Download Mesozooplankton in the Arctic Ocean in summer

Deep-Sea Research I 46 (1999) 1391}1415
Mesozooplankton in the Arctic Ocean in summer
Delphine Thibault , Erica J.H. Head, Patricia A. Wheeler*
INRS-Oce& anologie, 310 Alle& e des Ursulines, Rimouski, Que& bec, Canada G5L 3A1
Biological Oceanography Division, Bedford Institute of Oceanography, Dartmouth, Nova Scotia,
Canada B2Y 4A2
College of Oceanic and Atmospheric Oceanography, Oregon State University, Corvallis, OR 97331, USA
Received 29 December 1997; accepted 13 November 1998
Abstract
The biomass, species and chemical composition of the mesozooplankton and their impact on
lower food levels were estimated along a transect across the Arctic Ocean. Mesozooplankton
biomass in the upper 200 m of the water column was signi"cantly higher (19}42 mg DW m\)
than has previously been reported for the Arctic Ocean, and it reached a maximum at ca. 873N
in the Amundsen Basin. The lowest values were recorded in the Chukchi Sea and Nansen Basin,
where ice cover was lower (50}80%) than in the central Arctic Ocean. In the deeper strata
(200}500 m) of the Canadian and Eurasian Basins, the biomass was always much lower
(4.35}16.44 mg DW m\). The C/N (g/g) ratio for the mesozooplankton population was high
(6.5}8.5) but within the documented range. These high values (when compared to 4.5 at lower
latitudes) may be explained by the high lipid content. Mesozooplankton accounted for approximately 40% of the total particulate organic carbon in the upper 100 m of the water column.
Mesozooplankton species composition was homogeneous along the transect, consisting mainly
of copepods (70}90% of the total number). It was dominated by four large copepod species
(Calanus hyperboreus, C. glacialis, C. ,nmarchicus and Metridia longa), which together accounted for more than 80% of the total biomass. According to measurements of gut pigment
and gut turnover rates, the mesozooplankton on average ingested between 6 and 30% of their
body carbon per day as phytoplankton. Microzooplankton may have provided an additional
source of energy for the mesozooplankton community. These data emphasize the importance of
mesozooplankton in the arctic food web and reinforce the idea that the Arctic Ocean should
no longer be considered to be a &&biological desert''. 1999 Elsevier Science Ltd. All rights
reserved.
* Corresponding author. Fax: 001 541 737-2064; e-mail: [email protected]
0967-0637/99/$ } see front matter 1999 Elsevier Science Ltd. All rights reserved.
PII: S 0 9 6 7 - 0 6 3 7 ( 9 8 ) 0 0 0 0 9 - 6
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D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
1. Introduction
Information on the mesozooplankton community in the Arctic Ocean is relatively
scarce. The earliest data were collected during the drift of the Fram (expedition of
Fridtjof Nansen, 1893}1896). Subsequently, data were collected from Soviet ice
breakers (Sadko in 1935, Sedov in 1937}1939), ice islands (Johnson, 1963; Hopkins,
1969a, 1969b, Brodskiy and Pavshtiks, 1976; Dawson, 1978; Kosobokova, 1982;
Rudyakov, 1983) and submarines (Grice, 1962). Except for the drifting stations and
submarines, previous data were mainly collected in the eastern section of the Arctic
Basin (e.g., Hirche and Mumm, 1992). The western part of the Arctic Ocean has been
especially poorly sampled due to more extensive ice cover.
In previous studies, four large species represented the main bulk of zooplankton,
with two species of Calanus, Calanus hyperboreus and Calanus glacialis, being characterized as arctic species (Lee, 1974; Dawson, 1978; Rudyakov, 1983; Conover and
Huntley, 1991; Hirche, 1991; Hirche et al., 1994; Hirche and Nieho!, 1996). In the
Arctic, C. glacialis overwinters as stage V copepodite (Conover and Huntley, 1991)
completing its life cycle in 2 years. C. hyperboreus shows a 3 year life cycle overwintering as stage III}V copepodite (Hirche, 1991; Hirche and Nieho!, 1996). The other
major species, Metridia longa, was classi"ed by Grice (1962), Gronvik and Hopkins
(1984) and Ba mstedt et al. (1985) as an arctic deep water species that overwinters as
stage V copepodite and adults. The fourth main species, Calanus ,nmarchicus was "rst
characterized as a boreal species by Dawson (1978), but it is now generally regarded as
a North Atlantic species (Smith and Vidal, 1986; Smith, 1988; Smith and SchnackSchiel, 1990). The life cycle duration for this species is still debated, but C. ,nmarchicus
is known to overwinter in diapause in deep-water (Ba mstedt et al., 1990). This species
is imported into the Arctic Ocean by the main in#ow of Atlantic water running
through the Fram Strait (Ba mstedt, 1986; Hirche, 1991; Gislason and Astthorsson,
1995), so that its distribution in the Arctic Ocean is associated with the cyclonic
circulation of Atlantic waters (Jaschnov, 1970). Thus patterns of its dispersal in the
Arctic basins should be associated with patterns of #ow of Atlantic water into the
Arctic Ocean.
The Arctic Ocean was, until the Canada/USA joint expedition (AOS'94) in 1994,
characterized as an area of very low primary production (Apollonio, 1959; English,
1961) with an annual phytoplankton production rate of 1 g C m\ yr\. Preliminary
data reported by Wheeler et al. (1996) and Gosselin et al. (1997), however, have shown
that the central Arctic Ocean is at least 10 times more productive than was previously
reported. The di!erence lies in part in the contribution of ice algal production and the
assessment of the contribution of DOC release by pelagic and ice algae.
Concentrations of chlorophyll a and primary production rates in the Arctic Ocean
during the summer of 1994 were similar to values reported for other oligotrophic
areas (Gosselin et al., 1997). Thus, a complex pelagic food web should be expected,
which may have a classical food chain as well as microbial food web elements. In this
study, in addition to examining the biomass and the species composition of mesozooplankton, their role in the Arctic food web was investigated during the AOS'94
cruise using the so-called &&gut #uorescence'' method.
