. At the Canadian Ice Island in June 1988 (pre- nent of bacterial respiration Numbers of bacterla in thaw), bacterial secondary production in the upper the watei also showed llttle variation, not only during 50 m, measured by the uptake of 3H-leucine, was our 1993 crulse but at othel sites and seasons as well 0.2 ng C 1-' d-' (Pomeroy et a1 1990), compared with a

(l e Harnson et a1 1987, Pomeroy et a1 1990) mean of 120 _+ 3.9 (n = 5) for our statlons El and D3. Although microbial community respiration occurs We do not have the necessary sensitivity to measure throughout the year at all depths, and \v111 be little short-term respiratory rates in the upper mixed layer affected by the small seasonal differences In tempera- beneath multi-year ice. From the chlorofluoromethane ture, ~t may well be affected by seasonal and reglonal dlsti-ibution at the CESAR slte, Wallace et al. (1987) dlffe~encesin the standing stocks of phytoplankton, estimated the apparent oxygen utilization (AOU)in the whlch are one component of community ~espiiation cold halocline, 55 to 155 m, to be 0.016 to 0.042 PM 0, and are also the primary source of organlc carbon fo~ S-', or 4 8 to 12.7 g C m-2 yr-l. On the basis of the heterotrophic respiration Standlng stocks of labile usual low estimate of prlmary production in the central organlc matter must decrease during the long winter Arctic basins, they attribute all of the organic supply to season Th~smay have a p~onouncedeffect on bacter- the continental shelves. However, our revised esti- lal respiration and product~on,~f the bacterial commu- mates would permit most of their AOU estimate to nity has dlfflculty utilizing very low substrate concen- originate in the immediate water column during sum- tratlons at the low temperature (W~ebeet a1 1992) mer, although ~tseems reasonable to assume that some If, however, we extrapolate the microbial coinmunity organlc matter or~glnatesboth in the local water col- respiratory rate observed In August over 7 wintei umn and on the shelves. months, ~twoultl be equivalent to m~crobialutilization Our results show that the upper 50 m of the Chukchi of 12 g C mr2 for the uppei 50 m This ~mpl~esthat dis- Sea are b~olog~callydynamic, not only on the continen- solved oxygen In the upper m~xedlayer will be dbout tal shelves but In the waters over the continental slope 90 %, saturated In early spring, poss~blya blt lower than and in the Canadian Basin, at least up to the region of expected from observations (Engl~sh1961 Lyakhln & heavy multi-year ice cover. The physically dynamic Rusanov 1983 data f~omSverdrup as re-examined In events along the continental slope are not only those of Penta & Walsh 1995) At a 7 1 rat10 of C N, th~s1s equlv- seasonal melting and retreat of the ice pack but also alent to iemineralizat~onof 5 6 PM N 1 ', which 1s ap- vertical advect~onof nutrients by currents and edge proximately the wlnter-spring nltrate concentrat~onin waves (Johnson 1989, Aagaard & Roach 1990). The the uppel halocline at the T-3 and CESAR sites (Mac- effects of these klnds of events are seen in our data donald et a1 1987) That est~matedoes not Include ies- from the upper continental slope, where act~vevertical plratlon of organisms large and active enough to es- water movement had recently occurred or was occur- cape a Niskin sdmplei, such as many copepods ring down to 150 to 200 in (Fig 2). This was also the Nevertheless ~tIS probably dn overestimate which may region of highest biological activity at the time of our servc to put an upper limlt on the extent to which b~o- August crulse. Much of the primary production is, loglcal act~vitymay alter concentrations of dissolved however, being utilized rapidly in the heterotrophic oxygen, nitrate, and phosphate In the upper 50 m food web. At the stations over the upper continental slope photosynthesis s~gniflcantlyexceeded commu- nity respiration in August, but at all other stations, both Rate variations over time and space on the continental shelf and In the deep, ollgoti-ophic waters of the Canadian Basin, microbial community Data from the CESAR site over the Alpha R~dgesug- respiration usually exceeded primary production gest that metabolic rates of llvlng organisms and (Table 2). Photosynthesis probably exceeded commu- staildlng stocks of organlc materials In the water col- nity respiration early In the season, when nitrate umn continue to decrease at greater distances from the exceeds saturation for large phytoplankters. This dif- fers frClm nr;rnz,r>r >-rrrrl.