Journal of Plankton Research Vol.20 no.7 pp.1267-1291, 1998
Pathways of carbon cycling in the euphotic zone: the fate of largesized phytoplankton in the Northeast Water Polynya
S.Pesant, L.Legendre, M.Gosselin1, C.Ashjian2, B.Booth3, K-Daly4, L.Fortier,
H.-J.Hirche5, J.Michaud, R.E.H.Smith7, S.Smith6 and W.O.SmithJr4
GIROQ, Dipartement de biologie, Universite Laval, Ste-Foy, Quibec, G1K 7P4,
1
Dipartement d'ocianographie, Universite du Quebec a Rimouski, 310Allee des
Ursulines, Rimouski, Quibec, G5L 3A1, Canada,2Department of Biology, Woods
Hole Oceanographic Institution, Woods Hole, MA 02543,3 University of
Washington, School of Oceanography, Seattle, WA 98197,4Department of
Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996,
USA, 5Alfred-Wegener-Institut fur Polar- und Meeresforschung, Postfach 120161,
D-27515 Bremerhaven, Germany, 6Rosenstiel School of Marine and Atmospheric
Sciences, University of Miami, Miami, FL 33149, USA and 7Department of
Biology, University of Waterloo, Waterloo, Ontario, N2L 3G1, Canada
Abstract. The fate of large-sized phytoplankton and pathways of carbon cycling in surface waters, i.e.
recycling within or export out of the euphotic zone, were investigated in the Northeast Water (NEW)
Polynya (77-81 °N) from 23 May to 17 August 1993. Sampling represented a wide range of ice, hydrographic and nutrient conditions. Phytoplankton and zooplankton abundances, and phytoplankton
production rates were determined in the field, whereas potential rates of grazing by copepods, dinoflagellates and appendicularians were calculated from abundances and temperature, using assumptions from the literature. The potential downward and lateral export of phytoplankton was also
calculated by resolving a carbon budget for the euphotic zone. The present study suggests that, in the
NEW, different pathways for the cycling of carbon existed in seasonally ice-free (in the polynya) and
continuously ice-covered areas (outside the polynya). Outside the polynya, the fate of large-sized
phytoplankton could not be assessed because the heterotrophic community presumably grazed on a
variety of food items, including ice algae, microzooplankton and large-sized phytoplankton. In the
polynya, the fate of large-sized phytoplankton production was to be mostly recycled at the beginning
of sampling and to be mostly exported downward or laterally as the bloom of large-sized phytoplankton developed. Generally, copepods mostly contributed to recycling, but sometimes dinoflagellates or appendicularians alone recycled most of the large-sized phytoplankton production.
Introduction
The fate of particulate phytoplankton production in the euphotic zone depends
on the magnitude of losses to other trophic compartments (grazing), and toward
depth (sinking). When net particulate primary production exceeds the losses,
phytoplankton biomass may accumulate to form a bloom (Legendre, 1990).
When phytoplankton are grazed, the primary production may be exported to
depth in the form of fast-sinking faecal pellets and organic structures produced
by large-sized organisms (e.g. pelagic runicates) and/or it may be recycled within
the surface waters as a result of respiration and excretion by grazers, 'sloppy
feeding', production of relatively slow-sinking faecal material, and coprophagy
and coprorhexy of faecal pellets (Lampitt et ai, 1990; Noji et ai, 1991). When the
sinking rates of phytoplankton are high, as a result of physical aggregation
(McCave, 1984; Jackson, 1990; Hill, 1992) and physiological responses of intact
© Oxford University Press
1267
S.Pesant el al.
cells to environmental conditions (Waite et al, 1992; Riebesell, 1992), a significant proportion of the production may be exported to depth.
Because phytoplankton size influences the above processes (Smayda, 1970;
Ki0rboe, 1993; Fortier et al, 1994), the fate of phytoplankton production generally differs for the large and small size fractions (Legendre and Le Fevre, 1991).
The present paper considers the relative controls exerted by the various processes
on the fate of large-sized primary production (i.e. >5 urn) in the Northeast Water
(NEW), at the southern limit of the Arctic ice pack. In the present study, NEW
designates the ice-free waters of the NEW Polynya and also the surrounding ice
margin and ice-covered area.
Ashjian et al (1995, 1997), Daly (1997) and Hirche and Kwasniewski (1997)
have shown that, in the NEW ice-free waters, phytoplankton production exceeds
copepod grazing, leading to a potential downward export of intact cells, mostly
large-sized diatoms. However, the downward flux of biogenic carbon determined
at one location in the polynya, using a shallow-depth (130 m) sediment trap
(Bauerfeind et al, 1997), suggests that <5% of the daily production sinks from
the surface waters during the summer phytoplankton bloom. This is consistent
with field estimates of the potential sinking rates of phytoplankton assemblages
in the NEW, using settling columns (SETCOL; Bienfang, 1981), which indicate
that phytoplankton were generally buoyant in the polynya (S.P., unpublished
data). Under these conditions, and because the polynya is very productive, it
could be expected that phytoplankton accumulate in surface waters. This was not
the case, so that loss terms other than sinking probably contributed to maintain
relatively low phytoplankton standing stocks, e.g. advection out of the study area
and/or grazing by organisms other than copepods.
In addition to the traditional idea of a short diatom-to-copepod food chain,
recent investigations have shown that, in the Arctic, large-sized phytoplankton
are sometimes grazed by microzooplankton and appendicularians. Surprisingly,
as much as 180% of the primary production in a diatom-dominated ecosystem
could be ingested daily by protozooplankton (Nielsen and Hansen, 1995). In
temperate and Antarctic waters, microscopic analyses have shown the presence
of large diatoms in the faecal pellets of dinoflagellates (Nothig and von Bodungen, 1989; Buck and Newton, 1995); In the Arctic, large-sized dinoflagellates (e.g.
