primary production in the north pacific gyre: a comparison of rates determined by the 14c, o2...
TRANSCRIPT
Deep-Sea Research, VoL 36, No. 11, pp. 1621-1634, 1989. 0198-0149/89 $3.00 + 0.00 Printed in Great Britain, © 1989 Pergamon Press plc.
Primary production in the North Pacific gyre: a comparison of rates determined by the 14C, Oz concentration and 1SO methods
KAREN D. GRANDE,* PETER J. LEB. WILLIAMS,t JOHN MARRA,~ DUNCAN A. PURDIE,§ KRISTINA HEINEMANN,~ RICHARD W. EPPLEYII a n d MICHAEL L. BENDER*
(Received August 1988; in revised form 26 June 1989; accepted 15 June 1989)
Abstract--Primary production was measured at 28°N/155°W, north of Hawaii, during the late summer of 1985, using three independent in vitro techniques: (1) the 180 method, in which gross oxygen production is determined from the rate at which 1SO-labelled O2 is produced from 18D- labelled H20, (2) the O2 light/dark bottle method, and (3) the H14CO~ assimilation method. For samples incubated in situ, rates of gross 02 production, determined with 180, are similar to rates calculated by oxygen changes in light/dark bottles, 14C productivities range from -60 to 100% of 180 gross production. Assuming PQ i> 1, this implies that t4c production is ~>65% of gross C assimilation. However, in samples incubated on board ship (with neutral density filters at 35% of incident light intensity, and at surface seawater temperatures), the rates of gross oxygen production measured with 180 were up to two times the rates measured with light/dark bottles, and 2-3 times the rates of 14C production. We believe that the increase in 02 cycling and carbon cycling implied by these data is an artifact reflecting the response of metabolism to some condition of shipboard incubation, possibly the spectral quality of light.
INTRODUCTION
UNDERSTANDING and characterizing the nature of biological activity in the oligotrophic ocean require accurate estimates of the rates of gross and net photosynthetic production and community respiration. Unequivocal determination of these rates, however, has proven difficult. Virtually all estimates of primary production have been generated using one technique: assimilation of 14C bicarbonate during incubation of seawater in bottles. Recent work has led to important improvements in the 14C methodology. These improvements include the introduction of trace metal clean techniques (FITZWATER et
al., 1982), the use of filters with small enough pore sizes to collect the pO14C incorporated into picoplankton, and the more common determination of DO14C as well as pO14C. (POC and DOC refer to particulate and dissolved organic carbon, respect- ively.)
It is now generally believed that the 14C method gives a good approximation to the rate of primary production. Support for this view comes from a number of studies where comparative productivities have been measured using 14C and other methods (WILLIAM et
al., 1979, 1983; PLATr, 1984; DAVIES and WILLIAMS, 1984; BENDER et al., 1987).
*Graduate School of Oceanography, University of Rhode Island, Kingston, RI 02881, U.S.A. t School of Ocean Sciences, Marine Science Laboratories, Menai Bridge, Anglesey LL59 5EH, U.K. ~: Lamont Doherty Geological Observatory of Columbia University, Palisades, NY 10964, U.S.A. § Department of Oceanography, The University, Southampton SO9 5NH, U.K. II Institute of Marine Resources A-018, Scripps Institution of Oceanography, University of California, San
Diego, La Jolla, CA 92093, U.S.A.
1621
1622 K.D. GRANDE et al.
Nevertheless, significant problems remain. First, without ancillary information, it cannot be known whether the Iac technique measures the rate of gross production, net production, or some intermediate value. ("Production", as used here, refers to primary rather than secondary production.) Second, containment effects caused by enclosing samples in bottles during an incubation may cause 14C productivity (as well as other in vitro rate measurements) to be in error (EPPLEY, 1980; PETERSON, 1980; WILLIAMS et al., 1983).
In this paper, we report measurements of gross oxygen production using the stable isotope lSo as a tracer of photosynthesis. In this method (GRANDE, 1988; BENDER et al., 1987), the sample water is artificially enriched with ISO, and molecular oxygen, enriched in 180, is produced following the equation;
H2180 + CO 2 --')' CH20 + 180160.
The rate of 02 production is calculated from the experimentally measured increase in the lSO160 concentration. Fractionation of the oxygen isotopes during photosynthesis has been found to occur (see references below), but the effect of this fractionation is negligible in our experiments due to the large lSo enrichments of the water. The photosynthetically produced oxygen has a ~51So value similar to that of the source water (S~VENS et al., 1975; KROOPNICK, 1975; GUY et al., 1986; FOCEL et al., 1986), which, in our experiments, is raised to a value of about +2000 to +3000%0.
