Marine Chemistry, 35 ( 1991 ) 245-257Elsevier Science Publishers B.V., Amsterdam

245

Nutrient distributions and new production inpolar regions: parallels and contrasts between the

Arctic and Antarctic

Walker O. Smith, Jr.BotanyDepartmentand Graduate Program in Ecology. University ofTennessee, Knoxville,

TN 37996, USA

(Received I September 1990; accepted 20 January 1991 )

ABSTRACT

Smith, W.O., Jr., 1991. Nutrient distributions and new production in polar regions: parallels andcontrasts between the Arctic and Antarctic. Mar. Chern.. 35: 245-257.

Polar regions arc poorly understood components of global biogeochemical cycles. This paper dis­cusses the influences of nitrate and ammonium concentrations on nitrate uptake (and hence newproduction), particularly with regard to data collected within marginal ice zones in the Arctic andAntarctic. Subsurface ammonium maxima in waters over 150 m are frequently encountered in theArctic and occasionally in the Antarctic. Such maxima result from the heterotrophic rernineralizationof organic matter, and because stratified environments occur more frequently in the Arctic, signifi­cant concentrations of ammonium accumulate as a result of lower diffusive losses. Causal agents(bacteria vs. zooplankton) may also be different in the Arctic from those in the Antarctic. Elevatedammonium concentrations significantly reduce nitrate uptake, and it is suggested that this nutrientinteraction may playa significant role in controlling new production, particularly in open water re­gions. The new production of the Southern Ocean is estimated, and it is suggested that the productionand flux from the surface layer is significant relative to the world's oceans.

INTRODUCTION

Most models of coupled atmospheric-oceanic processes suggest that theocean plays a significant role in controlling atmospheric carbon dioxide con­centrations and hence global climate. In general, the Arctic is predicted to bea major sink of CO 2, whereas the role ofthe Southern Ocean as a major sourceor sink is unclear (Peng et al., 1987; Sarmiento et al., 1988). The rates of newproduction and vertical flux of organic matter to depth are critical variablesaffecting the global oceanic carbon budget, but only limited measurements ofthese processes have been made in polar regions, especially on the space andtime scales necessary to understand the importance of polar systems to theglobal carbon cycle.

0304-4203/91/$03.50 © 1991 Elsevier Science Publishers B.V. All rights reserved.

246 W.O. SMITH, JR.

Inorganic carbon is removed from the ocean's surface via incorporationinto organic matter by the process of photosynthesis and subsequent verticalflux of organic matter (particulate and dissolved) to depth. In general, nu­trients (and in particular, nitrogen) often limit photosynthesis and primaryproductivity in the ocean, although this is not necessarily true for polar re­gions, where irradiance often limits phytoplankton growth (Smith and Saks­haug, 1990). Eppley and Peterson (1979) defined 'new production' as theproduction based on nitrate and subsequently available for export from thesystem when at steady state. Hence, those regions with large amounts of newproduction can provide the largest vertical flux of organic matter to depth.Eppley and Peterson (1979) also estimated global new production, but spe­cifically excluded polar regions from their estimate.

Marginal ice zones have been intensively studied in the past decade, and ithas been shown clearly that they are sites ofelevated rates of primary produc­tion and particulate accumulation (e.g, Alexander and Niebauer, 1981; Smithand Nelson, 1985, 1990; Nelson et al., 1987, 1989). Because phytoplanktonblooms are formed primarily as a function of water column stratification (andtherefore input of low-density meltwater from the receding ice; Smith andNelson, 1986), they probably are of greater importance (relative to the totalregional production) in the Antarctic, where approximately 16X 106 km2

year- I are uncovered by the seasonal retreat of ice (Zwally et al., 1983). Phy­toplankton growth within ice edges is also largely dependent on nitrate, withmeanJratios (the ratio of nitrate-based production to that based on all nitro­gen sources) averaging 0.62 (Table 6 in Smith and Nelson, 1990). In con­trast, new production in regions not influenced by ice appears to be less (meanfratio 0.38; Smith and Nelson, 1990), and some areas have only negligiblenew production, with most growth being dependent on ammonium (e.g.Ronner et al., 1983; Koike et a1., 1986). It is unclear if the difference betweenmarginal ice zones and the open ocean is real or an artefact attributable tosampling bias; however, it is clear that such a relationship would have signif­icant effects on the region's potential to act as a sink (or a source) in theglobal CO2 budget.

