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Limnol. Oceanogr., 36(8), 1991, 1616-1630 Q 199 1, by the American Society of Limnology and Oceanography, Inc. The role of grazing in nutrient-rich areas of the open sea Bruce W. Frost School of Oceanography, WB- 10, University of Washington, Seattle 98 195 Abstract No single factor accounts fully for the persistently low phytoplankton stocks in the nutrient-rich areas of the open sea. However, grazing plays the necessary role of consuming phytoplankton produced in excess of losses due to physical processes and sinking. Without grazing, even if specific growth rate of the phytoplankton is less than optimal for the prevailing light and temperature conditions, as might be so under limitation by a trace nutrient such as Fe, the phytoplankton stock would still accumulate with attendant depletion of nutrients. Observations during spring and summer in the open subarctic Pacific argue against limitation of phytoplankton growth to the point where phytoplankton stock could not increase in the absence of grazing. An ecosystem process model of the phytoplankton-grazer interaction suggests that two processes-grazing control of phytoplankton stock and preferential utilization of NIH, by the phytoplankton-are sufficient to explain the continuously low phytoplankton stock and high concentrations of macronutrients. However, the grazing control may be exerted on a p:hytoplankton assemblage structured by Fe limitation. In particular, the intrinsic growth rates of potentially fast-growing diatoms seem to be depressed in the open subarctic Pacific. These conditions probably apply to two other nutrientrich areas of the open sea, the Pacific equatorial upwelling region and the subantarctic circumpolar ocean, although in the latter region light limitation of phytoplankton growth may be more severe and silica limitation may influence the specific composition of the phytoplankton assemblage. Realization that grazing zooplankton could control the abundance of phytoplankton in the sea dates back over half a century to the studies of the Kiel and Plymouth plankton study groups (Mills 1989). Inspired by Fleming’s (1939) analysis, Riley (1946, 1947) formulated the first mathematical model describing the dynamics of phytoplankton and grazer assemblages, and quantitatively demonstrated the potential capability of grazers to maintain low stocks of phytoplankton. Recent reviews (Frost 1980; Raymont 1980) stressed the likely major impact of grazing as implied by models, but also noted the need for corroborative field measurements of phytoplankton mortality rates due to grazing. Possibly because grazing mortality of entire phytoplankton assemblages has been so difficult to measure in the ocean, and cer- tainly because of recent rediscovery of the “microbial loop” containing a host of previously relatively unknown grazers whose study has required new methodology, the magnitude of grazing rates is not well established for most marine pelagic systems, especially those of the open sea. Consequently, several hypotheses besides control by grazing are potentially alternative explanations (e.g. Cullen 199 1) of the phenomenon under discussion in this symposium, namely, that in surface waters of several large, open-ocean areas concentrations of phytoplankton are perpetually low despite high concentrations of macronutrients. My view is that none of the hypotheses really are alternatives in the sense of being mutually exclusive explanations of the phenomenon, but all implicate processes that may simultaneously contribute, in differing degrees, to produce it. In this paper I demonstrate the argument by assessing the imAcknowledgments pact of grazing relative to other processes I thank B. C. Booth, J. N. Downs, D. L. Mackas, C. controlling phytoplankton 13.Miller, S. Tabata, N. A. Welschmeyer, and P. A. potentially areas Wheeler for providing data; special thanks to C. B. abundance in the large, nutrient-rich Miller for many useful discussions of subarctic Pacific of the open sea. To make the argument plankton dynamics. quantitative I emphasize observations at the Research supported by NSF grants OCE 86- 1362 1 former Ocean Weather Station P (5O”N, and OCE 89-17671. 145”W) in the Gulf of Alaska. However, I School of Oceanography, University of Washington, note points of similarity or dissimilarity with Contribution 1923. 1616 1617 Grazing in the open sea two other large, nutrient-rich areas of the open sea- the Pacific equatorial upwelling region and the circumpolar subantarctic region. Annual cycle of phytoplankton and NO3 in the open subarctic Pac$c Based on the quantity of Chl a integrated over O-50 m, there is virtually no seasonal variation in phytoplankton standing stock at Station P (Fig. IA). This seems to apply throughout the open subarctic Pacific (Frost 1987; Sambrotto and Lorenzen 1986). Clearly there is temporal variability in phytoplankton stock at Station P, but it is constrained within fairly narrow bounds; for the entire data set integrated Chl a ranges over a factor of only 8. The narrow range of variation contrasts with observed strong seasonal fluctuations of phytoplankton abundance, reaching bloom concentrations with attendant nutrient depletion, in the shelf waters (e.g. Landry et al. 1989; Denman et al. 198 1) and inland coastal waters (e.g. Kanda et al. 1990; Parsons et al. 1970) bordering the open Gulf of Alaska. In Dabob Bay, Washington, the phytoplankton stock range seasonally over a factor of 67 (Fig. 1B). The same contrast, with less intensive and complete seasonal coverage, is