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The Importance of the DOC Pool for Primary Production Estimates

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The Importance of the DOC Pool for Primary Production Estimates ICES mar. Sei. Symp., 197: 141-148. 1993 The importance of the DOC pool for primary production estimates George A. Jackson Jackson, G. A. 1993. The importance of the DOC pool for primary production estimates. - ICES mar. Sei. Symp.. 197: 141-148. Phytoplankton release of dissolved organic matter has important consequences for the planktonic ecosystem. Their effects can be compared with those expected at the rates of dissolved organic carbon (DOC) release measured in field incubations. Calculated DOC release rates must be consistent with other incubation measurements, such as those for bacterial growth and for nitrate and ammonia uptake. In this paper, comparisons are made between these different sets of measurements, showing that there is no need for DOC excretion of more than 0.1 of net primary production to account for ecological effects. Furthermore, a simple model of DOC release during productivity measurements shows that grazing on phytoplankton and on bacteria during an incubation can also be important sources of fixed C loss. George A. Jackson: Department of Oceanography, Texas A&M University, College Station, T X 77843, USA. Introduction characterization of DOM has shown it to be quite different in concentration and composition from that In no other part of oceanography have there been as indicated by Sugimura and Suzuki (1988) and Suzuki et many reversals of opinion, doubts about techniques, and al. ( 1985) (Benner et al., 1992). There remains consider­ uncertainties about concentrations and rates as there able uncertainty about the real concentrations of DOC have been associated with dissolved organic matter and DON, but the area remains an active and exciting (DOM) and its constituents dissolved organic carbon part of chemical oceanography (J. Hedges, in press). (DOC) and nitrogen (DON). The situation has not been DOM excretion by phytoplankton is important to the helped by the fact that DOM is a mixture of chemical understanding of algal physiology (e.g., Antia et al., compounds, most of which have not been identified. 1991). Williams (1990) has given a thoughtful overview Prior to about 1975, oceanic benthic regions were of phytoplankton DOM excretion and its ecological believed to use DOM to meet their metabolic needs consequences. Excretion affects estimates of primary (e.g. Craig, 1969; Menzel and Ryther, 1970). With the production rates and of nutrient uptake and is poten­ realization that there is rapid vertical transport of or­ tially important as a source of DOM for the large DOC ganic matter in relatively large, rapidly sinking particles and DON pools. such as fecal pellets (e.g. McCave, 1975; Deuser et al., Much of the biological interest in DOM has resulted 1981) and, more recently, marine snow, there was a loss from the realization that bacteria consume it at rates that of general interest in DOM. The recent development of are high relative to those measured for primary pro­ high temperature combustion techniques for measuring duction (e.g. Azam etal., 1983). The practice of present­ DOC and DON (Suzuki et al., 1985; Sugimura and ing bacterial production rates as a fraction of primary Suzuki, 1988) and the resulting associations that they production has tended to emphasize the role of ex­ observed with apparent oxygen utilization and nitrate cretion by algal cells, even to the point of suggested concentrations have brought DOM back to the attention elaborate interactions between chemotactic bacterial of the general oceanographic community. and algal cells (e.g., Azam and Ammerman, 1984). Higher concentrations of DOC and DON would re­ There are other possible sources. Williams (1981) noted quire profound changes in our understanding of the that large bacterial growth rates suggested DOM release distributions and fluxes of most biologically active ele­ by zooplankton. Jumars et al. (1989) refocused interest ments (e.g., Jackson, 1988; Toggweiler, 1989). Recent on zooplankton and their feces as DOM sources by 142 G. A. Jackson IC ESm ar. Sei. Symp., 197 (1W3) noting that an animal's complete adsorption of dissolved (e.g., Marra et al., 1981; Smith, 1982; Williams, 1990), organic matter produced during digestion of its food is although Williams (1990) briefly considered the effects neither practical nor desirable. Other potential sources of heterotrophs as well. These studies noted that inter­ of DOM include the dissolution of detritus. nal phytoplankton DOC pools would slow the initial The measurement of phytoplankton uptake of nitro­ release of labeled DOC during a 14C incubation. gen compounds could be affected by DON release. This article examines, first, how large algal excretion Uptake is usually measured by the accumulation of needs to be consistent with other properties of plank- material containing 15N in the particulate phase after a tonic ecosystems and, second, what the manifestation of