This paper is intended to synthesize the data on nitrogen (nitrate and am­monium) distributions and new production in polar regions and to provideinsight into how rates of production might be regulated in situ. It is not in­tended to be an exhaustive summation of the published literature on phyto­plankton growth and nitrogen uptake in polar regions (see Dugdale and Wilk­erson, 1989;Smith and Sakshaug, 1990), but it is hoped that it will emphasizesome important gaps in our present knowledge of factors influencing polarnitrogen cycles.

NEW PRODUCTION IN POLAR REGIONS 247

RESULTS AND DISCUSSION

Nitrateand ammonium distributions in polar regions

The seasonal distribution of nitrate in polar regions is, in principle, the in­verse of that of phytoplankton biomass (i.e. a unimodal minimum in nitrateand a maximum in phytoplankton in austral mid-summer; Smith and Sak­shaug, 1990). A number of processes act to increase the vertical transport ofnitrate to the surface layer (such as large-scale divergences and localized up­wellings), but, in general, stratification in the Arctic is stronger and lesseasilydisrupted (Muench, 1990). This difference in stratification results in a majordifference between the two polar oceans; that is, nutrient depletion is a regu­lar feature of many regions of the Arctic, whereas it rarely occurs in the Ant­arctic. The distribution of nitrate and ammonium near the ice edge illustratesthe significantly reduced concentrations of nutrients often found in the sur­face layer of the Arctic (Fig. 1). In contrast, similar distributions for the Ant­arctic show a surface reduction, but usually not to levels that might be consid-

ICE

100275

DISTANCE (km)50

278

~.01 N03 r 10

100· • / •

E--i= 50 .n, -,W . , .,C I

II

0.1 I,0.\

100l bl NH~ I

I

i= 500-WC

Slation No 283 28Z

StationNo. 283 282 281

Fig. I. Vertical distribution of (a) nitrate and (b) ammonium along a section taken perpendic­ular to the ice edge in the East Greenland Sea in summer 1983 (from Smith and Kattner, (989).

248 w.o.SMITH . JR .

ered limiting to growth (Fig. 2). This condition holds true for both themarginal ice zone and the open ocean.

One striking feature of nitrogen distributions in some polar regions (at lo­cations with depths greater than 150 m) is the presence of a subsurface am­monium maximum. Such a feature has been clearly shown in the Arctic (Sainoet al., 1983;Smith et al., 1985), but is less often encountered in the Antarctic.It has been hypothesized that such a maximum in deeper (greater than 150m) waters results from active heterotrophic processes, as well as from re­duced uptake because of the reduced irradiance availability (Smith et al.,1985), both of which allow ammonium to accumulate. However, Smith andHarrison (1991) demonstrated that nitrogen (especially ammonium) up­take is much less strongly coupled to irradiance than is carbon uptake, so thatthe ammonium maximum is more likely to be a result of ammonium produc­tion via the oxidation of proteinaceous material than reduced removal.

The ammonium maximum can be either vertically extensive (as was ob­served in the Ross Sea; Fig. 3) or sharply restricted to a narrow vertical zone(Whitledge et al., 1986; Fig. 4). The vertical extent of such maxima may in­dicate the causal mechanism. That is, the most likely cause for the extensive

01STANCE FROM SHORE I kml~OP(fr'l1ll'At[,.---------

so 100 I~O asoJ2 JO 29

EZO

i= ~ no~ .W040

.01 [NOi]I}lMl

60

60

Fig. 2. Vertical distribution of (a) nitrate and (b ) ammonium along a section taken perpendic­ular to the ice edge in the Ross Sea in austral summer 1983 (from Nelson and Smith , 1986) .