evident between waters of the deep basin and the broad continental shelf in the eastern Bering Sea (e.g. Sambrotto et al. 1986). The much more substantial seasonal variability of phytoplankton abundance in shelf and coastal waters and its cause are important topics to which I return later. At Station P, the seasonally relatively constant phytoplankton stock exists despite strong seasonal variation in properties of the physical environment that can have significant impact on the specific growth rate of the phytoplankton (Fig. 2). Growth conditions for the phytoplankton are surely very different, for example, between winter and summer. This is suggested by the annual cycle of NO3 (Fig. 3), which shows a distinct seasonal cycle (buildup in winter, drawdown in summer) in the surface layer. Notice, however, that NO, is not depleted in summer-a feature of the entire open subarctic Pacific (Anderson et al. 1969). Though seasonal coverage is much less A. Station P G 200 'a a 150 85 u O 100 I 0 60 120 180 240 300 360 B. Dabob Bay 400 I -0 60 120 180 240 Day of Year 300 360 Fig. 1. A. Phytoplankton standing stock (as Chl a) observed in the vicinity of Station P. Data cover all seasonsduring the years 196l-l 967 (Frost et al. 1983) and 1980-l 98 1 (Clemons and Miller 1984), and cover late spring-early summer and late summer-early fall during the SUPER cruises, 1987-l 988 (N. A. Welschmeyer pers. comm.). B. As panel A, but for Dabob Bay, Washington. Data for the years 1979 and 1982 (Frost 1985), 1985-1986 (Frost 1988), and 1990-1991 (B. Frost and J. Downs unpubl. data). complete, the subantarctic circumpolar waters are in some respects similar to the open subarctic Pacific. Concentrations of Chl a in the mixed layer are always low and in the range reported for the open subarctic Pacific (Fukuchi 1980). On the other hand, although NO3 is high, SiO, is low in surface waters (Kamykowski and Zentara 1985; van Bennekom et al. 1988). Although growth conditions for the phytoplankton must also be seasonally variable in the subantarctic circumpolar region, mixed layers can be deeper in summer than in the open subarctic Pacific (Levitus 1982; Foster and Middleton 1984). In regions of strongest upwelling in the equatorial Pacific, concentrations of Chl a and macronutrients are similar to those at Station P (Chavez et al. 1990). However, seasonality of growth conditions must be . 1618 Frost 60 - 0 120 0’ I I I 0 60 , 1 I 120 180 240 Day of the Year I 300 -4 360 Fig. 3. Concentration of NO, in the upper 20 m at Statton P, 1966-1976 (adapted from Parslow 198 1). Curve is a Sth-order polynomial fitted by least-squares to the data. Day of Year Fig. 2. Some physical properties at Station P in 1970. Data from Dep. Transport, Meteorol. Branch, Canada (I 97 1) and from a magnetic data tape provided by S. Tabata. much reduced compared to the subpolar open seas. It was for many years presumed that in the open subarctic Pacific grazing zooplankton keep phytoplankton stocks low, thereby preventing depletion of macronutrients in the surface layer (see Miller et al. 1988; Parsons and Lalli 1988). Indeed, models demonstrate that such a role for grazing is plausible (Evans and Parslow 1985; Frost 1987 in prep.). Yet an alternative proposal (Martin et al. 1989) that Fe limitation of phytoplankton growth is somehow responsible for low phytoplankton stocks and high nutrients indicates that the specific mechanisms need to be re-examined. Here, I treat the observations from Station P in two ways. First, I make a quan- titative assessment, leading to an inescapable conclusion, of the relative magnitude of processes that must be at work to maintain the low, relatively constant, phytoplankton stock, for this seems to be the essence of why the open subarctic Pacific is a nutrient-rich area that never exhibits phytoplankton blooms. The argument appears to be generic for the nutrient-rich, open ocean areas, as I show.. I then present the results of a model illustrating a possible dynarnical relationship between phytoplankton and grazers. Control of phytoplankton standing stock in the open subarctic Pacific Daily observations of Chl a concentration at Station P exhibit the same pattern as the seasonal data (Fig. 4). There is daily variability, but it is constrained. These data imply that the local rate of change of phytoplankton stock averages out very close to zero on a time scale of several days to a week or two. The local rate of change of phytoplankton stock (P) depends on several processes ap = at - growth - advection,,,,, + diffusion.,,,, - sinking - grazing. (1) Although all the necessary measurements to evaluate Eq. 1 have not been made simultaneously at Station P, it is nevertheless possible to estimate the relative magnitudes of the terms for specific time periods. c 1619 Grazing in the open sea 1 0020’ Chl o.oI 7 11 19 23 15 Day in May 1988 a (mg m-3) 31 27 iO”O0’ Fig. 4. Short-term temporal variation in surface Chl a at Station P in May 1988 (data provided by N. A. Welschmeyer). Estimates of phytoplankton standing stock and production rate were made during a cruise of the SUPER (Subarctic Pacific Ecosystem Research) investigation to Station P in May 1988. Using these data, I calculated finite specific growth rates for the phytoplankton assemblage in the mixed layer (Table 1). The mean finite specific growth rate was 0.57 d-l; the corresponding instantaneous growth rate (In 1.57) is 0.45 d-l (or a doubling time of - 1.5 d). This growth rate is based on measurements of phytoplankton production rate, and it is assumed, of course, that phytoplankton production