Ben A. Ward

The biogeography of marine plankton traits

Changes in marine plankton communities driven by environmental variability impact the marine food web and global biogeochemical cycles of carbon and other elements. To predict and assess these community shifts and their consequences, ecologists are increasingly investigating how the functional traits of plankton determine their relative fitness along environmental and biological gradients. Laboratory, field and modelling studies are adopting this trait-based approach to map the biogeography of plankton traits that underlies variations in plankton communities. Here, we review progress towards understanding the regulatory roles of several key plankton functional traits, including cell size, N2 -fixation and mixotrophy among phytoplankton, and body size, ontogeny and feeding behaviour for zooplankton. The trait biogeographical approach sheds light on what structures plankton communities in the current ocean, as well as under climate change scenarios, and also allows for finer resolution of community function because community trait composition determines the rates of significant processes, including carbon export. Although understanding of trait biogeography is growing, uncertainties remain that stem, in part, from the paucity of observations describing plankton functional traits. Thus, in addition to recommending widespread adoption of the trait-based approach, we advocate for enhanced collection, standardisation and dissemination of plankton functional trait data.

Interconnection of nitrogen fixers and iron in the Pacific Ocean: Theory and numerical simulations

[1] We examine the interplay between iron supply, iron concentrations and phytoplankton communities in the Pacific Ocean. We present a theoretical framework which considers the competition for iron and nitrogen resources between phytoplankton to explain where nitrogen fixing autotrophs (diazotrophs, which require higher iron quotas, and have slower maximum growth) can co-exist with other phytoplankton. The framework also indicates that iron and fixed nitrogen concentrations can be strongly controlled by the local phytoplankton community. Together with results from a three-dimensional numerical model, we characterize three distinct biogeochemical provinces: 1) where iron supply is very low diazotrophs are excluded, and iron-limited nondiazotrophic phytoplankton control the iron concentrations; 2) a transition region where nondiazotrophic phytoplankton are nitrogen limited and control the nitrogen concentrations, but the iron supply is still too low relative to nitrate to support diazotrophy; 3) where iron supplies increase further relative to the nitrogen source, diazotrophs and other phytoplankton coexist; nitrogen concentrations are controlled by nondiazotrophs and iron concentrations are controlled by diazotrophs. The boundaries of these three provinces are defined by the rate of supply of iron relative to the supply of fixed nitrogen. The numerical model and theory provide a useful tool to understand the state of, links between, and response to changes in iron supply and phytoplankton community structure that have been suggested by observations.

Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux

Significance Marine plankton commonly combine the autotrophic use of light and inorganic resources with the heterotrophic ingestion of prey. These mixotrophs blur the strict boundary between producers and consumers and allow energy and biomass to enter the food web across multiple trophic levels. Incorporating this flexibility into a global simulation of the surface ocean food web reveals that mixotrophy enhances the transfer of biomass to larger organisms at higher trophic levels, which in turn increases the efficiency of oceanic carbon storage through the production of larger, faster-sinking, and carbon-enriched organic detritus. Mixotrophic plankton, which combine the uptake of inorganic resources and the ingestion of living prey, are ubiquitous in marine ecosystems, but their integrated biogeochemical impacts remain unclear. We address this issue by removing the strict distinction between phytoplankton and zooplankton from a global model of the marine plankton food web. This simplification allows the emergence of a realistic trophic network with increased fidelity to empirical estimates of plankton community structure and elemental stoichiometry, relative to a system in which autotrophy and heterotrophy are mutually exclusive. Mixotrophy enhances the transfer of biomass to larger sizes classes further up the food chain, leading to an approximately threefold increase in global mean organism size and an ∼35% increase in sinking carbon flux.

Biophysical Aspects of Resource Acquisition and Competition in Algal Mixotrophs

Mixotrophic organisms combine autotrophic and heterotrophic nutrition and are abundant in both freshwater and marine environments. Recent observations indicate that mixotrophs constitute a large fraction of the biomass, bacterivory, and primary production in oligotrophic environments. While mixotrophy allows greater flexibility in terms of resource acquisition, any advantage must be traded off against an associated increase in metabolic costs, which appear to make mixotrophs uncompetitive relative to obligate autotrophs and heterotrophs. Using an idealized model of cell physiology and community competition, we identify one mechanism by which mixotrophs can effectively outcompete specialists for nutrient elements. At low resource concentrations, when the uptake of nutrients is limited by diffusion toward the cell, the investment in cell membrane transporters can be minimized. In this situation, mixotrophs can acquire limiting elements in both organic and inorganic forms, outcompeting their specialist competitors that can utilize only one of these forms. This advantage can be enough to offset as much as a twofold increase in additional metabolic costs incurred by mixotrophs. This mechanism is particularly relevant for the maintenance of mixotrophic populations and productivity in the highly oligotrophic subtropical oceans.

The impact of fine‐scale turbulence on phytoplankton community structure

We examined the effect of fine-scale fluid turbulence on phytoplankton community structure in an idealized, size-structured community model. It has been shown that turbulence can enhance nutrient transport toward a cell, particularly for larger cells in highly turbulent conditions. Our model suggests that under weak grazing pressure the effect of this mechanism on relative phytoplankton fitness and community structure is negligible. Under these conditions, the high nutrient affinity of small cells dominates relative fitness and allows them to outcompete larger cells. In contrast, when grazing pressure is strong, the turbulent enhancement of nutrient uptake and fitness for larger cells can become ecologically significant. Here, increasing turbulence broadens the size range of coexisting phytoplankton and increases the size of the dominant cell type at equilibrium. We also estimate and map open ocean turbulent dissipation rates as a function of climatological surface wind stresses. The turbulent enhancement of nutrient uptake is most likely to be ecologically significant in regions with low nutrient levels, strong grazing pressure, and relatively high turbulence, such as in windier portions of the subtropical gyre or post-bloom conditions at higher latitudes. In these regions, turbulence may help sustain larger cell populations through otherwise unfavorable environmental conditions.