NEW PRODUCTION IN POLAR REGIONS

STATION NUMBER

249

E 0

50"......

E'-"

II-

100n,w0

150

172 170 tall Hill 164 102160156 158 t:!4 152 1:10141!l1461H 1'42140 lJ!I lJ4 W

~ : I ~--J:~~~:r .D.,: i

::J ~::~':: r( <v:::.,~:':< :::J. . . .. .. .. . . ... .1 • 0,0

D'O. 1 11 : 00 :AMMONIUM (}<M)

o 75 150 225 300 375

DISTANCE (krn)

450 525 600

Fig. 3. Vertical distribution of ammonium along a section taken perpendicular to the ice edgein the Ross Sea in austral summer 1990 (D. Nelson, L. Gordon and P. Treguer, unpublisheddata, 1990).

AMMONIUM CuM)

0.0 0.2 o.~ 0.6 0.8 1.0 1.2

a\

NOJ -"

25

50

It 75

l.LJCl 100

125

150e 10 12

NITRATE (}.LM)

Fig. 4. Vertical distribution of nitrate (dashed line) and ammonium (solid line) near the iceedge in the East Greenland Sea in spring 1989. The profiles were obtained using a pump whichwas lowered at about 30 m min - I and which pumped water directly into an automated nutrientanalysis system (L. Codispoti, unpublished data, 1989).

ammonium maximum found in the Ross Sea (Fig. 3) is bacterial ammonifi­cation, because such vertically extensive concentrations of micro- or macro­zooplankton required to generate ammonium would be unlikely. Conversely,the localized accumulations found in the Arctic (Fig. 4) are much more likelyto result from the aggregation of migratory macrozooplankton into discretelayers. Subsurface ammonium maxima occur more frequently in the Arctic,

250 W.O. SMITH. JR.

0.002

and may result from the stronger stratification in the water column. Thestronger stratification greatly reduces diffusive losses, and may also allow forthe temporal succession of auto- and heterotrophic organisms and the accu­mulation of ammonium (Keene, 1990). Regardless of the causal mechanism,the absolute concentrations found within the subsurface maximum representa substantial increase relative to surface levels.

Relationship ofnitrate and ammonium to new production

It was originally suggested by Eppley and Peterson (1979) that the f ratiowas related to primary productivity by a hyperbolic response, with the maxi­mumfratio being 0.5. Platt and Harrison (1985), based on a more consistentdata set, suggested that the f ratio was related (again, hyperbolically) to ni­trate concentrations, with fmax == 0.8. An important feature of the latter anal­ysis was the selection of nitrate uptake data from stations with ammoniumconcentrations less than 0.1 ,uM. It is well established in temperate and trop­ical waters that ammonium can inhibit nitrate uptake, with the onset of in­hibition occurring at about 0.5,uM (MacIsaac and Dugdale, 1972; McCarthy,1981). A similar relationship was demonstrated in the East Greenland Sea inspring (Muggli, 1990; Fig. 5). Ammonium clearly inhibited nitrate uptake,with the onset of inhibition occurring at about 0.3 ,uM. Nitrate uptake wasinhibited by 45% at the highest ammonium concentration used (3.2 ,uM),and the relationship between the two waslogarithmic (Fig. 5). Garside ( 1981 )also noted a logarithmic decrease in nitrate uptake with increasing ammo­nium concentration, and found that at 2,uM nitrate uptake was about 50%ofthe maximum rate. He also noted that 'ammonia inhibition of nitrate uptakewas never complete and was highly variable'. Wheeler and Kokkinakis ( 1990),

0.004..,,-------------.....--..,

r-. 0.003

I.5d"

>z

Y-a + b logX-,0-2.455 x 10 -,b--1.118 x 10

0.001 +--..,.---.,...-.-,---,---,---,---10.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5

NH4 CuM)

Fig. 5. Relationship between ammonium concentration and nitrate uptake in a single assem­blage from the East Greenland Sea in spring 1990. The data (from Muggli, 1990) were fitted tothe equation v= (2.46 X 10-3 ) + (1.2 xlO- 3 )[NHt ].

