Limnol.
Oceanogr., 40(l),
0 1995, by the American
1995, 132-137
Society of Limnology
and Oceanography,
Inc.
Regulation of copper concentration in the oceanic nutricline
phytoplankton uptake and regeneration cycles
by
William G. Sunda and SusanA. Huntsman
Beaufort Laboratory,
NMFS, NOAA,
10 1 Pivers Island Road, Beaufort, North Carolina
285 16
Abstract
Similar sigmoidal relationships were observed between cellular Cu : C ratios and free cupric ion concentration for the neritic alga Thalassiosira pseudonana and two oceanic species (Thalassiosira oceanica and
Emiliania huxleyi) grown in trace metal ion buffered media. Only 5-g-fold variations in cell Cu : C were
observed for these species over the [Cu2+] range 3 x lo-l5 to 3 x lo-l2 M, with increasing cell copper vs.
[Cu2+] slopes above and below this range. At the mean [Cu2+] for the euphotic zone of the North Pacific
( 10-13.2M), cell Cu : C ratios for the three species were 4.4, 4.4, and 3.8 I.cmol mol-I, similar to values for
plankton taken from North Pacific waters. These values also match the mean Cu : C ratio of 4.1 pmol mol -I
determined from slopes of linear relationships between Cu and PO, in the nutricline of the central North
Pacific and the “Redfield” C : PO, ratio in plankton of 106 : 1. This agreement provides strong evidence that
copper concentrations in remote oceanic nutriclines are regulated by phytoplankton uptake and regeneration
processes.
marily from a lack of information about metal complexation by organic ligands.
Due to analytical advances, data have recently become
available on organic complexation of Cu in seawater, as
well as on that of other bioactive metals, such as Zn and
Cd (Moffett and Zika 1987; Bruland 1989, 1992). Results
from a number of investigations that used different techniques have revealed that copper is heavily complexed
in the euphotic zone by a strong organic ligand (or group
of ligands) possessing a conditional stability constant of
-1013 M-l (Coale and Bruland 1988, 1990; Moffett et
al. 1990; Sunda and Huntsman 199 1). The ligand concentration generally covaries with that of copper, resulting
in a relatively constant free cupric ion concentration of
- 10 - l3 M in coastal and near-surface oceanic waters.
In the present study we investigated relationships among
external free cupric ion concentration, cellular Cu : C ratios, chlorophyll a, and growth rate for four phytoplankton species. The Cu : C ratios observed in the phytoplankton at typical near-surface free cupric ion concentrations
were compared with “Redfield ratios” of Cu : C derived
from relative changes in copper and phosphate concentrations with depth in the oceanic nutricline and the Redfield ratio of C : P in plankton of 106 : 1. Comparisons
were also made with Cu : C ratios reported previously for
natural plankton samples from Pacific waters.
It is well established that the concentrations of major
nutrients, such as nitrate and phosphate, are controlled
by biological uptake and regeneration cycles in seawater.
In these cycles, nutrients are taken up by phytoplankton
in the euphotic zone and lost to deeper waters with the
sinking of biogenic particles such as intact algal cells and
zooplankton fecal pellets. The nutrients are then returned
to solution with the microbial degradation of the sinking
biogenic debris. Such uptake and regeneration cycles lead
to marked depletion of nutrients near the surface and
enrichment with depth. Increases in nitrate and phosphate concentrations with depth are linearly correlated
with one another, and the molar nitrate vs. phosphate
slopes (16 : 1) of these correlations approximate the ratios
of N : P found in marine plankton. This agreement provides strong evidence that planktonic uptake and regeneration cycles control the distributions
of nitrate and
phosphate concentrations in the ocean (Redfield et al.
1963).
