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The copper-complexing capacity of seawater
The Science of the Total Environment, 75 (1988) 151 167 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
151
THE C O P P E R - C O M P L E X I N G CAPACITY OF S E A W A T E R
DENIS J. MACKEY and HARRY W. HIGGINS
Division of Oceanography, CSIRO Marine Laboratories, P.O. Box 1538, Hobart, Tasmania 7001 (Australia)
ABSTRACT The strong copper-complexing capacity of seawater varies over three orders of magnitude. High values are associated with high phytoplankton biomass. When the biomass is low, the coppercomplexing capacity is low provided t h a t a moderate productivity (14C uptake) is sustained by a reliable source of nutrients. In such cases, the low biomass results from physical (deep mixing) or biological (heavy grazing) processes. In nutrient-limited, oligotrophic waters of low average productivity, the copper-complexing capacity is variable with occasional high values occurring. In the western Pacific, we found no evidence t h a t water upwelling along the equator was conditioned by the production of organic ligands. These results also suggest t h a t active grazing by herbivores does not release organic compounds into the water column.
INTRODUCTION
The biogeochemical cycling of the elements in tropical waters is different from that in temperate and polar waters. The high and constant solar irradiance throughout the year in the tropics produces a strong thermocline with phytoplankton-related parameters relatively independent of season. Thus, Dandonneau and Gohin (1984) detected no seasonal variations in seasurface chlorophyll concentrations at 15°S in the western Pacific over a 5-year period. The surface waters are depleted in both major (nitrate, phosphate and silicate) and minor nutrients (zinc and iron), as they are removed from the surface waters via particulates. New production in the euphotic zone is limited by the rate at which nutrients are added to the system. Nutrients are supplied at a low rate by aeolian deposition and vertical diffusion across the thermocline, while additional nitrate can be supplied from nitrogen fixation by cyanobacteria (Capone and Carpenter, 1982). Other mechanisms for supplying nutrients are localized in space (bottom topography) or time (wind events). While they may be locally important within the oligotrophic waters of the central ocean gyres, they will have little impact on the parameters associated with high turnover rates. Although phytoplankton biomass and chlorophyll concentrations may be low, it does not follow t h a t productivity (defined here as the uptake of 14C) is "also low. Heavy grazing by herbivores and rapid regeneration of nutrients (as
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152
proposed by Goldman et al., 1979) could lead to high productivity measurements even though the net addition to the biomass is small. Alternatively, as Eppley (1972) proposed, productivity is low because the phytoplankton are turning over at a low rate. In principle, it should be easy to distinguish between these alternatives, but in practice, there are difficulties (Eppley, 1980), including the following: (a) As surface waters in tropical regions are strongly depleted in trace metals as well as in the major nutrients, the endemic organisms are acclimatised to low trace-metal levels and should be studied under the clean conditions developed for measuring the concentrations of trace metals in seawater (Fitzwater et al., 1982). (b) The amount of 14C taken up after a fixed time (e.g. 24 h) gives no information on the rate of uptake unless the uptake is linear with time. Few measurements have been made at regular intervals over an appropriate time span. (c) There is generally a large dark uptake in oligotrophic waters; failure to recognize or satisfactorily account for this uptake renders many measurements of dubious value. (d) The particle-size distribution in oligotrophic surface waters changes dramatically within a few hours of sampling. How this affects subsequent measurements is unknown (see Harris et al., 1988). Sharp (1977) has questioned whether healthy phytoplankton cells normally exude organic matter, although they may do so under conditions of stress. Low nutrient levels, such as are found in oligotrophic waters, may be such a condition increasing the rate of release of organic matter by the organisms living in those waters (Ignatiades, 1973; Ignatiades and Fogg, 1973; Harris, 1978). In tropical and subtropical waters, there is no shortage of energy (light) or inorganic carbon (bicarbonate) to limit the production of organic compounds. If nutrient-stressed phytoplankton were releasing organic compounds, the stable thermocline would slow down the loss of such compounds through diffusion or convective overturn. These compounds could then accumulate above the thermocline if they had a long residence time. The high light intensities in the tropics could also lead to free radical-induced oxidative reactions, which would increase the number of ligand donor sites (oxygen atoms) and lead to an increase in the ability of compounds to complex trace metals. The mechanism would be similar to that proposed by Harvey et al. (1983) for the formation of marine humic and fulvic acids: it could increase the complexing capacity of the water while decreasing the concentration of the dissolved organic carbon (DOC). The complexing capacity of surface waters may therefore provide a long-term, integrated record of the nutrient stress of phytoplankton in the euphotic zone. The bioavailability of copper, iron, zinc and manganese has been shown to depend on the concentration of free metal ion; there is no evidence for the uptake of naturally occurring metal-organic complexes (Sunda and Guillard, 1976; Anderson et al., 1978; Anderson and Morel, 1982; Sunda and Huntsman, 1983). The formation of metal organic complexes must therefore decrease the fraction of trace metal available to the biota. Copper forms stronger metalorganic complexes in seawater than does any other trace metal at comparable
153 concentration, and hence most methods for measuring the complexing capacity of seawater determine the copper-complexing capacity. This parameter is of direct relevance to the biota, since copper is potentially the most toxic trace element in seawater. The copper-complexing capacity of seawater can be estimated by Mackey's (1983) method, an extension of Stolzberg and Rosin's (1977), which is based on the competition between Chelex-100 and naturally occurring ligands. The method determines only those ligands capable of forming copper complexes that are kinetically or thermodynamically stable to dissociation by Chelex-100. For thermodynamic stability, the effective stability constants must be > 10 H. In this paper, these measurements will be abbreviated as CuCC. In oceanic waters, the CuCC of seawater varies over approximately three orders of magnitude, while the concentration of DO C varies by a factor of about three (Williams, 1975). Organic compounds capable of complexing trace metals at the concentrations t h a t occur in seawater represent only a minor fraction of the total pool of DOC, which is not necessarily related to CuCC (the correlation coefficient between CuCC and DOC was found to be 0.08 in waters off north-east Australia; Mackey et al., 1987). The euphotic zone is a dynamic environment; when it is periodically stressed, the composition of the phytoplankton species in the water mass is likely to fluctuate (Harris, 1986). At any given time, a few species will be able to cope with the current conditions and will grow normally and assimilate nutrients at levels approximating the Redfield ratio (Redfield, 1934). Other species, perhaps a minor fraction of the biomass, will be stressed and will release the excess carbon accumulated in the attempt to acquire sufficient nutrients. Minor perturbations in the environment would therefore give a competitive advantage to one group, while another group declines, excreting organic compounds as the cells senesce. If this scenario is correct, a few species of phytoplankton would dominate the biomass and preserve the Redfield ratio, while other species, although a minor component of the biomass, would be responsible for the release of DOC into the environment. Consequently, an intermittent supply of nutrients to oligotrophic waters would produce large variations in CuCC, with occasional high values. Phytoplankton are also likely to exude organic ligands under conditions of trace-metal stress. The stress may be due to an excess of toxic metal, such as copper, or to a deficiency in an essential metal such as iron. These two categories overlap since some metals (e.g. zinc) may, depending on the concentration of the free metal ion in the environment, be either toxic or limiting. Trace-metal concentrations are high in coastal waters, so stress would most likely be caused by an excess of toxic metal. However, as the formation of metal-organics would decrease the concentration of free metal ion, any organism t h a t could exude organic ligands would have a competitive advantage. Upwelled waters may also produce an environment of trace-metal stress, since such waters are depleted in manganese and have a high ratio of free
