Shift-Up and the Nitrate Kinetics of Phytoplankton in Upwelling Systems

Shift-Up and the Nitrate Kinetics of Phytoplankton in Upwelling SystemsAuthor(s): Chris GarsideSource: Limnology and Oceanography, Vol. 36, No. 6 (Sep., 1991), pp. 1239-1244Published by: American Society of Limnology and OceanographyStable URL: http://www.jstor.org/stable/2837473 .

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Notes 1239

of Aqaba (Jordan. Red Sea). Proc. 5th Int. Coral Reef Congr. 6: 95-100.

, AND J. JAUBERT. 1990. Effect of light on ox- ygen and carbon dioxide fluxes and on metabolic quotients measured in situ in a zooxanthellate coral. Limnol. Oceanogr. 35: 1796-1804.

GRASSHOFF, K., AND H. JOHANNSEN. 1972. A new sensitive and direct method for the automatic determination of ammonia in seawater. J. Cons. Cons. Int. Explor. Mer 34: 516-521.

JACQUES, T. G., AND M. E. Q. PILSON. 1980. Exper- imental ecology of the temperate scleractinian coral Astrangia danae. 1. Partition of respiration, photosynthesis and calcification between host and symbionts. Mar. Biol. 60: 167-178.

KREMLING, K. 1983. Determination of the major constituents, p. 247-268. In K. Grasshoff et al. [eds.], Methods of seawater analysis. Verlag Chemie.

MILLIMAN, J. D. 1974. Marine carbonates. Springer.

SMITH, S. V., AND G. S. KEY. 1975. Carbon dioxide and metabolism in marine environments. Limnol. Oceanogr. 20: 493-495.

, AND D. W. KINSEY. 1978. Calcification and organic carbon metabolism as indicated by carbon dioxide, p. 469-484. In D. R. Stoddart and R. E. Johannes [eds.], Coral reefs: Research methods. Monogr. Oceanogr. Methodol. 5. UNESCO.

STODDART, D. R., AND R. E. JOHANNES [EDS.]. 1978. Coral reefs: Research methods. Monogr. Ocean- ogr. Methodol. 5. UNESCO.

WOOD, E. D., F. A. J. ARMSTRONG, AND F. A. RICH- ARDS. 1967. Determination of nitrate in seawater by cadmium-copper reduction to nitrite. J. Mar. Biol. Assoc. U.K. 47: 23-31.

Submitted: 15 February 1991 Accepted: 6 June 1991 Revised: 18 July 1991

Limnol. Oceanogr., 36(6), 1991, 1239-1244 X 1991, by the American Society of Limnology and Oceanography, Inc.

Shift-up and the nitrate kinetics of phytoplankton in upwelling systems

Abstract-The Michaelis-Menten model of enzyme kinetics has been applied widely to nutrient uptake in phytoplankton. Practically, the heavy nitrogen isotope (I5N) is used to measure nitrogen incorporation, and the uptake velocity of the Mi- chaelis-Menten expression has been obtained by normalizing the rate to particulate N. NO3- uptake velocity normalized to total particulate organic N (PON) in newly upwelled phytoplankton increases over several generation times, a process that has been described by the term "shift-up" borrowed from bacterial physiology. Michaelis- Menten kinetics do not adequately describe the process and more complicated descriptions have evolved in the literature.

In upwelling systems the proportion of phytoplankton biomass in the PON increases with time, affecting calculated NO3- uptake velocities. A simple model demonstrates that shift-up and related phenomena may be the result of normalizing to particulate N with a time-dependent phytoplankton N content.

Acknowledgments I am grateful to many colleagues for discussions that

led to the ideas in this note, Janet Campbell, John Cullen, Hugh Ducklow, John Marra, James McCarthy, Pat Wheeler, and two anonymous reviewers for com- ments on it, and my wife Jean who assisted with the program.

This work was supported by NSF grants OCE 87- 13166, OCE 87-16908, and OCE 90-00263. This is Bigelow Laboratory Contribution 91006.

Marine phytoplankton nutrient kinetics for single species and populations are usu- ally modeled with the Michaelis-Menten expression describing enzyme kinetics:

Vmax[IS] Ks + [SI (1)

The expression is hyperbolic and relates the reaction velocity (V) to a maximum velocity (Vmax), the concentration of the limiting substrate ([S]), and the substrate concentration (Ks) at which V= Vmax/2. Monod (1942) successfully applied Michaelis-Menten kinetics to bacterial growth on a single limiting external substrate, and Dugdale (1967) applied the same model to the uptake of nutrients by phytoplankton. The assumption is that in a particular physiological state there is a single enzyme process involving the limiting nutrient that regulates both its uptake and cell growth. Generally, constant values of Vmax and Ks have been assumed to be sufficient to describe nutrient-limited kinetics of a species or population by a single substrate. In other words, limitation by a particular substrate has been treated as a single physiological condition; this assump-



1240 Notes

tion has proved adequate for many pur- poses.