Concentrations of many trace metal micronutrients and
nutrient analogs (Zn, Fe, Cu, Ni, and Cd) also increase
with depth in the ocean and covary with concentrations
of major nutrients (Boyle et al 1976; Bruland 1980; Bruland and Franks 1983; Martin and Gordon 1988). This
covariance has led to speculation that concentrations of
these metals within the oceanic nutricline are largely regulated by uptake and regeneration cycles similar to those
for major nutrients (Morel and Hudson 1984). Quantitative assessment of this hypothesis, however, has been
difficult because of uncertainties in free metal ion concentrations in seawater- the primary variables controlling trace metal uptake by phytoplankton
(Sunda 19881989; Bruland et al. 199 1). This uncertainty resulted pri-
Materials and methods
Copper uptake and growth rate studies were conducted
with three diatoms [Thalassiosira pseudonana (clone 3H),
Thalassiosira weissflogii (clone Actin), and Thalassiosira
oceanica (clone 13- l)].and with the coccolithophorid Emiliania huxleyi (clone Al 387). The first two are coastal
isolates and the latter two are oceanic. Axenic cultures of
these algae were obtained from the Center for the Culture
of Marine Phytoplankton,
Bigelow Laboratory, and were
maintained in f/8 medium (Guillard and Ryther 1962)
using sterile technique until needed.
Acknowledgments
We thank Maria Bondura for technical assistance.
This work was supported by a grant from the Oceanic Chemistry Program of the Office of Naval Research.
132
133
Oceanic Cu weelation
The methods used in the experiments are comparable
to those used in previous algal studies with Mn, Cu, and
Zn (SundaandHuntsman
1983,1985,1986,1992).
Algal
cells were grown at 20°C and pH 8.2&O. 1 in 450-ml polycarbonate bottles containing 200 ml of 36%0 seawater
medium. They were grown under fluorescent lighting
(Vita-Lite, Duro Test Corp.; 500 bmol quanta m-2 s-l
PAR) on a 14 : 10 L/D cycle.
Experiments were conducted in enriched natural seawater containing added trace metal ion buffer systems.
The experimental seawater was collected from the Gulf
Stream with a peristaltic pumping system (Sunda and
Huntsman 1983) and was stored for 3.5 yr in the dark at
7°C before use. Media were prepared by passing the seawater through 0.4~pm pore Nuclepore filters and enriching it with 32 PM NaNO,, 2 PM Na,HPO,,
40 PM
Na,SiO,, 10 nM Na,SeO,, 0.1 pg liter-l vitamin Br2, 0.1
pg liter-’ biotin, and 20 yg liter-l thiamin. Trace metal
ion buffer systems were added to quantify and control
free ion concentrations of Cu and other trace metal nutrients. These buffers consisted of 0.1 mM EDTA, 100
nM FeCl,, 48 nM MnCl,, 100 nM ZnCl,, 40 nM CoCl,
100 nM NiC12, and different concentrations of CuCl,.
Copper was added along with an equivalent concentration
of EDTA so that its addition at high concentrations would
not alter the free EDTA concentration and thereby alter
free ion concentrations of other metals. After preparation,
the media were equilibrated for 24 h before inoculation
of cells.
Free ion concentrations of Cu and other trace metal
nutrients in the media were computed from the total metal concentration and the extent of metal complexation by
EDTA and inorganic ions. Total Cu ranged from 1.O nM
to 40 PM as computed from the sum of the measured
background concentration and the added concentration
of CuC12. Background Cu concentration in the medium
(1 .O nM) was measured by chemiluminescence
analysis
(Sunda and Huntsman 199 1). The extent of metal complexation was determined from equilibrium calculations
as in previous algal studies in EDTA/metal
ion buffer
systems (Sunda and Huntsman 1992). The computed ratio of [CuEDTA2-]
to [Cu2+] was 106.12in the presence
of 0.1 mM EDTA, sufficient for the EDTA to well-outcompete typical concentrations (l-3 nM) of strong natural
ligands (log K, - 13) that may have been present in the
Gulf Stream water when it was collected (Moffett et al.