rate measured by in situ incubations represents Table 1. Phytoplankton standing stock as Chl a (2 Chl a, mg Chl a m-2) and C (ZC, mg C mm2),phytoplankton production rate (PP, mg C m-2 d-l), and derived finite specific growth rate (PKX, d-‘) for the phytoplankton assemblage at Station P in May 1988. PP based on 24 or 48 h in situ incubations (dawn to dawn). Standing stocks and production rates are integral values for the mixed layer (Z,?,,m). Data provided by B. C. Booth and N. A. Welschmeyer. May Zn Xhl 8 11-12 14 17-18 20 22 27 80 60 60 60 60 80 70 23.6 16.6 23.3 18.7 22.6 15.6 12.3 a ZC* 1,258 885 1,242 997 1,205 831 656 PP PP/ZC 368 0.29 424 0.48 694 0.56 606 0.61 506 0.42 806 0.97 425 0.65 mean = 0.57 (SE = 0.10) * Estimated from Xhl a x y, where y is mean C:Chl a (53.3, SE = 2.3, N = 31) based on microscopical analysis of total phytoplankton assemblage (method described by Booth et al. 1988) for vertical profiles on 8, 14, 20, and 21 May. 19”40’ 145’20’ 145”OO’ 144’40’ Fig. 5. Spatial variation in surface Chl a on a 50 x 50-km grid centered on Station P (5O”N, 145’W), 14-15 May 1984. Based on a continuous record of chlorophyll fluorescence obtained from a pumped seawater flow (at -3-m depth); survey was done in 30 h. Figure provided by D. L. Mackas. something close to net rate of formation of organic matter in situ by the phytoplankton. To evaluate relative magnitudes of changes in phytoplankton stock due to horizontal advection and difhtsion, I utilize data from a spatial survey done at Station P on 14-15 May 1984 (Fig. 5). Again using Chl a as a measure of phytoplankton stock, the horizontal gradient of phytoplankton stock west of Station P (i.e. directly upstream of the station) was on the order 0.01 mg Chl a mm3 km-l. Given mean eastward geostrophic currents of 5-l 0 cm s-l (4-9 km d-l; Favorite et al. 1976), the change due to horizontal advection would be 0.04-O. 1 mg Chl a m-3 d-‘, which is an appreciable daily change, equivalent to - 1O-20% of the mean phytoplankton concentration in Fig. 5. However, the horizontal gradients of chlorophyll are neither regular nor fixed in space (cf. gradients east and west of Station P in Fig. 5), and there is not a consistent larger 1620 Frost scale upstream gradient farther to the east of Station P (Sambrotto and Lorenzen 1986). Thus, over a 5-10-d period the change due to advection at Station P must average out close to zero. With regard to vertical advection, Station :P is in a region of divergence, with a very slow rate of upwelling (15-20 m yr-I; Favorite et al. 1976), so vertical advection is negligible on a time frame of several days to a few weeks. The mean change in horizontal gradient of Chl a in Fig. 5 is -0.01 mg Chl a m-3 kmm2. With a likely magnitude for horizontal eddy diffusivity (1 O5cm2 s-l), the change in chlorophyll concentration due to horizontal diffusion must be very small (order 0.01 mg Chl a m-3 d-l, or a few percent of the phytoplankton stock per day). Finally, with the range of maximum vertical gradients of Chl a just below the mixed layer (0.003-0.023 mg Chl a m-3 m-l, based on seven vertical profiles in May 1988; N. A. Welschmeyer pers. comm.) and a probable range for vertical eddy diffusivity just below the mixed layer in May (3-8 cm2 s-l, Anderson et al. 1977), changes in phytoplankton stock due to vertical exchange between the mixed layer and the layer below ranged from 0.5 to 7.9% of the mixed layer standing stock per day. Taken together, diffusion and advection are likely to produce a net negative local change in phytoplankton stock in the mixed Layer that might be up to 10% d-l, but usually less. Although such physically induced changes could account for a significant part of the day-to-day variability in Fig. 4, they could not account for the month-long maintenance of phytoplankton stock within the narrow range observed, given a mean specific growth rate of 0.57 d-l (Table 1). The phytoplankton assemblage at Station P is dominated by pica- and nanoplanktonsized cells (Booth 1988) which probably explains the relatively small sinking losses of phytoplankton (on average, -2% d-l of the phytoplankton stock in the mixed layer; Miller et al. 1988; N. A. Welschmeyer pers. comm.). Staying with finite daily rates of change and combining the advection and diffusion terms in Eq. 1, we can summarize the pro- cesses causing change in phytoplankton stock for May 1988: g = (0.57 - 0.10 - 0.02 - g)P (2) where g represents the specific grazing mortality rate. Thus $ = (0.45 - g)P. Clearly, for APlAt to have been about zero at Station P over a period of several weeks in ‘May 1988 (Fig. 4) the finite grazing loss must have been a substantial fraction (- 80%) of the specific growth rate and must have been -0.45 d-l. One objective of the SUPER investigation was to directly assess gra.zing, and some results are presented elsewhere (Miller et al. 199 1; the experimental estimates of grazing in May 198 8 were of the: necessary magnitude to balance phytoplankton growth, and both rates were similar to the rates obtained by my analysis. Such calculations can be made for other seasons at. Station P, but no other comprehensive data set comparable to that of May 1988 exists. Nevertheless, it is worth noting that during the last SUPER cruise (5-25 August 1988), alternating between Station P and a station at 53”N, 145”W, the mean specific growth rate of the phytoplankton, calculated as outlined in Table 1, was 0.44 d-” (SE 0.035, N = 7). The value is lower, but not statistically significantly different, than that for May 1988 (Table 1) due to a larger C : Chl