timed incubation. Unfortunately, much of the l5N tracer such excretion would be in a bottle. cannot be found after the incubation. This has been observed when the compounds were ammonia (Glibert et al., 1982), urea (Hansell and Goering, 1989), and nitrate (Ward etal., 1989). If the missing tracer is taken Studies of whole ecosystems up, incorporated into organic compounds, and released, it can represent an important part of the tracer uptake Observations of DOC disappearance which is not included in the uptake calculations. Bronk Kirchman etal. (1991) have recently measured observed and Glibert (1991) have recently developed a technique disappearance rates for DOC in seawater samples col­ of measuring DON excretion by using 15N tracer tech­ lected as part of the JGOFS program. They measured niques. A comparison of estimated DON release rates DOC concentrations in water samples several days after yielded values ranging from 54 to 260% of estimated their collection using the technique of Sugimura and ammonia uptake rates. These large values suggest that Suzuki (1988). DOC disappearance rates varied, but technique cannot yet provide the information needed to were as high as 0.36 d” 1 over a day for initial DOC determine the fate of the missing l5N tracer. concentrations of 178 //M, equivalent to a decrease of Sharp (1977) noted that methods commonly used to DOC equal to 64,mM. Such high rates of DOC consump­ assess DOC production were subject to several artifacts tion should be matched by equally high rates of 0 2 which could give artificially high rates of DOC ex­ consumption. If the 0 2 to DOC consumption ratio is 1, cretion. Typical excretion rates were calculated from then the associated 0 2 concentration decrease in the measurements of radioactivity present in the filtrate environment should be 64 /<M. While simultaneous after algae had been incubated with l4C bicarbonate and production by photosynthesis and consumption by res­ removed by filtration and residual 14C bicarbonate piration complicates the interpretation of daily in situ removed by sample acidification and bubbling. Incom­ variations, there should still be large 0 2 changes, par­ plete removal, either of the phytoplankton particulate ticularly between night and day. material because of cell rupture during filtration or of Oxygen concentrations at the JGOFS stations showed the 14C bicarbonate because of too short a bubbling little variation during the days when Kirchman et al. period, would cause the measurement of radioactivity collected their water. For example, dissolved oxygen that had not been excreted by the algal cells. Today, we concentrations at 04.25, 10.50, and 20.55 h on 25 May would add algal cells small enough to pass through the 1989 at 0-10 m depth were 287, 287.5, and 285.7 ,mM. filter as another potential artifact. The presence of such The measured DOC change that day was 0.23 d large artifacts led Sharp to conclude that the evidence equivalent to a 45 «M change in 24 h. The oxygen varied for extensive DOC excretion was weak. less than 1.8,«M over the course of 16.5 h, much less than More recent work on DOC excretion has addressed the 20 /<M change which could be expected in the course these issues and provided measurements of excretion of a half day. Similar results hold for the other two days rates and of DOC composition (e.g., Fogg, 1983). The that Kirchman et al. collected samples. composition of the excreted material is rich in sugars and The fact that the measured high rates of DOC utiliz­ other carbon-rich compounds (e.g., Mague etal., 1980; ation are not consistent with the observed constancy of Lancelot, 1983; Myklestad etal., 1989). Typical rates of the oxygen concentrations suggests that those rates are excretion in cultures are about 10% of measured pri­ not representative of environmental processes. Kirch­ mary production rates when cells grow rapidly, possibly man et al. (1991) did note that bacterial properties in more when the algae are nutrient limited. Excretion their samples differed from those of normal marine measured in field samples averages about 13% of pri­ bacteria and that their measurements might not have mary production, although reported values vary widely been representative of the ocean. The oxygen concen­ (Baines and Pace, 1991). trations suggest that this was indeed the case. As a Models of how 14C incorporation and DOC excretion result, there is no need to invoke high rates of DOC affect productivity measurements have focused on a excretion by phytoplankton to supply their observed two-box system consisting of phytoplankton and DOC bacterial needs. ICES mar. S d. Symp.. 197 ( 1993) The DOC pool for primary production estimates 143 Analysis of ecosystem data Incubation model Estimates of organic matter excretion should be consist­ This model is designed to show the relationships be­ ent with other measured properties of a system. These tween measured quantities and planktonic processes might include rates of net particulate production, bac­ occurring within an incubation chamber.
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