1990; Sunda and Huntsman 199 1). The logs of the computed free Zn, Co, Mn, and Ni ion concentrations were
-10.99, -11.03, -8.53, and -12.89.
Prior to experiments, cells were transferred from the
maintenance medium to experimental medium containing no added copper (log[Cu2+] = - 15.1 at the measured
background [Cu] of 1.O nM). The cells were preacclimated
for a period of 5-9 d (depending on the growth rate) and
were then inoculated into experimental media at biomass
levels of 0.05-O-2 pmol cell C liter-’ of medium. The
algae were grown for 9-l 1 cell generations to the end of
the exponential phase, and total concentrations and volumes of cells were measured daily with a multichannel
electronic particle counter (Coulter Counter, model TAII).
Table 1. Responses of phytoplankton
to copper in EDTAtrace metal ion buffered media. Not detected-ND;
not analyzed - NA.
-log
[cu2+]
Cell Cu
km01
liter-‘)*
15.12
14.78
14.42
13.99
13.50
13.51
13.50
13.04
12.51
12.03
11.51
11.03
10.51
ND
ND
16.6
17.7
31.2
34.9
39.9
53.3
61
75
86
124
216
15.12
14.79
14.44
14.02
13.53
13.53
13.05
12.54
12.06
11.54
11.06
10.54
4.5
20.3
32.4
37.2
52.8
59.9
80.0
83.8
205
276
281
2,094
15.12
15.12
14.77
14.42
14.01
13.50
13.51
13.57
13.03
12.52
12.04
11.52
11.05
10.52
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
4.6
28.4
50.1
177
15.12
15.12
13.99
13.51
13.02
12.52
12.52
12.52
12.02
11.52
11.02
7.6
8.1
38.4
58.0
62.9
80.8
86.2
94.5
117
152
249
Cell
Chl a
Cell C
(mol
(mmol
liter - I)* liter - I)*
Mean
cell vol
&m3)
Specific
growth
rate (d-l)
Thalassiosira oceanica
12.7
12.5
12.3
10.6
10.2
10.6
10.4
10.6
10.2
10.9
10.4
10.4
10.4
92.6
95.6
93.7
97.9
95.7
97.8
98.8
96.7
96.4
98.2
97.6
1.95
2.21
2.27
2.25
2.04
1.93
2.14
2.01
2.06
1.61
2.19
2.18
2.19
107
108
1.53
1.54
1.53
1.63
1.60
1.58
1.60
1.59
1.63
1.62
1.62
1.61
1.62
Emiliania huxleyi
20.6
21.9
17.8
18.4
14.7
21.3
21.0
17.7
22.4
20.1
17.8
19.2
4.59
5.18
4.11
4.34
4.33
3.43
3.50
4.22
3.61
3.79
3.51
3.18
18.1
18.5
17.6
18.2
18.1
17.7
17.7
19.0
17.1
19.7
20.2
43.5
1.14
1.20
1.20
1.30
1.22
0.98
1.09
1.15
1.09
0.98
1.13
0.94
Thalassiosira weissjlogii
9.2
NA
9.1
8.7
7.9
9.4
NA
8.9
9.0
9.0
8.6
9.3
8.7
9.2
3.05
3.12
2.66
2.58
2.49
2.63
2.60
2.42
2.59
2.55
2.57
2.38
2.34
2.28
975
1,160
977
1,012
1,041
987
1,070
1,006
997
997
985
1,008
953
940
0.56
0.68
0.57
0.59
0.53
0.59
0.63
0.63
0.62
0.62
0.55
0.57
0.56
0.43
Thalassiosira pseudonana
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
48
47
45
45
46
45
46
45
45
46
44
1.86
1.89
1.87
1.86
1.86
1.85
1.86
1.86
1.85
1.87
1.74
Sunda and Huntsman
134
10
A
ol
ratio increased to a mean of 12.5 +0.2 mol liter- 1 at the
three lowest [Cu2+] values (Table 1); each of these ratios
was used within its corresponding [Cu2+] range to compute cellular Cu : C ratios in T. oceanica. For T. pseudonana, the cell C : cell volume ratio was 14 mol C liter- l,
as measured in parallel cultures at a [Cu2+] of 1O- 13.5M.