a ratio (87.3, SE 5.3, N = 17; B. Booth pers. comm.). Phytoplankton stocks did not change significantly at either station during the cruise. Thus assuming the same fractional losses of phytoplankton to advection, diffusion, and sinking estimated above, for APlAt to be zero in a phytoplankton assemblage growing at 0.44 d-l the specific grazing mortality rate must be -70% of the phytoplankton specific growth rate. ThLese two rates were also in the range of those estimated experimentally in August 1988 (Miller et al. 199 1). .4pplication of a phytoplankton pigment budget at Station P suggests that the grazing is due chiefly to very small (microzooplankton) grazers (Miller et al. 1988; N. A. Wlelschmeyer pers. comm.), which is con- 1621 Grazing in the open sea sistent with the dominance of the phytoplankton at Station P by pica- and nanophytoplankton, as noted earlier. The conclusion that grazing mortality rate must be a substantial fraction of the phytoplankton specific growth rate can also be drawn for the other two nutrient-rich, openocean areas under consideration here. For the Pacific equatorial upwelling region a more significant vertical advection term must be considered, with advective loss of phytoplankton stock due to divergence at the equator, but, with the observed vertical velocities (1 or 2 m d-l; Philander 1990) and a mixed-layer depth of 30 m, it must be a very small loss-a few percent per day at most. Cullen et al. (in press) and Pena et al. (199 1) also concluded that grazing must control phytoplankton stock in the Pacific equatorial upwelling region. In open subantarctic waters, light limitation might be a more severe constraint on phytoplankton growth than in the subarctic Pacific because of substantially deeper mixed layers in summer (Levitus 1982). In both regions the dominant grazers are also likely to be microzooplankters, since the phytoplankton assemblage is dominated by pica- and nanophytoplankton (Hewes et al. 1985; Probyn and Painting 1985; Chavez et al. 1990; Pefia et al. 1990). 10 1 I I 867 k ~6- 0 5 10 15 DAYS Fig. 6. Increase in phytoplankton stock (initially at 0.2 mg Chl a m-3) projected for different net specific growth rates (d-l) with no grazing. in grazer populations (Cushing 1959). Protozoans are not the types of grazers envisaged by Walsh (1976) nor would his proposed effect of frequency of variability of the physical environment explain the persistent balance in the open subarctic Pacific, where intense storms are frequent. Nevertheless, as reframed above, the hypothesis can be the basis for observational and experimental tests. Postponing discussion of episodic forcing events- to the next two sections, I have graphed the expected increase in a phytoplankton assemblage in Fig. 6, given different net specific growth rates and no grazing mortality, from an initial concentration of Grazing hypothesis 0.2 mg Chl a m-3 (i.e. the initial concentraThe analysis leads to a general hypothesis, tion observed at Station P in May 1988: Fig. modified and extended from that of Walsh 4). If, as in May 1988 (Table I), the net (1976), about the role of grazing in the nuspecific growth rate of the phytoplankton is trient-rich areas of the open sea. In the nu- 0.37 d-’ (the equivalent instantaneous net trient-rich areas ofthe open sea,phytoplankspecific growth rate from Eq. 3), then with ton net spec& growth rate and spec$c no grazing a phytoplankton bloom would grazing mortality rate tend toward approx- develop in a matter of 8-10 d (heavy line imate balance that may be perturbed, but in Fig. 6). Naturally, if a bloom occurred not fully disrupted, by episodic forcing events nutrients would be depleted. For the phyexternal or internal to the pelagic food web. toplankton stock to remain essentially unNet specific growth rate of the phytoplankchanged over 3 weeks as observed (Fig. 4), ton is defined here as the specific growth the specific grazing mortality rate must be rate adjusted for losses due to physical provery near 0.37 d-l. Such grazing would not cesses and sinking, but not grazing. The balonly keep the phytoplankton stock low, but ance is possible because the dominant graz- would also indirectly prevent macronutriers are very probably small heterotrophic ents from being depleted. protists, whose growth rates can equal or The other two curves in Fig. 6 are meant exceed those of their phytoplankton prey, to extend the range of possible net specific greatly reducing time lags between increase growth rates to phytoplankton assemblages in phytoplankton abundance and increase subjected to greater constraints on their in- 1622 Frost Herbi wrous Microzooplankton I n‘%w -hi 5 I Phytoplankton ” minipellets .Irn f q2 I 4 I NO3 4 I 6 * .r, ---- NH4 [ Pr-;t;fJ..in] / b & -HH 911 Fig. 7. Trophic interactions represented in the model. Solid lines are phagotrophic links; broken lines are N recycling links [q,, fraction of herbivore mortality released as NH,; q2,fraction of herbivore egestion (“minipellets”) released as NH& dashed line represents input of NO, by vertical turbulence and entrainment. ttinsic growth, such as might be imposed by more severe light limitation in the subantarctic region due to deeper mixed layers or by scarcity of a trace nutrient, such as soluble Fe, as has been suggested to occur in the nutrient-rich areas of the open subarctic Pacific and subantarctic seas (Martin et al. 1989, 199Ob).Note, however, that even at the low net specific growth rate of 0.1 d--l, which must be well below the observed values for nutrient-rich open sea areas, at least in summer (Banse 199 l), the