[The delta (~) notation, in units of permil (%o), is defined as:
~(%o) ----" [(180/16Osample/180/16Ostandard ) --1] x 103.]
The ~80 content of the dissolved oxygen pool is increased by photosynthesis, but is affected by respiration to an insignificant degree. The dissolved 02 pool, to which the label is added in the 180 technique, is much larger than the pool of biomass, to which the label is added in the 14C method. Hence, a given amount of respiration affects the production rates measured by the 61So method to a much smaller degree than produc- tion rates determined from ~4C data. As a result, while the 14C method measures a rate between net and gross production, the H2180 technique measures gross oxygen produc- tion. If the 02 produced photosynthetically is well mixed with the dissolved oxygen pool, consumption of lSo160 by respiration will not significantly reduce the measure of gross production by this technique in oceanic water. Thus the 180 technique provides a standard, an estimate of gross primary production, which is useful in interpreting results from other techniques.
We compare production rates from the 180 method with rates measured by two more commonly utilized bottle incubation techniques: the ~4C method and the dissolved oxygen light/dark bottle method. Utilizing these techniques on identical water samples allows for two valuable comparisons. First, comparing 14C production rates with net and gross oxygen production rates constrains the extent of 14C losses occurring as a result of respiration, DO14C excretion, and incomplete collection of pO14C. We are thus able to evaluate the possibility that these losses of 14C cause discrepancies between 14C and other production rate estimates. Second, we can calculate the rates of community respiration in the light from the difference between gross and net rates of oxygen production. These can then be compared to rates of respiration in dark bottles. A general limitation of our work is that, since all our methods require bottle incubations, we are not able to assess the effects of containment on measured values of production. A comparison of in vitro
Primary production in the North Pacific gyre 1623
and in situ production of dissolved 02 in the mixed layer during the PRPOOS cruise (see below) will be reported elsewhere (WILLIAMS and PURDIE, 1989).
Our study was undertaken in the North Pacific central gyre between 16 August and 8 September 1985, aboard the R.V. Melville (Alcyone Expedition, Leg 3), in conjunction with the research program PRPOOS (Plankton Rate Processes in Oligotrophic Oceans). The cruise site (located at about 28°N, 155°W) is in a region in which 14C production has been measured over the last 20 years, allowing our inter-technique comparisons to be meaningfully compared to previous data (HAYWARD, 1987; MARRA and HEINEMANN, 1987). A summary of much of the data collected during the PROPOOS cruise, including hydrography, nutrients, wind speeds, chlorophyll values, submarine irradiance and organism densities has been presented by EPPLEY et al. (1988).
METHODS
The chlorophyll concentrations were measured fluorometrically as described in SMITH et al. (1981). The daily radiation values (PAR) are provided by an on-deck LICOR cosine-corrected quantum sensor. Hydrography data (NBIS CTD) were supplied by the Physical and Chemical Oceanography Data Facility, Scripps Institute of Oceanography.
Water samples for all techniques were collected and handled by an identical pro- cedure. Water was collected using a nylon-covered Kevlar hydrowire and Go-Flo bottles which were pre-soaked with dilute HC1 and then rinsed with Milli-Q deionized water (FITzWATER et al., 1982). Analysis of dissolved Cu in deionized water which was stored in these bottles showed that the bottles were noncontaminating, at least for this element. Analysis of Cu in incubated samples also demonstrated the absence of contamination for samples handled according to the protocol of FITZWATER et al. (1982), as our samples were (MARRA and HEINEMANN, 1987). The water was collected starting 2-3 h before dawn. Because of the demand of multiple experiments for large quantities of water, samples from several separate casts to the same depth were pooled in 120 litre polycarbonate vats. In part to avoid oxygen supersaturation during the subsequent 12 h incubation, but mainly to insure complete mixing, we gently bubbled the vats with nitrogen gas for up to 5 min, lowering the dissolved oxygen concentration by about 10- 20% (for all except the in situ incubations described below). Samples were incubated in 140 ml Pyrex bottles. On a number of occasions, samples were also incubated in 110 ml quartz bottles for lSo and 14C productivity determinations. Bottles were soaked in dilute HC1 for at least 12 h prior to use. They were filled by siphon, with each bottle rinsed with sample water once and then fushed with at least three bottle volumes. Care was taken throughout the sampling and preparation procedure to avoid excessive bubbling and agitation. Incubations were begun within the half hour before dawn and were 12 h in duration. Rates of production and respiration are presented in terms of ~tmol 02 or lamol Corg produced per liter per 12 h photoperiod.