Gyrodinium spirale) were observed to feed on diatoms by direct engulfment
(Hansen, 1992). In contrast, ciliates are limited by their oral diameter, so that they
generally feed effectively on particles <10 urn (Kivi and Setaelae, 1995). Largesized tintinnids are an exception, but these organisms were not common in the
NEW (S.P., unpublished data). Hence, ciliates and small dinoflagellates (<20 um)
share the small-sized food items, whereas the larger dinoflagellates (>20 um)
compete with copepods for large-sized phytoplankton (Nielsen and Hansen,
1995; Hansen et al, 1996, Sherr et al, 1998). In early studies, appendicularians
were considered to ingest mainly particles <5 um (Alldredge and Madin, 1982;
Deibel and Powell, 1987), so that they are generally thought to be associated with
the microbial food web. It is now clear, however, that large-sized appendicularians (e.g. Oikopleura vanhoeffeni) sometimes ingest diatoms (Deibel and Turner,
1985; Urban et al, 1992). The latter authors showed that the composition of
1268
Fate of large-sized phytoplankton in Northeast Water Polynya
appendicularian faecal pellets was similar to the ambient plankton during bloom
and non-bloom situations. More recently, Acuna et al. (1996) modelled the
efficiency of particle retention by O.vanhoeffeni and showed that microplankton
(20-200 um) are captured and ingested by large-sized appendicularians
(O.vanhoeffeni and Oikopleura labradoriensis), but probably not by the smaller
species (e.g. Oikopleura dioica and Fritilaria spp.) In their Table III, phytoplankton <20 and >20 um represent 74 and 26% of phytoplankton in the water,
respectively, and constitute 70 and 30% of the food ingested by O.vanhoeffeni,
respectively, which leads us to conclude that the size composition of the natural
diet for O.vanhoeffeni corresponds to that of phytoplankton in the water.
The objectives of the present study are to determine the fate of large-sized
phytoplankton in the NEW and to assess the pathways of carbon cycling in
surface waters, i.e. recycling within or export out of the euphotic zone. Our
hypothesis is that, in addition to herbivorous copepods, large-sized dinoflagellates and appendicularians contributed significantly to maintain low standing
stocks of large-sized phytoplankton in the NEW Polynya. Alternatively, phytoplankton of all sizes might have been advected out of the polynya.
Method
Sampling and laboratory analyses
The NEW is located on the northeastern continental shelf of Greenland, where
a polynya extends from 79 to 81°N during spring and summer. Sampling was
conducted on board the RV 'Polarstem' from (i) 23 May to 22 June and (ii) 27
June to 22 July 1993 (cruises ARK IX/2 and 3) and on board the USCGC 'Polar
Sea' from (iii) 22 July to 17 August 1993. A total of 233 stations were sampled,
representing a wide range of ice cover, hydrographic and nutrient conditions. In
1993, the NEW polynya was limited to the north and south by ice barriers, to the
west by land-fast ice, and to the east by sea-ice, which retreated progressively
during the sampling period (Figure 1). Ice concentrations were monitored using
a satellite-borne Special Sensor Microwave/Imager (Garrity and Ramseier,
1994). Physical conditions were determined using CTD profilers (results in
Bud6us et al., 1994; Wallace et al, 1995; Buddus and Schneider, 1996). Water
samples were collected using a rosette sampler equipped with twelve 12-1 Niskin
bottles and a LI-COR185 B underwater quantum photosynthetically active radiation (PAR) meter. Zooplankton were sampled with Ring nets (23 May-22 July)
or a multiple opening closing net and environmental sensing system (MOCNESS;
Wiebe et al., 1976) after 22 July.
Niskin bottles were equipped with silicone- or Teflon-coated stainless steel
springs. Water samples were collected at eight depths, of which seven corresponded to irradiances 100,50,30,15,5,1 and 0.1% of surface PAR, and one was
at the depth of maximum chlorophyll a (Chi a) concentration as determined from
in vivo fluorescence (Haardt Instrument). Subsamples were immediately drawn
from the Niskin bottles for estimation of various plankton characteristics. These
included Chi a at all stations, and primary production and microscopic analysis
at 97 of the 233 stations. Subsamples (200 ml) for Chi a determination were size
1269
S.Pesant et al.
20»W
82°N
8CN
78"N
78«N
10W
Fig. L Map of the Northeast Water, showing the location of Belgica Bank (<200 m). Arrows, general
surface circulation; hatched areas, edge of the ice barriers; hatched lines, eastern limit of open waters
at the end of (a) June and (b) July. Open waters were limited to the north by the Ob Bank Ice Barrier,
to the south by the Norske Ice Barrier, to the west by land-fast ice, and to the east by pack ice.
fractionated in parallel on 25 mm Whatman GF/F filters (total phytoplankton
biomass: BT) and 25 mm Poretics polycarbonate membranes with 5 um nominal
pore size (biomass of large phytoplankton: BL). Filtration was under vacuum
pressure of <100 mmHg. Chlorophyll a was determined using a T\irner fluorometer (Model 112), after 24 h extraction in 90% acetone at 5°C without grinding
(Parsons et al., 1984). Subsamples (400 ml) from all depths were filtered on precombusted (500°C during 5 h) GF/F niters, which were frozen for later particulate organic carbon (POC) determination, using a Perkin Elmer CHN analyser
(Model 2400). Subsamples (250 ml) from the depth of maximum Chi a concentration and from the surface were preserved with acidic Lugol's solution for later
enumeration using an inverted microscope (Lund et aL, 1958). During counting,
the diatoms were identified to genus and dinoflagellates were distinguished by
size (cells <20 um and >20 um).
Daily net (versus gross) particulate primary production was estimated from
seven (see above) or four photic depths (100, 50, 30 and 5% of surface PAR),
1270
Fate of large-sized phytoplankton in Northeast Water Polynya
depending on space available in the incubators, using the 14C-uptake method
(Parsons etai, 1984). Inoculated bottles (500 ml; polycarbonate) were placed for
24 h in on-deck incubators that simulated in situ light and upper water column
(8 m) temperature conditions. At the end of incubations, the total volume of each
bottle was split into two 250-ml aliquots, each of which wasfilteredon GF/F (total
phytoplankton production: P T ) and Poretics 5 um filters (production of largesized phytoplankton: P L ), respectively. The filters were acidified to remove inorganic carbon.
The Ring nets consisted of a 200 um mesh net with a 0.67 m diameter mouth
and a 64 um mesh net with a 0.1 m diameter mouth. The two nets were mounted
on a conventional Bongo frame and were hauled vertically from 200 m (or
bottom) to the surface at a maximum speed of 1.0 m s"1. The MOCNESS
consisted of eight 150-um mesh nets with a i m 2 mouth, which were towed
obliquely over eight depth intervals that covered the 0-200 m (or bottom) layer
(Lane et ai, 1995, 1996). At 74 of the 233 stations, samples collected with the
various nets were preserved in 4% buffered formalin for zooplankton identification and enumeration under a dissecting microscope. When using Ring nets,
the large-sized copepods (i.e. Calanus and Metridia species) were counted from
the largest net, whereas the small-sized copepods (Oithona similis, Microcalanus
spp., Oncea spp. and Pseudocalanus minutus) and appendicularians were counted
from the smallest net, which is efficient at sampling zoopiankton with prosome
lengths <1.7 mm (Chaumillon etal, 1998).