phytoplankton stock would still quadruple in just 2 weeks and increase by 20 times in a month, if grazing did not consume the daily production remaining in excess of other losses. There must be a removal of excess phytoplankton production by grazing in all three nutrientrich areas considered here; limitation of phytoplankton growth, by either light or a trace nutrient such as Fe, is not sufficient as the sole explanation of those areas of the open sea where nutrient concentrations are persistently high and phytoplankton stocks are low. Even if the specific growth rate of the phytoplankton assemblage is less than optimal, grazing must still approximately balance phytoplankton net specific growth to prevent phytoplankton blooms and nutrient depletion in the nutrient-rich areas of the open sea. Returning to Station P, the primary production rate data for summer, indicating malderately high specific growth rates of the phytoplankton assemblage, argue against limitation of phytoplankton growth, by either light or a trace nutrient such as Fe, to the: point where phytoplankton stock could not increase in the absence of grazing. Thus, phytoplankton growth and grazing must be dynamically closely integrated, particularly in a seasonally variable growth environment such as the subarctic Pacific (Fig. 2). Seasonal plankton dynamics in the open subarctic Pa&& I[ have used an ecosystem process model to investigate the dynamic interactions between phytoplankton and grazers in the open subarctic Pacific. The details of ithe model and its predictions are described elsewhere (Frost in prep.), but the model is directly derived from an earlier version (Frost 1987, experiment 3) representing the dynamics of two functional trophic groups: phytoplan kton (pica- and nanophytoplankton) and their grazers (phagotrophic protistan grazers). Figure 7 schematically illustrates the modeled trophic interactions. The model is one-dimensional, with the ocean treated as a three-layered system 120 m deep (a homogeneous mixed layer, a 1623 Grazing in the open sea stratified intermediate layer, and the permanent halocline). Stocks of phytoplankton, herbivorous microzooplankton, and two nitrogenous nutrients (NO3 and NH4) are allowed to vary in the mixed layer and intermediate layer, but are fixed at 120-m depth. There is entrainment to and detrainment from surface populations and nutrient stocks when the mixed layer deepens and shoals. There is seasonally variable vertical turbulent mixing (isotropic in the intermediate layer) between the mixed layer and the layer below. The environmental forcing variables (incident solar radiation, mixedlayer depth, and mixed-layer temperature) are input to the model with daily observations obtained at Station P in 1970 (Fig. 2). A key feature of the model is the pattern of nutrient utilization and recycling. Based on experiments at Station P, Wheeler and Kokkinakis (1990) concluded that NO3 uptake by the phytoplankton is inhibited by the presence of regenerated forms of N, principally NH4. Because the mechanism and exact physiological basis of inhibition, particularly the dependence on concentrations of the two forms of nitrogenous nutrient, remain obscure (Dortch 1990), a simple contingency rule is used in the model. It is assumed that phytoplankton preferentially utilize NH4 and absorb it according to Michaelis-Menten kinetics. It is further assumed that phytoplankton growth is not limited by nitrogenous nutrient; any portion of the N requirement (set by C uptake) not satisfied by NH4 is met by the uptake of N03. Other forms of regenerated N (e.g. urea) are not distinguished from NH, in the model. A primary source of NH4 in the model is regeneration by grazers, but this is insufficient by itself (King 1987), and other sources of NH4 must be added to produce realistic concentrations (broken lines in Fig. 7). These include excretion by carnivores (predators of herbivorous microzooplankton), taken to be a fraction (4,) of daily herbivore predation mortality, and the recycling of a fraction (qJ of the N contained in fecal material (“minipellets”) produced by microzooplankton grazers. The model was applied by an essentially inverse method of fitting to the SUPER data. That is, grazing, growth, and predation co- o100 150 o! 100 I I I I 150 200 250 300 Ok 0 60 200 120 180 240 Day of the Year 300 250 300 360 Fig. 8. A. Phytoplankton standing stock (as integrated Chl a) predicted (line) and observed (0) during the SUPER cruises (1987, 1988). B. Phytoplankton production rate predicted (line) and observed (0) during the SUPER cruises. Observations provided by N. A. Welschmeyer. C. As panel A, but for entire year using data (0) from Fig. 1A. efficients for the herbivorous microzooplankton were first selected to give a fit to Chl a data (Fig. 8A). Then values of photosynthetic parameters were found that produced a fit to observed production rates (Fig. 8B). A major finding was that to simulate observed levels of phytoplankton production, maximum intrinsic growth rates had to conform to the optimal temperature-dependent rates (Eppley 1972); there was no field evidence that phytoplankton growth was less than expected for the prevailing light and temperature conditions. Given this fit to the seasonally restricted SUPER data, 1624 m h Frost 0 60 120 180 240 300 360 0 60 120 180 240 300 360 20 2 Z ; $ E3 .t: z 10 0 *1 b 0.4 z a I C 0.3- E E 0.2E" .z o.ig E 0.0 $ 0 . 1 60 . 1 120 1 - ' . ' . 