NEW PRODUCTION IN POLAR REGIONS 251

however, found that ammonium concentrations in the range of 0.1-0.3 ,uMcan completely inhibit nitrate uptake. If all of these results can be applied topolar regions, then the absolute rate of nitrate uptake (and therefore new pro­duction) may often be significantly reduced in many regions. Because manypolar regions experience elevated (i.e. more than 1.0,uM) ammonium con­centrations within the euphotic zone for significant periods of time (e.g, Ber­ing Sea: Whitledge et al., 1986; East Greenland Sea: Smith et al., 1985; ScotiaSea: Ronner et al., 1983; Koike et al., 1986), the rates of new production canbe strongly influenced by nutrient interactions.

Although a large amount of variability between measured nitrate uptakerates and ammonium concentrations is observed (Fig. 6), lower nitrate up­take rates occur at elevated ammonium concentrations, confirming the trendfound in Muggli's (1990) experiments. It should be emphasized that the rangeof ammonium values observed during the two cruises was small, and maxi­mal concentrations were much below those found at other times in other re~

gions (for example, the minimum value of Koike et al. (1986) was greaterthan 2 ,uM ). The large amount of variability within the field-based relation­ship probably arises from the influence of other environmental factors on ni­trate uptake, such as irradiance and the variable physiological state of thepopulations.

The concentrations of nitrate in the Ross and Weddell Seas are high enoughto be considered non-limiting (i.e. concentrations nearly always exceed20,uM in the Weddell Sea and 5,uM in the Ross Sea; Fig. 7). However, thereis a trend for the highest/ratios to occur at the highest nitrate concentrations(Fig. 7). This trend occurred for three independent cruises, and cannot be

o

0.008

o

o

o o

o

I" 0.006 0 0..c 000 Cb.......,

'bO~'OllDOIIII0

,., DO0 00" 00z 0.004 o 8 oo~o> 0E; D

DO"01 CJ olP o " ,,8 0 D

0.002o ahI!P 0 93

OD ~OOOO 19" 0

o 0 0 80 o

0.000

0.00 0.25 0.50 0.75 1.00

NH4

CuM)

Fig. 6. Relationship between ammonium concentration and nitrate uptake from cruises to theice edge in the Weddell Sea in austral spring 1983 and autumn 1986.

I (b) 1.0tv

(al 1.0 ! (e) 1.0 - \ I VItv• .• . .. .

•0.8 -I . I 0.8 -I- 0.8

• • •

.s o.s j...• • • • • •. ,

• • • •f] c s f . ..... .: .

f DA.. ~r • o •

00 .:. It.. 0

o:.. • • • 10 ..0 •• ,I. ••

0.4 00 - - -. 0.4. • 0

0 ,~ .-0 0 •- I

'~I0.2 -I I 0.2 +

0.0 I I 0.0 I Ii i r i 0 .0 -r5 10 15 20 25 30 20 25 30 35 2. 26 28 30 32

NitrQte (I'M) Nitrate (I'M) Nitrate (!J.M)

Fig. 7. Relationship between nitrate concentration andfratios from cruises to the ice edge in (a) Ross Sea, 1983; (b) Weddell Sea, 1 983~ and(c) Weddell Sea, 1986.

