From the Cover: A simple nutrient-dependence mechanism for predicting the stoichiometry of marine ecosystems

It is widely recognized that the stoichiometry of nutrient elements in phytoplankton varies within the ocean. However, there are many conflicting mechanistic explanations for this variability, and it is often ignored in global biogeochemical models and carbon cycle simulations. Here we show that globally distributed particulate P:C varies as a linear function of ambient phosphate concentrations, whereas the N:C varies with ambient nitrate concentrations, but only when nitrate is most scarce. This observation is consistent with the adjustment of the phytoplankton community to local nutrient availability, with greater flexibility of phytoplankton P:C because P is a less abundant cellular component than N. This simple relationship is shown to predict the large-scale, long-term average composition of surface particles throughout large parts of the ocean remarkably well. The relationship implies that most of the observed variation in N:P actually arises from a greater plasticity in the cellular P:C content, relative to N:C, such that as overall macronutrient concentrations decrease, N:P rises. Although other mechanisms are certainly also relevant, this simple relationship can be applied as a first-order basis for predicting organic matter stoichiometry in large-scale biogeochemical models, as illustrated using a simple box model. The results show that including variable P:C makes atmospheric CO₂ more sensitive to changes in low latitude export and ocean circulation than a fixed-stoichiometry model. In addition, variable P:C weakens the relationship between preformed phosphate and atmospheric CO₂ while implying a more important role for the nitrogen cycle.Nutrient elements are used by phytoplankton to synthesize molecules, in order to accomplish biochemical functions. Some of these molecules are absolutely necessary, and the nutrient elements have no substitutes. Examples are P in nucleic acids, N in amino acids, and Fe in the photosynthetic apparatus (1). However, there is a degree of plasticity in the molecular assemblage required per phytoplankton cell, which varies between species and between clades (2, 3). Furthermore, there is a capacity for plasticity in molecular composition of even a given species, as shown in culture experiments (4, 5). Such plasticity leads to variability in the elemental ratios of nutrients in marine phytoplankton, widely documented in laboratory and field measurements (2, 6, 7). Recent analyses of global nutrient and particulate observations have shown that N:P, the most commonly discussed ratio, varies regionally, including low N:P in the high-latitude Southern Ocean and high N:P in the oligotrophic regions (7–9). Explanations of high N:P in oligotrophic waters have often invoked an enhanced reliance on N-rich proteins for gathering scarce resources (1, 10), whereas low N:P in the Southern Ocean has been variously attributed to the abundance of P-rich molecules in cold, fast-growing plankton (11), or to the availability of Si, which supports P-rich diatom communities (8, 12).Despite an abundant literature on stoichiometric variability and its potential causes, no simple predictive relationship has been widely adopted in global biogeochemical models. Instead, the vast majority of global biogeochemical models assumes fixed C:N:P in organic matter, including most participants in the recent Coupled Model Intercomparison Project, CMIP5 (13). Thus, the potential impact of changes in organic matter stoichiometry on ocean carbon storage and oxygen consumption remain largely unexplored. The neglect of stoichiometric variability is due, at least in part, to the lack of a clear predictive framework.Here, it is argued that the concentration of a nutrient element in seawater can provide a suitable predictive framework, because it is a critical determinant of the rate at which that element will tend to be taken up by the organisms in the local community. This hypothesis builds on classic resource competition theory (14), which argues that if the concentration of an element is low, such that uptake is difficult, the community will be dominated by organisms that are well adapted to a low cellular quota of that nutrient (10). If, on the other hand, the concentration is high, facilitating high uptake rates, the community will be dominated by organisms that are capable of taking advantage of that nutrient to grow faster. This suggestion leads to clear predictions with significant biogeochemical consequences, as outlined below.