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
1393
2. Materials and methods
2.1. Cruise track and sampling
From 26 July to August 1994, the USCGC Polar Sea made a transect across the
Arctic Ocean running from Nome, Alaska, to Reykjavik, Iceland. The transect started
on the continental shelf of the Chukchi Sea, crossed the Chukchi Abyssal Plain, the
Arlis Plateau, the Mendeleyev Ridge, the Makarov Basin, the Lomonosov Ridge, the
Amundsen Basin, and ended in the deep Nansen Basin (Figs. 1 and 2a). Eighteen
stations were sampled for zooplankton along this transect (Fig. 1, Table 1).
At each station, water samples were collected using 10 L Niskin bottles mounted on
a rosette sampler equipped with a CTD probe (Sea-Bird Electronics). Sampling and
determination of chlorophyll a and primary production in the water column are
reported elsewhere (Gosselin et al., 1997).
Mesozooplankton samples were collected at each station by vertical net hauls using
a 200 lm mesh size WP2 net with a 0.75 m diameter mouth. No #ow meter was
available, but as the hydrodynamic properties of the WP2 (200 lm mesh size) net
(UNESCO, 1968) were carefully designed, this net can be considered quantitatively
Fig. 1. Cruise track, stations position and main topographic features.
1394
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
Fig. 2. Spatial variation of bottom depth (a), surface temperature (b) and salinity (c) across the Arctic Ocean
from CTD measurements.
accurate in the absence of actual volume measurements. The hauling speed was ca.
1.5 m s\. Where possible, three di!erent depth strata were sampled (0}100, 100}
200 m and 200}500 m) using an opening}closing device. Samples were collected at
di!erent times of the day, but the entire expedition occurred during the period of 24}h
daylight conditions.
2.2. Biomass
Immediately after capture, mesozooplankton samples from each depth were split
using a Motoda splitter. The "rst-half of each net tow was split again for dry weight
measurements and chemical composition analysis. These two sub-samples were "ltered separately onto preweighed GF/A "lters (47 mm), quickly rinsed with distilled
water and dried (603C) for 3 d onboard. The "lters were reweighed upon return to the
laboratory using a microscale electrobalance. Total dry weight (DW) represented the
di!erence in the weight of the "lter before and after "ltration. Zooplankton biomass
(DW) was expressed per m and m, assuming that the net sampled a vertical cylinder
(0.75 m in diameter) of water.
One of the "lters was ground with distilled water and homogenized, and 3 subsamples were taken for analysis of the chemical composition. Each sub-sample was
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
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Table 1
Coordinates of sampling sites for mesozooplankton study in the Arctic Ocean
Station
no.
Sampling
date
Sampling
time (h min)
Latitude
Longitude
2
3
4
5
7
8
13
17
19
21
23
24
25
26
30
31
32
33
07/26
07/27
07/28
07/30
08/01
08/03
08/06
08/09
08/11
08/13
08/15
08/16
08/18
08/19
08/20
08/22
08/25
08/26
15.30
19.40
21.00
2.00
6.00
8.00
4.45
5.45
12.10
11.30
7.10
4.00
10.00
7.00
11.00
4.30
10.00
13.30
70300N
72300N
74301N
75325N
76339N
78308N
80309N
81315N
82326N
84306N
85354N
87309N
88304N
88348N
89301N
90300N
85343N
84316N
168345W
168351W
168350W
170344W
173320W
176348W
173317W
179300E
175350E
174359E
166350E
160332E
147347E
143329E
137341E
037350E
034337E
Geographical
region
Chukchi Sea
Canada Basin
Makarov
Basin
Amundsen
Basin
Nansen Basin
Ice cover
(%)
Ice thickness
(m)
55
70
80
100
100
90
100
100
95
90
95
100
95
95
90
95
90
80
1.08
2.55
1.6
1.75
2.68
2.32
2
2.49
2.05
1.63
1.94
1.94
1.73
2.4
2.28
1.92
3.14
placed in a tin cup and dried at 603C for 3 d. The chemical composition (i.e. particulate organic carbon and nitrogen) of the samples was measured using a Perkin-Elmer
CHN 2400 Analyzer.
2.3. Abundance and species composition
The second-half of the net tow was preserved in a 4% bu!ered seawater : formalin
solution for later species determination, staging and sizing of the whole mesozooplankton community. Once back on shore, these sub-samples were sieved onto
a 350 lm mesh. The total fraction larger than 350 lm was counted, whereas only
5}10% of the fraction smaller than 350 lm was counted for the dominant zooplankton species. Regarding the copepod groups, the di!erent copepodite stages were
counted and measured under a dissecting microscope (equipped with a calibrated
eyepiece reticule). Prosome lengths and morphological characteristics were used to
distinguish between the three species of Calanus (C. hyperboreus, C. glacialis and C.
,nmarchicus) as described by Grainger (1961) and Jaschnov (1970). It was di$cult to
distinguish between the "rst three copepodite stages (CI}CIII), so that these individuals were classi"ed only as Calanus spp. Species determinations were conducted
using the descriptions of Rose (1933).
Individual dry weights of the dominant copepod species were determined on
preserved samples. A 20% loss in dry weight due to formaldehyde preservation was
assumed (Hopkins, 1968; Omori, 1978). For the di!erent species and stages, 5}15
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D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
individuals, depending on size, were pooled, rinsed with distilled water, placed on
a preweighed GF/A "lter and dried at 603C for 3 d. Triplicate measurements were
made whenever enough animals were collected.
2.4. Gut pigment contents and gut evacuation rates
An additional net haul from 0 to 100 m also was taken at each station to assess
mesozooplankton grazing using the gut #uorescence technique. The time of sampling
depended on the time of arrival at the station; thus sampling often occurred at
di!erent times of day. As soon as possible after collection ((5 min), the mesozooplankton samples were sieved through 1000, 500 and 200 lm mesh sizes. Each
subsample was collected on a 200 lm mesh size nylon disk, quickly rinsed with
distilled water and immediately frozen. Within 10 d of collection, samples were
quickly sorted to species and stages with a dissecting microscope under dim light
using cold "ltered sea water (at approximately 03C) and treated as described by
Mackas and Bohrer (1976). Aliquots of 15 individuals were sorted out for stage IV of
Calanus species and Metridia; for larger individuals or older stages (stage V and
adults), groups of "ve individuals were picked and analyzed for gut pigment contents.
