Grazing and iron limitation in the control of phytoplankton stock and nutrient concentration: a chemostat analogue of the Pacific equatorial upwelling zone

Frost, B.; Franzen, NC

doi:10.3354/meps083291

Cited by 143 publications

(80 citation statements)

References 12 publications

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“…In particular, Prochlorococcus cell division rate and mortality are tightly coupled in the equatorial Pacific Cullen 1991;Frost and Franzen 1992;Cullen 1995;DuRand 1995;Vaulot et al 1995;Binder et al 1996;Verity et al 1996;Liu et al 1997;Loukos et al 1997;Strom et al 2000). As pointed out in Landry et al (1997) and seen in this study, balanced cell division and mortality are not incompatible with iron limitation, and biomass can be constrained by both iron limitation (in terms of cell size and pigment content) and microzooplankton grazing (in terms of cell numbers).…”

Section: Resultsmentioning

confidence: 71%

“…A tight coupling between cell division rate and mortality for the picoplankton is one of the basic tenants of the ecumenical hypothesis (Frost and Franzen 1992;Price et al 1994) and the equatorial Pacific synthesis by Landry et al (1997). In particular, Prochlorococcus cell division rate and mortality are tightly coupled in the equatorial Pacific Cullen 1991;Frost and Franzen 1992;Cullen 1995;DuRand 1995;Vaulot et al 1995;Binder et al 1996;Verity et al 1996;Liu et al 1997;Loukos et al 1997;Strom et al 2000).…”

Section: Resultsmentioning

confidence: 99%

“…These are relatively high values for a picoplankton-dominated community (Chisholm 1992;Cullen et al 1992), which suggests that these cells are growing at near maximal growth rates. Estimated ratios of new production to total primary production are low (McCarthy et al 1996), which indicates that most of this growth is fueled by regenerated nutrients, which are produced by the intensive grazing that keeps the picoplankton community in check (Wheeler and Kokkinakis 1990;Chavez et al 1991;Cullen et al 1992;Frost and Franzen 1992;Price et al 1994;Landry et al 1997;Loukos et al 1997).…”

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confidence: 99%

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Iron limits the cell division rate of Prochlorococcus in the eastern equatorial Pacific

Mann

Chisholm

2000

Limnology & Oceanography

120

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Prochlorococcus, a small unicellular cyanobacterium, is an important member of the phytoplankton community in the eastern equatorial Pacific. When these waters were enriched with iron during IronEx II, the chlorophyll per cell and cell size of Prochlorococcus increased, implying that they were iron limited. The extent of this limitation was unclear, however, and the number of Prochlorococcus remained constant. To examine whether cell division rates were stimulated significantly by iron, we used a cell cycle analysis approach to measure them in and out of the Fe-enriched patch and in Fe-enriched bottles. The cell division rate increased from 0.6 to 1.1 d Ϫ1 over 6 d of exposure to the elevated iron concentrations in the patch. Cells incubated in bottles with additional iron had rates of 1.4 d Ϫ1 or two doublings per day. Prochlorococcus mortality rates, measured independently, nearly doubled after the addition of iron. This matched the increase in the cell division rate and maintained a relatively constant population size. Thus the cell division rates of even the smallest phytoplankton in the equatorial Pacific are significantly iron limited, but biomass is constrained by both iron limitation and microzooplankton grazing. The differential response of individual phytoplankton groups to the addition of iron during IronEx II was at least partially a result of differential mortality rates over the time course of the experiment. How the community would respond to sustained fertilization, however, is not obvious.Nitrate and phosphate concentrations are persistently high in the euphotic zone of the equatorial Pacific, and phytoplankton biomass and productivity are lower than expected based on nutrient availability (Cullen 1991;Frost and Franzen 1992). The phytoplankton community is dominated by small picoplankton (Chavez 1989), which have a large surface area to volume ratio and are less likely to be diffusion limited by either nutrients or trace metals than larger cells (Morel et al. 1991a). Measured cell division rates are often 0.5 d Ϫ1 or higher, both for the phytoplankton community as a whole (Barber and Chavez 1991;Chavez et al. 1991;Cullen 1991;Cullen et al. 1992;Landry et al. 1995;Verity et al. 1996;Latasa et al. 1997;Lindley and Barber 1998) and for the small cyanobacterium Prochlorococcus (DuRand 1995;Landry et al. 1995;Vaulot et al. 1995;Binder et al. 1996;Latasa et al. 1997;Liu et al. 1997; Vaulot and Dom-1 Corresponding author (chisholm@mit.edu). AcknowledgementsWe thank the captain and crew of the RV Melville, as well as Kenneth Coale and the Moss Landing IronEx group, for making the experiment possible. We also thank R. Michael Gordon for iron concentration measurements, and Richard Barber, William Cochlan, Michael R. Landry, and Makoto Saito for sharing unpublished data. Comments by J. Cullen, P. Falkowski, and an anonymous reviewer helped improve the manuscript.