~oU>1!::=l,;:r:

?i

NEW PRODUCTION IN POLAR REGIONS 253

explained on the basis of uptake kinetics (the K, value for nitrate uptake bypolar phytoplankton is less than 1.0 ,uM; Smith and Harrison, 1991 ). Becausethe lowered nitrate levels in all likelihood resulted from phytoplankton up­take, the increased biomass and heterotrophic turnover of that biomass (ab­solute rates of regeneration increase with biomass and productivity; Harri­son, 1981) and low phytoplankton growth rates may allow ammonium toaccumulate and result in decreased f ratios. This trend was not observed inthe Canadian Arctic (Harrison et al., 1987); however, if such a trend wereconsistent throughout the Antarctic, the chemical and biological controls ofnew production in nitrate-replete environments would need to be carefullyreassessed.

Newproduction in the Southern Ocean

Despite the uncertainties imposed by the extreme spatial and temporal as­pects ofprimary productivity in the Antarctic, it is important to begin to com­pile the available data to estimate the quantitative role of the Southern Oceanin the global carbon cycle and oceanic vertical flux. In Eppley and Peterson's( 1979) original estimate ofglobal new production, polar regions were treatedas a neritic region, and were not included in the analysis. Furthermore, polarareas were omitted because it was unclear if the relationship proposed (thatbetweenfratios and primary productivity) could be applied to nutrient-richareas. Despite continuing uncertainties about the relationships among pri­mary productivity, new production, nutrients and irradiance (e.g. Smith andHarrison, 1991), it is possible to estimate new production in the SouthernOcean by incorporating recent productivity values from the literature (Table1). Most of the estimates in Table 1 are those of Eppley and Peterson (1979),but the revised estimate of Chavez and Barber (1987) for equatorial produc­tion is included. The Antarctic is also included, and is divided into two zones:the ice-edge zone and open water. The open water area is much greater (it isdefined as the areas south of the mean position of the Antarctic Convergence,or 36 X 106 km"; El-Sayed, 1978), but its mean productivity (based on 14Cestimates) is much less (about 16 g C m-2 year- I; Holm-Hansen et al., 1977).Furthermore, although the mean f ratio from a variety of oceanic regimes is0.36 (Smith and Nelson, 1990), this average includes samples from neriticregions, and thefratio of the deep waters of the Southern Ocean may be evenlower. As a result, the averagefratio obtained by Ronner et al. (1983) is usedto compute the open ocean new production. The total new production com­puted in this manner is only 0.09 X 1015 g C for the oceanic region. Con­versely, the ice edge is more productive but is spatially restricted (an esti­mated 38 g C m- 2 year- I in an area of 16.4x 1012 km"; Smith and Nelson,1986), has ahigherfratio (0.62; Smith and Nelson, 1990), and a much greateramount of calculated new production (0.39 XI 0 15 g C year- I ). Therefore,the ice edge is potentially a much greater source of organic material availablefor export to the deeper waters of the ocean.

254

TABLE I

Ocean primary production in offshore ocean areas and estimates of new production

W.O. SMITH, JR.

Ocean Offshore Primary Primary production J ratio New production NP/Aarea production (X 10" g C yea r-I) (X 10 15 g C yea r:") (g C m- 2

(X 1012 m2 ) (g C m- 2 year- I) year>')

Ind ian 7 1.0 84 5.96 0.21 1.25 )8Atlant ic 83.9 102 8.56 0.26 2. 18 26Pacific 167 55 9.14 0.14 1.26 7.5

Coastal' 0.18 834 0.15 0.50 0.08 440Equa torial" 11.3 176 1.98 0.44 0.85 75

Anta rcticOpen ocean 38.1b 16' 0.61 0. 15d 0.09 2.4Ice edge 16.4' 38r 0.62 0.62 r 0.38 23Total 38.1 1.23 0.47 12

Arctic 13.1 0.13 0.00 0.00 0Totals 27.2 6.1

NP, New production ; A, area. All numbers from Eppley and Peterson (1979 ) unless indicated. Areas of sub-regions are included in tot al area ofoceans , but p roductivity va lues are no t.' Fro m Chavez and Barber (1987) . "From El-Sayed (197 8). ' From Holm-Hansen et al. ( 1977 ). dFrom Rennerct al. ( 1983). ' From Sm ith and Nelson ( 1986 ). rFrom Smith and Nelson ( 1990 ).