Calculations
During incubations, the simulated in situ irradiance was not corrected for the
attenuation of PAR by the ice cover, i.e. we simulated open-water conditions
only. To correct a posteriori for this effect, all values of integrated primary production were transformed by taking into account the proportion of ice-covered (4>)
and open (1 - <t>) waters, as determined from satellite images for the area
(25 x 25 km centred on the station location), at the time of sampling:
^corrected = (1 - * ) ^uncorrected + (1 ~ £*) ( * ) ^unconected
(1)
where k9 = 91 % is the attenuation of incident PAR due to snow, ice and ice algae
in the NEW estimated from measurements of incident irradiance above and
below the ice cover at a few stations (M.G., unpublished data). In the present
paper, P L and B L were depth integrated from 0 m to the depth at which the underwater irradiance is 0.1% of surface PAR (i.e. over the euphotic zone).
The volumes and plasma contents of diatoms collected in the NEW were calculated at the genus level from mean cell sizes determined under the microscope,
using a computer-assisted image analyser (Booth, 1993), and were converted to
organic carbon biomass following Strathmann (1967). The carbon to Chi a ratio
(C:Chl a) of the diatom assemblage was calculated as the slope of the regression
of the organic carbon biomass of the diatom assemblage on BL.
The community biomass of heterotrophic dinoflagellates >20 um was
1271
S.Pesant et al.
calculated from field abundances, combined with a mean cell volume of 21 121
um3 [n = 156; corresponding to an equivalent spherical diameter (ESD) of -34
um] for dinoflagellates >20 um sampled in the NEW (T.Nielsen, unpublished)
and a volumetric carbon content of 0.12 pg C unr 3 (Hansen et al., 1997).
Community carbon biomass in the euphotic zone was calculated using the
average biomass of samples collected at the surface and the depth of maximum
fluorescence and assuming a mean zone thickness of 30 m. T.G.Nielsen and
P.K.Bj0rnsen (personal communication) determined a maximum weight-specific
growth rate of 0.3 day 1 from growth experiments on the dinoflagellate Cspirale
(ESD 30 um) collected in the NEW and grown at a maximum temperature of 5°C.
This experimental result was converted to in situ temperature (T; °C) by using a
Qw of 3 (see arguments in the Discussion), so that:
Specific growth rate = 0.173 exp (0.109 T)
(2)
For each copepod species and development stage that potentially fed on largesized phytoplankton in the euphotic zone (see the Discussion), the biomass was
the product of body weight (mg C) estimated from the literature (Table I) and
field abundance. The community biomass was the summation over all taxa. The
weight-specific growth rate was determined using the equation of Huntley and
Lopez (1992):
Specific growth rate = 0.0445 exp (0.111 T)
(3)
where T is the in situ temperature (°C). The carbon content of copepod dry
weight was taken as 0.54 (mass:mass; mean value from Table IV in Daly, 1997).
The community biomass of large-sized appendicularians was calculated from
the field abundances of O.vanhoeffeni and O.labradoriensis, assuming a mean
carbon content of 21.3 ug C ind."1 (calculated from Deibel and Acuna, 1995).
Using the equation of Deibel (1988; clearance rate = 12.6 trunk length1-79) for cold
waters (i.e. -1.6 to +4.5°C), we estimated that the clearance rate of the average
sized O.vanhoeffeni collected in the NEW (i.e. 2.73 mm; Deibel and Acuna, 1995)
was 0.0018 m3 ind.-1 day 1 . Deibel (1988) concluded that temperature in cold
waters has no effect on clearance rate, so that we did not adjust the clearance rate
for the in situ temperature. Clearance rates were multiplied by the mean integrated value of in situ Chi a concentrations in the large size fraction, and
converted to carbon units using C:Chl a = 15 (see arguments in the Discussion).
The community grazing rates (mg C nr 2 day 1 ) of dinoflagellates and copepods
were estimated as the product of community biomasses (mg C nr 2 ) and weightspecific growth rates (day 1 ), divided by the gross growth efficiencies (no units).
The gross growth efficiencies of dinoflagellates and copepods were assumed to be
0.40 (Fenchel, 1982) and 0.33 (Peterson, 1988; Berggreen et al, 1989), respectively. The community grazing rate of appendicularians was calculated as the
product of field abundance (ind. nv 2 ), individual clearance rate (m3 ind."1 day 1 )
and mean integrated biomass of large-sized phytoplankton in the euphotic zone
(mg C m-3).
1272
Fate of large-sized phytoplankton in Northeast Water Porynya
Table L Body weights (ug C) of individual copepods for five species and seven developmental stages.
Species are listed, from top to bottom, in increasing order of average biomass in the NEW. Bold
indicates the species and stages with prosome lengths £0.4 mm
Taxon
Cl
C2
C3
C4
C5
AM
AF
Chyperboreus*
C.glacialis'
Cfinmarchicus'
Oithona similis*
Pseudocalanus minutus*
LI
0.52
0.50
0.14
0.19
8.6
3.2
1.1
0.20
0.53
41
17
3.8
0.36
L3
218
51
92.
0.48
604
162
24
0.62
2.9
583
198
30
0.66
2.6
1180
370
38
0.78
43
Body weights were converted into carbon from dry weights (DW) using C:DW = 054. Dry weights
were determined using the prosome length (L; mm)-weight (DW; ug) relationships from: 'McLaren
and Leonard (1995) for Cfinmarchicus collected on the Scotian Shelf during winter-spring, In DW =
1.919 + 3.300 In L; ^abatini and Ki0rboe (1994) for O.similis collected in Oresund (Denmark) during
summer, DW = 0.56 L 216 , modified using C:DW = 0.47; 'Corkett and McLaren (1978) for Pseudocalanus spp., DW = 11.8 L?M.
Results
Size distributions of phytoplankton characteristics
Chlorophyll a biomass and production of small-sized (<5 um; subscript S) phytoplankton were determined by subtracting the large-sized fraction (>5 um;
subscript L) from the total, i.e. Bs = By - BL and Ps = PT - PL, respectively. In
the NEW, Bs and Ps did not increase proportionally to total values (Figure 2),
i.e. the slopes of the relationships Bs = f(Br) and Ps = /(P T ) were not significantly
different from zero (ANCOVA F-test; P > 0.05). Bs and Ps seldom exceeded 10
mg Chi a m~2 and 500 mg C nr 2 day 1 , respectively. In contrast, the biomass and
production of the large-sized phytoplankton (S L a °d PO showed significant positive relationships (Model I regression) with the corresponding total values:
BL = 0.83 Br (r2 = 0.96, P < 0.001, n = 143)
2
PL = 0.71 PT (r = 0.94, P < 0.001, n = 55)
(4)
(5)
Regressions were forced through the origin so that when BT or PT = 0, the values
for the large size fraction are also zero. Data in Figure 2 represent a wide range
of ice-cover conditions and are from the first and the second sampling periods
only, because phytoplankton were not size fractionated during the third period.