Gut pigment analysis was done on board with a Turner Design #uorometer. Pigments
were extracted in 10 ml of 90% acetone at !203C overnight. Chlorophyll a and
pheopigment concentration were measured according to the method of Yentsch and
Menzel (1963) modi"ed by Holm-Hansen et al. (1965). The gut pigment contents (ng
Chl a eq ind\) were calculated according to Wang and Conover (1986), where ng
chlorophyll a equivalents (ng Chl a eq)"Chl a#pheopigment.
Instantaneous gut evacuation rate (GER) was measured at each station. Freshly
harvested animals were screened over a 2000 lm mesh netting to exclude large
animals and concentrated on a 350 lm mesh, quickly rinsed with fresh "ltered sea
water and transferred to 8 L plastic carboys containing "ltered sea-water. The carboys
were kept in a controlled temperature incubator in the dark. Zooplankton usually
were subsampled at 0, 5, 10, 15, 30, 45, 60, 90, 120, 180 min and frozen immediately in
liquid nitrogen. Pigment measurements were conducted as for the gut contents. Gut
evacuation rate constant (k) was estimated by "tting values to a negative exponential
curve following the equation:
C "C e\IR,
R
where C is the gut pigment content after time t (in min) and C is the initial gut
R
content. Gut pigment contents were transformed into in situ ingestion rates (I)
assuming the animals were feeding at equilibrium, i.e. defecation rate equaled ingestion rate, following this equation:
I"C k.
If we assume ingestion rate is constant over 24 h and if we know the abundance of
the species, we can obtain its total daily ingestion rate (lg Chl a eq d\). The grazing
impact of each species then can be estimated, i.e. its daily removal of phytoplankton.
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
1397
In order to express gut pigment contents in term of carbon and thus to assess the
rate of phytoplankton ingestion in terms of copepod daily ration, the phytoplankton
carbon content must be determined. The PC/Chl a ratio of phytoplankton was
derived from the slope of the regression line between PC and Chl a. The ordinate at
the origin gives an estimate of the detrital part of the seston. The ingestion of
phytoplankton carbon by copepods can then be calculated in terms of their daily
ration (% copepod body carbon per day), or of their grazing impact on the phytoplankton (% primary production of C per day, or % standing stock of phytoplankton C per
day). This ingested phytoplankton carbon can then be used by the copepods to fuel
their physiological needs (i.e. respiration, reproduction and growth).
Linear correlation (Pearson Product Moment) and linear regression for assessing
relationships among variables were determined with the Sigma-Stat and Statgraphics
statistics package.
3. Results
3.1. Characterization of the study area
Sea surface temperatures decreased slightly along the transect from !1.273C in the
Chukchi Sea to !1.653C in Nansen Basin with a minimum of !1.733C over the
Lomonosov ridge (Fig. 2b). The 0}100 m layer had the coldest temperatures, which
varied little along the transect (Swift et al., 1997). The temperature increased evenly
between 100 and 200 m. The layer of Atlantic water characterized by the 03C isotherm
(potential temperature) was located between 200 and 800 m (see Fig. 2a in Swift et al.,
1997). In the eastern sector the 03C isotherm shoaled towards the surface reaching ca.
150 m depth. Warm cores within the Atlantic layer were observed along the transect,
where the temperatures reached 13C in the western sector and '1.53C in Nansen
Basin. Salinity increased from 23.5 in the Chukchi Sea to 33.0 in Nansen Basin (Fig.
2c). Ice cover was lowest (55}70%) at Stations 2 and 3 the Chukchi Sea (Table 1).
Thick ice covered most of the transect at this time of year, but thin ice was observed in
the Chukchi Sea and over the Lomonosov Ridge (Table 1).
In Table 2 we report latitudinal variations of algal biomass and primary production. More details can be found in Gosselin et al. (1997). Total phytoplankton biomass
was very high ('100 mg Chl a m\) at Stations 2 and 3, but was much lower between
Stations 4 and 32 (1.18}26.82 mg Chl a m\). There was an increase in algal biomass
at the last station in Nansen Basin (Table 2). The biomass of large cells ('5 lm)
showed a pattern of variation similar to that of total biomass. At Station 21 the
primary production rate measured for the large cells was'60% of the total primary
production rate (Table 2), but at most stations with '80% ice cover the large cells
accounted for (50% of the total primary production.
3.2. Zooplankton biomass
The integrated mesozooplankton standing stock (g DW m\, 0}500 m) ranged
from a minimum of 0.4 in the Chukchi Sea, to a level ca. 7 in Nansen Basin, with
2
3
4
5
6
7
8
11
13
16
17
19
21
23
24
25
26
30
31
32
33
Station
0.01
0.10
3.29
0.21
0.55
0.38
27.58
1.57
273.42
3.50
49.49
1.94
1.25
0.45
3.74
0.62
0.83
0.74
27.92
2.91
309.52
3.50
51.76
4.04
1.63
Large cells
production
mgC m\ d\
0.61
56.09
Total production
mg C m\ d\
Ice algae
0.96
4.20
0.64
0.37
14.25
0.07
0.03
0.1
0.14
1.88
0.17
0.02
0.39
0.07
2.90
Total biomass
mg Chl a m\
15.01
23.35
520.65
27.36
10.22
9.39
73.17
56.52
26.48
12.37
55.16
2569.06
750.00
87.52
24.40
Total production
mg C m\ d\
Phytoplankton
2.6
4.5
287.3
4.2
1.2
0.1
44.7
6.0
9.4
2.0
10.1
2282.9
600.0
0.6
4.5
Large cells
production
mg C m\ d\
4.51
8.89
62.03
445.04
162.43
8.08
22.41
26.82
12.21
11.43
9.67
11.21
9.04
4.34
1.18
22.32
9.45
5.61
4.85
10.55
Total biomass
mg Chl a m\
1.22
2.16
37.72
0.98
1.01
0.27
15.49
1.6
1.34
3.31
1.91
437.23
101.48
1.97
4.28
Large cells biomass
mg Chl a m\
Table 2
Latitudinal variations of ice algae biomass and primary production and phytoplankton biomass and primary production. Data from Figs. 5 and 6 in Gosselin et
al. (1997)
1398
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
1399
Table 3
Mesozooplankton biomass for the three layers (0}100, 100}200 and 200}500 m) and integrated over the
upper 500 m. PC (g C m\) for the upper 100 m is taken from Wheeler et al. (1997). Percent zooplankton
carbon (C-Zoo) is calculated as [C-Zoo/(PC#C-Zoo)]a;100
Biomass (mg DW m\)
Station
no.