154
copper ions to free manganese ions (Sunda and Huntsman, 1983). Steemann Nielsen and Wium-Andersen (1970) proposed that the production of extracellular organic matter capable of complexing trace metals was an important factor in the preconditioning of these waters before the biota could take advantage of the supply of major nutrients. As noted above, oligotrophic surface waters are strongly depleted in the essential trace metals zinc, manganese and iron. Copper is depleted to a lesser extent. The bioavailability of zinc, manganese and iron is, therefore, further reduced by competition with copper. The addition of organic ligands to these waters will preferentially complex copper. Although some iron and zinc may also be complexed, these metals (and manganese) should be more available to the biota. Thus the addition of organic-complexing agents may be beneficial under conditions of both high and low trace-metal abundances. While it is debatable whether organic compounds are exuded by healthy phytoplankton, they would certainly be released by cell lysis at the end of a phytoplankton bloom. Organic compounds may also be released during grazing by herbivorous zooplankton. The CuCC should therefore increase in the final stages of a phytoplankton bloom. Obviously, this would not reduce trace-metal stress for the bloom-organisms, but it could affect species succession. In summary, high CuCC values would be expected to occur during or after a period of high phytoplankton biomass. When the biomass is low, the CuCC will depend on the productivity of the water mass and, in particular, on whether the phytoplankton are subject to nutrient or trace-metal stress. Eutrophic waters are not considered in this paper. EXPERIMENTAL CuCC values were determined by spiking seawater with CuSO4 to a final concentration of 800 nM, leaving the sample to stand for a period of 3-6 months, filtering the solution (0.45#m) and removing the excess copper ions with Chelex-100, destroying the organic matter by UV photo-oxidation and analyzing the resultant solution for copper after preconcentration by a mixed dithiocarbamate/freon procedure. After spiking the seawater, all sample manipulations were carried out in a Class 100 clean room. Full details are given in Mackey (1983, 1984). For the PROLIGO samples, the UV photo-oxidation and preconcentration steps were omitted and copper was determined directly by GFAAS with Zeeman background correction (Perkin Elmer Zeeman 5000). These samples had CuCC values close to the detection limit of the direct injection technique (1-2 nM). A Variosens III (Impulsphysik GmbH) was used to measure in situ fluorescence and turbidity during cruises FR04/85 and FR09/86. On the first cruise, the instrument was lowered to a depth of 100 m and the response was measured on an analogue chart recorder using the deck unit supplied with the instrument. On FR09/86, the instrument was powered by a submersible battery
155 p a c k a n d t h e o u t p u t w a s i n t e r f a c e d t o a N e i l B r o w n C T D u n i t . S u r f a c e fluorescence on this cruise was also continuously monitored by a Turner fluorometer. D e t a i l s o f t h e a r e a s s a m p l e d a n d t h e t i m e s o f s a m p l e c o l l e c t i o n are g i v e n i n T a b l e 1. RESULTS T h e v a l u e s o f C u C C o v e r t h e top 2000 m for t h e G u l f o f C a l i f o r n i a a n d o p e n o c e a n w a t e r s are s h o w n i n F i g s 1-7. W i t h t h e e x c e p t i o n o f t h e S o u t h P a c i f i c a n d TABLE 1 Summary of sampling sites Cruise
Location
SP04/82 SP10/82 SPll/82 SP10/83 SP10/83
Indian Ocean South Pacific Coral Sea Wreck Reef GBR Lagoon Port Hacking Gulf of California Equatorial Pacific Fiji Basin Southern Ocean
SOMAP FR04/85 PROLIGO FR09/86
Dates 12-20°S, 5~20°S, 25~32°S, 22°S, 24°S, 34°S, 27°N, 0°S, 15°S, 43-57°S,
11~130°E 170°E 160°E 155°E 152°E 151°E lll°W 143-150°E 173°E 155°E
80
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i
i 0.8
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i
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0.8
i 1.0
Depth
[]
[] I
I
I
1.2
(kml
Fig. 1. CuCC on the SOMAP cruise in the Gulf of California.
] 1.4
D []
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n
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9.8
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May Oct Oct Jun
1982 1982 1982 1983
Nov Aug Sep Nov
1984 1985 1985 1985 1986
156 80
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'
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I
0.8 Depth
Fig. 2. CuCC
on
FR04/85
in
the
western
1.2
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1.8
2.0
Ikm)
equatorial
Pacific
Ocean.
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~%[][]oq ~ Dd=
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Depth (krn}
F i g . 3. C u C C o n S P 0 4 / 8 2 o n t h e N o r t h W e s t
Coral Sea generally In the (FR04/86)
Shelf
of Australia.
s t a t i o n s (SP10/82, S P l l / 8 2 ; Figs 4 and 5), t h e v a l u e s b e l o w 200 m w e r e < 10 nM, w i t h m a n y v a l u e s being < 5 nM. s u r f a c e w a t e r s (defined as < 200m), the CuCC varied from 0 . 1 n M to 77 n M (SP11/82; M a c k e y , 1986). On t h e basis of the r a n g e of v a l u e s
157 80
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Depth (km)
Fig. 4. CuCC on SP10/82 in the South Pacific Ocean. 8O
70
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1.2
I
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1.4
i
1.6
i
1.8
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Depth (I.¢m ]
Fig. 5. CuCC on SPll/82 in the Coral Sea. found in deeper waters, it is r e a s o n a b l e to s u g g e s t that ~ 5 n M is a baseline v a l u e in the e u p h o t i c zone, and that CuCC v a l u e s > 10 n M can be attributed to the in situ p r o d u c t i o n of o r g a n i c ligands. S u c h v a l u e s were measured at some stations from S O M A P , SP10/82, S P l l / 8 2 and SP10/83. CuCC v a l u e s in surface water were e s s e n t i a l l y indistinguishable from baseline v a l u e s for all stations
158 80
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[]
[] []
O
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Depth
I
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1.4
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1.8
2.0
1.4
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1.8
2.0
I
I
I
I
(~m}
Fig. 6. CuCC at the PROLIGO station in the Fiji Basin. 80
70
60
5O
E v O O
40
3 50
2O []
10
[3
o.
[]
o O.O
0.2
0.4
0.6
0.8 Depth
1.0
1.2
[ km}
Fig. 7. CuCC on FR09/86 in the Southern Ocean. s a m p l e d d u r i n g FR04/85, S P 0 4 / 8 2 , P R O L I G O a n d F R 0 9 / 8 6 (apart f r o m o n e s a m p l e c o l l e c t e d f r o m 6 m at 53°30'S, 155°E). C u C C d e p t h p r o f i l e s at h a l f - d e g r e e i n t e r v a l s a c r o s s t h e e q u a t o r a r e s h o w n in Fig. 8. M o s t o f t h e v a l u e s a r e < 10 n M , a n d m a n y a r e < 2 n M .
159 O.O
[]
D
[3
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0 []
0.1
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D []
[] []
[]
0.2
[]
[]
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[]
[]
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0.3 0.4-
[]
[]
[]
1.0°N
1.5°N
0.5
0.0
0.5°N
10%
0.5°S
0.6 [] []
0.7
O
0.8
[]
[] [] []
[] []
[]
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0.9 1.0 []
1.1 1.2_
i
0
[]
I
l
l
I
10
10
10
10
I
10
0
10
0
(riM)
CuCC
Fig. 8. C u C C a c r o s s the e q u a t o r at half-degree i n t e r v a l s from 1.5°N to 1.0°S at 150°E.
Values of CuCC from Wreck Reef and the lagoon of the Great Barrier Reef are shown in Figs 9 and 10. The variations in the CuCC to 300m have been attributed to local effects arising from the topography (Mackey et al., 1987). The PROLIGO cruise differed from the other cruises in that one station (at 80
70
60
50
0 0
4.0 [] 3O
[]
[]
D
[]
B
]
[]
10
[]
i
0.0
i
0.2
i
i
i
0.4
0.6
i
i
i
0.8
i
1.0
Depth (kin)
Fig. 9. C u C C o n SP10/83 at W r e c k Reef.
i
i
1.2
i
i
i
1.4
1.6
i
i
1.8
i
2.0
160 80
70
6O
50
vE 0
40
0 30 n 20 El [ ]
!