For the latter period, f?L a n d PL were estimated from 5 T and P T using equations
(4) and (5), respectively.
Values of the C:Chl a ratio in the NEW ranged from 2 to 2012. The regression
line for the relationship between the organic carbon biomass of diatoms and BL
has a slope of 75 (Figure 3; closed circles; r2 = 0.46; P < 0.05; n = 144) and is at
the lower limit of the scatter for POC:flL (Figure 3; crosses).
Growth and clearance rates
Temperatures in the NEW euphoric zone ranged from -1.7 to +5.2°C, so that by
using a Qw of 3 the temperature-adjusted specific rates [equations (2) and (3)]
1273
S.Pesant el al.
CVI
B
S
o
51
t/i
xt
0
20
40
60
80
100
Total phytoplankton biomass (mg Chla m"2)
1500
1000
T3
O
500 -
41
<B
TO
a S
co a.
0
500
1000
1500
2000
9
Total phytoplankton production (mg C m
1
d
)
Fig. 2. Relationships between size-fractionated and total phytoplankton biomass (a) and production
(b). Solid lines: Mode) 1 regressions (forced through the origin) between the large size fraction and
total values. Dashed lines: suggested upper limits for the small size fraction.
500
1
2
Chla biomass (mg m"3)
Fig. X Scatter plot of POC (crosses) and of diatom carbon computed from microscopic determinations (closed circles), as a function of SL. The regression line (Model I) for the latter is y = 75JT, J* =
0.46; P < 0.05; n = 144.
1274
Fate of large-sized phytoplankton in Northeast Water Polynya
Table IL Results of non-parametric Kruskall-Wallis tests, comparing plankton community
characteristics (biomass and carbon utilization rate) INSIDE and OUTSIDE the polynya, and among
the sampling periods for INSIDE and OUTSIDE the polynya, separately. The tests either rejected the
hypothesis that the groups of samples came from the same statistical population (P < 0.05 or P < 0.01)
or failed to reject it (ns, not significant). Results were the same for the two community characteristics
Phytoplankton Dinoflagellates Copepods Appendicularians
Between INSIDE and OUTSIDE P<0.01
Among periods; INSIDE only
P<0.01
Among periods; OUTSIDE only P<0.01
P<0.05
P<0.01
ns
/><0.01
/><0.01
ns
ns»
P<0.05»
ns
"In the case of appendicularians, only values <500 were used to compute the statistics, as explained
in the text.
were about twice as high for the maximum as for the minimum temperatures
encountered. The estimated specific growth rates of dinoflagellates [equation (2)]
and copepods [equation (3)] ranged from 0.14 to 0.30 day 1 and from 0.036 to
0.079 day-1, respectively. Compared to these ranges of specific rates, the range of
plankton biomasses (estimated from abundances) covered three orders of magnitude (Table II), so that grazing rates in the NEW were mostly a function of the
abundances and their conversion factors. The relative dominance of copepods in
the NEW, in terms of average biomass for the whole sampling period, follows the
ordering in Table I, from top to bottom.
Horizontal and temporal distributions of plankton characteristics
The abundances of appendicularians were determined during the first and second
periods only. During the second period, the horizontal distributions of appendicularian biomass and grazing rate were bimodal, i.e. grazing values were generally
<500 mg C irr 2 day 1 , but at five stations they were >500 mg C nr 2 day 1 , with
values ranging from 745 to 1662 (median = 862 mg C m~2 day 1 ). In order to
investigate the general trend, statistical analyses were performed on the first
mode only, i.e. excluding thefivevalues >500 mg C m~2 day 1 . Thefivehigh values
occurred at the northern and the eastern edges of the polynya, so that the first
mode was representative of most of the study area (Figure 4). The few southernmost sampled stations (<77°N) were also characterized by high appendicularian biomass (not shown), but the grazing rates were low (Figure 4) because
phytoplankton biomass and temperature there were low.
In the four plankton communities, the calculated rates of carbon utilization
varied considerably among stations located to the north of Belgica Bank, i.e. in
the polynya (Figure 3). The same is also true for biomass in the polynya. There,
the two community characteristics (biomass and carbon utilization rate) differed
significantly among the three sampling periods (Table II) and the median values
generally increased from May through August (Tables III and IV).
At stations located to the south of and on Belgica Bank, i.e. outside the
polynya, phytoplankton and dinoflagellate community characteristics (biomass
and carbon utilization rate) were significantly lower than inside the polynya,
whereas copepod community characteristics were significantly higher than in the
1275
S.Pesant et al.
20'W
B2'N
82'N
80'N
80'N
78'N
78'N
76'N
76'N
78'N
78'N
76'N
76'N
20'W
1O'W
1O'W
Fig. 4. Horizontal distributions of phytoplankton production determined at sea, and calculated
grazing rates of dinoflagellates, copepods and appendicularians. Values are depth integrated over the
euphotic zone and are for the whole sampling period (23 May-17 August 1993). Hatched lines, edges
of the ice barriers.
polynya (Table II). Although appendicularian community characteristics were
not significantly different in and outside the polynya, the maximum values were
inside the polynya, due in part to higher phytoplankton biomass there. Outside
the polynya, the two community characteristics did not differ significantly among
the three sampling periods, except for phytoplankton and appendicularians
(Table II). In these two communities, values generally increased from May
through August (Tables III and TV).
1276
Fate of large-sized phytoplankton in Northeast Water Polynya
Table IIL Median values, ranges and numbers of samples (in parentheses) of community biomass for
the four plankton groups. Statistics are for the three sampling periods and for INSIDE and OUTSIDE
the polynya (ND, no available data)
Period
INSIDE the polynya
23May-22June
27June-22July
22 July-17 August
Community biomass (mg C nr 2 )
Phytoplankton (BL)
Dinoflagellates Copepods
Appendicularians
392
32-662 (58)
1590
15-5261 (56)
1991
290-6962(74)
7
2-94 (31)
47
0-304 (36)
67
0-1032 (22)
79
14-499 (13)
273
22-1006 (30)
331
222-1933 (9)
45
5-198(17)
56
5-596(23)
ND
4
3-6(8)
9
2-258(11)
26
2-410 (9)
397
131-1033 (10)
409
79-1205 (11)
647
(1)
23
5-64(4)
108
30-244 (6)
ND
OUTSIDE the polynya
23May-22June
59
56-124 (7)
27June-22July
87
48-332 (24)
22 July-17 August
672
490-3349 (14)
Table IV. Median values, ranges and numbers of samples (in parentheses) of community carbon
utilization rate for the four plankton groups. Statistics are for the three sampling periods and for
INSIDE and OUTSIDE the polynya (ND, no available data)
Period
INSIDE the polynya
23May-22June
27June-22July
22 July-17 August
Community carbon utilization rate (mg C rrr2 day-')
Phytoplankton (PL) Dinoflagellates
Copepods
Appendicularians
24
4-728 (10)
174
0-1479 (30)
373
69-1016 (30)
1
0-35 (31)
21
0-201 (36)
45
2-306 (21)
9
2-55 (13)
36
2-148 (30)
62
35-247 (9)
8
1-218 (17)
19"
0-376 (23)
ND
1
1-2(5)
4
0-111(11)
11
2-149 (8)
45
14-116(10)
43
9-137(11)
78
(1)
6
2-9(4)
18
8-40(6)
ND
OUTSIDE the polynya
23May-22June
3
1-22(5)
27 June-22 July
13
0-245 (11)
22 July-17 August
123
15-486(11)
'In the case of appendicularians, only values >500 mg C rrr2 day 1 were used to compute the statistics for the second period, as explained in the text.