Nevertheless, many observations in nutrient-rich upwelling systems suggest that newly upwelled populations which would be expected to have a high Vdo not. Often, measurements of V increase over a period of days, and the increases may not be simply first-order. If the Michaelis-Menten expression describes the appropriate kinetics under nutrient-rich conditions, then Vmax must change, and a change in the physiological state of the phytoplankton is implied.

Many bacteria are capable of growth on simple mineral substrates and a source of organic C, but increase their growth rate following transfer to complex extracts and broths. Over a period of several bacterial generation times these undefined but richer suites of substrates induce a well-docu- mented synthesis of cellular machinery for their utilization. The process involved is termed "shift-up" (Schaechter 1968).

The time scale of increase of V in upwelled phytoplankton populations is com- parable (generations) and the similarity to the bacterial response has led to the adop- tion of the term shift-up to describe it. Al- though there is evidence suggesting that some cellular activity changes on that time scale in upwelled phytoplankton (nitrate re- ductase, for example-Wilkerson and Dug- dale 1987), the concept is largely justified by observations of natural populations. Wilkerson and Dugdale (1 987) and Dugdale et al. (1990) have also suggested that the time rate of increase of V (acceleration) de- pends on the initial concentration of limiting nutrient. They also hypothesized that higher initial N03- concentrations induce greater shift-up, which takes longer to achieve.

The observations of shift-up depend on measurements of the incorporation of in- organic N into particulate material, with the heavy isotope of nitrogen (15N) as a tracer. Analytically 15N incorporation is measured as a mass ratio in a quantity of particulate organic N (PON), which results in an ac- curate determination of an absolute rate, p (M x T1). The Michaelis-Menten expression is written in terms of the specific rate V(Th1) which can be calculated by dividing

p by N biomass. Unfortunately, the PON measured either by elemental analysis or from the 15N mass-spectrometer inlet man- ifold pressure is a measure of total PON. Thus the VPiON (p/PON) is a measure of V (hereafter used to represent the real value of the uptake velocity) that is biased to the extent that PON contains detrital material that does not contribute to uptake. This has been pointed out by others, including Dug- dale and Wilkerson (1986), and while they mention this consideration elsewhere (Wilkerson and Dugdale 1987; Dugdale et al. 1990), they dismiss it as an artifactual source of their observed shift-up.

Zimmerman et al. (1987) created a math- ematical model of nutrient dynamics in coastal upwelling that includes a term for acceleration of V, as well as a mixed layer and euphotic zone, and reproduces most of the features predicted in the shift-up hypothesis. Dugdale et al. (1990) provided a further model of new production in coastal upwelling which also incorporates an acceleration term to account for shift-up.

Here I use a simple time-dependent model involving only the Michaelis-Menten expression and a PON-dependent grazing term to simulate the shift-up phenomenon and an acceleration of V that is dependent on the initial NO3- concentration. All the shift- up phenomena that the model produces will be shown to be artifacts resulting from normalizing p to PON.

The model is initialized with values for N03- (AM), PON (AM), and Chl a (,g liter-') pools, and is iterative with a small time step, dt. The PON includes Chl a, and the equiv- alence of 1 Ag Chl a liter-' and 1 gM N is assumed (Strickland 1965; McCarthy et al. 1977; cf. Wilkerson and Dugdale 1987). Production is controlled by N uptake:

dChl a = Chl a(V dt-G dt) (2) and

dNO3- =-Chl a Vdt = -p dt (3)

where Vis defined by the Michaelis-Menten expression (Eq. 1). Vmax is calculated from Chl a and the maximum growth rate, spec- ified in the model as a doubling time, D (d). Removal of particles in the model is un- selective and is accomplished with a single



Notes 1241

PON-specific grazing term, G (d-l), which includes all loss terms, but results in no regeneration:

dPON = dChl a - (PON - Chl a) G dt. (4)

The model is simple enough to simulate on a PC with a spreadsheet.