10
[] []
0
i 0.0
i 0.2
i
i
0.4
~
i
0.6
1
i
I
0.8
i
i
1.0
i
1.2
I
J 1.4
I
i 1.6
I
i
1.8
]
2.0
D e p t h (km)
Fig. 10. CuCC on SP10/83 in the Great Barrier Reef. 15°S, 173°E) was o c c u p i e d almost c o n t i n u a l l y for 22 days. The e x p e d i t i o n was designed to m o n i t o r physical, chemical and biological p a r a m e t e r s o v e r an e x t e n d e d period in an o l i g o t r o p h i c r e g i o n w h e r e seasonal influences on product i v i t y and biomass were expected to be minimal ( D a n d o n n e a u and Gohin, 1984). M e a s u r e m e n t s of CuCC were g e n e r a l l y confined to the e u p h o t i c zone and to depths of 500-800m (Fig. 6). High v a l u e s of CuCC had been m e a s u r e d n e a r the salinity m i n i m u m on cruises SP10/82 and S P l l / 8 2 , but this was not the case on the P R O L I G O s t a t i o n w h e r e the salinity m i n i m u m o c c u r r e d at ~ 650m. All CuCC v a l u e s w i t h i n the top 200 m were averaged, e a c h day, o v e r four depth ranges. T h e s e a v e r a g e values are plotted as a f u n c t i o n of time in Fig. 11. A p a r t from one high value, t h e r e were no significant changes in CuCC, even t h o u g h the r a t e of in situ fixation of c a r b o n i n c r e a s e d by a f a c t o r of a b o u t five w h e n n u t r i e n t s were added to the e u p h o t i c zone by b r e a k i n g i n t e r n a l waves ( D a n d o n n e a u and Lemasson, 1987). As five cruises (SP10/82, S P l l / 8 2 , SP10/83, FR04/85 and FR09/86) were at l o n g i t u d e s of 155 ° _+ 15°E, the d a t a for the top 200m (exlcuding the G r e a t B a r r i e r R e e f l a g o o n values) are combined in Fig. 12 to o b t a i n an i n d i c a t i o n of the v a r i a t i o n of CuCC in the e u p h o t i c zone with latitude. CuCC values were g e n e r a l l y < 10 n M at high and low latitudes. B e t w e e n 20°S and 3O°S h i g h e r v a l u e s were often observed, but t h e r e was m u c h variability. In the T a s m a n and Coral Seas, along 155°E, J i t t s (1965) f o u n d t h a t the u p t a k e of 14C was high at 45°S, d e c r e a s e d by more t h a n an o r d e r of m a g n i t u d e at 20°S and i n c r e a s e d again t o w a r d s 5°S (Fig. 13). W i t h o u t full details of his m e t h o d o l o g y , it is difficult to d i r e c t l y c o m p a r e his and o u r data; however, r e c e n t m e a s u r e m e n t s of productiv-
161 10
8 7
C V 0 0
5 4
\ 5
\
1 I
0 260
l
l
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262
l
l
l
264-
l 266
I
i
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270
I
i 272
i
I 274
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i 276
I
i 278
I 280
Jution Day
Fig. 11. V a r i a t i o n of CuCC w i t h t i m e at the PROLIGO station. V a l u e s w e r e averaged over depth i n t e r v a l s of ( ~ 5 0 m (D), 5 1 - 9 0 m ( O ) , 91 1 4 0 m (zx) a n d 141 2 0 0 m ( v ) .
80
70
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4-0 [] []
50
[]
i rlD
20
DB
[]
D D
10 ]
0
D 10°N
i 10%
30%
50%
70°s
Fig. 12. Variation of CuCC in the top 200m along 155°E. ity by Harris et al. (1987) h a v e confirmed the s a m e g e n e r a l trend. In contrast, the CuCC v a l u e s w e r e l o w at t h e e q u a t o r and at 57°S, w h i l e h i g h v a l u e s w e r e f o u n d at i n t e r m e d i a t e latitudes. Barber and R y t h e r (1969) s u g g e s t e d that w a t e r u p w e l l i n g a l o n g t h e e q u a t o r
162 70
[] []
60
[]
50 D E []
40
D
\ o [] 30 [] oL []
CI~DD
20 [] rT~
[]
[]
[]
10 []
5~ r~ [33
[] []
0
D 1 (3°N
I 10%
I
I
[
30°5
I 50%
I 70%
Fig. 13. Variation in productivity along 155E (from Jitts, 1965). in the eastern Pacific required ~preconditioning' before it was suitable for active growth of phytoplankton. They postulated t h a t marine organisms released organic compounds into the water, thereby increasing the bioavailability of trace metals. Steeman Nielsen and Wium-Andersen (1970) subsequently proposed th at the conditioning was due to organic compounds decreasing the bioavailability of toxic trace metals - - probably copper. Active growth of p h y t o p l a n k t o n was observed after the upwelled water had been advected 1-2 degrees away from the equator. However, we observed no minimum in the CuCC values of surface waters at the equator. Low values were found at l°S and, apart from one value at 846 m, the CuCC was < 0.6 n M b e t w e e n the surface and 1100 m. Surface samples were collected from H ung ry Point in Port Hacking estuary from F e b r u a r y t hr ough November 1984 (Mackey and Szymczak, 1988). The results are shown in Fig. 14. The estuary, 20 km south of Sydney, is marinedominated, comparatively free of pollution and has copper concentrations of 19 _+ 15 n M (n = 50) (Mackey and Szymczak, unpublished results). During the period th at p h y t o p l a n k t o n blooms are known to occur, the CuCC increased smoothly from 5-10 to 59 nM, remaining > 10 n M for about a month. It is not known whether the peak value of CuCC coincided with the peak in productivity or biomass, or whether it occurred after the bloom had crashed, as the productivity was not measured. DISCUSSION Complexing capacity values ranging from < 10 n M in the Sargasso Sea to 1681 n M in the productive waters off the s out heast ern coast of the U.S.A. have
163
80
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o
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0 25
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1O0
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350
Julian Day
Fig. 14. Variation of CuCC in Port Hacking during 1984. been reported by Wood et al. (1983), who used a technique similar to ours. The elevated values (up to 136 n M ) we found near 1000 m in the South Pacific and Coral Sea can n ot be due to in situ production by phyt opl ankt on and are unlikely to originate from marine bacteria t hat produce organic ligands at intermediate depths only in this general region. The high CuCC values found at depth during these cruises (Mackey, 1986) are attributable to horizontal advection from the S o u t h e r n Ocean since they occurred near the salinity minimum t h a t defines the Antarctic Intermediate Water (AIW). If this interpretation is correct, CuCC values in excess of 136nM should occur in the S ou th er n Ocean at times of high biomass. In the present study, CuCC values in surface waters varied from 0. 1nM (FR09/86) to 7 7 n M (SPll/82) and the latter value may not be indicative of those t hat could occur at very high chlorophyll or biomass concentrations. High p h y t o p l a n k t o n biomass was not observed in the Sout hern Ocean during FR09/86. While the productivity was moderate (0.4-1.8 mg C m 3h- 1), the chlorophyll a levels were low (0.2~).6 pg l- 1; D. Everitt, unpublished results) and the in situ fluorescence and turbidity of surface waters were near the limits of detection of the Variosens III. Reasonable depth profiles of in situ fluorescence and turbidity were obtained at a number of stations, but the lack of reliable surface data prevented us from comparing the instrument response with th at of the T u r n e r fluorometer. At these latitudes, the biomass is limited by convection. A stable thermocline had not developed by November. Strong winds (Force 11) during the cruise would have caused deep mixing and kept the biomass low. During FR04/85, the in situ fluorescence and turbidity were below the
164