0}100 m
2
3
4
5
7
8
13
17
19
21
23
24
25
26
30
31
32
33
18.79
7.12
19.07
24.9
37.42
28.56
34.68
38.36
36.48
31.37
37.75
37.6
42.23
41.29
42.51
39.01
25.18
26.24
100}200 m
n.s
n.s
7.19
n.s
23.82
19.54
22.68
40.37
40.11
20.69
27.32
21.29
32.54
22.5
24.01
31.94
10.4
19.18
200}500 m
Integrated biomass
(g DW m\)
PC
(g C m\)
C-Zoo Abundance
%
(ind m\)
n.s
n.s
n.s
n.s
4.35
9.66
5.11
16.44
13.23
8.86
10.53
11.75
4.9
7.84
8.62
n.d
5.81
8.43
0.66
0.36
4.33
2.49
7.43
7.71
7.27
12.80
11.63
7.86
9.67
9.14
8.95
8.79
9.24
n.d
5.30
7.07
n.d
n.d
5.02
n.d
4.81
5.03
4.99
3.55
3.68
4.48
4.09
n.d
3.93
n.d
n.d
4.09
3.73
4.21
n.d
n.d
25.66
n.d
38.19
38.00
36.82
59.06
55.83
41.25
48.60
n.d
47.66
n.d
n.d
n.d
36.24
40.16
79.95
35.85
33.77
53.83
42.96
40.61
35.99
74.70
41.74
55.28
60.62
54.55
37.85
30.74
80.38
The sampling depth was 0 to 35 m.
Biomass estimated from preserved sample.
n.s: not sampled.
n.d: not determined (1) from Wheeler et al. (1997).
a maximum of 12.8 in Makarov Basin and otherwise levels of about 9 in Amundsen Basin (Table 3). Highest mesozooplankton biomass concentrations (19}
42 mg DW m\) were observed in the upper layer (0}100 m) and lowest concentrations (4}16 mg DW m\) in the deepest layer (200}500 m) (Table 3). The biomass in
the intermediate layer (100}200 m) ranged between 20 and 40 mg DW m\ and was
on average 30% lower than in the upper 0}100 m layer except at Stations 17 and 19 in
Amundsen Basin, where it exceeded that in the upper layer (Table 3). This di!erence in
observed vertical distribution was probably not associated with daily migration.
Vertical migrations are known to be very limited or absent under conditions of
constant light (BeH et al., 1971; Hirche and Mumm, 1992; Mumm, 1993; Nielsen and
Hansen, 1995; Falkenhaug et al., 1997). Between 82 and 93% of the total biomass was
located in the top 200 m at this time of the year.
Zooplankton biomass in the upper 100 m showed signi"cant (p(0.05) negative
correlation with total phytoplankton biomass (r"!0.758), biomass of large cells of
phytoplankton (r"!0.740) and with primary production (r"!0.721) (Table 4).
On the other hand, zooplankton biomass was signi"cantly correlated with ice cover
1
1
2
!0.553
*
1
1
ns
ns
3
4
1.
1
*
ns
ns
5
0.992
***
0.993
***
1
!0.553
*
ns
6
ns
1
ns
!0.559
*
0.913
***
ns
7
ns
0.927
***
1
ns
!0.549
*
0.994
***
ns
1 } Latitude.
2 } Phytoplankton total primary production (mg C m\ d\).
3 } Ice Algae total primary production (mg C m\ d\).
4 } Ice algae primary production (mg C m\ d\) by large cells.
5 } Ice algae total biomass (mg Chl a m\).
6 } Large cells phytoplankton primary production (mg C m\ d\).
7 } Phytoplankton total biomass (mg Chl a m\).
8 } Phytoplankton large cells biomass (mg Chl a m\).
9 } Water depth (m).
10 } Ice cover (%).
11 } Ice thickness (m).
12 } Zooplankton abundance (ind m\) for the 0}100 m layer.
13 } Zooplankton biomass (mg DW m\) for the 0}100 m layer.
*P'0.01, **P'0.0001, ***P(0.0001.
11
12
13
9
10
8
7
5
6
4
3
2
1
1
ns
0.934
***
0.992
***
ns
!0.548
*
0.992
***
ns
8
1
ns
ns
ns
ns
ns
ns
0.820
***
ns
9
Table 4
Correlation table (correlation coe$cient in bold, P value) between biological and physical variables
10
!0.866
***
!0.839
***
ns
1
ns
!0.806
**
ns
0.483
*
!0.879
***
ns
11
1
ns
ns
ns
ns
!0.568
*
ns
ns
ns
ns
ns
12
ns
!0.508
*
ns
1
ns
ns
ns
ns
ns
0.589
*
ns
ns
13
0.740
**
ns
0.765
**
ns
ns
1
!0.758
**
ns
ns
ns
0.749
**
!0.72
**
ns
1400
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
1401
Fig. 3. Spatial variations of C/N ratio (a) and %C (b) for the mesozooplankton population in the Arctic
Ocean for di!erent depth intervals. (䊏) 0}50 m; (*): 0}100 m, (䊉) 100}200 m, (䉭): 200}500 m.
(r"0.765), and also with temperature (r"0.710, not shown). Zooplankton biomass
showed a positive correlation with latitude (r"0.749), but the latitude per se
might not be the driving force since it re#ects a combination of di!erent physical
features of the environment (including ice cover and temperature) that vary with
latitude as well. Ice cover and latitude showed a low but signi"cant correlation
(r"0.483). The abundance of large zooplankton ('350 lm) was not signi"cantly
(p'0.1) correlated with total biomass, but the abundance of the largest copepod
species, Calanus hyperboreus, was strongly correlated with total biomass (r"0.910,
not shown).
3.3. Carbon and nitrogen contents
With the exception of the two shallow stations in the Chukchi Sea (Stations 2
and 3, sampling depth 0}35 and 0}50 m, respectively), the C/N ratio for mesozooplankton (Fig. 4a) varied between 6 and 8.5, and these values are in the range
previously observed for zooplankton at high latitudes (between 6.3 and 12.5, see
Ba mstedt, 1986).