Three different incubation procedures were employed during the cruise. In the in situ experiment, borosilicate bottles were suspended on a free-floating line at depths corresponding to those of collection: 10, 20, 50, 70 and 90 m. Borosilicate bottles were used for oxygen productivity determinations, and polycarbonate for 14C. In the simu- lated in situ procedure, bottles were incubated on deck at temperatures and irradiances corresponding to the depths of collection (10, 20, 50 and 90 m; roughly corresponding to 100, 35 and 1%, respectively, of surface irradiance). Appropriate light intensities were
1624 K . D . GRAI~E et al.
obtained using neutral density screens. Temperature of the mixed layer samples was regulated using surface seawater. Temperatures for the incubations simulating depths below the mixed layer were controlled by circulating the incubation tank water through thermo-regulated baths. In the 'shipboard incubation' experiments, water was collected from between 20 and 30 m and was incubated on deck at 35% of incident irradiance (achieved with neutral density screens). Temperature was controlled by pumping surface seawater through the incubation tanks.
The 180-labelled water used to spike samples (95% 180, Monsanto Research Corp., Miamisburg, Ohio) had been triple distilled in teflon bottles. Cu, Mn and Cd concentra- tions were measured by direct injection into a Perkin-Elmer 5000 flameless atomic absorption spectrophotometer, and found to be <0.1 ppb. Nitrate levels in the H2180 spike were <1.0 ~tmol 1-1 and would cause the sample [NO~] to increase by <0.005 ~tmol 1-1 in the 180 incubated samples. In order to test for an effect of nitrate enrichment, we doubled spike volumes for several samples. We observed no significant differences between 14C productivities in these and normally spiked samples, suggesting that contamination or nutrient enrichment from the H2180 spike did not detectably alter the results.
The analytical details for the H2180 method can be found elsewhere (GRANDE, 1988). In the remainder of the text, we will refer to the rate derived from this technique as the rate of 180 gross oxygen production.
Rates of net community production and respiration in the dark were measured with an automated Winkler technique (WILLIAMS and JENKINSON, 1982). The 02 gross production rate can be estimated by summing the change in concentration in light and dark bottles. This estimate will be in error of gross production if the rate of respiration in the light is different from the rate in the dark.
14C production rates were measured as described by MARRA and HEINEMANN (1987). In the simulated in situ experiment, pO~4C was collected on a 0.2 ~tm Nuclepore filter, rather than on the HA filters used for all other experiments. Since the Nuclepore filters were found to collect about 25% less 14C-labelled carbon than the HA filters in the planktonic communities studied during the PRPOOS cruise (R. KNOECHEL, personal communication), the data have been corrected by a factor of 1.33. The ~4C spike was cleaned as described in FrrzWA~R et al. (1982). We were unable to measure DOlaC production due to high background values in the 14C stock solutions. Prior to incubation, a subset of samples was filtered immediately for a zero time correction for nonphotosyn- thetic uptake of 14C.
We must assume a photosynthetic quotient in order to compare the carbon- and the oxygen-based methods of measuring production. The constant and very low concentra- tion of nitrate in the euphotic zone (<100 nanomolar; EPPLEY et al., 1988) observed during the PRPOOS cruise suggests that reduced nitrogen was used by the phyto- plankton, and that PQ is in fact close to 1.25 (PARSONS et al., 1977; WILLIAMS et al., 1983).
We used light extinction data gathered on the PRPOOS cruise by E. Swift (EPPLEY et al., 1988) to ascertain the light intensity of the in situ samples at the various depths sampled. The average extinction coefficient of light in the upper 110 m was measured to be 0.042 + 0.003 m -~.
R E S U L T S
The results of the rate comparisons are dependent on the incubation conditions. Therefore, we present and discuss (in the following section) the results from each
Tabl
e 1.
P
rodu
ctio
n an
d re
spir
atio
n ra
tes f
or s
ampl
es f
rom
the
'in
sit
u' i
ncub
atio
n an
d 's
imul
ated
in
sit
u' i
ncub
atio
n ex
peri
men
ts.
All
rat
es
are
repo
rted
in
units
of
Ixm
ol 1
-1 1
2 h -
1. T
he 1
4C p
rodu
ctio
n ra
te i
s m
ulti
plie
d by
the
pho
tosy
nthe
tic
quot
ient
( P
Q)
for
com
pari
son
wit
h th
e ox
ygen
pro
duct
ion
rate
s. A
va
lue
of 1
.25
/s a
ssum
ed f
or t
he P
Q
Res
pir
atio
n
Dep
th
~4C
14
C P
rod
. 0
2 D
ark
0
2 N
et
Oe
Gro
ss
180
Gro
ss
Lig
ht
resp
. ra
te c
on
stan
t (m
) P
rod
. x
PQ
re
sp.
pro
d.
pro
d.
pro
du
ctio
n
rate
(d
ay -1
)
'In
situ
' (2
Sep
t. 1
985)
10
0.