Temperature-Correlated Changes in Phytoplankton Community Structure Are Restricted to Polar Waters

Globally distributed observations of size-fractionated chlorophyll a and temperature were used to incorporate temperature dependence into an existing semi-empirical model of phytoplankton community size structure. The additional temperature-dependent term significantly increased the model’s ability to both reproduce and predict observations of chlorophyll a size-fractionation at temperatures below 2°C. The most notable improvements were in the smallest (picoplankton) size-class, for which overall model fit was more than doubled, and predictive skill was increased by approximately 40%. The model was subsequently applied to generate global maps for three phytoplankton size classes, on the basis of satellite-derived estimates of surface chlorophyll a and sea surface temperature. Polar waters were associated with marked decline in the chlorophyll a biomass of the smallest cells, relative to lower latitude waters of equivalent total chlorophyll a. In the same regions a complementary increase was seen in the chlorophyll a biomass of larger size classes. These findings suggest that a warming and stratifying ocean will see a poleward expansion of the habitat range of the smallest phytoplankton, with the possible displacement of some larger groups that currently dominate. There was no evidence of a strong temperature dependence in tropical or sub-tropical regions, suggesting that future direct temperature effects on community structure at lower latitudes may be small.

When everything is not everywhere but species evolve: an alternative method to model adaptive properties of marine ecosystems.

The functional and taxonomic biogeography of marine microbial systems reflects the current state of an evolving system. Current models of marine microbial systems and biogeochemical cycles do not reflect this fundamental organizing principle. Here, we investigate the evolutionary adaptive potential of marine microbial systems under environmental change and introduce explicit Darwinian adaptation into an ocean modelling framework, simulating evolving phytoplankton communities in space and time. To this end, we adopt tools from adaptive dynamics theory, evaluating the fitness of invading mutants over annual timescales, replacing the resident if a fitter mutant arises. Using the evolutionary framework, we examine how community assembly, specifically the emergence of phytoplankton cell size diversity, reflects the combined effects of bottom-up and top-down controls. When compared with a species-selection approach, based on the paradigm that “Everything is everywhere, but the environment selects”, we show that (i) the selected optimal trait values are similar; (ii) the patterns emerging from the adaptive model are more robust, but (iii) the two methods lead to different predictions in terms of emergent diversity. We demonstrate that explicitly evolutionary approaches to modelling marine microbial populations and functionality are feasible and practical in time-varying, space-resolving settings and provide a new tool for exploring evolutionary interactions on a range of timescales in the ocean.

The Implications of Eco-Evolutionary Processes for the Emergence of Marine Plankton Community Biogeography

Models of community assembly have been used to illustrate how the many functionally diverse species that compose plankton food webs can coexist. However, the evolutionary processes leading to the emergence of plankton food webs and their interplay with migratory processes and spatial heterogeneity are yet to be explored. We study the eco-evolutionary dynamics of a modeled plankton community structured in both size and space and physiologically constrained by empirical data. We demonstrate that a complex yet ecologically and evolutionarily stable size-structured food web can emerge from an initial set of two monomorphic phytoplankton and zooplankton populations. We also show that the coupling of spatial heterogeneity and migration results in the emergence of specific biogeographic patterns: (i) the emergence of a source-sink structure of the plankton metacommunities, (ii) changes in size diversity dependent on migratory intensity and on the scale at which diversity is considered (local vs. global), and (iii) the emergence of eco-evolutionary provinces (i.e., a spatial unit characterized by some level of abiotic heterogeneity but of homogenous size composition due to horizontal movements) at spatial scales that increase with the strength of the migratory processes.

The Size Dependence of Phytoplankton Growth Rates: A Trade-Off between Nutrient Uptake and Metabolism

Rates of metabolism and population growth are often assumed to decrease universally with increasing organism size. Recent observations have shown, however, that maximum population growth rates among phytoplankton smaller than ∼6 μm in diameter tend to increase with organism size. Here we bring together observations and theory to demonstrate that the observed change in slope is attributable to a trade-off between nutrient uptake and the potential rate of internal metabolism. Specifically, we apply an established model of phytoplankton growth to explore a trade-off between the ability of cells to replenish their internal quota (which increases with size) and their ability to synthesize new biomass (which decreases with size). Contrary to the metabolic theory of ecology, these results demonstrate that rates of resource acquisition (rather than metabolism) provide the primary physiological constraint on the growth rates of some of the smallest and most numerically abundant photosynthetic organisms on Earth.

Assessing an efficient “Instant Acclimation” approximation of dynamic phytoplankton stoichiometry

The variable elemental ratios of carbon to essential nutrients in marine organic matter affect the productivity of marine food-webs and the sequestration of carbon in the deep ocean. It is important that models of these systems are able to correctly reproduce observed trends. “Dynamic Quota” models have achieved some success in this regard, but the computational expense of transporting each state variable in ocean models has prevented many large-scale models from moving beyond a simpler “Fixed Stoichiometry” formulation. This article compares the Dynamic Quota and Fixed Stoichiometry models to a recent “Instant Acclimation” model, which combines the stoichiometric flexibility of the Dynamic Quota model with the computational efficiency of the Fixed Stoichiometry model. The Instant Acclimation model is mathematically equivalent to the Dynamic Quota model at equilibrium, and provides an accurate approximation under a wide range of dynamic conditions. The accuracy and computational efficiency of the Instant Acclimation model recommend it as a candidate for incorporating flexible stoichiometry into marine ecosystem models, especially in situations where the number of model state-variables is restricted.