*r+;-- --* --I-- continental marqlns FOI example POC In the 1lppc.r yAA.,Au.l y.VUUCLL~I~ LLWL WLLLY quulILlLa- 50 m at the CESAR site was 13 8 pg 1-' (Gordon & tively, but also qualitatively (Andersen 1988, Walsh et Cranford 1985) However, not all Arctlc continental al. 1989), wlth the major producers during blooms shelves are hlghly pioductive At the Canadian Ice Is- being larger diatoms or Phaeocystisthat tend to aggre- Mar Ecol Prog Ser 135: 247-258, 1996

gate and sink, at least into the pycnocline, before rates on the order of 1 to 5 g C m-' As we have noted. being utilized (Smetacek & Pollehne 1986, Smith et al. English's (1961) dissolved oxygen data yield an inde- 1991). Later in th.e season, the dominant primary pro- pendent estimate of annual primary production of at ducers are mostly < 10 pm, their consumers are l~kelyto least 13 g C m'? Most oxygen-based estimates of be protozoans, whose feces and other particulate prod- annual primary production in the Arctic suggest values ucts of the heterotrophic food web sink slowly, if at all, of 13 to 38 g C m-2 are more reasonable (Pomeroy and will not penetrate the density barrier presented by 1996). According to the models of Wallace et a1 (1987), the halocline. Organic materials accumulate, and their the minimal approximation of AOU for the upper 55 m regeneration produces the nutrient maximum-oxygen should be 4 g C m-* for 4 summer months, an amount minimum. In late summer, most of the photosynthesis which may be supported by local primary production. is probably dependent upon ammonium. This hypoth- This diminishes considerably the amount of labile esis is supported by our estimatcs of the f-ratio of 0.05 organic carhon that must be transported laterally over to 0.38 (Table 2). It also is reflected in English's (1961) the course of decades of time. Indeed, the errors dissolved oxygen data. Oxygen begins to rise above around these estimates are so large, they do not elimi- saturation in July but reaches a plateau on or about nate the possibility that the central polar basin pro- mid-August, remaining above saturation until October. duces enough organic carbon to balance AOU This would happen if new production occurred largely (Pomeroy 1996). We reiterate the statement of Subba during the first 20 to 30 d of the productive season. Rao & Platt (1984) that more data are needed from the The recognition of higher biological activity than offshorc regions of the Arctic Ocean. Seasonal dynam- previously assumed in the upper mlxed layer of the ICS of biological communities and ice cover are critical Arctic Ocean does not eliminate the possibility of lat- to better understand the productivity of polar regions. eral transport of organic matter from the continental shelves during winter. Walsh et al. (1989) postulate that organic matter sinks to the bottom of continental Acknowledgements. Our research was supported by grants DPP 9122887 (G.F.C.) and DPP 9223007 (L.R.P.)horn the U.S. shelves in late spring-early summer at the time of the National Science Foundation and grant N00014-93-1-0976 phytoplankton bloom and is then transported into the (G.F.C. and L.R.P.) from the U.S. Office of Naval Research. basin along isopycnals in wlnter by the production and Additional support was provided by the Canadian Depart- transport of cold brine. While observing these phe- ment of Fishenes and Oceans. We thank L. Cooper, Chief Sci- entist, and J. Crebmeier for their support and cooperation nomena has proven to be elusive (Aagaard & Roach during the cruise. Amino acid analyses were done by Joan 1990), there is indirect evidence that shelf-derived Sheldon. brines contribute to the maintenance of the halocline. The cold brine is transported along isopycnals for probably 20 to 40 yr into the central basin (Jones & LITERATURE CITED Anderson 1986, Wallace et al. 1987). Wallace et al. 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This article was presented by S. Y Newel1 (Senior Editorial Manuscript first received: June 12, 1995 Advisor], Sapelo Island, Georgia, USA Revised version accepted: October 30, 1995