Discussion
Temporal changes in phytoplankton biomass (Afl/Af) are described here as the
balance between net (versus gross) paniculate phytoplankton production (P,
which is the quantity determined by the 14C method) and losses within and out
1277
S-Pesanl et al.
of the euphotic zone (L), which are the sum of zooplankton grazing and sinking
of intact cells and detritus:
ABlAt = P-L
(6)
All terms have dimensions of mass area"1 time"1. Viral lysis is accounted for in P,
so that it does not contribute to the loss term in equation (6). Because production, grazing and sinking are largely determined by phytoplankton size (Smayda,
1970; Legendre and Le Fevre, 1991; Ki0rboe, 1993; Fortier et al., 1994),
the balance of equation (6) and, consequently, the changes in phytoplankton
biomass, generally differ for small- and large-sized phytoplankton. The balance
between production and export is often at equilibrium for small-sized phytoplankton because of sustained grazing (e.g. Cushing, 1989) and low sinking velocities. In contrast, grazing and sinking for large-sized phytoplankton can vary
considerably, which often leads to an imbalance between production and export.
It follows that, generally:
Ps-Ls
=0
(7)
ABJAt = P L - L L * 0
(8)
and often:
Figure 2 clearly shows that, in the NEW, blooms consisted of large-sized phytoplankton, whereas the biomass of small-sized phytoplankton was consistently
low. The latter result corresponds to a tight balance between production and
export for small-sized phytoplankton [equation (7)]. It could be argued that the
trends in Figure 2 reflect the quantity of small cells that pass the 5 um pore size
filters before these get clogged by larger cells. After clogging occurs, the smallsized cells would add to the large-sized fraction, so that the contribution of small
cells would be underestimated. However, microscopic analysis of preserved
samples showed that the abundance of small-sized flagellates was similar in nonbloom and bloom conditions (Pesant et al., 1996).
Calculations and assumptions
Our calculations are based on a number of assumptions regarding (i) the choice
of heterotrophs that feed on large-size phytoplankton, (ii) the weight- or densitydependent rates from the literature, (iii) the use of Q I0 values to adjust these rates
to ambient temperature and (iv) the calculation of phytoplankton carbon
biomasses.
The first set of assumptions concerns the choice of copepod species and stages
that potentially graze large-sized phytoplankton. These were chosen on the bases
of predatonfood size ratios from the literature and the vertical distributions of
copepods in the NEW. In the literature, the ratio of copepod to food size
(length:diameter), calculated for various species and stages (not including
1278
Fate of large-sized phytoplankton in Northeast Water Potynya
nauplii), ranges from -80 to 500 (reviewed in Fortier et al, 1994; Hansen et al,
1994; Legendre and Michaud, 1998). We used a minimum value of 80 for the ratio
and a food size of 5 um, which separates large- from small-sized phytoplankton
in the present study (see above), so that copepods must be >0.4 mm long in order
to feed efficiently on large-sized phytoplankton. In the case of nauplii, the ratio
grazenfood size is generally <80 (see references above) and the size of Calanus
nauplii can be -400 um, so that these could efficiently graze on large-sized phytoplankton. Because copepod nauplii were not sorted by size or species, these are
not considered in the present paper as potential grazers of large-sized phytoplankton. Although Metridia longa and some late stages of Microcalanus spp. and
Oncea spp. met the size criterion of 0.4 mm prosome length (weights not given in
Table I), they were not included in the calculation of copepod grazing on phytoplankton because these taxa were not present in the euphotic zone, i.e. they were
generally abundant below 100 m (Ashjian et al, 1997). Thus, the latter taxa may
have ingested phytoplankton material that sank from the euphotic zone, but they
did not graze within the euphotic zone. In contrast, copepod species included in
the calculation of copepod grazing (Table I) were found in or slightly below the
euphotic zone (0-50 m; Ashjian et al, 1997; C.Ashjian et al, unpublished data),
so that these species are potential grazers of phytoplankton in the euphotic zone.
There was no evidence of a diel pattern in the vertical distribution of copepods
(Ashjian era/., 1995).
The second set of assumptions concerns the calculation of weight-specific
growth rates and individual specific clearance rates of heterotrophs. These were
determined independently of body size and species composition, i.e. as a function
of field temperature alone [equations (2) and (3)]. Our estimates of weightspecific growth rates for dinoflagellates (0.14-0.30 day 1 ) are within the range of
values determined experimentally for ice-covered, ice-edge and ice-free waters
in the Barents Sea (0.06-0.54 day 1 ; Hansen, 1992) and in the NEW (T.G.Nielsen
and P.K.Bj0rnsen, personal communication). Our estimates of weight-specific
growth rate for copepods (0.036-0.079 day 1 ) are generally in good agreement
with values calculated from egg production rates in the Barents Sea (<0.08;
Hansen et al., 1996), Greenland Sea (<0.061; Hirche and Bohrer, 1987) and the
NEW (<0.12; Hirche and Kwasniewski, 1997). In the latter study, however, 66%
of the experiments yielded weight-specific growth rates lower than those calculated here. A possible explanation is that copepod growth in the NEW was
limited by food [see the arguments about equation (3) in Kleppel etal. (1996) and
Huntley (1996)]. The latter author argues that egg production may underestimate
the specific growth rate of juveniles by a factor >3 (Peterson et al., 1991), so that
equation (3) could be a better estimate than egg production to calculate
community grazing. We believe that specific growth rates calculated using equation (3) should be interpreted as maximum values, in a way similar to the equation of Eppley (1972) for phytoplankton growth.