Results
Fig. 1. Relationships
between cellular Cu: C ratios and
log[Cu*+] for Thalassiosira oceanica (Cl), Emiliania huxleyi (A),
Thalassiosira pseudonana ( x ), and Thalassiosira weissflogii (*).
Specific growth rates of cultures were computed from
linear regressions of In cell volume vs. time for the exponential phase of growth.
Cellular Cu concentrations were measured in exponentially growing cultures, 9-l 0 cell divisions after inoculation. To measure Cu, we filtered cells onto 3-pm-pore
Nuclepore filters (1 pm for clone A 1387) and washed
them with 3 ml of filtered Gulf Stream water. Filter blanks
were prepared by passing the culture filtrates through a
second set of filters. The experimental and blank filters
were placed in 5-ml Teflon vials and digested at 60°C for
3 d in the presence of 0.4 ml of redistilled HN03. The
filter digests were diluted to 4 ml with water from a Milli-Q
system (Milli-Q water) and measured for Cu concentration by graphite furnace atomic absorption spectrometry.
The cellular Cu concentrations were corrected for filter
blanks and divided by the total volume of cells to give
cellular Cu concentrations in units of mol Cu per liter of
cell volume. Triplicate determinations
of cellular Cu at
log[Cu2+] of - 12.6 for T. pseudonana and - 13.5 for T.
oceanica (Table 1) yielded standard deviations about the
mean of 4 8 and + 12%.
Cellular Cu concentrations were converted to molar
Cu : C ratios by dividing them by mean values of experimentally measured cell C : cell volume ratios, determined in either the same cultures at the time of copper
measurement (T. oceanica, T. weissflogii, and E. huxleyi;
see Table 1) or in separate cultures (T. pseudonana). Cell
C was measured by standard 14C techniques after exposing the cells to HCl fumes to remove inorganic C (including CaCO,). Cell volume was measured by Coulter
Counter as described above. The mean C : cell volume
ratios (&SD) were 19+2 and 8.9kO.4 mol C liter-l for
E. huxleyi, and T. weissflogii, and there was no trend in
the ratios with variations in [Cu2+] (Table 1). For T.
oceanica, the mean C : cell volume ratio was 10.5 20.2
mol liter-l down to a [Cu2+] value of 10-13.9 M, but the
Measured relationships between cellular Cu : C ratios
and free cupric ion concentration are shown in Fig. 1.
Cellular Cu : C curves for T. pseudonana, T. oceanica,
and T. huxleyi were virtually superimposable over most
of the experimental range, while the curve for T. weissflogii deviated downward from the other three. The curves
for the first three species had sigmoidal shapes, characterized by broad regions in [Cu2+] ( 10-14.5 to 1O-11.5 M)
where cellular Cu : C varied by only 5-9-fold despite a
1,OOO-fold variation in free Cu. Above this range, the
Cu : C curves for the three species steepened, especially
for E. huxleyi. By contrast, the cellular Cu : C curve for
T. weissfogii approached those for the other three species
at the highest copper level but deviated downward with
decreasing cupric ion concentrations and fell below the
detection limit for cellular Cu at [Cu2+] < lo-l2 M. For
this species, cellular Cu : C was approximately
proportional to [Cu2 ‘1 over the measurable experimental range.