detection limits of the Variosens III even though the equator is a moderately productive region with nutrients being continually supplied by upwelling. Measurements of 14C uptake during this cruise (F.B. Griffiths, unpublished results) indicated grazing rates were high, which probably limited the biomass in these waters. The low CuCC values observed in surface waters on both these cruises are therefore indicative of low biomass in productive waters. In contrast to the uniformly low values of CuCC found near the equator and in the Southern Ocean, the CuCC was very variable within the euphotic zone at intermediate latitudes (Fig. 12). No measurements of biomass were made for the stations in the Coral and Tasman Seas (SP10/82 and SPll/82), but these stations are in regions that are generally considered oligotrophic (Dandonneau and Lemasson, 1987). Surface concentrations of nutrients were low (0.050.12 pMPO4, (~0.5 p M N Q ) . The variations in CuCC near Wreck Reef could be attributed to local effects (Mackey et al., 1987), but similar values were obtained during SP10/82, SPl l / 82 and within the lagoon of the Great Barrier Reef on SP10/83 (Fig. 10). This pa t t e r n supports the hypothesis t hat high CuCC values can occur in oligotrophic waters under conditions of n u t r i e n t limitation or trace-metal stress (see Introduction). The PROLIGO station was expected to exhibit the high variability in CuCC found earlier on cruises SP10/82, SPll/82 and SP10/83. However, none of the 57 samples analyzed from the top 200 m had CuCC values > 10 nM. The results, which are similar to those obtained from near the equator and from the S ou th er n Ocean (Fig. 12), indicate t hat productivity was high and biomass low. In tropical waters this would imply t hat there is a reliable source of nutrients (in this case from breaking internal waves; D andonneau and Lemasson, 1987) and a high grazing rate. New production at the site was estimated to be 2 2 m g C m - 2 h 1. Low values of CuCC were also observed on the North West Shelf of Australia (Fig. 3). N u t r i e n t enrichment was attributed to a combination of terrestrial run-off and interaction with the sediments. At the time of sampling, in situ measurements of fluorescence (using a Variosens II) suggested t hat the biomass was low and was not correlated with n u t r i e n t concentrations in the surface water (Mackey, 1984). The data from Port Hacking give an indication of the range of CuCC values expected during blooms in coastal waters. The CuCC values were comparable to the copper concentrations in the estuary. No measurements of productivity or biomass were u n d e r t a k e n during this time, as the site is one of the best characterized in Australia, with over 40 years of data collected. Diatom blooms t h at occur about October are triggered by the i n t r u s i o n of nutrient-rich slopewater into the euphotic zone (Mackey and Szymczak, 1988). Chlorophyll a levels rise to > 250mgm 2 (Hallegraeff, 1981), which is about an order of magnitude higher t han the level found at the PROLIGO site (Dandonneau and Lemasson, 1987). The concentrations of chlorophyll within the water column can rise as high as 15pgl ' (Hallegraeff, 1981). The high CuCC values found
165
during October 1984 are due to high phytoplankton biomass, but it is not known whether the organic ligands were released into the water column by actively growing cells or from senescent cells. CONCLUSIONS
When the biomass is high, the CuCC of seawater may be as high as 60 n M (Port Hacking) and possibly much higher, if the values in the AIW found during SPll/82 are due to ligands produced within the euphotic zone at high latitudes. High biomass in these waters is strongly dependent on season (light) and on the wind dropping long enough for the water column to become stratified. High CuCC values are expected to be localized in these waters. The association of high biomass with high copper complexing capacity (1681 nM) has also been observed by Wood et al. (1983). Low biomass in oceanic waters can be a result of one of three processes. The first is characterized by high productivity (14C uptake) and active removal of new production, leading to a high flux of nutrients and energy through the system. There must be a steady supply of nutrients, which can arise from upwelling (FR04/85, FR09/86) or the breaking of internal waves (PROLIGO) and also a rapid removal of autotrophic organisms by processes such as grazing (FR04/85, PROLIGO) or deep mixing (FR09/86). Under such conditions, all the phytoplankton are growing at near-optimal rates and excrete little organic matter, with the result t h a t the CuCC is uniformly low. The association of high grazing rates with low values of CuCC implies that 'sloppy grazing' by herbivores is not a significant source of organic ligands in seawater. Since there is no reason to expect 'sloppy grazing' to release only organic compounds capable of complexing trace metals, it is inferred that this process does not contribute significantly to the DOC in seawater. The low CuCC values found near the equator implies t h a t the organisms growing in the freshly upwelled water are not subject to trace-metal stress. In the second process, productivity is intermittently high, with strong fluxes localized in space and time. Patchiness of nutrients in phytoplankton communities has been found to extend down to millimeter scales (Lehman and Scavia, 1982). The average productivity and flux of matter through such a system is low, as is the average concentration of grazers. Some autotrophs would be growing under conditions of nutrient stress, and the low concentration of grazers would allow cells to senesce when the supply of nutrients was exhausted. The strong thermocline would enable organic compounds, released under these conditions, to accumulate. The CuCC of such waters would be variable, with occasional high values occurring, as was found during SP10/82, SPll/82 and SP10/83. The third process, which produces low productivity on all spatial and temporal scales, is the traditional picture of oligotrophic waters with new production always occurring under conditions of nutrient limitation. Recent work suggests that this scenario does not apply to the oligotrophic regions of
166 t h e o c e a n s ( K e r r , 1986) a n d i t is d i f f i c u l t t o s e e h o w l o w u n i f o r m p r o d u c t i v i t y could produce the range of CuCC values found in subtropical waters. ACKNOWLEDGEMENTS T h e a u t h o r s w o u l d l i k e t o t h a n k L. L e m a s s o n f o r i n v i t i n g u s t o p a r t i c i p a t e i n t h e P R O L I G O e x p e r i m e n t , A. Z i r i n o f o r i n v i t i n g u s t o p a r t i c i p a t e i n t h e S O M A P cruise, and t h e m a s t e r s and c r e w of t h e N.O. J e a n C h a r c o t , U.S.N.S. D e S t e i g u e r , R.V. S p r i g h t l y a n d R.V. F r a n k l i n f o r t h e i r h e l p i n c o l l e c t i n g s a m p l e s . W e w o u l d a l s o l i k e t o e x p r e s s o u r a p p r e c i a t i o n t o R. S z y m c z a k , G. D a l P o n t and J. A t a c k for p e r f o r m i n g the analyses. F i n a l l y , we w o u l d like to e x p r e s s o u r a p p r e c i a t i o n o f o u r u s e f u l d i s c u s s i o n s w i t h G. H a r r i s , F . B . G r i f f i t h s a n d D. E v e r i t t . REFERENCES Anderson, M.A. and F.M.M. Morel, 1982. The influence of aqueous iron chemistry on the uptake of iron by the coastal diatom Thalassiosira weissflogii. Limnol. Oceanogr., 27: 789-813. Anderson, M.A., F.M.M. Morel and R.R.L. Guillard, 1978. Growth limitation of a coastal diatom by low zinc ion activity. Nature (London), 276; 70-71. Barber, R.T. and J.H. Ryther, 1969. Organic chelators: factors affecting primary production in the Cromwell Current upwelling. J. Exp. Mar. Biol. Ecol., 3:191 199. Capone, D.G. and E.J. Carpenter, 1982. Nitrogen fixation in the marine environment. Science, 217: 1140-1142. Dandonneau, Y. and F. Gohin, 1984, Meridional and seasonal variations of the sea surface chlorophyll concentration in the southwestern tropical Pacific (14 to 32°S, 160 to 175°E). Deep-Sea Res., 31: 1377-1393. Dandonneau, Y. and L. Lemasson, 1987. Water-column chlorophyll in an oligotrophic environment: correction for the sampling depths and variations of the vertical structure of density, and observation of a growth period. J. Plankton Res., 9: 215-234. Eppley, R.W., 1972. Temperature and phytoplankton growth in the sea. Fish. Bull., 70: 1063-1085. Eppley, R.W., 1980. Estimating phytoplankton growth rates in the central oligotrophic oceans. In: P.G. Falkowski (Ed.), Primary productivity in the sea, Plenum, New York, pp. 231 242. Fitzwater, S.E., G.A. Knauer and J.H. Martin, 1982. Metal contamination and its effect on primary production measurements. Limnol. Oceanogr., 27: 544~551. Goldman, J.C., J.J. McCarthy and D.G. Peavey, 1979. Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature (London), 279: 210-215. Hallegraeff, G.M., 1981. Seasonal study of phytoplankton pigments and species at a coastal station off Sydney: importance of diatoms and the nanoplankton. Mar. Biol.i 61:107 118. Harris, G.P., 1978. Photosynthesis, productivity and growth: the physiological ecology of phytoplankton. Arch. Hydrobiol. Beih. Ergeb. Limnol., 10:1 171. Harris, G.P., 1986. Phytoplankton Ecology: Structure, Function and Fluctuation. Chapman and Hall, London. Harris, G.P., G.G. Ganf and D.P. Thomas, 1987. Productivity, growth rates and cell size distributions of phytoplankton in the SW Tasman Sea: implications for carbon metabolism in the photic zone. J. Plankton Res., 9:1003 1030. Harris, G.P., F.B. Grifftihs and D.P. Thomas, 1988. Light and dark uptake and loss of 14C: methodological problems with productivity measurements in oceanic waters. Hydrobiologia, in press. Harvey, G.R., D.A. Boran, L.A. Chesal and J.M. Tokar, 1983. the structure of marine fulvic and humic acids. Mar. Chem., 12: 11~132.