The mesozooplankton carbon content was relatively constant over the whole
survey area (around 40% of the dry weight), although it was lower at stations at the ice
edge (Stations 3 and 4, Fig. 3b). No variations with depth or latitude were observed
(Fig. 3a and b). At this time of the year, the mesozooplankton accounted for
approximately 40% of the total particulate carbon in the upper 100 m of the water
column (Table 3).
1402
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
3.4. Zooplankton species composition
Only the results from the 0}100 m layer are presented here. Community composition was consistent along the transect, with 21% of the taxa present at every station
and 70% present at more than "ve stations. The population was clearly dominated by
copepods, which represented 80}93% of the total number of individual zooplankters.
Twenty-three di!erent species of copepod were identi"ed. Only a few genera were
found in the 200}350 lm size class. These included Oithona, Oncaea and Pseudocalanus, which, because of their small size (average individual weight around 3 lg
during this study), were not an important component of the total biomass. Since the
smaller species represent a small proportion of the total biomass, the focus of this
paper will be on the larger species. Four species of copepods dominated the size class
over 350 lm: Calanus hyperboreus, C. glacialis, C. ,nmarchicus and Metridia longa.
Those four species represented, in term of numbers, over 70% of the population larger
than 350 lm (Fig. 4a). Non-copepod genera included chaetognaths, pteropods, amphipods, ostracods and gelatinous forms (Fig. 4b). Those genera showed highest
values at Station 13 in Canada Basin (main components: amphipods and pteropods)
and at Station 26 in Amundsen Basin (main components: chaetognaths and ostracods). The copepod community showed three maxima in terms of abundance (Fig. 5a).
Fig. 4. Spatial distribution of abundance of copepods (a) and non-copepods (b).
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
1403
Fig. 5. Spatial variations of abundance of the 4 main species along the transect: Calanus hyperboreus (a),
Calanus glacialis (b), Calanus ,nmarchicus (c) and Metridia longa (d). (䊏) Copepodite C4, (䊉) Copepodite
C5, (*) female.
The "rst was at Station 4 in the Chukchi Sea, at which stage IV C. hyperboreus was
dominant. At the other end of the transect, at Station 32 in Nansen Basin, another
maximum was observed, but in this case young stages and adults of both C. glacialis
and C. ,nmarchicus were dominant. The third maximum, located at Station 23 in
Makarov Basin, was dominate by adults and stage V C. hyperboreus, which accounted
for over 50% of the copepods (Fig. 5a). The highest concentration of C. hyperboreus
was found in the central part of Makarov Basin, and there was a minimum in their
abundance in Nansen Basin (Fig. 5a). In the Chukchi Sea, at Station 4, young stages
(copepodite II and III) of C. hyperboreus were very abundant (13.67 and 49.44 ind
m\, respectively). Calanus glacialis densities were of the same order of magnitude as
C. hyperboreus, and both showed a maximum in Makarov Basin (Fig. 5b). Very low
concentrations also occurred in Nansen Basin. The numerical abundance of Metridia
longa showed two maxima (81.153N in Canada Basin and 893N in Amundsen Basin)
and a very low level in Makarov Basin (Fig. 5d). Young stages of M. longa were not
1404
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
abundant, maximal values of 2}3 ind m\ (copepodite II and III), while older stages
(copepodite IV and V) reached abundance of 14}16 ind m\. Calanus ,nmarchicus
was also present but in lower numbers (range from 0}7 ind m\). Although considered
to be a North Atlantic species, it was found even in the western part of Canada Basin
(Fig. 5c), but highest concentrations were found at the last two stations, the closest to
the Fram Strait, which carries the main in#ow of Atlantic water into the Arctic ocean
(Jaschnov, 1970; Aagaard et al., 1991; Hirche and Mumm, 1992; McLaughlin et al.,
1996).
The total abundance of copepods was negatively correlated with the ice cover
(r"!0.508, Table 4) due to the high number of copepods that occurred at Station
2 (i.e. high number of copepodite C III and IV of C. hyperboreus) and the last stations
(i.e. high number of C. ,nmarchicus/glacialis copepodite and female), where the ice
cover was the lowest (Table 1). However, integrated biomass and individuals are
lowest over the shelf (see Table 3). The total abundance was positively correlated with
total phytoplankton primary production (r"0.589, Table 4).
3.5. Phytoplankton ingestion
The C/Chl a ratio was estimated from the slope of the regression line between PC
and Chlorophyll a (R"0.85, p(0.001: Spearman Rank Order). Over the whole
survey area the PC/Chl a ratio was estimated to be 29.8. Three stations (2, 3 and 33
shallow station) had the greatest PC and Chl a concentrations (Fig. 6), distinguishing
them from all other stations. These three stations were at or close to the ice edge. If
these three stations are removed from the regression, the PC/Chl a ratio becomes 41,
which is similar to the value found using microscopic measurements (Booth and
Horner, 1997).
Gut pigment values of Calanus hyperboreus females exhibited a wide range of values
from 0.5 to 34 ng Chl a eq. ind\. The highest values were found in Nansen Basin and
Fig. 6. Comparison of Chlorophyll a concentration (Gosselin et al., 1997) and PC (Wheeler et al., 1997)
across the Arctic Ocean. (**) Linear regression line (PC"63.5#29.8 * Chl a, R"0.85, p(0.001).
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
1405
Fig. 7. Spatial variations of gut pigment contents for Calanus hyperboreus female, Calanus glacialis and
Metridia longa and phytoplankton biomass '5 lm along the transect.
also at 843N in Makarov Basin (Fig. 7). The variation in gut contents may be
explained in part by the variation in concentration of phytoplankton bigger than
5 lm (R"0.42). Gut pigment concentrations (except for Station 21) increased with
concentrations of phytoplankton larger than 5 lm. Younger stages had lower gut
contents (0.44}17.61 ng Chl a eq ind\). The other common Calanus species, C. glacialis, showed values about 2}3 times lower than those of C. hyperboreus, and highest
values were also observed at the two last stations (Fig. 7). Gut pigment levels of C.
glacialis females did not show any correlation with either total or '5 lm chlorophyll a concentration. The few data available for younger stages (copepodite IV
and V) were similar to those of the females. Metridia longa female gut contents (Fig. 7)
showed a scattered variation with a tendency to increase towards the east. Overall M.
longa showed the lowest values near the Lomonosov Ridge (87}883N), in the eastern
part of the Makarov Basin and in the Amundsen Basin (except at the North Pole
station). Higher gut contents observed for all three species at the eastern end of
the eastern section were related to a higher proportion of centric and pennate diatoms
(see Table 3 in Gosselin et al., 1997).