Copper is an algal nutrient, but it is also toxic at elevated concentrations. Evidence for toxicity, in terms of
reduced growth rate, decreased cell chlorophyll,
or increased volume per’ cell, was observed for E. huxleyi, T.
weissjlogii, and T. pseudonana at [Cu2+] 1 1O- 11 M (Table 1). No toxicity was apparent at the highest experimental [Cu2+] for T. oceanica except perhaps for a slight
(- 10%) increase in mean volume per cell. No nutritional
limitation of growth rate was observed for T. weiss$!ogii,
T. pseudonana, or E. huxleyi at the lowest [Cu2+] for
these species (lo- 15.1 M), but a slight decrease (5%) was
observed at this [Cu2+] for T. oceanica. Cu limitation of
T. oceanica was verified in a subsequent experiment in
which the lowest [Cu2+] was decreased further by a 5-fold
higher concentration of EDTA. In this latter experiment,
the growth rate of T. oceanica was decreased by 19% at
a [Cu2+] of lo- 15e8M and by 9% at [Cu2+] of 10-1501M,
relative to the rate at the highest free cupric ion concentration (1 O-‘4.2 M) (data not shown).
Discussion
Cellular Cu accumulation curves-The sigmoidal curves
for cellular Cu vs. [Cu2+] for T. pseudonana and the two
oceanic species are similar to those for algal accumulation
of Zn in the same species (Sunda and Huntsman 1992).
Like Cu, Zn is a micronutrient
metal which is toxic at
elevated concentrations. The intermediate portions of the
cellular Zn vs. [Zn”+] curves which possess minimum
slopes are associated with a negative feedback regulation
of cellular Zn uptake by an inducible high-affinity trans-
Oceanic Cu regulation
port system. Similar negative feedback regulation has been
observed for other micronutrient
metals (Mn and Fe) in
these species (Sunda and Huntsman 1986; Harrison and
Morel 1986). Regulation of cellular Cu may also explain
the broad intermediate region of the Cu accumulation
curves over which there is minimal variation in cell Cu.
The region of minimal variation in cell Cu could also be
due to saturation of cellular Cu uptake sites.
The contrasting near-linear relationship between cellular Cu and [Cu2+] in T. weissflogii suggests that Cu is
not regulated in this species. This apparent lack of regulation, and the lack of measurable cellular accumulation
at [Cu2+] below lo- l2 M, suggests that Cu is not an essential nutrient for this species, as it is for T. oceanica.
Whether it is a required nutrient for the other two species
is not known.
Regulation of Cu concentrations in the oceanic nutricline by algal uptake and regeneration-Results of our
study, combined with field observations, support the hypothesis that Cu uptake by phytoplankton and subsequent
regeneration at depth control the distribution
of Cu in
many oceanic nutriclines. Data from depth profiles in the
nutricline (-0-800
m) of the central North Pacific show
consistent linear relationships between Cu and PO, concentrations (Fig. 2). Linear regression analysis of Cu vs.
PO4 relationships from four North Pacific profiles reveals
high-correlation
R2 values (0.966-0.992) and consistent
Cu : PO4 slopes of 0.43-0.45 mmol mol-1 (Table 2). If
the observed linear Cu vs. PO4 relationships are controlled by phytoplankton
uptake and regeneration, then
the ACu/APO, slopes in the nutricline should equal the
ratios in which these elements occur in phytoplankton
cells. According to this reasoning and the above linear
regression slopes, the mean ratio of Cu : P in North Pacific
phytoplankton should equal 0.44 f 0.0 1 mmol mol- l (Table 2). If we assume a C : PO, ratio of 106 : 1 (the classic
Redfield ratio), then we compute a Cu : C ratio for the
North Pacific plankton of 4.1 pmol mol-I.