167 Ignatiades, L., 1973. Studies on the factors affecting the release of organic matter by Skeletonema costatum (Greville) Cleve in field conditions. J. Mar. Biol. Assoc. U.K., 53: 923-935. Ignatiades, L. and G.E. Fogg, 1973. Studies on the factors affecting the release of organic matter by Skeletonema costatum (Greville) Cleve in culture. J. Mar. Biol. Assoc. U.K., 53:937 956. Jitts, H.R., 1965. The summer characteristics of primary productivity in the Tasman and Coral Seas. Aust. J. Mar. Freshwater Res., 16: 151-162. Kerr, R.A., 1986. The ocean's deserts are blooming. Science, 232: 1345. Lehman, J.T. and D. Scavia, 1982. Microscale patchiness of nutrients in p l a n k t o n communitites. Science, 216: 729-730. Mackey, D.J., 1983. The strong complexing capacity of seawater - - an investigation of southeastern Australian coastal waters. Mar, Chem., 14: 73-87. Mackey, D.J., 1984. Trace metals and the productivity of shelf waters off North West Australia. Aust. J. Mar. Freshwater Res., 35: 505-516. Mackey, D.J., 1986. Copper-complexing capacity of South Pacific Waters. Aust. J. Mar. Freshwater Res., 37:437 450. Mackey, D.J. and R. Szymczak, 1988. Seasonal variations in the copper complexing capacity of Port Hacking. Aust. J. Mar. Freshwater Res., in press. Mackey, D.J., R. Szymczak, M. Tomczak Jr. and Y. Gu, 1987. Effects of mixed-layer depth and an isolated coral reef on the strong complexing capacity of oligotrophic waters. Aust. J. Mar. Freshwater Res., 38: 491499. Redfield, A.C., 1934. James J o h n s t o n e Memorial Volume. Liverpool University Press. Sharp, J.H., 1977. Excretion of organic matter by marine phytoplankton: Do healthy cells do it? Limnol. Oceanogr., 22:381 399. Steemann Nielsen, E. and S. Wium-Andersen, 1970. Copper ions as poison in the sea and in freshwater. Mar. Biol., 6: 93-97. Stolzberg, R.J. and D. Rosin, 1977. Chromatographic measurement of submicromolar strong complexing capacity in phytoplankton media. Anal. Chem., 49: 226-230. Sunda, W. and R.R.L. Guillard, 1976. The relationship between cupric ion activity and the toxicity of copper to phytoplankton. J. Mar. Res., 34:511 529. Sunda, W.G. and S.A. Huntsman, 1983. Effect of competitive interactions between manganese and copper on cellular manganese and growth in estuarine and oceanic species of the diatom Thalassiosira. Limnol. Oceanogr. 28: 924~934. Williams, P.J.Le.B., 1975. Biological and chemical aspects of dissolved organic material in sea water. In: J.P. Riley and G. Skirrow (Eds), Chemical Oceanography, Vol. 2. Academic Press, London, pp. 301-363. Wood, A.M., D.W. Evans and J.J. Alberts, 1983. Use of an ion exchange technique to measure copper complexing capacity on the continental shelf of the southeastern United States in the Sargasso Sea. Mar. Chem., 13: 305-326.
151
THE C O P P E R - C O M P L E X I N G CAPACITY OF S E A W A T E R
DENIS J. MACKEY and HARRY W. HIGGINS
Division of Oceanography, CSIRO Marine Laboratories, P.O. Box 1538, Hobart, Tasmania 7001 (Australia)
ABSTRACT The strong copper-complexing capacity of seawater varies over three orders of magnitude. High values are associated with high phytoplankton biomass. When the biomass is low, the coppercomplexing capacity is low provided t h a t a moderate productivity (14C uptake) is sustained by a reliable source of nutrients. In such cases, the low biomass results from physical (deep mixing) or biological (heavy grazing) processes. In nutrient-limited, oligotrophic waters of low average productivity, the copper-complexing capacity is variable with occasional high values occurring. In the western Pacific, we found no evidence t h a t water upwelling along the equator was conditioned by the production of organic ligands. These results also suggest t h a t active grazing by herbivores does not release organic compounds into the water column.
INTRODUCTION
The biogeochemical cycling of the elements in tropical waters is different from that in temperate and polar waters. The high and constant solar irradiance throughout the year in the tropics produces a strong thermocline with phytoplankton-related parameters relatively independent of season. Thus, Dandonneau and Gohin (1984) detected no seasonal variations in seasurface chlorophyll concentrations at 15°S in the western Pacific over a 5-year period. The surface waters are depleted in both major (nitrate, phosphate and silicate) and minor nutrients (zinc and iron), as they are removed from the surface waters via particulates. New production in the euphotic zone is limited by the rate at which nutrients are added to the system. Nutrients are supplied at a low rate by aeolian deposition and vertical diffusion across the thermocline, while additional nitrate can be supplied from nitrogen fixation by cyanobacteria (Capone and Carpenter, 1982). Other mechanisms for supplying nutrients are localized in space (bottom topography) or time (wind events). While they may be locally important within the oligotrophic waters of the central ocean gyres, they will have little impact on the parameters associated with high turnover rates. Although phytoplankton biomass and chlorophyll concentrations may be low, it does not follow t h a t productivity (defined here as the uptake of 14C) is "also low. Heavy grazing by herbivores and rapid regeneration of nutrients (as
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proposed by Goldman et al., 1979) could lead to high productivity measurements even though the net addition to the biomass is small. Alternatively, as Eppley (1972) proposed, productivity is low because the phytoplankton are turning over at a low rate. In principle, it should be easy to distinguish between these alternatives, but in practice, there are difficulties (Eppley, 1980), including the following: (a) As surface waters in tropical regions are strongly depleted in trace metals as well as in the major nutrients, the endemic organisms are acclimatised to low trace-metal levels and should be studied under the clean conditions developed for measuring the concentrations of trace metals in seawater (Fitzwater et al., 1982). (b) The amount of 14C taken up after a fixed time (e.g. 24 h) gives no information on the rate of uptake unless the uptake is linear with time. Few measurements have been made at regular intervals over an appropriate time span. (c) There is generally a large dark uptake in oligotrophic waters; failure to recognize or satisfactorily account for this uptake renders many measurements of dubious value. (d) The particle-size distribution in oligotrophic surface waters changes dramatically within a few hours of sampling. How this affects subsequent measurements is unknown (see Harris et al., 1988). Sharp (1977) has questioned whether healthy phytoplankton cells normally exude organic matter, although they may do so under conditions of stress. Low nutrient levels, such as are found in oligotrophic waters, may be such a condition increasing the rate of release of organic matter by the organisms living in those waters (Ignatiades, 1973; Ignatiades and Fogg, 1973; Harris, 1978). In tropical and subtropical waters, there is no shortage of energy (light) or inorganic carbon (bicarbonate) to limit the production of organic compounds. If nutrient-stressed phytoplankton were releasing organic compounds, the stable thermocline would slow down the loss of such compounds through diffusion or convective overturn. These compounds could then accumulate above the thermocline if they had a long residence time. The high light intensities in the tropics could also lead to free radical-induced oxidative reactions, which would increase the number of ligand donor sites (oxygen atoms) and lead to an increase in the ability of compounds to complex trace metals. The mechanism would be similar to that proposed by Harvey et al. (1983) for the formation of marine humic and fulvic acids: it could increase the complexing capacity of the water while decreasing the concentration of the dissolved organic carbon (DOC). The complexing capacity of surface waters may therefore provide a long-term, integrated record of the nutrient stress of phytoplankton in the euphotic zone. The bioavailability of copper, iron, zinc and manganese has been shown to depend on the concentration of free metal ion; there is no evidence for the uptake of naturally occurring metal-organic complexes (Sunda and Guillard, 1976; Anderson et al., 1978; Anderson and Morel, 1982; Sunda and Huntsman, 1983). The formation of metal organic complexes must therefore decrease the fraction of trace metal available to the biota. Copper forms stronger metalorganic complexes in seawater than does any other trace metal at comparable