Gut evacuation rates were calculated only at eight stations and estimated for female
and copepodite VI and V of the large species pooled together (Table 5). Values of
k (gut evacuation rate constant) were variable, lower values being observed at Station
21 in Makarov Basin (0.28 h\), and at Station 30 in Amundsen Basin (0.57 h\). For
the other stations k was relatively constant at about 0.8}1 h\. The gut evacuation
rate constants were in the same range as those (0.66}1.04 h\) given by Head (1988).
Canada
Basin
13
13
17
17
19
19
21
21
23
23
25
25
30
30
31
31
Total phytoplankton.
Phytoplankton '5 lm.
Amundsen
Basin
Makarov
Basin
Geographical
region
Station
no.
1.00
0.570
0.870
0.858
0.283
0.761
1.187
0.751
k
(h\)
562
33
187
55
65
14
541
354
291
50
114
29
272
65
187
67
Chl a
lg m\
24.22
8.68
11.19
11.18
47.05
30.48
66.91
26.65
ng pig ind\ h\
1.13
0.59
1.02
1.18
3.53
2.47
4.46
1.57
lg pig lg C\ d\
Ingestion
6.39
9.67
16.51
21.05
32.82
29.38
50.52
22.037
lg pig d\
7.84
'100.00
54.04
'100.00
90.40
'100.00
12.14
18.54
14.46
84.18
28.96
'100
7.18
30.06
7.84
19.08
Grazing
impact on
phytoplankton
%
16.88
41.48
'100.00
'100.00
'100.00
'100.00
25.84
41.08
18.94
'100.00
25.30
'100.00
25.84
'100.00
6.78
31.60
Impact on
primary
production
%
7.54
3.97
6.78
7.84
23.52
16.48
29.74
10.46
Daily ration
%
Table 5
Gut evacuation rate constant (k), Ingestion, impact of herbivorous grazing on phytoplankton biomass and on primary production and daily body ration along
the transect for the 0}100 m layer. Pig"Chl a eq
1406
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
1407
When copepods feed on phytoplankton some of the chlorophyll a they ingest is not
converted to a-type pheopigment, but rather to a non-#uorescent colorless product.
Since this process happens early during ingestion, a correction factor must be applied
in order to get a more realistic estimate of ingestion. Degrees of chlorophyll a destruction reported in the literature are variable (Kiorboe and Tiselius, 1987; Redden, 1994;
Head and Harris, 1996). Head (1992) and Head and Harris (1996) showed that the
degree of pigment destruction varies with ingestion rate and hence is related to
ambient chlorophyll a concentration. In the case of low in situ chlorophyll concentrations, the correction factor will be high (Redden, 1994; Head and Harris, 1996). They
found degrees of destruction of between 20 and 100% for chlorophyll a concentration
range of 19}0.2 lg L\. Head and Harris (1996) carried out grazing incubation
experiments with mixtures of Calanus spp. feeding on natural mixtures of phytoplankton. In their experiments, when the phytoplankton mixtures were dominated by
diatoms and concentrations were (2 lg Chl a L\. (see Fig. 1, Expt. A1), the degree
of destruction was ca. 90%. By contrast, when the mixtures contained prymnesiophytes and total phytoplankton were (2 lg Chl a L\ (see Fig. 1, Expt. A2),
degrees of destruction were even higher. During the present study, chlorophyll
concentrations were low (0.1}0.5 lg L\). Thus, a correction factor of 10 is considered
to be reasonably conservative.
Overall the ingestion of phytoplankton by the large species ranged from 8.68 to
66.91 lg Chl a eq ind\ d\ (Table 5). The lowest values were observed in Makarov
and Amundsen Basins and the highest value at Station 17 on the east side of Makarov
Basin. If we use a correction factor of 10, the daily impact of grazing on the total
phytoplankton biomass ('0.7 lm) by copepods would have varied between 7 and
90% (Table 5), while for chlorophyll a'5 lm, it would have reached over 100%. At
Station 21 the community ingestion rate was high, but the impact on phytoplankton
and primary production was very low, so that at this station the phytoplankton was
apparently poorly used by the zooplankton population. The impact of grazing on
primary production was higher on the cells larger than 5 lm than on the total
phytoplankton. The daily body ration in terms of carbon ranged from 4 to 30%
(Table 5). The lowest values occurred in Makarov and Amundsen Basins. Mesozooplankton grazing measured by gut #uorescence does not assess for ingestion of
heterotroph #agellates/ciliates, and mesozooplankton species can sometimes feed
extensively on microzooplankton. During this study, biomass of heterotrophic protists in the size class 6}20 lm (Sherr et al., 1997) and mesozooplankton biomass were
relatively well correlated (r"!0.696, P(0.05) suggesting that, even during the
productive season of the year, both phytoplankton and protists may contribute to the
mesozooplankton diet.