This Redfield Cu : C ratio is consistent with the value
we would predict from recent measurements of free cupric
ion concentration in North Pacific seawater and the measured relationships between Cu : C and [Cu2+] in our oceanic algal isolates (T. oceanica and E. huxleyi) and in the
coastal species T. pseudonana. Coale and Bruland (1990)
recently measured profiles of free cupric ion concentration and organic Cu complexation at the same stations
where Martin et al. (1989) determined nutricline profiles
for Cu and PO4 concentrations. They found that Cu was
highly complexed by organic ligands within the euphotic
zone and that [Cu2+] varied little within this layer from
one station to next. Free cupric ion concentration in the
euphotic zone varied from 1O- 13.5to 1O- 12m7
M, with a
mean value of - 1O- 13.2M. That value falls near the middle of the broad plateau region of the cellular Cu : C curves
for T. oceanica, E. huxleyi, and T. pseudonana, where
there is minimum change in cellular Cu with variations
in [Cu2+]. At that [Cu2+], these three species had Cu : C
ratios of 4.4, 3.8, and 4.4 pmol mol-I, consistent with
the above mean Redfield value of 4.1 bmol mol- 1 deter-
135
I
2
5-
0
E
5
5
_
4-
E
-
s
8
m
3-
2-
l-
Fig. 2. A. Cu vs. PO, relationships for depth profiles in the
central North Pacific (A-39.6”N,
140.8”W; 20-1,500 m; Martin
et al. 1989), the Southern Ocean m-60.8”S,
63.4”W; 30-1,850
m; Martin et al. 1990), and the North Atlantic (El-47”N, 2O”W;
20-2,900 m; Martin et al. 1993). B. Cu vs. PO, relationships
for depth profiles from the central North Pacific (A-32.7”N,
145.O”W; O-4,875 m) and two stations off the central California
coast m--37.0”,
124.2”W; 25-3,900 m; Cl-36.9”N,
122.9”W;
1O-2,250 m). (Data in panel B from Bruland 1980.) In all cases,
data from within the nutricline are represented by the lower
portions of curves to the left of the sharp break in slope.
mined from Cu vs. PO4 regressions in the nutriclines of
North Pacific stations.
Cu : C ratios of 3.8-4.4 hmol mol-’ are also consistent
with those for actual net plankton samples collected from
near-surface Pacific waters (Table 3), providing additional strong evidence that plankton uptake and regeneration
Sunda and Huntsman
136
Table 2. Regression slopes of Cu : PO, and resulting Cu : C ratios, based on depth-dependant
phosphate in oceanic nutriclines.
in dissolved copper and
cu:c*
(pm01 mol-I)
R*
n
Reference
0.44
0.45
0.43
0.43
4.2
4.3
4.0
4.0
0.992
0.959
0.964
0.966
7
11
12
12
Bruland 1980
Martin et al. 1989
Martin et al. 1989
Martin et al. 1989
O-800
0.30
2.8
0.914
11
Martin
et al. 1993
30-300
0.68
6.4
0.923
5
Martin
et al. 1990
Location
Depth
b-0
North Pacific
32.7”N, 145.O”W
39.6”N: 140.8”W
45.O”N, 142.9”W
50.0°N, 145.O”W
O-985
O-780
O-900
O-800
North Atlantic
47”N, 2O”W
Drake Passage
60.8”S, 63.4”W
variations
ACu/APO,
(mmol mol
I)
* Based on Redfield C : P ratio of 106 : 1.
regulate nutricline Cu concentrations. For example, the
mean Cu : P ratio was O-49+0.24 mmol mol-’ in a set of
2 1 net (50~pm mesh) plankton samples collected in transects running from - 50 to 1,100 km off the coasts of
southern California and northern Mexico (Martin et al
1976). This value converts to a mean Cu : C of 4.6k2.3
hmol mol- 1 if we once again assume a C : P ratio of 106 :
1. Much of the large standard deviation about the mean
results from two unusually high values; if we exclude
these, we obtain a mean Cu : C ratio for the remaining 19
samples of 3.9+ 1.2 pm01 mol-l.