52 +
0.
06
0.65
0.
56 +
0.
05
0.46
+
0 1.
02
+
0.06
0.
82 _
0.
06
0.36
+
0.06
1.
0 30
0.
46 +
0.
02
0.58
0.
43 +
0.
05
0.41
+
0.
03
0.84
+
0.05
0.
72 +
0.
03
0.31
+
0.
04
0.9
50
0.67
+
0.05
0.
84
0.60
_
0.12
0.
34 +
0.
08
0.94
+
0.12
0.
97 +
0.
02
0.63
+_
0.08
0.
6 70
0.
42 +
0.
0 0.
53
0.28
+
0.17
-0
.20
+
0.23
0.
08 +
0.
22
0.59
+
0.02
0.
79 +
0.
23
0.5
90
0.38
+
0.02
0.
48
0.20
+
0.06
0.
22 +
0.
04
0.43
+
0.06
0.
47 +
0.
02
0.25
+
0.04
0
'Sim
ula
ted
in
situ
' (4
Sep
t. 1
985)
10
0.
51
+
0.1"
0.
64
-0.1
5
+
0.1
1t
0.86
_
0.13
0.
71
+
0.17
1.
30 +
0.
06
0.44
+
0.14
3.
3 20
0.
59 +
0.
02*
0.74
0.
28 +
0.
09
0.53
+
0.10
0.
80 +
0.
10
0.75
+
0.02
0.
22 +
0.
10
0 50
0.
21
+
0.05
* 0.
26
0.30
+
0.08
0.
11
+
0.10
0.
41
+
0.10
0.
20 +
0.
02
0.09
+
0.10
?
90
0.20
+
0.02
* 0.
25
-0.1
6 +
0
.10
t 0.
04 +
0.
07
-0.1
2 +
0.
08
0.27
+
0.01
0.
23 +
0.
07
0.3
"14C
dat
a fr
om
th
e 's
imu
late
d i
n si
tu'
incu
bat
ion
s h
ave
bee
n c
orr
ecte
d f
or
use
of
>0
.2 ~
tm N
ucl
epo
re r
ath
er t
han
a H
A f
ilte
r.
tPo
siti
ve
02
ch
ang
e w
as m
easu
red
in
the
dar
k i
ncu
bat
ion
.
1626 K.D. GRANDE et al.
incubation procedure separately. The rates of production and dark respiration from the in situ incubations are presented in Table 1 and plotted in Fig. lB. The depth profile of chlorophyll concentrations is plotted in Fig. 1A. At the time of sampling, the mixed layer depth was 60 m and sigma-t was 23.75.
The data from the simulated in situ incubations are included in Table 1 and Fig. 2B. The chlorophyll concentrations at the depths sampled in this experiment are plotted in Fig. 2A. Upper water column hydrography was unchanged from the in situ experiment 2 days earlier.
Table 2 contains the ~4C production rates determined for samples collected from the mixed layer and incubated in situ. No effect of bottle type is evident from these data, but firm conclusions are impossible since samples were not simultaneously incubated in glass and polycarbonate bottles (Table 2).
Results from a series of 'shipboard' incubations are presented in Table 3 and in Fig. 3. The chlorophyll concentrations in the mixed layer, and the daily integrated radiation
C h l o r o p h y l l • (ktg/L) P r o d u c t i o n R a t e (pmol/I.J12 hrs)
J= g
0.00 0.20 0.30 0
50
100
0.10 0.0 ~, ' 0 I
? (A) 20
'"~ 40
• 60 y
g."
'""--...... 80
IO0
0.3 0,6 0.9 1.2 • , • , • , • ,
~ O Gross Prod.
..... • ~ w : ~ [ ] 02 Gross Prod. - ~ O 2 Net Prod.
[~ ] 14C Prod.
Fig. 1. (A) Depth profile of chlorophyll a concentrations. (B) Depth profile of rates of 14C production, net 02 production, gross 02 production and ]80 gross production for in situ incubations on 2 September 1985. Iso Gross production is defined in the text. Gross 02
production is the sum of net 02 production and dark respiration.
