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

Abstract

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.arine ecosystems provide essential nutrition to more than half the world's population via fisheries (1) and mediate global cycles of climatically important elements including carbon (2). Current models of marine biogeochemical cycles assume that the plankton can be clearly divided into two mutually exclusive guilds: the autotrophic phytoplankton and the heterotrophic zooplankton. According to this view, phytoplankton are responsible for all photosynthetic carbon fixation, ultimately controlled by the supply and consumption of inorganic nutrients.There is clear evidence that such a strict dichotomy between producers and consumers does not reflect the true nature of marine microbial communities. Autotrophic and heterotrophic traits are not mutually exclusive, and a large and increasing number of plankton taxa have been shown to simultaneously exploit both inorganic resources and living prey (3). These mixotrophic plankton, found throughout the eukaryotic tree of life (4), and particularly in the 2-to 200-μm size range (5-7), can sustain photosynthesis even when chronically outcompeted for the most-limiting inorganic nutrient, in clear contrast to the way we typically describe and model marine systems (8).Although mixotrophy is known to be common throughout the global ocean (6, 7), its contribution to net community production is difficult to quantify, and its integrated impact on global biogeochemical cycles remains unknown. Numerical simulations provide a platform to address these questions, but to date, no global ocean models have resolved this important lifestyle. Here, we examine the global role of mixotrophy in a numerical "thought experiment," comparing two simulations of the marine plankton food web in the global ocean (9) that differ only in their representation of trophic strategy (Fig. 1). The traditional "two-guild" model encapsulates the default view of the marine ecosystem, with each of the 10 simulated size classes divided into separate phytoplankton and zooplankton populations. In the alternative "mixotrophy" model, this unrealistically strict distinction is not made, and each size class contains just one population that is capable of both inorganic resource uptake and predation, dependent ...

Modelling the plankton groups of the deep, peri-alpine Lake Bourget

“…Incorporation of mixotrophy is another novel aspect of the current study, given that mixotrophy has been, with exceptions (e.g., Ward and Follows, 2016), neglected in ecosystem scale model applications. Here, the description of mixotrophy is quite simplistic, relying on the assumption that there exists a linear trade-o between autotrophic and heterotrophic abilities (Crane and Grover, 2010), and the assumption that the parameters of heterotrophic and autotrophic traits re ect the conditions that enforced pure heterotrophy or autotrophy in the meta-analysis data that formed the basis for parameterization in this study.…”

“…Mixotrophy has been addressed mainly by theoretical work so far (e.g., Thingstad et al, 1997;Flynn and Mitra, 2009;Crane and Grover, 2010;Berge et al, 2017). The recent work of Ward and Follows (2016) constitutes the rst example where mixotrophy is resolved in a global ocean model.…”

Bridging the Gap between Knowing and Modeling Viruses in Marine Systems—An Upcoming Frontier

“…Yet, they don't compromise the knowledge on bacterial population control exerted by viral-induced mortality. Other recent studies, however, are questioning the paradigm where bacteria are central in the mechanisms for nutrient recycling, by pointing instead to the importance of mixotrophic organisms (Berge et al, 2016;Caron, 2016;Ward and Follows, 2016), although the question on the importance mixotrophs has previously been raised (Hall et al, 1993;Arenovski et al, 1995;Fenchel, 2008). According to this new paradigm, communities of mixotrophic protist plankton support the bulk of the base of the microbial food webs, having some fundamental differences in the flow of energy and nutrients from the bacteria-dominated microbial food web paradigm (Mitra et al, 2014).…”

“…Mixotrophy is of particular interest given that mixotrophic organisms also have a significant impact on bacterial populations. Despite being known as important player in the microbial food webs, only recently mixotrophs have received attention in modeling studies (Ward et al, 2011;Mitra et al, 2014;Berge et al, 2016;Ward and Follows, 2016). The inclusion of these "perfect beats" combining several modes of nutrition requires additional inclusion of complexity into models, as shown by Flynn and Mitra (2009); stoichiometric implication must be considered by the model, by which the C-to-nutrient ratios must be explicitly expressed for the mixotrophs and food source, otherwise the model is doomed to fail to reflect the reality of the trophic interactions, both at the mixotrophs level as on the ecosystem level.…”

EcoGEnIE 0.1: Plankton Ecology in the cGENIE Earth system model

“…In future we expect to bring in a wider range of trait-based functional types, including siliceous plankton (e.g. Follows et al, 2007), calcifiers (Monteiro et al, 2016), nitrogen fixers (Monteiro et al, 2010), and mixotrophs (Ward and Follows, 2016 …”