4. Discussion
4.1. Zooplankton biomass
The Arctic Ocean was for a long-time considered as a biological desert but recent
studies have shown that there is signi"cant biological activity at various trophic levels
1408
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
(Wheeler et al., 1996; Gosselin et al., 1997; Sherr et al., 1997). Zooplankton also show
relatively high biomass. In our study, the integrated mesozooplankton biomass in
the upper 500 m was much greater than previously reported in the literature for the
same region. Conover and Huntley (1991), in a review of mesozooplankton biomass
throughout the Arctic Ocean, reported values between 0.12 g DW m\ in the central
Arctic Basin and 4.52 g DW m\ in Fram Strait. On the other hand, recent studies in
the Eurasian Basin (Hirche and Mumm, 1992; Mumm, 1993; Nielsen and Hansen,
1995), showed mesozooplankton biomass in the same range as the data presented
here. Di!erences or similarities observed between this survey and previous ones may
have occurred because of di!erences in the size of the mesh of the net that was used for
sampling. Mesh size in previous studies ranged from 64 to 500 lm (Conover and
Huntley, 1991). Small mesh nets (64 lm) will sample the small class fraction e!ectively
but will lead to a higher avoidance rate by larger organisms, and thus may underestimate the mesozooplankton biomass (Hopkins, 1969a, b), which is, in this area,
dominated by large copepods. Larger meshes (333 and 500 lm) will, on the other
hand, undersample small organisms but are more e!ective for sampling the larger
ones (Hirche and Mumm, 1992; Mumm, 1993; Nielsen and Hansen, 1995). The
standard net (WP2 with a mesh size of 200 lm) used in this study gives a more
representative sampling of both small and large species (Thibault et al., 1994). Another
explanation of the di!erence may lie in the preservation techniques. Most of the
previous studies measured biomass from preserved (formaldehyde) or frozen samples,
and a loss of weight is known to occur under these circumstances (Hopkins, 1968;
Omori, 1978). In this study, biomass was measured on fresh samples. The high
biomass was not due to increase in the depth or thickness of the Atlantic layer.
During this survey, the mesozooplankton biomass was concentrated in the upper
200 m, above the Atlantic layer. Deep layers (around and below 1000 m) were not
sampled, so that the biomass of individuals occupying the deep waters (e.g. diapausing
Calanus species) may have been missed. Kosobokova (1982), however, found in
summer the maximum zooplankton biomass was in the upper 300 m in the central
Arctic Ocean, even though sampling was to depths of 1000}2000 m. Also, the data
presented here is only for one period of the year, and it may represent a maximum
annual level, since samples were taken at the end of the productive season. In fact,
Kosobokova (1982) reported an increase of 6}8 times zooplankton biomass between
June and August in the central Arctic Basin.
4.2. Contribution of zooplankton to PC
C/N (g/g) ratio for zooplankton was high (6.5}8.5), and values were within the range
of reported data for high latitudes (6.3}12.5; Ba mstedt, 1986). This ratio is higher than
commonly observed at lower latitudes (4.5 in temperate waters: Ba mstedt, 1986). The
C/N ratio is indicative of the proportion of fat and protein in the zooplankton body.
Nitrogen is present in protein and carbon in both protein and fat, hence the high C : N
ratios observed were probably indicative of the animals' accumulation of lipid
reserves, which would be expected to be maximal at the end of the productive season
(Hopkins et al., 1984, 1985; Conover and Cota, 1985; Arashkevich and Kosobokova,
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
1409
1988). Lower C/N ratios were observed at the two "rst stations on the continental
shelf of the Chukchi Sea, where a higher proportion of young stages of C. hyperboreus
were observed. Percentage of body lipid is known to be smaller for young stages
(Kattner and Krause, 1987). The percentage of carbon (around 40%) at these two
locations was in the same range as has been reported for other latitudes (Ba mstedt,
1986; Ikeda and Skjoldal, 1989). In terms of carbon, the overall zooplankton biomass
represented, over the course of this survey at the end of the productive season, a large
portion of the carbon standing stock, up to 48% of the total particulate carbon in the
Arctic Ocean. During the JGOFS North Atlantic Bloom Experiment, mesozooplankton represented in late spring only a small fraction of the POC (1.6}16.7% in Lochte
et al. (1993), calculated from their Figs. 3 and 10).
4.3. Structure of the zooplankton assemblages
The species composition of the zooplankton observed during the survey was similar to that reported previously (Grice, 1962; Jaschnov, 1970; Brodskiy and Pavshtiks,
1976; Dawson, 1978), with a high predominance of copepods. Copepods have always
been identi"ed to be the major component of the mesozooplankton community in the
Arctic Ocean (Jaschnov, 1970; Dawson, 1978; Longhurst et al., 1984, 1989; Longhurst,
1985; Hirche et al., 1994; Nielsen and Hansen, 1995). The copepod community clearly
was dominated by calanoid copepods, and in terms of biomass, speci"cally by C.
hyperboreus, C. glacialis and M. longa. The two Calanus species are commonly found
in the Arctic Basin (Lee, 1974; Dawson, 1978; Rudyakov, 1983; Hirche et al., 1994).
The fourth main species, C. ,nmarchicus was usually limited to Fram Strait and part
of Nansen Basin (Grainger, 1961), but during this study it spread over the central
Arctic Basin. As this species was always associated with Atlantic water entering the
Arctic Ocean through Fram Strait as the North Atlantic current (Ba mstedt, 1986;
Hirche, 1991; Gislason and Astthorsson, 1995), an alteration in the characteristics or
in#ow of the Atlantic water could modify the dispersion of the species. Actually during
this cruise we observed an Atlantic layer with internal core 13C warmer than
previously reported (Swift, 1996; Swift et al., 1997), which could have allowed C. ,nmarchicus individuals to survive longer as they were advected further north. Jaschnov
(1966) noted also that in years of a strongly pronounced warm Atlantic current, this
species was found in northern areas of the Laptev Sea. Also, during this cruise
Wheeler et al. (1997) measured nutrients concentrations and found that the front
separating the two main in#ows of saline waters, the Atlantic waters (i.e. high N : P
ratio, and low silicate concentrations) and the Paci"c waters (i.e. low N : P ratio and
high silicate concentrations), had shifted west from over the Lomonosov Ridge to over
the Mendeleyev Ridge. This shift seems to have taken place in the last decade
(McLaughlin et al., 1996; Swift et al., 1997; Wheeler et al., 1997).
In an area near the North Pole, Brodskiy and Pavshtiks (1976) found a maximum of
15 ind m\ in August for C. hyperboreus, which is in the same range as our data.
Hirche (1991) observed lower numbers of individuals (females, CVs, CIVs) in the
Atlantic water and the Greenland Sea gyre in November (18.7}128 ind 10 m\). An
abundance of 102 ind 1000 m\ was observed for C. hyperboreus by Hirche et al.
1410
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
(1994) in the northern part of Nansen Basin, which is close to the abundance found at
Station 33 (Fig. 3a). C. glacialis was present in the Atlantic waters and the Greenland
Sea gyre in November in lower numbers (1.8}29.3 ind 10 m\: Hirche, 1991) than
we observed during this study. The number of female M. longa was much lower here
than that found in September in Balsfjorden, northern Norway (Bas mstedt et al., 1985).