C h l o r o p h y l l a (~g/L) Prod. rate (l~mol/L/h)
£
0.00 0.10 0.20 0.30 0.0 0 0
50
(A)
50
e.
",,....
100 100
0.5 1.0 1.5
' i~ (B) p . ~
P V [ ' O ' ] ~ 180 Gross Prod.
/ l / [ ] 02 Gross Prod. [ ] o2.= Prod.
1~14C Prod.
Fig. 2. (A) Depth profile of chlorophyll a concentrations. (B) Depth profile of rates of 14C 18 production, net 02 production, gross 02 production and O gross production for simulated in
• 18 s t tu incubations on 4 September 1985. O Gross production is defined in the text. Gross 02 production is the sum of net 02 production and dark respiration.
Primary production in the North Pacific gyre 1627
Table 2. ~4C Production rates o f mixed layer samples incubated in situ. Rates are reported in units o f Imaol 1-1 12 h -1
Depth of collection Date (m) ~4C Production Bottle type
21 Aug. 30 0.47 + 0.01 Polycarb., 250 ml
22 Aug. 30 0.41 + 0.02 Polycarb., 250 ml
28 Aug. 20 0.38 + 0.03 Polycarb., 250 ml 30 0.46 + 0.05
2 Sept. 30 0.46 + 0.02 Glass, 140 ml
Mean: 0.44 + 0.04
Table 3. Production and respiration rates for samples from the 'shipboard' incubation experiments. All rates are reported in units o f lamol 1-1 12 h -1. Values in parentheses are standard deviations from the mean. Some incubations for the 180 and 14C techniques were carried out in both Pyrex and quartz bottles. Lack o f data is indicated by ND. The rates o f dark respiration are given for the incubation from 0 to 12 h and for the following 12 h (12-24 h). The column entitled '% 14C night loss' lists the percentage o f l4C fixation in Pyrex bottles that was lost in the dark from the 12 to the 24 h time points. The 4 September sample listed in this table is the same as that
listed in Table 1 in the data for the 'simulated in situ' experiment
14C production Date 180 Gross 02 Gross 02 Net Light Dark resp. % 14C Depth production prod. prod. resp. 0-12 h at 12 h at 24 h Night loss
Pyrex quartz Pyrex quartz Pyrex 19 Aug. 1.44 ND ND ND ND ND 0.47 0.39 0.30 36 30 m (0.01) (0.11) (0.10) (0.02)
23 Aug. 1.66 1.80 0.84 0.73 0.93 0.11 0.89 0.73 0.57 36 25 m (0.11) (0.20) (0.13) (0.20) (0.28) (0.12) (0.15) (0.15) (0.03)
25 Aug. 1.61 ND 0.79 0.58 1.03 0.21 0.74 0.70 0.55 26 25 m (0.18) (0.10) (0.08) (0.20) (0.11) (0.04) (0.06) (0.01)
29 Aug. 1.86 1.70 0.79 0.31 1.55 0.49 ND 0.80 ND ND 20 m (0.23) (0.13) (0.08) (0.08) (0.24) (0.07) (0.13)
4 Sept. 1.30 ND 0.71 0.86 0.44 --0.15" 0.51 ND ND ND 10 m (0.06) (0.17) (0.13) (0.14) (0.11) (0.01)
* A negative respiration rate, or 02 production in the dark, does not make sense; thus we consider that there w as zero respiration.
values for the period from 19 August to 4 September, are also plotted in Fig. 3. Rates of 14C production and 180 gross production were measured in quartz bottles (110 ml) and Pyrex bottles (140 ml) incubated simultaneously (Table 3). Bottle size had no effect on the rate of 14C production (LAws et al., 1987). In Table 3, we report respiration rates measured in two ways: (1) dark respiration rates measured in the first 12 h of incubation and (2) light respiration rates as calculated from the difference between 180 gross and 02 net production. For several experiments, the loss of particulate 14C was measured in the dark after the incubation. These data are also presented in Table 3 as '% 14C night loss'.
D I S C U S S I O N
We expect that in all cases the measured 180 gross production rate will be greater than or equal to net oxygen production. Assuming no systematic errors, the difference
1628 K.D. GRANDE et al.
2.0 A
i 1.51 o
E 1.0 ¢g
0.5
D .
0.¢ Au,
(A)
" I '
, , , , . , , . . . , , , , , .
1 9 Sept 4 Date
['o'] 180 Gross Prod.
[ ] 02 Gross Prod. ~']O2 Not Prod. ~'] 14C Prod.
A . J
C~
o=
O
0,15
0.10
0.051
0.00 Au,
55
so W
45
4o
351
- 3 0
Au!