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Section: Resultsmentioning

confidence: 71%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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Iron limits the cell division rate of Prochlorococcus in the eastern equatorial Pacific

Mann

Chisholm

2000

Limnology & Oceanography

120

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“…Typically, this inhibition is represented by a simple mathematical expression multiplied by the nitrate uptake term (e.g., Wroblewski 1977;Fasham et al 1990;Frost and Franzen 1992). However, use of the same functional form everywhere may be incorrect.…”

Section: Discussionmentioning

confidence: 99%

An optimization‐based model of iron—light—ammonium colimitation of nitrate uptake and phytoplankton growth

Armstrong

1999

Limnology & Oceanography

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The ability to model ''new'' (nitrate-based) production is crucial to predicting the ocean's role in the global carbon cycle. The ability to model the distribution of high-nutrient/low-chlorophyll (HNLC) areas is particularly important in this regard. Here I draw together three elements that appear to be necessary for constructing the required model: (1) iron limitation of algal growth rates as an ultimate cause of the HNLC condition; (2) ammonium inhibition of nitrate uptake and utilization as a proximate mechanism that leads to reduced nitrate use; and (3) the dependence of both processes on algal cell size. In the model, cells are postulated to maximize their growth rates by partitioning scarce iron between nitrogen-and carbon-related demands. The effect of iron limitation is postulated to depend on cell size through surface/volume effects on uptake efficiency; this dependence on cell size in turn affects phytoplankton community structure and community-level uptake of nitrate. The efficacy of the model is demonstrated by its ability to reproduce community-level curves of nitrate uptake versus ammonium concentration from both HNLC and non-HNLC areas. The partition formalism can be incorporated directly into ecosystem models; when implemented in an ecosystem model with multiple size classes, the model should produce HNLC versus non-HNLC conditions in appropriate locations and for appropriate reasons. In particular, the model's ability to produce iron-light and iron-light-nitrogen colimitation should be useful in understanding and predicting the HNLC condition in parts of the Southern Ocean. With suitable changes to parameter values, the postulated mechanism for iron partitioning may also prove useful in modeling iron and energy partitioning in nitrogen fixers. The ability to model the distribution of high-nutrient/lowchlorophyll (HNLC) areas, where concentrations of nitrate and phosphate remain high throughout the year, is critical to prognostic studies of the global carbon cycle. Empirical evidence suggests that the ability to model iron limitation of growth and nitrate uptake will be a key element in predicting HNLC conditions. As the prime example, a scarcity of iron has recently been shown to limit phytoplankton growth, biomass accumulation, and size and taxonomic structure in the equatorial Pacific, a major HNLC region (Coale et al. 1996). Addition of iron to surface waters of this region caused a massive phytoplankton bloom and drawdown of nitrate, accompanied by a marked reduction in the fugacity of CO 2 (Cooper et al. 1996). The possibility of similar conversion of the subarctic Pacific (La Roche et al. 1996) and the Southern Ocean (de Baar et al. 1995;Kumar et al. 1995) from HNLC to non-HNLC by the addition of iron is supported by more indirect evidence. AcknowledgmentsConversations with Richard Geider helped greatly in the development of these ideas, particularly in the realization that it could be extremely useful scientifically to have a single model of iron limitation that both biogeochem...

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“…The importance of losses resulting from grazing cannot be underestimated (FRosT, 1987;BANSE, 1992;FROST and FRANZEN, 1992), especially where size selection can exert control on the community structure (RaE~MAN, KtnPERS, NOORDELOOS and WI~E, 1993). Similarly loss by sedimentation is commonly observed during bloom conditions and lysis, even in the absence of grazers, is conceivable, in which viruses may play a role (BRATBAK, EC~E and HELDAL, 1993).…”

Section: Concepts Of Phytoplanlcton Growth and Biomassmentioning

confidence: 99%

von Liebig's law of the minimum and plankton ecology (1899–1991)

Baar

1994

Progress in Oceanography

237

132

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-The Law of the Minimum was originally formulated by Justus yon Liebig, as one of the 50 interlinked laws concerned with agriculture. The original writings ofJ. von Liebig often were misinterpreted by his successors. BRAt, rOT (1899) took this one law out of its context and proposed that limitation by nitrogen is a dominant factor in plankton ecology, far beyond its original application to agriculture. This was opposed by NAmANSOrn~ (1908) who suggested instead a dynamic balance of growth and loss terms. Towards validating, or eventually falsifying Brandt's hypothesis, Atkins, Harvey, Cooper and others developed the chemical methods necessary for re-defining ocean nutrient cycling and growth limitation. The major exception to these modem perspectives was the Antarctic Paradox of higla nutrients and low chlorophyll which inspired Gran, Atkins, Harvey and Cooper to pioneer the concept of iron limitation. An exhaustive overview is given of efforts to define Fe in seawater and its controlling effect on in situ plankton growth, for the 1920-1984 period. Somewhat parallel work in the laboratory on single species of algae in chelation-controlled mediahas provided much insight, but is sketched only briefly. Martin and contemporaries developed the chemical methods necessary for defming the ocean chemistry of Fe and its role for in situ growth. These developments are sketched for the 1982-1991 period. Once again the Law of the Minimum and associated bold hypotheses served, albeit briefly, to bring a nutrient element in the forefront of research. This, and the recent awareness of CO 2 as rate limiting factor, underline the conclusion that advances in sciences often hinge on advances in technology, confirming Kta-~ (1962). In this case the new analytical techniques developed by Atkins, Harvey, Cooper, Martin and their associates have proven revolutionary for plankton ecology. Some observations in plankton ecology may be reminiscent of the agricultural Law of the Minimum, but this would not warrant its direct application, beyond its original context and agriculture, to plankton ecology. Rather the net rate of increase ofphytoplankton is the dynamic balance of multiple growth and loss terms, together also determining the biomass at given time and space. 347

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Grazing and iron limitation in the control of phytoplankton stock and nutrient concentration: a chemostat analogue of the Pacific equatorial upwelling zone

Cited by 143 publications

References 12 publications

Iron limits the cell division rate of Prochlorococcus in the eastern equatorial Pacific

Iron limits the cell division rate of Prochlorococcus in the eastern equatorial Pacific

An optimization‐based model of iron—light—ammonium colimitation of nitrate uptake and phytoplankton growth

von Liebig's law of the minimum and plankton ecology (1899–1991)

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