Over most of the ocean, the amount of new production (net increase in organic matter) by phytoplankton is regulated by the availability in the surface layer of the plant nutrient nitrate. In the so-called ‘high-nitrate, low-chlorophyll’ (HNLC) regions, however, phytoplankton biomass remains low throughout the year despite high concentrations of nitrate. The condition has long been regarded as a paradox, but increasing evidence has indicated that, in these regions, phytoplankton production is limited by iron availability.
In their paper on page 270 of this issue1, Dugdale and Wilkerson now add an additional facet to the debate. They analyse data from the equatorial upwelling zone (EUZ) of the eastern Pacific — an HNLC region — and, with the aid of a simple budgetary model, show that the magnitude of new production there is a function of the input of dissolved silica (silicate) by upwelling of deeper water. This limitation occurs because new production is monopolized by diatoms (silica-shelled, unicellular algae) whose growth rates are limited by the supply of silicate.
The finding puts an upper limit on the rate of new production in the EUZ, and hence on the export of organic carbon from surface to deeper layers through the biological pump2. This has implications for CO2 exchange between ocean and atmosphere because the EUZ, a broad belt of water stretching across the entire eastern Pacific, annually degasses about 1 gigatonne (109 tonnes) of CO2 (ref. 3), equivalent to 20 per cent of current anthropogenic output. The regression lines and intercepts of dissolved inorganic carbon, silicate and nitrate concentrations, measured in the upper 200 m of the EUZ, indicate that silicate availability regulates both carbon and nitrate uptake and fate. The slope of the highly significant regression between nitrate and silicate is 1, which coincides with the known requirement of these two elements by diatoms. The intercept represents the excess nitrate (about 4 mmol m−3) that confers HNLC status on the EUZ.
Silicate is bound in mineral shells (biogenic silica) of no food value. In the EUZ model, the diatom shells are packaged in zooplankton faeces and exported wholesale from the surface layer. In contrast, nitrogen is selectively retained by the diatom grazers which, in the course of their metabolism, excrete ammonia; in turn the ammonia is assimilated by the photosynthesizing cyanobacteria (<2 μ m) and small flagellates (2-10 μm) of the ‘microbial loop’. This ubiquitous community (pico- and nanoplankton) is additionally composed of small protozoa that feed on the minute algae and bacteria, as well as on one another, which also release ammonia (see Fig. 2 of Dugdale and Wilkerson's paper, page 272). The ammonia-based production within this tightly geared community — termed regenerated production — contributed four-fifths of the total daily production (new plus regenerated) in the EUZ. Because of the low variability in nutrient and biomass concentrations observed over different cruises and seasons, the pelagic system of the EUZ seems to have settled into a steady state which can be likened to a silicate-limited chemostat.
The silicate-to-nitrate ratios in the other HNLC regions — the Southern Ocean and the subarctic Pacific — are much higher than in the EUZ, yet fairly similar community structures, total production rates and ratios of new-to-regenerated production are routinely measured there. Diatom growth is evidently not silicon-limited, so other factors, such as deep mixing, iron deficiency and heavy grazing pressure, have been invoked to explain the HNLC condition. An in situ iron fertilization experiment (IronEx II), carried out in the South Equatorial Current adjacent to the EUZ, yielded a spectacular diatom bloom4 and showed that iron availability indeed limited new production in this region.
Dugdale and Wilkerson argue that, as the EUZ diatoms are already silicate-limited, adding iron should have no effect on them. They suggest that iron upwelling with the other nutrients in the EUZ is sufficient to meet the demands of the diatoms. In the iron-limited waters of the South Equatorial Current, iron-fertilized diatom growth would eventually be halted by silicate but not nitrate exhaustion.
Yet the paradox persists. Virtually all phytoplankton species, including the picoplankton, are able to use nitrate; indeed, phytoplankton other than diatoms routinely exhaust nitrate in the surface waters of the non-HNLC ocean. So why does this not happen in the EUZ and other low-silicate HNLC regions? Differences in grazing pressure have been proposed as an explanation5. One widely held view is that the small algae of the microbial loop are kept in check by heavy grazing pressure, whereas diatoms, because of their larger size (and possibly also the protection offered by the silica shell), are less prone to being grazed by the smaller protozoa6. So relaxation of a limiting factor (such as iron) results in accumulation of diatom but not picoplankton cells. Whether continued iron fertilization will eventually lead to nitrate exhaustion by non-diatom phytoplankton in low-silicate HNLC regions remains to be tested.
In Dugdale and Wilkerson's steady-state EUZ model, the biomass-to-production ratio of the diatoms indicates that they were growing at least as fast as, if not faster than, the microbial algae. To maintain steady state, grazing pressure on the diatoms, presumably by copepods (zooplanktonic crustacea, equipped with mandibles edged with silica the better to crush diatom shells with), must have been similar to or even higher than that on the microbial algae. The growth performance of the diatoms is all the more surprising as nitrate reduction requires energy and the mediating enzyme contains iron. Indeed, why diatoms can be so much more efficient than the other algae despite the nitrate handicap needs to be explained.
Balancing pelagic ecosystem budgets is still an art because we know so little about the abilities and predilections of the organisms and their interactions with one another5. Whatever the outcome of studies on the limiting factors in the various HNLC regions and their subsystems, the status of diatoms as key players will not be challenged. The work-horses running pelagic systems are recruited from this algal group: their new production not only fuels the food chains leading to fish but also provides the raw material driving the biological pump and ultimately the great biogeochemical cycles of the ocean. It is time we gained a better understanding of the properties that make diatoms so special.
Dugdale, R. C. & Wilkerson, F. P. Nature 391, 270–273 (1998).
Doney, S. C. Nature 389, 905–906 (1997).
Tans, P. P., Fung, I. Y. & Takahashi, T. Science 247, 1431–1438 (1990).
Coale, K. H. et al. Nature 383, 495–501 (1996).
Banse, K. Oceanography 7, 13–20 (1994).
Banse, K. ICES J. Mar. Sci. 52, 265–277 (1995).
About this article
Remarkable structural resistance of a nanoflagellate-dominated plankton community to iron fertilization during the Southern Ocean experiment LOHAFEX
Marine Ecology Progress Series (2018)
The epibiotic life of the cosmopolitan diatom Fragilariopsis doliolus on heterotrophic ciliates in the open ocean
The ISME Journal (2018)
Shifting Diatom—Dinoflagellate Dominance During Spring Bloom in the Baltic Sea and its Potential Effects on Biogeochemical Cycling
Frontiers in Marine Science (2018)
Annual Review of Marine Science (2018)
Biodiversity effects on resource use efficiency and community turnover of plankton in Lake Nansihu, China
Environmental Science and Pollution Research (2017)