The third set of assumptions concerns the adjustment of dinoflagellate and
copepod growth rates to ambient temperatures. We did not consider fixed values
for ice-free and ice-covered regions because water temperature was not always
correlated to ice conditions. For example, at the beginning of sampling, the
1279
&Pesant et at.
average temperature in the euphotic zone was similar in ice-free and ice-covered
regions. For various zooplankton taxa ranging in size from 2 to 2000 um (e.g.
flagellates, ciliates, copepods), the Q10 values used to temperature adjust the
growth rates ranged from 1.4 to 55 and averaged 2.8 (reviewed in Kleppel et aL,
1996; Hansen et aL, 1997). For simplicity, we decided to round that value to the
first integer and thus use a value of 3 for dinoflagellates and copepods.
The calculation of phytoplankton carbon biomasses from a C:Chl a ratio of 75
(Figure 3) also deserves some discussion because it affects the carbon budget. It
is not recommended to use POC values to calculate the C:Chl a ratio of phytoplankton, because POC includes heterotrophs and detritus whose distributions
often co-vary with that of phytoplankton (Banse, 1977). To avoid this problem,
we calculated the carbon content of the large size fraction from diatom counts,
assuming that diatoms made up the whole biomass of phytoplankton >S urn. The
slope of the relationship between large-sized phytoplankton carbon and Chi a was
75, which may appear high for bloom conditions. Bloom conditions in the NEW,
however, differ from those in temperate or tropical seas in that (i) phytoplankton
growth is limited by temperature (-1.7 to +5.2°C) to values <0.5 doubling day 1
(Eppley, 1972) and (ii) phytoplankton grow under continuous light. Under such
conditions, Goldman (1980) reported C:Chl a values generally >80, whereas for
temperate conditions the accepted values range from 40 to 60 (see Figure 9 in Li
era/., 1993).
The fate of large-sized phytoplankton carbon
One major export pathway of phytoplankton carbon from the euphotic zone
is grazing. The carbon assimilation efficiency [(growth + respiration +
excretion)/ingestion] of small-sized poikilotherms is generally » 5 0 % (Peters,
1983). Conversely, « 5 0 % of the carbon ingested by phytoplankton grazers is
egested in various forms and sizes (e.g. membrane-bound pellets and unconsolidated faeces), which sometimes sink rapidly. Carbon assimilation efficiencies
close to 50% for copepods are associated with high food concentrations (Landry
et aL, 1984), which was not the case in the NEW. It follows that, generally, most
of the carbon ingested by grazers in the euphotic zone was recycled through respiration and excretion or allocated to biomass (e.g. reproduction, structural growth,
storage), which could be further respired by carnivores preying on herbivores in
the euphotic zone. Carbon ingested in the euphotic zone can be exported at depth
by vertically migrating copepods (e.g. Longhurst et aL, 1990) but, as mentioned
previously, that did not occur in the NEW during summer (Ashjian et aL, 1995).
Sloppy feeding by copepods also contributes to the release of phytoplankton
carbon in the euphotic zone (Banse, 1995). Hence, in the NEW, unless phytoplankton carbon sank below the euphotic zone in the form of cell aggregates or
as repackaged by grazers, its fate was mostly to be recycled in surface waters.
Particles that sink out of the euphotic zone are generally phytoplankton aggregates, mostly intact diatoms, and faecal pellets (Honjo, 1996). Dinoflagellates are
known to egest unconsolidated faeces, but they can also produce membranebound pellets when feeding on diatoms (Buck and Newton, 1995). Their pellets
1280
Fate of large-sized phytoplankton in Northeast Water Polynya
and those of copepods and appendicularians have similar sizes (lOVlO7 um3;
Buck and Newton, 1995) and sinking velocities (K^-IO2 m day 1 ; Fortier et al,
1994), so that these could potentially sink rapidly out of the euphotic zone. Faecal
pellets, however, seldom contribute significantly to material collected in deep
sediment traps (Bathmann etal, 1987; Gonzales etal, 1994; von Bodungen etal,
1995; Ki0rboe et al, 1996). In the NEW, faecal pellets made up <5% of the carbon
collected in a sediment trap at 130 m during the summer of 1993 (E.Bauerfeind,
personal communication). This could reflect the patchy distributions of grazers
which fed on algae in the layer above, or fed directly in the traps (i.e. 'swimmers';
Michaels et al, 1990). It could also reflect the patchy distributions of animals that
disrupted or fed on faecal pellets (e.g. Oithona; Gonzales and Smetacek, 1994).
The ingestion of sinking pellets (i.e. coprophagy; Paffenhofer and Knowles, 1979)
and their disruption by copepods (i.e. coprorhexy and coprochaly; Lampitt et al,
1990; Noji et al, 1991) prolong the residence time of faecal material in the
euphotic zone and favour its recycling (Smetacek et al, 1990). Failure to recognize partially degraded pellets in the trap samples is also a possible explanation
(Angel, 1984; U.Bathman, personal communication). The undegraded nature of
the material collected in the sediment trap during the NEW summer bloom (C:N
= 8-9; E.Bauerfeind, personal communication) indicates, however, that phytoplankton in the trap did not undergo partial degradation in the guts of grazers.
Hence, in the NEW, pellets produced in the euphotic zone during summer were
mostly recycled in surface waters.
In addition to producing faecal pellets, appendicularians shed their mucilaginous house several times per day (Taguchi, 1982; Fenaux, 1985). The abandoned
houses generally contain large amounts of food particles (e.g. diatoms, faecal
pellets, protozooplankton) and sometimes contribute greatly to the downward
carbon flux (Alldredge and Silver, 1988; Hansen et al, 1996). The sinking velocity of appendicularian houses is similar to that of intact faecal pellets (Fortier et
al, 1994), but little is known concerning the degradation of houses or their ingestion by water-column grazers. Compared to phytoplankton repackaged into
faecal pellets, those adhering to houses are undegraded and, thus, more resistant
to degradation within the euphotic zone. It is sometimes assumed that abandoned
houses contribute significantly to the downward flux because they scavenge
particles as they sink through the euphotic zone. Hansen et al (1996) determined
the contribution of scavenged particles to the total abundance of particles trapped
in appendicularian houses, and concluded that this process is insignificant because
most particles trapped in the houses resulted from the filtering activity of animals
that inhabited the houses. Faecal pellets found in abandoned houses would be
those of their inhabitant (Taguchi, 1982; Hansen et al, 1996). Thus, the magnitude of the particle flux entrained by houses would mostly depend on the grazing
activity of appendicularians. As mentioned above, appendicularians in the NEW
probably ingested half the particles cleared from water, whereas the other half
would have been trapped in their houses (Acufia et al, 1996).