(B)
' ' ' ' ' ' ' ' 1 l =
19 Sept 4 D a t e
(c) O r l
[ ] • [ ] [ ]
[] [] • [] [] [] •
[] []
, , , , , , , , , , , , i J , ,
19 Sept 4 Date
Fig. 3. (A) Rates of of 14C production, net 02 production, gross 02 production and 1 8 0 gross production for shipboard incubations from 19 August to 4 September 1985. 180 Gross production is defined in the text. Gross 02 production is the sum of net O2 production and dark respiration. (B) Chlorophyll a concentrations of mixed layer. (C) Total daffy integrated radiation (photo-
synthetically active radiation).
between these two rates is the rate of total respiration in the light. The rate of 0 2 gross production is given by the sum of dark oxygen respiration and net oxygen production. This rate can therefore be greater or less than 180 gross production depending on whether dark respiration is greater or less than light respiration. 14C production rates are not as simple to interpret relative to the oxygen-based measurements. If we assume a photosynthetic quotient of 1.25, we expect that rates of 14C production should be intermediate between values equal to 0.8 times the rates of gross and net oxygen production. 14C production would approach 0.8 times gross O2 production if no new photosynthate is remineralized during an incubation. It would approach 0.8 times net production if new 14C-labelled carbon is the substrate for all CO2 respired by the community during an incubation. Much of the following discussion centres around examining the observed relationship between the rates of light and dark respiration, and the rates of net 02, gross 02 and 14C production.
Primary production in the North Pacific gyre 1629
In situ incubations
The production rates measured by the 14C technique are 0.38--0.52 ~tmol 1-1 12 h -1 throughout the water column, except at 50 m, where production peaks at 0.67 I~mol 1-1 12 h -1. A similar peak in production rate is observed with both the light/dark bottle method and the H2180 technique. This peak is at the same depth as the dissolved oxygen maximum in the North Pacific central gyre in the summer (SCHULENBERGER and REID, 1981; REID and SHULENBERGER, 1986; CRAIO and HAYWARD, 1987; WILLIAMS and PURDIE, 1989). It is located well above the subsurface chlorophyll maximum (Fig. 1) and the nitracline (EPPLEY et al., 1988).
At each depth, the measured value of the 14C production rate, multiplied by PQ (1.25), is intermediate between the rate of net O2 community production and the rate of lSo gross production, as expected. In the mixed layer, the PQ-corrected rate of 14C production is close to the rate of net oxygen production, suggesting that the respired carbon was from the most recently fixed (14C-labelled) carbon pool. At 50 and 70 m, the PQ-corrected 14C production rate is midway between the rates of gross and net oxygen production. In this depth range, respired carbon comes from both a labelled and an unlabelled carbon pool. At the deepest depth (90 m), PQ-corrected 14C production closely approximates 180 gross production, and respired carbon is apparently from an old, unlabelled carbon pool. The convergence of 14C production and gross production rates at the base of the euphotic zone has been previously noted (HARRIS and PICCI~IN, 1977; SAVtDGE, 1978; SMrrH and GLIDER, 1985; MARRA and HEIr~EMA~,~, 1987). In our experiment, the relationship between 14C production and oxygen production with depth may also be affected by a depth dependence of DO14C excretion rates on the photo- synthetic quotient. Since we were not able to measure DO14C excretion, due to high background concentrations of DO14C, we cannot distinguish the effects of respiration from DOC excretion.
The turnover time of newly produced organic carbon can be estimated from the 14C and 180 productivity data. To do this, we assume constant rates of gross 14Corg and 180 production, PQ = 1.25, and 14Corg remineralization at a rate proportional to its concen- tration. Then,
d14C/dt = (1 /PQ)(P- R) = P/(PQ) - k14C dlSO/dt = P,
where P is the rate of O2 production, R is the rate of respiratory consumption, 14C is the concentration of 14C-labelled Corg, 180 is the 1so-labelled 02 concentration, k is the respiration rate constant, (PQ) is the photosynthetic quotient, and t the time after the start of the incubation, k has the units of day -1. 1/k is equal to the mean life of 14C- labelled organic matter (FRIEDLANDER et al., 1964, p. 69). The boundary condition is:
(PQ) x 14C = 180 = 0 when t = 0.
The solutions are:
14C = (P/(PQ)) x ( 1 - e-kt)/k 180 = Pt.
Dividing gives:
140180 = (1/(PQ)) x ( 1 - e-kt)/kt.