180 240 300 360 Day of the Year Fig. 9. Mixed-layer concentrations predicted by the model. A. Phytoplankton (P) and herbivorous microzooplankton (H). B. NO, (data from Fig. 3-O). C. NH,. Vertical mixing and nutrient recycling efficiency parameterized as for the cases with heavy lines in Fig. 12. the model predicts an annual cycle for integrated Chl a that is similar to the observed annual cycle, though not reproducing the full variability of the observations (Fig. 8C). The predicted annual cycles for concentration of Chl a and herbivorous microzooplankton indicate that phytoplankton growth and grazing are in balance throughout the year, as evidenced by the continuously low phytoplankton stock (Fig. 9A), despite large seasonal changes in growth conditions (Fig. 2). A wide range of parameter values for herbivore ingestion rate, growth rate, and mortality produce this general pattern of balanced phytoplankton growth and grazing (Frost in prep.). Again, the balance is possible because the modeled grazer is a protozoan with relatively high potential grazing and growth rates (Frost 1987). In addition, a fundamental property of this pelagic ecosystem, first noted by Evans and Parslow ( 198 5), is that even in winter positive phytoplankton production is possible because the shallow permanent halocline limits the depth of winter mixing. This means that herbivores can be nourished and grow in winter, ensuring that a responsive grazer population is continuously present. The predicted fluctuations in stocks of phytoplankton and grazers (Fig. 9A) are driven by daily variability in insolation and mixed-layer depth (Fig. 2), although the intensity of the fluctuations can be amplified by biological interactions, as illustrated below. NO, is drawn down in the summer (Fig. 9B), but is not fully depleted because of rapid recycling of N and the preferential utilization of NH, by the phytoplankton in the mixed layer. NO3 increases in fall and winter because of the combined effects of declining phytoplankton production due to decreasing insolation, and cooling and destratification of the upper layer, entraining NO3 from below. NH4 is always low, but very dynamic (Fig. 9C); its concentration de:pends on both utilization by the phytoplankton and the recycling efficiency of the food web, as illustrated below. The full range of natural variability is generally not reproduced by the model (Fig. 8), except perhaps in spring when the upper water is restratifying. It is useful to look in more detail at that period, not only because it illustrates the effect of episodic forcing events, but also because it suggests some constraints on tests of the grazing hypothesis. Figure 10 gives predicted and observed Chl a and NH, concentrations in the mixed layer for May. Note the predicted fluctuations (Fig. 1OA) that are driven in the model by rapid changes in mixed-layer depth; variability of the physical environment perturbs the balance but does not disrupt it to the extent that a phytoplankton bloom occurs. An even larger perturbation is evident in early June (Fig. 9A, day 155), driven by rapid shoaling of mixed-layer depth to only 10 m (Fig. 2). Clearly, there are times when p‘hytoplankton growth and grazing may not be in balance or even close to it. Thus, spot Grazing in the open sea0.7 = b 0 0.0 A . 0.6 1625 - I =- ’ . 1. - - ’ 1 - . - - 1 - * - ’ ’ . . - - ’ . . . * 1 121 126 131 136 141 146 151 MODEL DAY (MAY) 0.51 0.4 I 0 b . 0.3 . 0.2 .b . . *~zooo 0 0.1 0 0 b oo . beog 0 0. 0 bob 0 00 00 0 1 6 11 DAY 16 IN MAY 21 1988 26 120 180 240 300 9 360 - Day of the Year . . . 60 31 Fig. 10. A. Daily model predictions for mixed-layer concentrations of phytoplankton (0) and NH, (0). B. Observations of same, at Station P in May 1988. Data in panel B provided by P. A. Wheeler and N. A. Welschmeyer. measurements of grazing and growth may not be sufficient to test the grazing hypothesis; measurements should be made over a significant time period, say, on the order of 5-10 doubling times of the phytoplankton (as was done during the SUPER investigation; Miller et al. 1991). Two essential features of the plankton dynamics in the open subarctic Pacific are accounted for by this model-the relatively low phytoplankton stock and the year-round high NO3 concentration. First, the predicted phytoplankton stock is strongly influenced by both the modeled feeding behavior of the grazer and the predation mortality imposed on the grazer (Fig. 11). For a given value of insolation the concentration of phytoplankton determines the phytoplankton production rate in this model, as it seems to do in the ocean as well (N. A. Welschmeyer unpubl. data), which is a strong argument for studying not only the feeding responses of microzooplankton, but also those of their predators. Notice that the magnitudes of the fluctuations produced by episodic physical forcing (chiefly change in Fig. 11. Annual cycle of phytoplankton standing stock (as Chl a) predicted by the model with different combinations of herbivore feeding threshold (P,, mg C m-3) and herbivore maximum specific mortality rate (g, d-l). Lower curve: P,, = 7.5, g = 0.2; middle curve: P, = 10.0, g = 0.2; upper curve: PO = 10.0, g = 0.3. (See equations 18 and 19 of Frost 1987 for context of parameters in model.) mixed layer depth) are amplified at high rates of predation. In fact, predation on the grazers, a process internal to the food web, has the potential to perturb the balance by itself, as noted below. Second, the predicted annual cycle of NO, depends, of course, not only on the rate of utilization of NO3 by the phytoplankton, but on the rate of vertical mixing and the nitrogen recycling efficiency of the pelagic food web (Fig. 12). A steady annual cycle of NO3 