Because large-sized phytoplankton often form chains and/or large floes, their
sinking velocities are potentially similar to or higher than those of faecal pellets
and appendicularian houses (Smayda, 1970; Ki0rboe, 1993; Fortier et al, 1994).
1281
&Pesant et at.
It was hypothesized thatfloeswere essentially made of senescent cells (Smetacek,
1985), incapable of regulating their buoyancy. However, floes sometimes consist
of mostly healthy cells (e.g. Alldredge and Gotschalk, 1989; Riebesell, 1992),
which can regulate their buoyancy in response to the distributions of environmental factors such as nutrient concentrations and irradiance [e.g. Estrada and
Berdalet (1997) and references therein]. Combination of buoyancy regulation
and turbulent conditions often results in accumulation of biomass in the euphotic
zone, which can take the form of a deep chlorophyll maximum (Cullen, 1982;
Lande and Wood, 1987). This feature was common in the polynya (Pesant et aL,
1996). Mechanisms involved in the accumulation of phytoplankton in the
euphotic zone are not clear, so that we simply considered that intact phytoplankton had the potential to be exported downwards or accumulate in the
euphotic zone.
The NEW is characterized by an anticyclonic circulation of surface waters
(Schneider and Bud6us, 1994; Budgus and Schneider, 1995), with an average
velocity of 10 cm srl. It follows that, in the polynya, phytoplankton that accumulated in the euphotic zone could be transported laterally over long distances (i.e.
on average 8.6 km day 1 ) and thus be partly exported outside the polynya. The
surface currents and movements of ice in the NEW (Bignami and Hopkins, 1997;
Ramseier et aL, 1997) suggest that phytoplankton thus exported were generally
advected towards the ice-covered waters south of the polynya (Figure 1).
Potential export of large-sized phytoplankton carbon
To summarize the above ideas, we further developed the loss term (LL) of equation (8) into three flux rates, i.e. recycling within the euphotic zone (/?L), downward export (£>L) and lateral advection out of the polynya (AL):
PL-ABL/At
= LL = RL + DL + AL*0
(9)
Phytoplankton carbon ingested by grazers (in the case of appendicularians half
the carbon grazed is exported; see above) and released by sloppy feeding
contributes to recycling (/?L)» whereas intact phytoplankton aggregated in floes
or trapped in abandoned appendicularian houses contribute to the downward
export and advection terms (Z>L + -^L)- We used two approaches to quantify the
fate of large-sized phytoplankton in the NEW. The first was to calculate R\JP\, at
stations where phytoplankton production and the abundance of grazers were
determined concurrently, during the second sampling period only (Figure 5; n =
28). The second approach was to construct a carbon budget based on equation
(9) and using median values reported in Tables III and IV. Because phytoplankton production and grazing in the polynya varied considerably in space and
time (Figure 4), it could be argued that medians should not be used to budget
these characteristics. In order to reduce this variability, carbon budgets were
constructed for each sampling period and did not include the few stations in the
polynya where appendicularian grazing exceeded production. The latter case will
be discussed separately.
1282
Fate of large-sized phytoplankton in Northeast Water Polynya
20"W
82'N
80'N
78'N
76#N
Fig. 5. Horizontal distribution of RJPL in the NEW during the second period, (a) Appendiculanans
grazed >100% of the large-sized phytoplankton production, (b) Dinoflagellates grazed >100% of the
large-sized phytoplankton production. Hatched lines, edges of the ice barriers.
First approach. During the second sampling period, the heterotrophic community
generally recycled 25-50% of the carbon produced by phytoplankton inside the
polynya, whereas, outside the polynya, the heterotrophic community recycled
more carbon than was produced by phytoplankton (RJPL » 50%; Figure 5). At
a few locations inside the polynya, however, the heterotrophic community
recycled >50% or <25% of the carbon produced by phytoplankton. As mentioned
above, that case will be discussed later. Outside the polynya, the copepod
community alone could graze » 1 0 0 % of the primary production in the region
(Table IV). One possible explanation is that our calculations overestimated the
community grazing rate of copepods, which could have indeed been food limited
outside the polynya because phytoplankton biomass there was low (Table III).
Two experimental studies in the NEW, however, are counter to that hypothesis:
copepods outside the polynya (e.g. mostly Calanus glacialis) were producing faecal
pellets (Daly, 1997) and eggs at a rate which was too high to be driven solely by
their lipid reserves (Hirche and Kwasniewski, 1997). This situation, which was also
observed in other areas of the Arctic (Longhurst and Head, 1989; Hansen et ai,
1990), could be attributed to the potentially wide spectrum of food items ingested
by copepods. In addition to large-sized phytoplankton, sea ice algae and microzooplankton are potential food for copepods (Conover and Huntley, 1991;
Gifford, 1991), which may be especially important when the production of largesized phytoplankton is low (Fessenden and Cowles, 1994; Nielsen and Ki0rboe,
1994; Ohman and Runge, 1994). These resources were available in ice-covered
areas outside the polynya (Gutt, 1995; P.K.Bj0msen and T.G.Nielsen, personal
comments and M.G., unpublished data), where they presumably were grazed
1283
S.Pesant el al.
intensively by copepods. Hence, the structure of the food web there was probably
not solely based on the production of large-sized phytoplankton. It follows that
we could not assess the fate of large-sized phytoplankton outside the polynya, so
that carbon budgets in the second approach were constructed for the area of
seasonally ice-free waters only, i.e. inside the polynya.
Second approach. Most terms of the carbon budgets are the median values
reported in Tables III and IV, except the potential export and advection of intact
phytoplankton aggregated in floes and/or in appendicularian houses (£>L + AL).
The latter potential was determined by balancing equation (10):
RL
(10)
Using the second sampling period as an example:
A5 L
At
(median BL[2] - median
0.5(Ar[l] + At[2])
(ID
where AS L is the difference between median B L for the second [2] and first [1]
periods (Table III; ABL = 1198 mg C nr 2 ) and At is the duration of a period (At[l]
= 30 days; Ar[2] = 25 days). Thus, the estimated change in phytoplankton biomass
during the second period was 43.6 mg C m~2 day 1 . If BL < 392 mg C m~2 prior to
the first sampling period, then ABJAt may have been as low as 0 mg C nr 2 day 1 .
For the carbon budget, we assumed that the magnitude of S L during the 30 days
prior to the beginning of sampling was probably similar to the phytoplankton
biomass estimated outside the polynya at the beginning of sampling, i.e. 124 mg
C m~2 (Table III). The calculated grazing rate of appendicularians was split into
ingested carbon and carbon trapped in houses (each fraction being half of the
grazing). Although the grazing rate of appendicularians could not be calculated
for the third sampling period because of absence of data, Ashjian et al. (199S)
reported that, in late summer 1992, appendicularians in the polynya grazed - 4 %
of the primary production and, occasionally, 100%. We therefore considered that
the carbon budget for the third period would resemble that of the second period
as far as appendicularians are concerned.