1630 K.D. GRANDE et al.
From the 14Cff180 ratio, k can be calculated at each depth, k varies between 1.0 and 0 day -1, decreasing with depth (see Table 1). The corresponding values of the laCorg mean lives increase from 1 day at the surface to ~ at 90 m. The carbon pool is obviously more complex than we assume here. Nevertheless, our results give an idea of how rapidly photosynthate is cycled, and suggest that, at the time of our experiment, the turnover was much faster in surface waters than at the base of the euphotic zone.
Near the surface (10 and 30 m depth), the measured rates of 180 gross production are about 20% less than the rates of 02 gross production. Thus at the surface, the respiration rate in the light is sightly less than the respiration rate in the dark. At 50 and 90 m depth, the rates of gross production estimated by both methods are equal, from which we deduce that the rate of respiration in these samples is largely independent of irradiance.
Simulated in situ incubations
In the simulated in situ incubation experiment, the 10 m sample was incubated at sea surface temperature and at 35% of incident light intensity, as for the 'shipboard' samples. The results were similar to those of the 'shipboard' incubations and will be included in that discussion.
In the simulated in situ samples, the rates of production measured by the different techniques tend to decrease with depth, showing no mid-depth maximum as was observed in the in situ depth profile. The relationships between the different rates of production are more complex than for the in situ experiment.
'Shipboard' incubations
In the 'shipboard' incubations, 14C production rates vary between 0.47 and 0.89 lamol 1-1 12 h -1 (Table 3). This variability may be partly explained by variability in ambient chlorophyll concentrations and integrated solar irradiance. Thus, both chlorophyll concentrations and 14C productivities were higher on 23 and 29 August as compared to 19 August and 4 September (Fig. 3). This was also observed by LAWS et al. (1987), who did shipboard incubations in 4 litre polycarbonate bottles in order to examine 14C incorporation into protein and chlorophyll. On 19 August, the low integrated irradiance may also be a factor contributing to the low rate measured.
180 Gross production rates show the same trends as the 14C production rates, with the lowest rates observed on 19 August and 4 September. 14C Production rates were generally greater than net 02 production rates. The shipboard incubation sample of 4 September is an exception; for this sample, 14C production was - 50% less than net 02 production. This result is puzzling. We would expect the product of the 14C production rate and the photosynthetic quotient to be greater than or equal to net 02 production, a result clearly not obtained for this sample. 02 Net production rates reflect small differences between initial and final 02 concentrations. It may be that the 02 net production rate measured for this sample is in error. Alternatively, it is possible that this sample exhibited DOC release. However, comparison of the time-zero dissolved samples with the final did not show significant release. To be sure, as pointed out in the Methods section, the DO14C blank was high for these samples, making release difficult to interpret.
There are two striking differences between the 'shipboard' incubation results and those observed in the in situ incubations. First, in the shipboard incubations, 180 gross production rates exceed other measures of productivity by a greater amount than in the
Primary production in the North Pacific gyre 1631
in situ experiments. The rates of 180 gross production in the shipboard experiments are on average 2.2 times greater than the rates of 14C production, while in the in situ experiment they are 1.4 times higher. The lSo gross production rates in the shipboard experiments are on average 2.0 times greater than gross O2 production rates measured with light/dark bottles; in the in situ experiments, these two rate terms are nearly equal. In the shipboard experiments, the rate of respiration in the light is higher than the rate in the dark, by a factor of 3-8. In contrast, light and dark respiration rates are roughly equal in the in situ experiments. Second, absolute rates of metabolic activity are generally higher in the shipboard experiments. For example, 14C production rates are system- atically higher in the shipboard incubations (mean and standard error are 0.65 _+ 0.10 gmol 1 -a 12 h -i) than for mixed layer samples incubated by the in situ technique (0.44 _+ 0.02 gmol 1-1 12 h-I).
Discrepancy between productivities measured by 'shipboard' and in situ incubation procedures
The results outlined above suggest (1) anomalously high rates of 14C assimilation and 180 gross production and (2) anomalously high rates of respiration, for samples incubated on board ship. This implies enhanced cycling of oxygen and carbon relative to that prevailing in the in situ samples. In situ experiments more closely replicate the natural conditions, and are assumed to give truer estimates of metabolic rates in the wild.
The difference in behaviour between the two sets of samples must reflect some difference in incubation conditions. A number of possibilities can be easily eliminated. Temperature was identical for both sets of samples. Irradiance in the shipboard incubations was equivalent to irradiance in situ at a depth of 25 m, similar to the collection and incubation depths for most of the comparable in situ samples. Water collection and handling was similar for both sets of experiments, except for the fact that Na gas was bubbled through the 'shipboard' samples only; we believe that Ne gas purging could not have caused these discrepancies. UV light cannot be a factor, as most samples were incubated in Pyrex bottles.