is not easily produced by the model; NO, concentration at the end of the year may be higher or lower than at the beginning of the year, just as observed interannually at Station P (Parslow 198 1). Parameterization of the vertical and seasonal variation in mixing rate, especially winter mixing, is important in the model (Fig. 12A). However, in the ocean a few brief, intense mixing episodes in winter may be very significant in establishing the winter NO3 concentration (Large et al. 1985), and such episodes are not included in the model. To achieve concentrations of NH, and NO3 similar to those observed in the mixed layer at Station P during the SUPER cruises (Wheeler and Kokkinakis 1990) requires the recycling efficiency (N released by consumers/total N Frost 1626 0 0 I I I I I I 60 120 180 240 300 360 processes-grazing and preferential utilization of NH4 by the phytoplankton-are sufficient to explain why the phytoplankton ass,emblage remains continuously rare and NO3 remains high year-round. It was not included in the model, so Fe limitation of phytoplankton growth (Martin et al. 1989) need not be invoked. Nevertheless, before these conclusions from the model can be applied to the open subarctic Pacific, two presumptions about food-web interactions nee:d to be examined; one of these may indeed involve Fe limitation. Food- web interactions % a 2 0.28 0.19 10 0.13 , iu" '5 h .z % I o! 0 60 120 I I I II 180 240 300 360 Day of the Year Fig. 12. A. Predicted mixed-layer concentration of NO3 for different intensities of turbulent vertical mixing (K,, cm2 s-l) in the intermediate layer. Upper line: case with constant K, (2.0 cm2 s-l); middle line: case with seasonally variable K,, = ~(0.01Z,,) where Z,, is mixed-layer depth and K = 2.0 cm2 s-l m-l; lower (heavy) line: case with the same dependence of K,, on Z,,, but K = 1.5 cm2 s-l m-l. B. Effect of N recycling efficiency on mixed-layer concentration of N03; in all cases the herbivorous microzooplankton excrete N at a rate equivalent to 40% of their N ingestion rate, and K, is seasonallv variable as in the lower curve in panel A. Upper line: high recycling efficiency (q, = 0.6, q2= 0.75); middle (heavy) line: medium recycling efficiency (q,= 0.5, q2= 0.5); bottom line: low recycling efficiency (q, = 0.4, q2= 0.25). Numbers to the right of curves are mean mixed-layer NH, concentrations (mmol N m -‘) during days 180-280. Data from Fig. 3 -0. ingested) to be - 65% on average (heavy line in Fig. 12B). Phytoplankton stock and NH4 concentration remain relatively constant over the year, so, on average, NO3 uptake comprised 35% of the total N uptake by the phytoplankton and represents a measure of the extent of preferential utilization of NH, by the phytoplankton. Despite the range of predictions, the model suggests that a combination of two The first presumption is that in the ocean, as in the model, the entire phytoplankton assemblage is under grazing control. Takahashi et al. (1990) reported large seasonal variations of vertical fluxes of diatom fi-ustules in deep sediment trap collections at Station P. Among the several species sampleld were some very large diatoms (several tens of micrometers in largest dimension) such as Chaetoceros atlanticus, Chaetoceros concavicorne, Corethron criophilum, and Rhizosolenia alata. The implication of these flux data is that there are substantial seasonal changes in growth rates and abundance of large diatoms. Although the surface-layer abundances of large diatoms are indeed highly variable at Station P, the species are always extremely rare, contributing a very small fraction of the total phytoplankton biomass (Clemons and Miller 1984; Horner and Booth 1990; B. C. Booth pers. comm.). In contrast, one of these species (C. concavicorne) was the dominant or codominant species in fall phytoplankton blooms in coastal Dabob Bay (Puget Sound, Washington) in 1973,1979,1982, and 1990 (my unpubl. data). Clearly in Dabob Bay this large diatom is not controlled by grazing, yet extensive analysis of abundances of phytoplankton species at Station P show that neither this species nor any of about a dozen others has ever reached concentrations remotely approaching those observed during the blooms in Dabob Bay (Homer and Booth 1990; B. C. Booth pers. comm.). A possible explanation of the absence of blooms of large diatoms in open waters of the subarctic Pacific is that these species are Grazing in the open sea limited in their growth by a micronutrient, perhaps soluble Fe, which is very scarce there (Martin et al. 1989). Large phytoplankton species may be more susceptible to Fe limitation (Hudson and Morel 1990). Perhaps their growth rate is so low that combined effects of physical losses and sinking dominate their dynamics, and grazing plays a minor, if any, role in controlling their numbers. For example, previously I (Frost 1987) suggested that large suspension-feeding copepods (Neocalanus spp.) might be important grazers of large phytoplankton cells, but abundances of these copepods are at seasonal lows when high autumn diatom fluxes are recorded (Miller et al. 1984; Miller and Clemons 1988). Coastal waters, on the other hand, have such high concentrations of dissolved Fe that limitation of phytoplankton growth by Fe is not expected (Martin et al. 1989). The occurrence of blooms of large diatoms in coastal waters must then be attributed to low grazing rates, presumably because microzooplankton are inefficient grazers of the large cells while meso- and macrozooplankton grazers respond too slowly in their population growth to changes in phytoplankton