The purpose of the model is to see if increases in VPON can be produced in simu- lations of upwelling, without an explicit Vmax acceleration term; in other words, to test whether the shift-up hypothesis is necessary. Wilkerson and Dugdale (1987) have published numerous experiments in which they followed the time-course (up to 4 d) of bloom development in upwelled water in shipboard containers. Their data provide NO3-, Chl a, PON, and VPON that the model should reproduce if it is able to generate shift-up. The growth rate, Ks, and grazing are the variables that are adjustable, since the time step is simply made small enough that further reduction does not change the behavior of the model.

By adjusting these parameters, it is possible to get a reasonably good simulation of the data presented graphically by Wilkerson and Dugdale (1987). For example, the four panels of Fig. 1 are the model output of the time-course of NO3-, Chl a, VPON, and PON overlaid on the data digitized from their figure 8 (74B3 "major upwelling" water). The model results were obtained with initial values of NO3- = 18 AM, Chl a = 0.3 Ag liter-', PON = 1.5 AM estimated from the digitized data, and fit with D = 0.9 d, Ks = 1.0 AM, G = 0.175 d-, and a time step of 0.25 d. The Ks is not critical because any reasonable value would be < 10% of NO3-, causing the concentration-dependent part of the Michaelis-Menten expression to ap- proximate 1 and the uptake to be close to maximum for the Chl a present.

By changing the initial NO3- concentration, but otherwise using the above parameterization, a series of different time-courses of VPON is obtained (Fig. 2-cf. figure 2 of Dugdale et al. 1990) and these show three other characteristics of the shift-up hypothesis. First, below some critical initial N03- concentration (1-2 AM in this case), there

is no appreciable shift-up. Second, the acceleration of VPON increases as the initial NO3- concentration increases. Third, the time taken to reach maximum observed VPON' or fully shift-up, increases as initial NO3- increases. The form of these responses is qualitatively similar, but large changes in time scale and magnitude can be effected by changing the model parameterization with- in the bounds of field observation and laboratory measurements of physiological parameters. For example Zimmerman et al. (1987) presented a model illustration "hypothesis 3," to demonstrate the necessity of shift-up, with a constant V= 0.02 h-l (doubling time of 1.44 d) and a starting Chl a = 0.01 Ag liter-'. In their model, NO3- depletion takes 20 + d to occur at high N03-; substituting these parameters in the present model, I obtained a similar result. They concluded that such long depletion times are unrealistic in natural upwelling systems, and that shift-up is necessarily implied.

The shift-up hypothesis introduces much complication to the parameterization of phytoplankton nutrient kinetic relation- ships in vivo and in models. Simply, it im- plies that nutrient limitation involves several or a continuum of physiological states characterized by variable Vmax and Ks that respond to external nutrient concentration history over time scales of a few generations. The assumption that nutrient limitation is a single physiological state described by one Vmax and one Ks would be invalid, and time and nutrient history dependence of these parameters would be critical and generally unknown.

It is not my purpose to assert that shift- up does not occur in phytoplankton, but rather to suggest that many of the observations that have been thought to make the hypothesis necessary can be explained without it. Because the model containing only Michaelis-Menten uptake kinetics, and a PON-dependent grazing term does reproduce the shift-up phenomenon and its cor- ollaries observed in upwelling systems, it is instructive to examine how this comes about.

In upwelling systems, newly upwelled water contains a lot of PON, and little of it is living plant material (Chl a -20% in the



1242 Notes

25 rLv0.04 a~~~~~~~~~~~~~~

0.03 -------------------------r-------------- ------------

:E1C ----- -------'----5)x- 0.02 ------------------t--- ---------'--- --------

0~~~~~~~6.2 z 1 0 ------------------------01 -- ------- I----------- -------

5~~~~~~~~~~~~~~~~~~~~~~~~~~~~ ~ --------------------------------------------------------- 0.01 -

0 20 40 60 80 100 0 20 40 60 80 100

Time (h) Time (h)

4 4 _ | _|

3 ------------- I- --------------- -------- 3-i--------- 3 - - ------------- ------------. /

e 2 p~~~~~~~~~~~~~~~~

--;--------- --------- - --- --- /---------------2~ -x------

L 2 --------------------------- z

C~~~~~~~~

a,~~~~~~~~~~~~~~~~~~~a

0~~~~~~~~~~~~~~~~

0 0 0 20 40 60 80 100 0 20 40 60 80 100

Time (h) Time (h)

Fig. 1. Model output (solid lines) superimposed on data (lines with data points) digitized from Wilkerson and Dugdale (1987).