The total (open ocean plus ice-edge related) new production of the Antarc­tic is 0.48 X Iat5 g C year- I (Table 1), Although this is a substantial (about8% of the total) contribution to global productivity, it is less than that ofother regions and oceans. A similar estimate of new production in the Arcticwas not attempted, because data on new production are limited and the po­tential for nutrient limitation precludes the use of such a simple model. How­ever, it should be noted that Anderson et al. (1990) estimated from chemicaltracer data that the new production for a portion of the Arctic continentalshelves was at least 45 g C m- 2 year: ' , which clearly is a substantial rate.Comparison of the rates of new production per unit area in each region of theWorld Ocean shows that the Antarctic production is similar to that of theother oceans (using the total new production divided by the total area to givea ratio of 0.012; Table 1), despite the large area encompassed. The ice edgeas a specific feature is less productive per unit area than either coastal orequatorial upwelling regions, which suggests that the large-scale productivityof the Antarctic may be limited by the temperature-limited phytoplanktongrowth rates and low surface irradiances which occur throughout much of theyear. However, these same factors may reduce heterotrophic oxidation of or­ganic matter and cause the vertical flux to be highly episodic, as has beenfound in some regions of the Antarctic (Dunbar et al., 1985; Fischer et al.,1988; Karl et al., 1991). lfthe estimates summarized in Table I are reasona­bly accurate, the Southern Ocean can be an active site of new production andremoval of biogenic material from the surface layer.

Few data are available to test adequately whether the Southern Ocean is a

NEW PRODUCTION IN POLAR REGIONS 255

source or a sink of CO2 for the atmosphere. The presence of extensive circum­polar biogenic deposits suggests that vertical flux from the surface may besignificant (or that remineralization rates within the water column are ex­tremely slow), and therefore at steady state the Antarctic may be acting as acarbon sink and an important region in global biogeochemical cycles. How­ever, a consensus is needed on the manner in which Antarctic systems arestructured and how they function. From the published data it is possible tohypothesize that the open ocean and ice-edge zones in the Antarctic appearfundamentally different, with the open ocean being extremely unproductive,dependent on ammonium as a nitrogen source, with relatively small seasonaloscillations in phytoplankton biomass and new production, and contributingrelatively little organic material to the vertical flux from the surface layer. Incontrast, the marginal ice zone is highly productive (but restricted in time atone point), dependent on nitrate as a nitrogen source, characterized by sub­stantial seasonal variations, and contributes substantial amounts of biogenicmaterial to the vertical flux of the region. A thorough understanding on allspace and time scales for these two environments is needed to provide a quan­titative estimate of the role of the Southern Ocean in the global carbon cycleand vertical flux of biogenic matter to the deep sea.

ACKNOWLEDGMENTS

I thank my colleagues who provided unpublished data and insights thatwere used in this paper: L. Codispoti, D. Nelson, L. Gordon, P. Treguer andD. Muggli. D. Nelson offered valuable insights into the information pre­sented in Table 1.H. Kelly and J. Rich were instrumental in preparing a num­ber of the regression analyses used. This research was supported by the Officeof Naval Research and NSF Grants DPP-20213 and DPP-8817070.

REFERENCES

Alexander, V. and Niebauer, H.J., 1981. Oceanography of the eastern Bering Sea ice-edgezonein spring. Limnol. Oceanogr., 26: 1111-1125.

Anderson, L.G., Dyrssen, D. and Jones, E.P., 1990. An assessment of the transport of atmos­pheric CO2 into the Arctic Ocean. J. Geophys. Res., 95: 1703-1712.