abundance (Cushing 19 5 9). Whether the net specific growth rate of the phytoplankton assemblage in the open subarctic Pacific is lower than expected, given the light and temperature of the mixed layer, because of scarcity of Fe is a contentious issue (Banse 1990a,b; Martin et al. 1990a). Without getting into the details of the debate, it seems to me that the lack of an effect of Fe enrichment on phytoplankton production rate (Martin et al. 1989) is particularly crucial negative evidence. It suggests that the bulk of the indigenous phytoplankton assemblage (i.e. that responsible for most of the phytoplankton production) is not Fe limited in its growth. However, Martin et al. (1989) did observe an effect of Fe enrichment on population growth rate and final yield of phytoplankton after several days of incubation. Associated change in species composition of the phytoplankton suggests release from Fe limitation of a normally rare component that perhaps is not efficiently grazed by the indigenous grazer assemblage. 1627 Thus, if we incorporate a possible effect of Fe deficiency on phytoplankton species composition, surface waters of the open subarctic Pacific may remain nutrient-replete because of grazing control of phytoplankton stock, coupled with preferential utilization of NH4 by the phytoplankton, yet the grazing control may be exerted on an assemblage structured by Fe limitation. A large part of the indigenous phytoplankton assemblage- that responsible for the bulk of the phytoplankton production - appears not to be Fe limited. Hence a model can describe the annual cycle of phytoplankton stock and nutrients quite well without invoking Fe limitation of phytoplankton growth. However, when a natural phytoplankton assemblage is exposed to Fe enrichment, a rare component of the phytoplankton assemblage, normally contributing little to total phytoplankton production, is released from Fe limitation. This component seems to be large-sized species, chiefly diatoms (Martin et al. 1989), that cannot be grazed efficiently by the indigenous grazer assemblage. This interpretation could apply to the other two nutrient-rich areas of the open ocean as well, with a possible additional effect of silica limitation of diatom growth in the subantarctic circumpolar seas (Sommer and Stabel 1986). However, the magnitude of the necessary grazing control would vary among the nutrient-rich regions depending on the actual magnitudes of phytoplankton net specific growth rates. The second presumption concerns the fact that control or regulation of phytoplankton stock is a property of the entire pelagic ecosystem, not solely a consequence of grazing (Thingstad and Sakshaug 1990). It is presumed that the grazer trophic guild is insulated from potentially destabilizing predation (Hastings and Powell 199 1; Steele and Henderson in prep.), otherwise grazer populations would occasionally be depressed by predation and phytoplankton blooms with attendant nutrient depletion would occur. Such events would certainly have been evident, had they occurred, in the long time-series of observations at Station P, yet there is no record of a phytoplankton bloom of the magnitude of those 1628 Frost in coastal waters (Fig. 1). Although a model of an entire pelagic ecosystem is unattainable, the grazing hypothesis implies a pelagic food chain with the following general hierarchy of control: predators of microzooplankton predators vood limited) + predators of microzooplankton suspensionfeeders (predator limited) + microzooplankton suspension-feeders (food limited) -+ phytoplankton (predator limited). That. is, in order that the hypothesized balance between phytoplankton growth and grazing mortality not be disrupted, the predators of microzooplankton suspension-feeders must be kept largely under control by their predators. The composition of the upper two trophic guilds in nutrient-rich, open seas is unknown, but I have suggested (Frost in prep.) that in the open subarctic Pacific the fourth trophic guild must be mesozooplankton-the size fraction of the zooplankton dominated by the large Calanoid copepods Neocalanus spp. Conclusions The nutrient-rich areas of the open sea are not as biologically productive as they might be. Grazing and Fe limitation have recently been portrayed as alternative explanations for why phytoplankton stocks are low and nutrients are underutilized in these ocean areas. But no single factor can completely explain the pattern, and, like all interesting scientific controversies, the full explication probably will inco.rporate aspects of both of these hypotheses and perhaps even others. Surface waters of the Pacific equatorial upwelling zone and the open subarctic Pacific may remain nutrient-replete because of grazing control of phytoplankton stock, coupled with preferential utilization of NH4 by the phytoplankton. Yet, the grazing control may be possible only because certain components of the phytoplankton assemblage, particularly potentially fast-growing, inefficiently grazed species, are limited in their growth by a trace nutrient such as dissolved Fe. The subantarctic circumpolar region may offer the epitome of multifactor control. Deep mixed layers even in summer impose greater light limitation on phytoplankton growth than in the other two nutrient-rich areas. Scarcity of dissolved Fe, or even Si04, may place an added constraint on growth of certain components of the phytoplankton, leading to dominance by species, chiefly pica- and nanoplankton-size, with low requirements for Fe or SiOZ. 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