The fate of phytoplankton production in the polynya differed in several ways
among the three sampling periods. From the beginning to the end of sampling
(Figure 6a-c), a progressively smaller fraction of the large-sized primary production (Pi) was accumulated as phytoplankton biomass (ABjAt) and, conversely, a
progressively larger fraction was lost (L L ). Along the same time sequence, a
smaller fraction of P L was recycled in the euphotic zone and, conversely, a larger
fraction was exported downward and/or advected laterally. In Figure 6, the fluxes
are ordered, from right to left, according to the sinking velocity and the resistance to degradation of plankton and their waste products in the euphotic zone
(see above): dinoflagellates < copepods < appendicularians < ungrazed phytoplankton.
During the first sampling period, the grazing community recycled 100% of the
1284
Fate of large-sized phytoplankton in Northeast Water Porynya
(a) 22 May to 22 June
Large-sized
phytoplankton
Large-sized
phytoplankton
Ungrazed
phytoplankton
Ungrazed
phytoplankton
Appendi- Copepods Dinoflagcularians
ellaies
Appendi- Copepods Dlnoflagcularians
ellates
(c) 22 July to 17 August
Large-sized
phytoplankton
Ungrazed
phytoplankton
Appendi- Copepods Dinoflagculartans
ellates
Export
Recycling
ingested
' trapped in houses
Fig. 6. Carbon budgets for the three sampling periods. Values in the open arrows are rates, expressed
as a per cent of PL and calculated from values in Tables III and IV. Values in the boxes are biomasses
(mg C m*2) from Table III. Values in black arrows were calculated by balancing the carbon budget
[equation (11)]. The fluxes are ordered from right to left according to their contributions to recycling
versus export. ND, no available data.
phytoplankton production, which did not allow downward or lateral export of
intact phytoplankton [RL > LL; equation (9), Figure 6a]. It is possible, however,
that a small fraction of phytoplankton production (17%; Figure 6a) could have
1285
S.Pesant et al.
been exported downwards or advected laterally, as repackaged in appendicularian houses. Owing to the generally low phytoplankton abundance during the first
period, it is possible that the food web structure in the polynya at that time resembled that presumed to have existed outside the polynya, i.e. grazers feeding on
alternate food such as ice algae and microzooplankton. In contrast, 32 and 67%
of phytoplankton production could be exported downwards and advected laterally during the second and third periods, respectively. The downward carbon flux
in the polynya, which was determined from a sediment trap at 130 m, was <5%
of PT (E.Bauerfeind, personal communication), so that a large fraction of the
production was probably advected laterally. This requires that phytoplankton in
the polynya were buoyant, which indeed they were (S.P., unpublished data). Once
in ice-covered light-limited waters, the diatoms could lose the capability to regulate their buoyancy and thus sink to depth (Waite et al., 1992). It follows that,
given the general circulation of surface waters from the polynya towards icecovered areas (Figure 1), lateral advection of phytoplankton could have led to
downward export of phytoplankton in the latter region, south of the polynya.
For the second period, the carbon budget yields a value RJPt = 38%, which
generally corresponds to values determined in the polynya using the first
approach (Figure 5). At some stations, however, values of RJP^ were either
>50% or <25%. At these locations, the carbon budgets were probably different
from that computed here, which concerns the whole polynya. At two stations
(Figure S; pointer a), appendicularians were very abundant, the calculated ingestion rate of these organisms alone being higher than the phytoplankton production. Ashjian et at. (1995) also observed high abundances of appendicularians at
some stations to the north of the polynya, where these grazed >100% PL. That
area was characterized by relatively high abundance of a non-colonial form of
Phaeocystis sp., which may not be included in PL and could be an important food
source for appendicularians. At another station (Figure 5; pointer b), dinoflagellates were very abundant, the calculated ingestion rate of these organisms alone
being higher than P L . This is in agreement with the idea that phytoplankton
blooms may sometimes be mostly channelled through microzooplankton (e.g.
Nielsen and Hansen, 1995; Hansen et al., 1996).
Conclusions
The present study suggests that, in the NEW, different pathways for the cycling
of carbon existed in seasonally ice-free waters (inside the polynya) and continuously ice-covered areas (outside the polynya). Outside the polynya, the fate of
large-sized phytoplankton could not be assessed because the heterotrophic
community presumably grazed on a variety of food items, including ice algae,
microzooplankton and large-sized phytoplankton. Inside the polynya, the fate of
large-sized phytoplankton production was to be mostly recycled at the beginning
of the sampling period (May-June) and to be mostly advected and exported
downwards as the bloom of large-sized phytoplankton progressed. Generally,
copepods mostly contributed to recycling, but dinoflagellates and appendicularians sometimes recycled most of the large-sized phytoplankton production.
1286
Fate of large-sized phytoplankton in Northeast Water Polynya
According to the carbon budgets, the polynya (assuming a size of 25 000 km2)
could have exported downwards and laterally -1600 and 6300 t C day 1 during
the second and third sampling periods, respectively. Downward export would
lead to a transferring of POC to depth within the polynya, whereas lateral advection would lead to a transfer of POC to depth outside the polynya, in ice-covered
waters.
Acknowledgements
We thank the masters and crews of the RV 'Polarstern' and USCGC 'Polar Sea'
for their efficient assistance, J.Acuna, G.Bergeron, D.Deibel, C.Fraiken, P.Lane,
S.Lessard and F.McGuiness, B.Niehoff, V.0resland, P.Rowe and J.Wegener for
assistance in the field and providing data, and C.Belzile for assistance with laboratory and data analyses. The authors also thank G.Kattner, W.Ritzrau, Mark
Ohman and two other, anonymous, reviewers for helpful comments on the manuscript. This research was funded by a Collaborative Special Project grant from the
Natural Sciences and Engineering Research Council of Canada (NSERC) and
by grants to L.L., M.G., L.F. and R.E.H.S. from NSERC, to GIROQ (Groupe
interuniversitaire de recherches oceanographiques du Quebec) from NSERC and
the Fonds FCAR of Quebec, to W.O.S., K.D. and S.L.S. from National Science
Foundation (OPP-911378), and to S.P. from the DA AD (Deutscher Akademischer Austauchdienst). This is a contribution to the programme of GIROQ and
contribution no. 1392 of the Alfred Wegener Institute for Polar and Marine
Research.
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