Having dismissed these four variables, we suggest that it was the difference in spectral quality of light between 'shipboard' and in situ incubations which caused the observed differences in production rates. In the open ocean, light of wavelengths less than -350 nm and greater than -520 nm is preferentially attenuated with depth (JERLOV, 1968). We envision two ways in which the difference in spectral quality could have raised productivities of the 'shipboard' samples. First, higher rates of production observed in 'shipboard' incubations may have been caused by a photosynthetic response to the presence of visible light of those wavelengths where attenuation is very rapid in seawater. Work of NEORI et al. (1984), GLOVER et al. (1987) and SATHYENDRANATH et al. (1987) suggests that algal populations can adapt their pigment complement to the in situ wavelength spectrum of light examined, although spectral adaptation is not always observed in natural oceanic populations (LEwis et al., 1985). Perhaps we should heed the precaution of KIEFER and STRICKLAND (1970), who stated "sampling depths cannot be set by matching the in situ quanta meter readings with the readings for deck incubators fitted with neutral filters; in productivity w o r k . . , deck incubators that simulate submarine light intensity and spectral composition are required."
Second, spectral quality could influence production rates by influencing redox transfor- mations of trace metals in solution. The broader wavelength range of visible light in the
1632 K.D. GRANDE et al.
'shipboard' incubations may have allowed more rapid redox cycling of bioactive trace metals (either directly or by reaction with hydrogen peroxide). This process could alter photosynthetic rates by changing the concentrations of both essential and toxic trace metals in the incubated seawater (ZIr, A et al., 1985; SUNDA, 1987; HON~ and KESXER, 1986; W. MILLER, personal communication). Of course, this hypothesis requires trace metal limitation of phytoplankton in the North Pacific central gyre (ANDERSON and MOREL, 1982; MARTIN and FITZWATER, 1988; MARTIN and GORDON, 1988), a controversial hypothesis.
CONCLUSIONS
In summary, three independent techniques of measuring production show good agreement in in situ incubations, as well as in simulated in situ experiments where the surface illumination is reduced by >65%. Rates of 14C production, multiplied by the assumed photosynthetic quotient of 1.25, are found to lie between rates of net and 180 gross production. Rates of light respiration (180 gross production minus 02 net production) are within 20% of rates of respiration in the dark.
In incubations where bottles are kept at sea surface temperatures and exposed to 35% of incident light intensity, rates of gross production, measured by the He180 method, are 2-3 times greater than production rates measured by other techniques. The 14C production rates of mixed layer samples are on average 48% greater in 'shipboard' incubations than in in situ incubations (Tables 2 and 3). The 02 light/dark bottle technique for measuring production is relatively unaffected by incubation conditions. Rates of both gross oxygen production and respiration are therefore postulated to have increased in these incubations. These high rates of production and respiration are quite enigmatic and are considered to probably be an artifact of the experimental light field.
Our results imply that, in the top few meters of the ocean, where the spectral quality of light is similar to that at the sea surface, biological cycling may be considerably more rapid than in the underlying portion of the mixed layer. Our data certainly point to a problem in generalizing results from on-deck incubations in which neutral density screening is used to reduce irradiance by <35% from in situ values.
Previously, close agreement has been obtained between the 02 light/dark bottle method and the 14C method (WILLIAMS et al., 1983), with an incubation procedure similar to that used for our 'shipboard' incubations. In this study, we again found generally good agreement between these measures of production. However, with the 180 method, we also noted a marked photoenhancement of respiration in the 'shipboard' incubations. It may, in fact, be fortuitous that rates of 14C production and 02 gross production are equivalent when incubated at greater than in situ light intensities (e.g. SMITH et al., 1984).
Acknowledgements--We wish to thank all of the members of the PRPOOS cruise who provided analytical support, most notably, Ed Renger and Joe Orchardo. We would also like to thank Barbara Nowicki for nitrate analysis of the H2180 water and Doug Cullen for trace metal analyses. This research was supported by National Science Foundation grants OCE 84-10815 and OCE 86-09923 (Bender), OCE 81-21011 (Marra), OCE 83- 15448 (Eppley), and OCE 83-17382 (Williams); by UK Natural Environment Research Council grant GR3/ 4538 A (Williams), by Swedish National Research Council grant NFR 511940100-7 (Williams), and by travel grants form The Royal Society and the University of Southampton (Purdie). We gratefully acknowledge the support of the Master and crew of the R.V. Melville.
Primary production in the North Pacific gyre 1633
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