Linear relationships between Cu and PO, concentrations in the nutricline are also found in other remote
oceanic locations, including
the North Atlantic
and
Southern Ocean (Fig. 2A; Table 2). For these two locales,
we compute Redfield Cu : C ratios of 2.8 and 6.4 pmol
mol-I, respectively, from Cu vs. PO4 regressions and a
C : P ratio of 106 : 1. These values bracket those found in
the central North Pacific and fall within the range of
values found for natural plankton samples (Table 3). Slight
differences in Cu : P relationships within oceanic nutriclines may reflect local differences in free cupric ion concentration or species composition of plankton. We note
that a Cu : C ratio of 2.8 pmol mol-’ would occur in our
two oceanic phytoplankton
species (T. oceanica and E.
huxleyi) at free cupric ion concentrations of 10-13a7 and
10-13.5 M and a ratio of 6.5 pmol mol-1 would occur at
10-12.2 and lo- 12.3M. These values are consistent with
the range in [Cu”] measured previously in open ocean
waters of the North Atlantic and Pacific Oceans (Coale
and Bruland 1990; Moffett et al. 1990).
Although phytoplankton
uptake and regeneration ap-
pear to dominate Cu cycling in the nutriclines of most
remote oceanic regions, other processes such as inputs of
Cu from aeolean and riverine sources and scavenging by
nonbiogenic particulates (e.g. Mn and Fe oxyhydroxides)
become increasingly important as one approaches the
continents. In stations sampled by Bruland (1980) off the
central California coast, such processes mask the effects
of biogenic cycling, resulting in a lack of correlation between copper and phosphate within the nutricline (Fig.
2B). In regions where there are intense aeolean inputs
from deserts, such as the northwestern Indian Ocean,
distinct surface maxima are observed in Cu concentrations (Saager et al. 1992).
Redfield-type behavior also is not observed below the
nutricline in the world oceans. Below the phosphate maximum at roughly 1,000 m in the North Pacific, Cu concentrations continue to increase with depth as phosphate
concentrations decrease, resulting in negative correlations
between the two (Fig. 2B). The increase in Cu concentrations with depth in the deep sea has been attributed
to difhtsion of this metal from Cu-rich bottom sediments
combined with midwater scavenging by unknown particulate phases (Boyle et al. 1977; Bruland 1980).
The marked difference in Cu behavior between the nutricline and deeper waters in the Pacific may reflect large
differences in the ventilation age of the water-the
time
since it last resided at the surface and was subject to
surface processes, such as algal growth. Water in the nutricline (upper 800 m) of the North Pacific contains 14C
released by hydrogen bomb testing during the early 1960s
(Williams and Druffel 1987). Thus, this water is relatively
young and has recently experienced near-surface biogenic
Table 3. Cu : PO, and resultant estimated Cu : C ratios in natural plankton
samples from the Pacific.
cu:c*
n
Location
Equatorial Pacific
Pacific off S. California
and N. Mexico
* Based on assumed C : PO, of 106 : 1.
6
21
Cu : PO,
(mmol mol- I)
0.54kO.09
0.49 f0.24
(Ccmol
mol- I)
5.1
4.6
Reference
Collier and Edmond
Martin et al. 1976
1983
Oceanic Cu regulation
scavenging. By contrast, intermediate and deep waters of
the North Pacific have estimated ages of - 1,000 yr.
Conclusions
We observed a close agreement among estimated Cu :
C ratios in oceanic plankton obtained from three entirely
different sources: measured relationships between cellular
Cu : C ratios in algal cultures as functions of cupric ion ’
concentration combined with recent measurements of free
cupric ion concentrations in near-surface North Pacific
seawater; measurements of Cu concentrations in plankton samples from the Pacific Ocean; and slopes of Cu vs.
phosphate relationships in the nutricline of the North
Pacific combined with the Redfield C : PO, ratio in plankton. This agreement shows a basic coherence between our
laboratory data and the various field measurements. It
also provides strong evidence that phytoplankton uptake
and regeneration represent the dominant processes regulating copper concentrations in the nutriclines of remote
oceanic regions.
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Submitted: 4 January 1994
Accepted: 25 July 1994
Amended: 23 August 1994