153 concentration, and hence most methods for measuring the complexing capacity of seawater determine the copper-complexing capacity. This parameter is of direct relevance to the biota, since copper is potentially the most toxic trace element in seawater. The copper-complexing capacity of seawater can be estimated by Mackey's (1983) method, an extension of Stolzberg and Rosin's (1977), which is based on the competition between Chelex-100 and naturally occurring ligands. The method determines only those ligands capable of forming copper complexes that are kinetically or thermodynamically stable to dissociation by Chelex-100. For thermodynamic stability, the effective stability constants must be > 10 H. In this paper, these measurements will be abbreviated as CuCC. In oceanic waters, the CuCC of seawater varies over approximately three orders of magnitude, while the concentration of DO C varies by a factor of about three (Williams, 1975). Organic compounds capable of complexing trace metals at the concentrations t h a t occur in seawater represent only a minor fraction of the total pool of DOC, which is not necessarily related to CuCC (the correlation coefficient between CuCC and DOC was found to be 0.08 in waters off north-east Australia; Mackey et al., 1987). The euphotic zone is a dynamic environment; when it is periodically stressed, the composition of the phytoplankton species in the water mass is likely to fluctuate (Harris, 1986). At any given time, a few species will be able to cope with the current conditions and will grow normally and assimilate nutrients at levels approximating the Redfield ratio (Redfield, 1934). Other species, perhaps a minor fraction of the biomass, will be stressed and will release the excess carbon accumulated in the attempt to acquire sufficient nutrients. Minor perturbations in the environment would therefore give a competitive advantage to one group, while another group declines, excreting organic compounds as the cells senesce. If this scenario is correct, a few species of phytoplankton would dominate the biomass and preserve the Redfield ratio, while other species, although a minor component of the biomass, would be responsible for the release of DOC into the environment. Consequently, an intermittent supply of nutrients to oligotrophic waters would produce large variations in CuCC, with occasional high values. Phytoplankton are also likely to exude organic ligands under conditions of trace-metal stress. The stress may be due to an excess of toxic metal, such as copper, or to a deficiency in an essential metal such as iron. These two categories overlap since some metals (e.g. zinc) may, depending on the concentration of the free metal ion in the environment, be either toxic or limiting. Trace-metal concentrations are high in coastal waters, so stress would most likely be caused by an excess of toxic metal. However, as the formation of metal-organics would decrease the concentration of free metal ion, any organism t h a t could exude organic ligands would have a competitive advantage. Upwelled waters may also produce an environment of trace-metal stress, since such waters are depleted in manganese and have a high ratio of free
154
copper ions to free manganese ions (Sunda and Huntsman, 1983). Steemann Nielsen and Wium-Andersen (1970) proposed that the production of extracellular organic matter capable of complexing trace metals was an important factor in the preconditioning of these waters before the biota could take advantage of the supply of major nutrients. As noted above, oligotrophic surface waters are strongly depleted in the essential trace metals zinc, manganese and iron. Copper is depleted to a lesser extent. The bioavailability of zinc, manganese and iron is, therefore, further reduced by competition with copper. The addition of organic ligands to these waters will preferentially complex copper. Although some iron and zinc may also be complexed, these metals (and manganese) should be more available to the biota. Thus the addition of organic-complexing agents may be beneficial under conditions of both high and low trace-metal abundances. While it is debatable whether organic compounds are exuded by healthy phytoplankton, they would certainly be released by cell lysis at the end of a phytoplankton bloom. Organic compounds may also be released during grazing by herbivorous zooplankton. The CuCC should therefore increase in the final stages of a phytoplankton bloom. Obviously, this would not reduce trace-metal stress for the bloom-organisms, but it could affect species succession. In summary, high CuCC values would be expected to occur during or after a period of high phytoplankton biomass. When the biomass is low, the CuCC will depend on the productivity of the water mass and, in particular, on whether the phytoplankton are subject to nutrient or trace-metal stress. Eutrophic waters are not considered in this paper. EXPERIMENTAL CuCC values were determined by spiking seawater with CuSO4 to a final concentration of 800 nM, leaving the sample to stand for a period of 3-6 months, filtering the solution (0.45#m) and removing the excess copper ions with Chelex-100, destroying the organic matter by UV photo-oxidation and analyzing the resultant solution for copper after preconcentration by a mixed dithiocarbamate/freon procedure. After spiking the seawater, all sample manipulations were carried out in a Class 100 clean room. Full details are given in Mackey (1983, 1984). For the PROLIGO samples, the UV photo-oxidation and preconcentration steps were omitted and copper was determined directly by GFAAS with Zeeman background correction (Perkin Elmer Zeeman 5000). These samples had CuCC values close to the detection limit of the direct injection technique (1-2 nM). A Variosens III (Impulsphysik GmbH) was used to measure in situ fluorescence and turbidity during cruises FR04/85 and FR09/86. On the first cruise, the instrument was lowered to a depth of 100 m and the response was measured on an analogue chart recorder using the deck unit supplied with the instrument. On FR09/86, the instrument was powered by a submersible battery
155 p a c k a n d t h e o u t p u t w a s i n t e r f a c e d t o a N e i l B r o w n C T D u n i t . S u r f a c e fluorescence on this cruise was also continuously monitored by a Turner fluorometer. D e t a i l s o f t h e a r e a s s a m p l e d a n d t h e t i m e s o f s a m p l e c o l l e c t i o n are g i v e n i n T a b l e 1. RESULTS T h e v a l u e s o f C u C C o v e r t h e top 2000 m for t h e G u l f o f C a l i f o r n i a a n d o p e n o c e a n w a t e r s are s h o w n i n F i g s 1-7. W i t h t h e e x c e p t i o n o f t h e S o u t h P a c i f i c a n d TABLE 1 Summary of sampling sites Cruise
Location
SP04/82 SP10/82 SPll/82 SP10/83 SP10/83
Indian Ocean South Pacific Coral Sea Wreck Reef GBR Lagoon Port Hacking Gulf of California Equatorial Pacific Fiji Basin Southern Ocean
SOMAP FR04/85 PROLIGO FR09/86
Dates 12-20°S, 5~20°S, 25~32°S, 22°S, 24°S, 34°S, 27°N, 0°S, 15°S, 43-57°S,
11~130°E 170°E 160°E 155°E 152°E 151°E lll°W 143-150°E 173°E 155°E
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s t a t i o n s (SP10/82, S P l l / 8 2 ; Figs 4 and 5), t h e v a l u e s b e l o w 200 m w e r e < 10 nM, w i t h m a n y v a l u e s being < 5 nM. s u r f a c e w a t e r s (defined as < 200m), the CuCC varied from 0 . 1 n M to 77 n M (SP11/82; M a c k e y , 1986). On t h e basis of the r a n g e of v a l u e s
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Fig. 5. CuCC on SPll/82 in the Coral Sea. found in deeper waters, it is r e a s o n a b l e to s u g g e s t that ~ 5 n M is a baseline v a l u e in the e u p h o t i c zone, and that CuCC v a l u e s > 10 n M can be attributed to the in situ p r o d u c t i o n of o r g a n i c ligands. S u c h v a l u e s were measured at some stations from S O M A P , SP10/82, S P l l / 8 2 and SP10/83. CuCC v a l u e s in surface water were e s s e n t i a l l y indistinguishable from baseline v a l u e s for all stations
158 80
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Fig. 6. CuCC at the PROLIGO station in the Fiji Basin. 80
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Fig. 7. CuCC on FR09/86 in the Southern Ocean. s a m p l e d d u r i n g FR04/85, S P 0 4 / 8 2 , P R O L I G O a n d F R 0 9 / 8 6 (apart f r o m o n e s a m p l e c o l l e c t e d f r o m 6 m at 53°30'S, 155°E). C u C C d e p t h p r o f i l e s at h a l f - d e g r e e i n t e r v a l s a c r o s s t h e e q u a t o r a r e s h o w n in Fig. 8. M o s t o f t h e v a l u e s a r e < 10 n M , a n d m a n y a r e < 2 n M .
159 O.O
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CuCC
Fig. 8. C u C C a c r o s s the e q u a t o r at half-degree i n t e r v a l s from 1.5°N to 1.0°S at 150°E.
Values of CuCC from Wreck Reef and the lagoon of the Great Barrier Reef are shown in Figs 9 and 10. The variations in the CuCC to 300m have been attributed to local effects arising from the topography (Mackey et al., 1987). The PROLIGO cruise differed from the other cruises in that one station (at 80
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Fig. 9. C u C C o n SP10/83 at W r e c k Reef.