Chavez, F.P. and Barber, R.T., 1987. An estimate of new production in the equatorial Pacific.Deep-Sea Res., 7: 1229-1243.

Dugdale, R.C. and Wilkerson, F.P., 1989. Regional perspectives in global new production. In:M. Denis (Editor), Oceanologie: Actualite et Prospective. Centre d'Oceanologie, Marseille,pp. 289-305.

Dunbar, R.B., Anderson, J.B. and Dornack, E.W., 1985. Oceanographic influences on sedimen­tation along the Antarctic continental shelf. In: S.S. Jacobs (Editor), Oceanology ofthe Ant­arctic Shelf. Am. Geophys. Union, Washington, DC, pp. 291-312.

El-Sayed, S.Z., 1978. Primary productivity and estimates of potential yields of the Southern

256 W.O. SMITH, JR.

Ocean, In: M.A. McWhinnie (Editor), Polar Research. Westview Press, New York, pp. 141­160.

Eppley, R.W. and Peterson, BiL, 1979. Particulate organic matter flux and new production inthe deep ocean. Nature, 282: 677-680.

Fischer, G., Fiitterer, D., Gersonde, R., Honjo, S., Ostermann, D. and Wefer, G., 1988. Seasonalvariability of particle flux in the Weddell Sea and its relation to ice cover. Nature, 335: 426­428.

Garside, C., 1981. Nitrate and ammonia uptake in the apex of the New York Bight. Limnol.Oceanogr., 26: 731-739.

Harrison, W.G., 1981. Nutrient regeneration and primary productivity in the sea, In: P.G. Fal­kowski (Editor), Primary Productivity in the Sea. Plenum, New York, pp. 433-460.

Harrison, W,G., Platt, T. and Lewis, M.R., I987.fRatio and its relationship to ambient nitrateconcentration in coastal waters. J. Plankton Res., 9: 235-248.

Holm-Hansen, 0., EI-Sayed, 8.Z., Franceschini, G.A. and Cuhel, R.L., 1977. Primary produc­tion and the factors controlling growth in the Southern Ocean. In: G. Llano (Editor), Ad­aptations within Antarctic Ecosystems. Gulf, Houston, pp. 11-50.

Karl, D.M., Tilbrook, B.D. and Tien, G., 1991. Seasonal coupling of organic matter productionand particle flux in the Bransfield Strait, Antarctica. Deep-Sea Res., in press.

Keene, N.K., 1990. Nitrogen dynamics in the East Greenland Sea. Ph.D. Dissertation, Univer­sity of Tennessee, Knoxvill, TN, 140 pp.

Koike, I., Holm-Hansen, O. and Biggs, D.C., 1986. Inorganic nitrogen metabolism by Antarcticphytoplankton with special reference to ammonium cycling. Mar. Ecol. Prog. Ser., 30: 105­116.

Maclsaac, J.1. and Dugdale, R.C., 1972. Interactions oflight and inorganic nitrogen in control­ling nitrogen uptake in the sea. Deep-Sea Res., 19: 209-232.

McCarthy, J.J., 1981. The kinetics of nitrogen utilization. In: T. Platt (Editor), PhysiologicalBases of Phytoplankton Ecology. Can. Bull. Fish. Aquat. Sci., 210: 211-233.

Muench, R.D., 1990. Mesoscale phenomena in the polar oceans. In: W.O. Smith, Jr. (Editor),Polar Oceanography, Part A. Academic Press, San Diego, pp. 223-280.

Muggli, D.L., 1990. The uptake of nitrogenous nutrients by phytoplankton in the waters of theFram Strait during spring 1989. M.S. Thesis, University of Tennessee, Knoxville, TN, 92 pp.

Nelson, D.M. and Smith, W.O., Jr., 1986. Phytoplankton bloom dynamics of the western RossSea ice edge. II. Mesoscale cycling of nitrogen and silicon. Deep-Sea Res., 33: 1389-1412.

