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.2016 Mar 15;113(11):2958-63.
doi: 10.1073/pnas.1517118113. Epub 2016 Feb 1.

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

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

Ben A Ward et al. Proc Natl Acad Sci U S A..

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.

Keywords: biological pump; mixotrophy; plankton; size; trophic transfer.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Emergent global mean community structure in the two-guild (A) and mixotrophy (B) models. Circular nodes represent global carbon biomass (surface area proportional to the annual mean), and black links represent global carbon fluxes (thickness proportional to the square root of the annual mean, with all fluxes directed upwards). The horizontal position of the nodes denotes plankton size, whereas the vertical position denotes trophic level (T). For each population,T is calculated as 1 plus the average trophic level of each prey item, weighted by the contribution of each prey to the total carbon intake, including photosynthesis (T is calculated sequentially from small to large;Methods). Colors represent the balance of autotrophic and heterotrophic carbon assimilation in each population (Inset, color scale). (C) Representation of the total annual carbon flux across each trophic level in the two-guild (blue) and mixotrophy (red) models. The fluxes were calculated for each value ofT by summing all fluxes beginning at a lower level and ending at a higher level. Solid lines represent the total flux, whereas dotted lines represent only the photosynthetic flux.
Fig. S1.
Fig. S1.
Observed and modeled global annual mean distributions of surface chlorophylla (0–10 m), depth-integrated primary productivity (48), and geometric mean plankton size.
Fig. S2.
Fig. S2.
Observed (49, 50) and modeled global annual mean surface (0–10 m) nutrient distributions.
Fig. S3.
Fig. S3.
Observed and modeled seasonal cycles of surface chlorophylla and nutrients. Gray dots correspond to all observations, regardless of year. Each line represents one of an additional 5 y of model integration (years 11–15), with the two-guild model in blue and the mixotrophy model in red. Chlorophyll, nitrate, and phosphate observations correspond to the exact time-series locations (51). Dissolved iron data within the surface 50 m were taken from a global database (50), with observations matched to time-series sites if they fall within 2° latitude and longitude.
Fig. 2.
Fig. 2.
(A) Total annual mean size distribution of carbon biomass in the two-guild (blue) and mixotrophy (red) models. (B) Global size-fractionated annual mean chlorophylla biomass and annual primary production from the two-guild (blue) and mixotrophy (red) models in comparison with empirical estimates (black). Empirical estimates were derived from a synthesis of in situ and satellite observations (17, 18).
Fig. 3.
Fig. 3.
(A–D andF–I) Depth-integrated balance of autotrophic and heterotrophic acquisition of C, N, P, and Fe by nanoplankton in the two-guild (A–D) and mixotrophy (F–I) models. Black dots inG–I indicate sites where in situ nutrient addition experiments have identified (at least occasional) limitation by that nutrient element (30). (E) Global balance of depth-integrated nanophytoplankton and nanozooplankton C biomass in the two-guild model. (J) Relative change between the two models in the molar ratio of photosynthetic C acquisition to the uptake of the most-limiting nutrient (N, P, or Fe;Supporting Information).
Fig. 4.
Fig. 4.
Modeled and observed large-scale variation in C:P ratios of particulate organic matter. Blue and red lines show regional C:P in the surface 100 m, with error bars showing ±1 SD. Observed particulate C:P ratios from ref. are shown, with boxes marking the 25th, 50th, and 75th percentiles and whiskers covering ∼99.3% of the data. The remaining points are represented by plus symbols. Observations in regions with<10 data points are plotted individually (dots). Inverse model estimates of exported C:P ratios are also shown by black lines (24), with error bars again showing ±1 SD. The global mean “Redfield” (31) C:P ratio of 106 is shown by a horizontal dashed line.
Fig. S4.
Fig. S4.
Limitation terms in the mixotroph model. Annual mean community light limitation within the mixed layer and annual mean community N, P, and Fe limitation in the surface (0–10 m) layer (fromγI,γN,γP, andγFe in Eqs.S14,S6, andS7). Community means are biomass-weighted. Black circles indicate sites where in situ nutrient addition experiments have identified (at least occasional) limitation by the nutrient element in question (30).
Fig. 5.
Fig. 5.
Relationship between mixotrophic dominance and the relative increase in global carbon export (A) and global geometric mean plankton size (B) in the sensitivity experiments (Supporting Information), relative to the two-guild model. Dots represent the global average from each simulation, whereas the error bars show the degree of spatial variability in the annual average for each simulation. In the legend, the parameterτ describes the strength of the tradeoff (a larger number represents a stronger penalty for mixotrophy). This penalty may be applied to the resource affinities and the maximum resource uptake rates (affinity and saturation) or just to the maximum resource uptake rates (saturation) (Supporting Information and ref. 32). The relative uptake functions for the mixotrophs in each experiment are illustrated schematically inB (Inset). With no tradeoff, the mixotrophs have identical uptake functions to the specialists (black line).
Fig. S5.
Fig. S5.
Size dependence ofPCmax. Black dots represent data from ref. , and gray dots indicate the model size classes. The equation for the curve is given in Eq.S19.
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References

    1. Hollowed AB, et al. Projected impacts of climate change on marine fish and fisheries. ICES J Mar Sci. 2013;70(5):1023–1037.
    1. Hain MP, Sigman DM, Haug GH. The Biological Pump in the Past. Treatise on Geochemistry. 2nd Ed. Elsevier; Oxford: 2014. pp. 485–517.
    1. Stoecker DK. Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur J Protistol. 1998;34(3):281–290.
    1. Stoecker DK. Acquired phototrophy in aquatic protists. Aquat Microb Ecol. 2009;57(3):279–310.
    1. Zubkov MV, Tarran GA. High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature. 2008;455(7210):224–226. - PubMed

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