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Fig. 10. CuCC on SP10/83 in the Great Barrier Reef. 15°S, 173°E) was o c c u p i e d almost c o n t i n u a l l y for 22 days. The e x p e d i t i o n was designed to m o n i t o r physical, chemical and biological p a r a m e t e r s o v e r an e x t e n d e d period in an o l i g o t r o p h i c r e g i o n w h e r e seasonal influences on product i v i t y and biomass were expected to be minimal ( D a n d o n n e a u and Gohin, 1984). M e a s u r e m e n t s of CuCC were g e n e r a l l y confined to the e u p h o t i c zone and to depths of 500-800m (Fig. 6). High v a l u e s of CuCC had been m e a s u r e d n e a r the salinity m i n i m u m on cruises SP10/82 and S P l l / 8 2 , but this was not the case on the P R O L I G O s t a t i o n w h e r e the salinity m i n i m u m o c c u r r e d at ~ 650m. All CuCC v a l u e s w i t h i n the top 200 m were averaged, e a c h day, o v e r four depth ranges. T h e s e a v e r a g e values are plotted as a f u n c t i o n of time in Fig. 11. A p a r t from one high value, t h e r e were no significant changes in CuCC, even t h o u g h the r a t e of in situ fixation of c a r b o n i n c r e a s e d by a f a c t o r of a b o u t five w h e n n u t r i e n t s were added to the e u p h o t i c zone by b r e a k i n g i n t e r n a l waves ( D a n d o n n e a u and Lemasson, 1987). As five cruises (SP10/82, S P l l / 8 2 , SP10/83, FR04/85 and FR09/86) were at l o n g i t u d e s of 155 ° _+ 15°E, the d a t a for the top 200m (exlcuding the G r e a t B a r r i e r R e e f l a g o o n values) are combined in Fig. 12 to o b t a i n an i n d i c a t i o n of the v a r i a t i o n of CuCC in the e u p h o t i c zone with latitude. CuCC values were g e n e r a l l y < 10 n M at high and low latitudes. B e t w e e n 20°S and 3O°S h i g h e r v a l u e s were often observed, but t h e r e was m u c h variability. In the T a s m a n and Coral Seas, along 155°E, J i t t s (1965) f o u n d t h a t the u p t a k e of 14C was high at 45°S, d e c r e a s e d by more t h a n an o r d e r of m a g n i t u d e at 20°S and i n c r e a s e d again t o w a r d s 5°S (Fig. 13). W i t h o u t full details of his m e t h o d o l o g y , it is difficult to d i r e c t l y c o m p a r e his and o u r data; however, r e c e n t m e a s u r e m e n t s of productiv-
161 10
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Fig. 11. V a r i a t i o n of CuCC w i t h t i m e at the PROLIGO station. V a l u e s w e r e averaged over depth i n t e r v a l s of ( ~ 5 0 m (D), 5 1 - 9 0 m ( O ) , 91 1 4 0 m (zx) a n d 141 2 0 0 m ( v ) .
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Fig. 12. Variation of CuCC in the top 200m along 155°E. ity by Harris et al. (1987) h a v e confirmed the s a m e g e n e r a l trend. In contrast, the CuCC v a l u e s w e r e l o w at t h e e q u a t o r and at 57°S, w h i l e h i g h v a l u e s w e r e f o u n d at i n t e r m e d i a t e latitudes. Barber and R y t h e r (1969) s u g g e s t e d that w a t e r u p w e l l i n g a l o n g t h e e q u a t o r
162 70
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D 1 (3°N
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[
30°5
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I 70%
Fig. 13. Variation in productivity along 155E (from Jitts, 1965). in the eastern Pacific required ~preconditioning' before it was suitable for active growth of phytoplankton. They postulated t h a t marine organisms released organic compounds into the water, thereby increasing the bioavailability of trace metals. Steeman Nielsen and Wium-Andersen (1970) subsequently proposed th at the conditioning was due to organic compounds decreasing the bioavailability of toxic trace metals - - probably copper. Active growth of p h y t o p l a n k t o n was observed after the upwelled water had been advected 1-2 degrees away from the equator. However, we observed no minimum in the CuCC values of surface waters at the equator. Low values were found at l°S and, apart from one value at 846 m, the CuCC was < 0.6 n M b e t w e e n the surface and 1100 m. Surface samples were collected from H ung ry Point in Port Hacking estuary from F e b r u a r y t hr ough November 1984 (Mackey and Szymczak, 1988). The results are shown in Fig. 14. The estuary, 20 km south of Sydney, is marinedominated, comparatively free of pollution and has copper concentrations of 19 _+ 15 n M (n = 50) (Mackey and Szymczak, unpublished results). During the period th at p h y t o p l a n k t o n blooms are known to occur, the CuCC increased smoothly from 5-10 to 59 nM, remaining > 10 n M for about a month. It is not known whether the peak value of CuCC coincided with the peak in productivity or biomass, or whether it occurred after the bloom had crashed, as the productivity was not measured. DISCUSSION Complexing capacity values ranging from < 10 n M in the Sargasso Sea to 1681 n M in the productive waters off the s out heast ern coast of the U.S.A. have
163
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Fig. 14. Variation of CuCC in Port Hacking during 1984. been reported by Wood et al. (1983), who used a technique similar to ours. The elevated values (up to 136 n M ) we found near 1000 m in the South Pacific and Coral Sea can n ot be due to in situ production by phyt opl ankt on and are unlikely to originate from marine bacteria t hat produce organic ligands at intermediate depths only in this general region. The high CuCC values found at depth during these cruises (Mackey, 1986) are attributable to horizontal advection from the S o u t h e r n Ocean since they occurred near the salinity minimum t h a t defines the Antarctic Intermediate Water (AIW). If this interpretation is correct, CuCC values in excess of 136nM should occur in the S ou th er n Ocean at times of high biomass. In the present study, CuCC values in surface waters varied from 0. 1nM (FR09/86) to 7 7 n M (SPll/82) and the latter value may not be indicative of those t hat could occur at very high chlorophyll or biomass concentrations. High p h y t o p l a n k t o n biomass was not observed in the Sout hern Ocean during FR09/86. While the productivity was moderate (0.4-1.8 mg C m 3h- 1), the chlorophyll a levels were low (0.2~).6 pg l- 1; D. Everitt, unpublished results) and the in situ fluorescence and turbidity of surface waters were near the limits of detection of the Variosens III. Reasonable depth profiles of in situ fluorescence and turbidity were obtained at a number of stations, but the lack of reliable surface data prevented us from comparing the instrument response with th at of the T u r n e r fluorometer. At these latitudes, the biomass is limited by convection. A stable thermocline had not developed by November. Strong winds (Force 11) during the cruise would have caused deep mixing and kept the biomass low. During FR04/85, the in situ fluorescence and turbidity were below the
164
detection limits of the Variosens III even though the equator is a moderately productive region with nutrients being continually supplied by upwelling. Measurements of 14C uptake during this cruise (F.B. Griffiths, unpublished results) indicated grazing rates were high, which probably limited the biomass in these waters. The low CuCC values observed in surface waters on both these cruises are therefore indicative of low biomass in productive waters. In contrast to the uniformly low values of CuCC found near the equator and in the Southern Ocean, the CuCC was very variable within the euphotic zone at intermediate latitudes (Fig. 12). No measurements of biomass were made for the stations in the Coral and Tasman Seas (SP10/82 and SPll/82), but these stations are in regions that are generally considered oligotrophic (Dandonneau and Lemasson, 1987). Surface concentrations of nutrients were low (0.050.12 pMPO4, (~0.5 p M N Q ) . The variations in CuCC near Wreck Reef could be attributed to local effects (Mackey et al., 1987), but similar values were obtained during SP10/82, SPl l / 82 and within the lagoon of the Great Barrier Reef on SP10/83 (Fig. 10). This pa t t e r n supports the hypothesis t hat high CuCC values can occur in oligotrophic waters under conditions of n u t r i e n t limitation or trace-metal stress (see Introduction). The PROLIGO station was expected to exhibit the high variability in CuCC found earlier on cruises SP10/82, SPll/82 and SP10/83. However, none of the 57 samples analyzed from the