example in Fig. 1) (cf. Wilkerson and Dug- dale 1987). Even though Chl a is taking up N03- at near the maximum possible absolute rate in the model, the calculated VPON is low because PON is high. As the bloom progresses, the model (and real world data) shows that Chl a increases and approaches 100% of PON, and VPON increases because the proportion of PON contributing to uptake increases. Thus the growth rate and grazing terms in the model can be adjusted to modify the model output to match real data, but shift-up is inherent in normalizing p to PON. VChl a (p/Chl a-dashed line in Fig. lb) is a proper measure of V in the model and has units of h-I (1 ,ug Chl a liter-'

1 ,uM N) and VChla decreases only slightly and entirely as a result of the effect of de- creasing N03- in the Michaelis-Menten expression. By back-calculating uptake from

VPON and PON and then dividing by Chl a to obtain VChl a in the Wilkerson and Dug- dale (1987) figure 8 data set, VChl a actually decreases steadily, except for the first data point, by a factor of three from 0.045 to 0.016 AM N03- (,tg Chl a)-' d-'! In several other of their data sets that I have digitized, VChl a calculated as described is either constant or declines well before N03- reaches concentrations at which VChl a should be re- duced significantly below Vmax. The ques- tion of why these populations actually shift- down is intriguing.

It is perhaps less obvious how some of the other phenomena associated with shift- up come about, but in the model they are all related to a biased VPON when Chl a is <PON. A critical minimum initial N03- concen-

tration for shift-up to occur has several



Notes 1243

causes. First, at lower initial concentrations near or below K&, Vis low as the Michaelis- Menten equation predicts; initially VPON is even lower, as already discussed. Second, unless there is sufficient NO3- to produce enough Chl a for it to be a significant part of the total PON, VPON will always be arti- factually low. The higher the initial PON, the higher the initial NO3- concentration needed to overcome this. Finally, initial low Chl a and NO3- and high PON will result in VPON values below or close to the analytical limit of detection. It is possible then that no significant rate or change of rate may be observed, giving the impression that there is a threshold initial NO3- below which shift- up does not occur.

The initial NO3--dependent acceleration of VPON is simply an extension of this idea. That is, as the initial NO3- concentration increases, uptake predicted by Michaelis- Menten kinetics increases, so that the rate of production of Chl a also increases. Chl a becomes a larger fraction of PON more quickly at higher initial NO3-, and thus VPON approaches V more rapidly.

Finally, it follows that as the initial NO3- concentration increases, there is a larger re- source of material to increase the proportion of Chl a in the PON (Dugdale 1985; MacIsaac et al. 1985). Chl a can continue to approach PON while NO3- is high and V can remain near Vmax longer. VPON can continue to increase longer and reach higher values after longer periods of time as the initial NO3- increases.

It is interesting that both the Zimmerman et al. (1987) model and the present model predict that depletion of high initial N03- will take on the order of 20 d given essen- tially the same parameterization, but not surprising in their shallow mixed-layer case because the complex model converges on the simpler. What is surprising is that this can be inferred to support the shift-up hypothesis. For example, by means of simple arithmetic, it requires an initial biomass of 0.01 ,ug liter-' Chl a to double almost 11 times to consume 20 ,uM NO3-; if we as- sume that this all takes place at the fastest possible doubling time of 1.44 d, 15.8 d are required. Thus, even in the absence of any

0.04

>0 0 20

0.0 1 r------

0 2 4 6 8 10

Time (d)

Fig. 2. The time-course of VPON vs. time for 1, 2, 3, 5, 10, and 20 AM NO3-, with all other parameters the same as in the Fig. 1 data set (see text).

kinetic response or grazing, NO3- depletion will be unrealistically long, but only pre- sumably because initial biomass or maximum growth rates or both were unrealistically low. The failure of either model to achieve what is mathematically impossible cannot be taken as support for the shift-up hypothesis.

The model does an adequate first-order approximation of the form of data reported in the literature, although it does not reproduce it in detail. This should not be expected because experimental data are subject to sampling and analytical variance, autotro- phic and heterotrophic populations undergo temporal change, and many factors such as NH41 regeneration, NH4+ inhibition ofNO3- uptake, and the light dependence of N03- uptake, which complicate the evolution of bloom populations in mesocosms and the real world, are not present in the model. The model was only designed to demonstrate the shift-up phenomenon with the minimum parameterization necessary to demonstrate its artifactual characteristics.

I have shown here that the shift-up hypothesis suggested by apparent changes in Vin upwelled phytoplankton populations is not necessary to explain these observations. I am not suggesting that shift-up does not occur in phytoplankton, but laboratory studies of phytoplankton physiology might best test this. Shift-up is not necessary to explain the ecological physiology of phy-



1244 Notes

toplankton in upwelling systems, and the principle of Occam's razor should prevail.