Nelson, D.M., Smith, W.O., Jr., Gordon, LJ. and Huber, B.A., 1987. Spring distributions ofdensity, nutrients, and phytoplankton biomass in the ice-edge zone of the Weddell-ScotiaSea. J. Geophys. Res., 92: 7181-7190.

Nelson, D.M., Smith, W.O., r-, Muench, R.D., Gordon, L.I., Sullivan, C.W. and Husby, D.M.,1989. Particulate matter and nutrient distributions in the ice-edge zone of the Weddell Sea:relationship to hydrography during late summer. Deep-Sea Res., 36: 191-209.

Peng, T.H., Takahashi, T., Broecker, W.S. and Olafsson, J., 1987. Seasonal variability of carbondioxide, nutrients and oxygen in the northern North Atlantic surface water: observations anda model. Tellus, 39: 439-458.

Platt, T. and Harrison, W.G., 1985. Biogenic fluxes of carbon and oxygen in the ocean. Nature,318: 55-58.

Ronner, U., Sorensson, F. and Holm-Hansen, 0., 1983. Nitrogen assimilation by phytoplank­ton in the Scotia Sea. Polar BioI., 2: 137-147.

Saino, T., Otobe, H., Wada, E. and Hattori, A., 1983. Subsurface ammonium maximum in theNorth Pacific and the Bering Sea in summer. Deep-Sea Res., 30: 1157-1171.

Sarmiento, lL., Toggweiler, J.R. and Najjar, R., 1988. Ocean carbon-cycle dynamics and at­mospheric pC02• Philos. Trans. R. Soc. London, Ser. A, 325: 3-21.

NEW PRODUCTION IN POLAR REGIONS 257

Smith, S.L., Smith, W.O., Jr., Codispoti, L.A. and Wilson, D.L., 1985. Biological observationsin the marginal ice zone of the East Greenland Sea. J. Mar. Res., 43: 693-717.

Smith, W.O., Jr. and Harrison, W.G., 1991. New production in polar regions: the role of envi­ronmental controls. Deep-Sea Res., in press.

Smith, W.O., Jr. and Kattner, G., 1989. Inorganic nitrogen uptake by phytoplankton in themarginal ice zone of the Pram Strait. Rapp. P.-V. Reun. Cons. Int. Explor. Mer, 188: 90-97.

Smith, W.O., Jr. and Nelson, D.M., 1985. Phytoplankton bloom produced by a receding iceedge in the Ross Sea: spatial coherence with the density field. Science, 227: 163-167.

Smith, W.O., Jr. and Nelson, D.M., 1986. Importance of ice edge phytoplankton blooms in theSouthern Ocean. BioScience, 36: 251-257.

Smith, W.O., Jr. and Nelson, D.M., 1990. Phytoplankton growth and new production in theWeddell Sea marginal ice zone during austral spring and autumn. Limno1. Oceanogr., 35:809-821.

Smith, W.O., Jr. and Sakshaug, E., 1990. Polar phytoplankton. In: W.O. Smith, Jr. (Editor),Polar Oceanography, Part B. Academic Press, San Diego, pp. 477-525.

Wheeler, P.A. and Kokkinakis, SA, 1990. Ammonium recyclinglimits nitrate use in the oceanicsubarctic Pacific. Limnol, Oceanogr., 35: 1267-1278.

Whitledge, T.E., Reeburgh, W.S. and Walsh, J.J., 1986. Seasonal inorganic nitrogen distribu­tions and dynamics in the southeastern Bering Sea. Cont. Shelf Res., 5: 109-132.

Zwally, H,J., Comiso, J.c., Parkinson, CL., Campbell, W,J., Carsey, F.D. and Gloersen, P.,1983. Antarctic sea ice. 1973-1976: Satellite passive-microwave observations. NASA Spec.Publ, 459. NASA, Washington, DC.