top 200 m had CuCC values > 10 nM. The results, which are similar to those obtained from near the equator and from the S ou th er n Ocean (Fig. 12), indicate t hat productivity was high and biomass low. In tropical waters this would imply t hat there is a reliable source of nutrients (in this case from breaking internal waves; D andonneau and Lemasson, 1987) and a high grazing rate. New production at the site was estimated to be 2 2 m g C m - 2 h 1. Low values of CuCC were also observed on the North West Shelf of Australia (Fig. 3). N u t r i e n t enrichment was attributed to a combination of terrestrial run-off and interaction with the sediments. At the time of sampling, in situ measurements of fluorescence (using a Variosens II) suggested t hat the biomass was low and was not correlated with n u t r i e n t concentrations in the surface water (Mackey, 1984). The data from Port Hacking give an indication of the range of CuCC values expected during blooms in coastal waters. The CuCC values were comparable to the copper concentrations in the estuary. No measurements of productivity or biomass were u n d e r t a k e n during this time, as the site is one of the best characterized in Australia, with over 40 years of data collected. Diatom blooms t h at occur about October are triggered by the i n t r u s i o n of nutrient-rich slopewater into the euphotic zone (Mackey and Szymczak, 1988). Chlorophyll a levels rise to > 250mgm 2 (Hallegraeff, 1981), which is about an order of magnitude higher t han the level found at the PROLIGO site (Dandonneau and Lemasson, 1987). The concentrations of chlorophyll within the water column can rise as high as 15pgl ' (Hallegraeff, 1981). The high CuCC values found
165
during October 1984 are due to high phytoplankton biomass, but it is not known whether the organic ligands were released into the water column by actively growing cells or from senescent cells. CONCLUSIONS
When the biomass is high, the CuCC of seawater may be as high as 60 n M (Port Hacking) and possibly much higher, if the values in the AIW found during SPll/82 are due to ligands produced within the euphotic zone at high latitudes. High biomass in these waters is strongly dependent on season (light) and on the wind dropping long enough for the water column to become stratified. High CuCC values are expected to be localized in these waters. The association of high biomass with high copper complexing capacity (1681 nM) has also been observed by Wood et al. (1983). Low biomass in oceanic waters can be a result of one of three processes. The first is characterized by high productivity (14C uptake) and active removal of new production, leading to a high flux of nutrients and energy through the system. There must be a steady supply of nutrients, which can arise from upwelling (FR04/85, FR09/86) or the breaking of internal waves (PROLIGO) and also a rapid removal of autotrophic organisms by processes such as grazing (FR04/85, PROLIGO) or deep mixing (FR09/86). Under such conditions, all the phytoplankton are growing at near-optimal rates and excrete little organic matter, with the result t h a t the CuCC is uniformly low. The association of high grazing rates with low values of CuCC implies that 'sloppy grazing' by herbivores is not a significant source of organic ligands in seawater. Since there is no reason to expect 'sloppy grazing' to release only organic compounds capable of complexing trace metals, it is inferred that this process does not contribute significantly to the DOC in seawater. The low CuCC values found near the equator implies t h a t the organisms growing in the freshly upwelled water are not subject to trace-metal stress. In the second process, productivity is intermittently high, with strong fluxes localized in space and time. Patchiness of nutrients in phytoplankton communities has been found to extend down to millimeter scales (Lehman and Scavia, 1982). The average productivity and flux of matter through such a system is low, as is the average concentration of grazers. Some autotrophs would be growing under conditions of nutrient stress, and the low concentration of grazers would allow cells to senesce when the supply of nutrients was exhausted. The strong thermocline would enable organic compounds, released under these conditions, to accumulate. The CuCC of such waters would be variable, with occasional high values occurring, as was found during SP10/82, SPll/82 and SP10/83. The third process, which produces low productivity on all spatial and temporal scales, is the traditional picture of oligotrophic waters with new production always occurring under conditions of nutrient limitation. Recent work suggests that this scenario does not apply to the oligotrophic regions of
166 t h e o c e a n s ( K e r r , 1986) a n d i t is d i f f i c u l t t o s e e h o w l o w u n i f o r m p r o d u c t i v i t y could produce the range of CuCC values found in subtropical waters. ACKNOWLEDGEMENTS T h e a u t h o r s w o u l d l i k e t o t h a n k L. L e m a s s o n f o r i n v i t i n g u s t o p a r t i c i p a t e i n t h e P R O L I G O e x p e r i m e n t , A. Z i r i n o f o r i n v i t i n g u s t o p a r t i c i p a t e i n t h e S O M A P cruise, and t h e m a s t e r s and c r e w of t h e N.O. J e a n C h a r c o t , U.S.N.S. D e S t e i g u e r , R.V. S p r i g h t l y a n d R.V. F r a n k l i n f o r t h e i r h e l p i n c o l l e c t i n g s a m p l e s . W e w o u l d a l s o l i k e t o e x p r e s s o u r a p p r e c i a t i o n t o R. S z y m c z a k , G. D a l P o n t and J. A t a c k for p e r f o r m i n g the analyses. F i n a l l y , we w o u l d like to e x p r e s s o u r a p p r e c i a t i o n o f o u r u s e f u l d i s c u s s i o n s w i t h G. H a r r i s , F . B . G r i f f i t h s a n d D. E v e r i t t . REFERENCES Anderson, M.A. and F.M.M. Morel, 1982. The influence of aqueous iron chemistry on the uptake of iron by the coastal diatom Thalassiosira weissflogii. Limnol. Oceanogr., 27: 789-813. Anderson, M.A., F.M.M. Morel and R.R.L. Guillard, 1978. Growth limitation of a coastal diatom by low zinc ion activity. Nature (London), 276; 70-71. Barber, R.T. and J.H. Ryther, 1969. Organic chelators: factors affecting primary production in the Cromwell Current upwelling. J. Exp. Mar. Biol. Ecol., 3:191 199. Capone, D.G. and E.J. Carpenter, 1982. Nitrogen fixation in the marine environment. Science, 217: 1140-1142. Dandonneau, Y. and F. Gohin, 1984, Meridional and seasonal variations of the sea surface chlorophyll concentration in the southwestern tropical Pacific (14 to 32°S, 160 to 175°E). Deep-Sea Res., 31: 1377-1393. Dandonneau, Y. and L. Lemasson, 1987. Water-column chlorophyll in an oligotrophic environment: correction for the sampling depths and variations of the vertical structure of density, and observation of a growth period. J. Plankton Res., 9: 215-234. Eppley, R.W., 1972. Temperature and phytoplankton growth in the sea. Fish. Bull., 70: 1063-1085. Eppley, R.W., 1980. Estimating phytoplankton growth rates in the central oligotrophic oceans. In: P.G. Falkowski (Ed.), Primary productivity in the sea, Plenum, New York, pp. 231 242. Fitzwater, S.E., G.A. Knauer and J.H. Martin, 1982. Metal contamination and its effect on primary production measurements. Limnol. Oceanogr., 27: 544~551. Goldman, J.C., J.J. McCarthy and D.G. Peavey, 1979. Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature (London), 279: 210-215. Hallegraeff, G.M., 1981. Seasonal study of phytoplankton pigments and species at a coastal station off Sydney: importance of diatoms and the nanoplankton. Mar. Biol.i 61:107 118. Harris, G.P., 1978. Photosynthesis, productivity and growth: the physiological ecology of phytoplankton. Arch. Hydrobiol. Beih. Ergeb. Limnol., 10:1 171. Harris, G.P., 1986. Phytoplankton Ecology: Structure, Function and Fluctuation. Chapman and Hall, London. Harris, G.P., G.G. Ganf and D.P. Thomas, 1987. Productivity, growth rates and cell size distributions of phytoplankton in the SW Tasman Sea: implications for carbon metabolism in the photic zone. J. Plankton Res., 9:1003 1030. Harris, G.P., F.B. Grifftihs and D.P. Thomas, 1988. Light and dark uptake and loss of 14C: methodological problems with productivity measurements in oceanic waters. Hydrobiologia, in press. Harvey, G.R., D.A. Boran, L.A. Chesal and J.M. Tokar, 1983. the structure of marine fulvic and humic acids. Mar. Chem., 12: 11~132.
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