Chris Garside Bigelow Laboratory for Ocean Sciences West Boothbay Harbor, Maine 04575

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Dynamics, identification and significance. Lim- nol. Oceanogr. 12: 685-695.

1985. The effects of varying nutrient concentrations on biological production in upwelling regions. CalCOFH Rep. 26: 23-96.

, AND F. P. WILKERSON. 1986. The use of 15N to measure nitrogen uptake in eutrophic oceans; experimental considerations. Limnol. Oceanogr. 31: 673-689.

AND A. MOREL. 1990. Realization of new production in coastal upwelling areas: A means to compare relative performance. Limnol. Ocean- ogr. 35: 822-829.

MCCARTHY, J. J., W. R. TAYLOR, AND J. L. TAFr. 1977. Nitrogenous nutrition of the plankton in the Chesapeake Bay. 1. Nutrient availability and phytoplankton preferences. Limnol. Oceanogr. 22: 996-1011.

MACISAAC, J. J., R. C. DUGDALE, R. T. BARBER, D. BLASCO, AND T. T PACKARD. 1985. Primary production cycle in an upwelling center. Deep-Sea Res. 32: 503-529.

MONOD, J. 1942. Recherches sur la croissance des cultures bacteriennes. Herman and Cie.

SCHAECHTER, M. 1968. Growth: Cells and populations, p. 136-162. In J. Mandelstam and K. McQillen [eds.], Biochemistry of bacterial growth. Wiley.

STRICKLAND, J. D. H. 1965. Production of organic matter in the primary stages of the marine food chain, p. 478-610. In J. P. Riley and G. Skirrow [eds.], Chemical oceanography. V. 1. Academic.

WILKERSON, F. P., AND R. C. DUGDALE. 1987. The use of large shipboard barrels and drifters to study the effect of coastal upwelling on phytoplankton dynamics. Limnol. Oceanogr. 32: 368-382.

ZIMMERMAN, R. C., J. N. KREMER, AND R. C. DUGDALE. 1987. Acceleration of nutrient uptake by phytoplankton in a coastal upwelling ecosystem: A mod- eling analysis. Limnol. Oceanogr. 32: 359-367.

Submitted: 19 October 1990 Accepted: 7 May 1991 Revised: 28 May 1991

Limnol. Oceanogr., 36(6), 1991, 1244-1249 ? 1991, by the American Society of Limnology and Oceanography, Inc.

Reconstruction of a regional, 12,000-yr silica decline in lakes by means of fossil sponge spicules

Abstract- A newly developed technique for re- constructing past dissolved reactive silica (DRSi) concentrations in lakes demonstrated an unex- pected, regional decline in DRSi in northern Wis- consin lakes over the Holocene. Previously, mea-

Acknowledgments We thank Steve Blumenshine, Judy Hayducsko, Sue

Holloway, Tim Meinke, Pam Montz, and John Mor- rice for help in the field and laboratory. Marge Winkler allowed us to use her piston corer and John Beauchamp and Paul Rasmussen provided statistical advice. An- namarie Beckel, Steve Carpenter, Jim Hurley, Jim Kitchell, Dave Krabbenhoft, John Magnuson, Peter Leavitt, and John Smol helped improve the manu- script.

Research was funded by the U.S. National Science Foundation (BSR 85-14330 and BSR 86-15352) for studies on Northern Temperate Lakes Long-Term Eco- logical Research and on Autotrophy and Heterotrophy in Freshwater Sponges. Oak Ridge National Labora- tory is managed by Martin-Marietta Energy Systems, Inc., under contract DE-AC05-840R21400 with the U.S. Department of Energy.

surements of lake DRSi, an important nutrient for certain phytoplankton, have been limited to time periods for which direct observations were available, typically years to decades. The new paleolimnological technique is based on the sizes of siliceous sponge spicules preserved in lake sed- iments; it shows that DRSi declined gradually, but significantly, over the past 12,000 yr in each of eight lakes cored (geometric mean decline of 35-fold; range 4.1-270-fold). Mass balance considerations show that the decline could be caused by decreases in groundwater DRSi concentration or groundwater inseepage rates, by increases in net Si sedimentation, or by a combination of these factors. Although we cannot rule out any of these possible mechanisms, the most likely seems to be decline in groundwater DRSi concentration due to differential weathering of the silicate gla- cial tills. With appropriate calibration, paleospic- ule techniques may be useful in assessing long- term silica dynamics in other regions.

Silicon is an essential element for a va- riety of aquatic organisms and its avail-



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Shift-Up and the Nitrate Kinetics of Phytoplankton in Upwelling Systems