For the Atlantic waters o! the coast of Greenland, Hirche (1991) found only
6.8}37.3 ind m\ of M. longa in November.
Stage CV copepodite and adults dominated the population larger than 350 m at
this time of the year, representing up to 80% of the total population. Hirche (1991)
and Gislason and Astthorsson (1995) observed only late stages (CIVs and CVs) and
adult C. hyperboreus in the Greenland Sea in late fall. Females were concentrated in
the surface waters only between April and August where they were feeding and
forming large lipid reserves (this study; Hirche and Nieho!, 1996). On the other hand,
Longhurst et al. (1984) found in the Canadian Archipelago that during August female
C. hyperboreus were already leaving the upper 400 m to concentrate at depths of
500}1500 m. In summary, the mesozooplankton population observed in this study
followed the main characteristics already noted for the Arctic Ocean: small numbers
of species, large body size resulting from slow growth rates and generation times of
1}3 years.
4.4. Herbivory and omnivory
The copepod community was dominated by omnivorous and herbivorous species
(e.g., Calanus sp., Metridia sp.), and only a few predatory forms were found (e.g.,
Euchaeta sp., Appendicularia, Parathemisto sp.). Longhurst (1985) and Longhurst et
al. (1989) also found that predatory mesozooplankton represented only 23% in the
Arctic compared with 38% in temperate oceans and 47% in tropical oceans.
The importance of the classical food web (i.e. ingestion of phytoplankton by
zooplankton) was assessed through the measurements of gut pigment contents. Gut
pigment contents for C. hyperboreus and C. glacialis were similar to previously
reported values. For example, in Ba$n Sound in September Head et al. (1985) found
gut pigment contents ranging from 5.7 ng Chl a eq ind\ during the day to 27.1 ng
Chl a eq ind\ at night for CV C. hyperboreus and from 0.8 to 7 ng Chl a eq. ind\ for
female C. glacialis. In the present study, no attempt was made to study the daily
variations of gut contents because of time and personnel constraints, but vertical
migrations are known to be limited under conditions of 24 h daylight (Bogorov, 1946),
and it is possible that variations in ingestion rates were not following a diel pattern. In
this study, M. longa females showed gut pigment contents that were much higher than
those previously reported (0}3.2 ng Chl a eq ind\) by Ba mstedt et al. (1990).
During this survey copepods were apparently consuming a wide proportion of
the total daily primary production (3}55%). However, the proportion of large cells in
the total phytoplankton community was generally low (Table 3) with cells '5 lm
representing only from 5}30% of the total biomass at most station. Copepods
generally consume large phytoplankton cells more e$ciently than small ones (Poulet,
1973, 1978). If this is true for the copepods in the Arctic Ocean, then their rates of
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
1411
consumption would often have exceeded the primary production rates for the large
phytoplankton. On the other hand, grazing by phagotrophic protists could have
accounted for much of the primary production of the small phytoplankton cells (Sherr
et al., 1997). Daily rations for C. hyperboreus similar to these have been observed
previously (Ba mstedt et al., 1990) and it has been suggested that a daily ration around
20% body C d\ implies that food was not limiting (Herman, 1983), so that during
this transect, the mesozooplankton may have been able to obtain su$cient energy
from ingested phytoplankton to sustain their metabolism and to form lipid reserves.
During this study, a great deal of e!ort was put into studying ice algae (Wheeler et al.,
1996; Gosselin et al., 1997). Most of the time ice algae represented a lower biomass
than phytoplankton, but at Stations 25 and 31, they represented a larger pool of
carbon. Ice algae can be consumed by copepods (Grainger, 1991), but in this study we
did not evaluate its role as a food source for copepods.
When the phytoplankton population is dominated by small cells, a signi"cant
source of carbon for copepods may be microzooplankton (Ba mstedt and Ervik, 1984;
Ba mstedt et al., 1985; Hopkins et al., 1985; Gi!ord, 1993; Landry et al., 1994, 1995;
Nielsen and Hansen, 1995). Fessenden and Cowles (1994) estimated that non-phytoplanktonic prey in copepod diets can represent 16}100% of the carbon ingested.
Non-phytoplanktonic prey may have provided an extra source of carbon for the
omnivorous species. Both Metridia longa and Calanus hyperboreus/glacialis have been
shown to utilize microzooplankton (Haq, 1967; Huntley et al., 1987). In this study
mesozooplankton biomass was relatively well correlated (p(0.05) with the biomass
of heterotrophic protists in the size class 6}20 lm (r"!0.696), suggesting that, even
during the productive period of the year, protists may contribute to the mesozooplankton diet. Copepods in the Arctic Ocean were for a long time considered to be
essentially herbivorous (Hopkins et al., 1984), but our results suggest that there may
be an omnivorous component.
5. Conclusions
This "rst transect across the Arctic Ocean showed that zooplankton biomass was
higher than has previously been reported and that at the end of the productive season
mesozooplankton carbon accounted for about 50% of the PC. The distributions of
the di!erent species were in#uenced by currents and environmental conditions. At this
time of the year zooplankton were not food limited and their diet included phytoplankton and probably microzooplankton. During summer the pelagic food web in
the Arctic Ocean may be as complex as those at lower latitudes, including elements of
the classic food chain together with those of a microbial food web. In this study
biomass and production rates of various trophic levels (e.g. phytoplankton, microzooplankton and mesozooplankton) were higher than reported in past studies.
Clearly, signi"cant biological production and consumption of carbon take place in the
central Arctic. More complete data sets on the temporal variations over the annual
cycle are needed to determine whether autotrophic and heterotrophic processes are
balanced, or if the Arctic is a net source or sink for organic carbon.
1412
D. Thibault et al. / Deep-Sea Research I 46 (1999) 1391}1415
Acknowledgements
We are grateful to the crew of the USCGC Polar Sea for technical assistance during
sampling, and the Bedford Institute of Oceanography for supplies and for providing
excellent facilities. We thank M. Gosselin for providing the algal biomass and
production data. We appreciate critical comments by two anonymous reviewers on an
early draft. This work was supported in part by an NSF grant (OPP-9400256)
awarded to P.A. Wheeler).
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