Evolutionary tradeoffs among nutrient acquisition, cell size, and grazing defense in marine phytoplankton promote ecosystem stability

Abstract

To survive, an algal species must maximize its reproduction rate via efficient nutrient acquisition and assimilation while minimizing rates of mortality from grazing or other sources. In a survey of 11 well studied marine algal species (including 3 racial variants of a single species, Emiliania huxleyi) in ammonium-limited cyclostat cultures, we observed variations in ammonium uptake rates and associated growth rates, which were linked to cell size and, apparently, also to grazing defense. The 5 largest species (10-12 µm cell diameter) had similar low ammonium uptake rates and associated ammonium-limited growth rates owing to diffusion limitation of uptake. Diffusive flux per unit of cell volume decreases with the inverse square of the cell diameter; hence, cells can minimize diffusion limitation and increase nutrient uptake by becoming smaller. However, this comes at the cost of higher susceptibility to grazing mortality. The 7 smallest isolates (2.7-4.6 µm diameter) had higher rates of ammonium uptake and growth as predicted from theory, but there was considerable variation for similarly sized cells. All 4 of the small algal species or isolates that are known to be poorly grazed or poorly assimilated by grazers had unusually low ammonium uptake rates and associated growth rates for their size, which we hypothesize to be due to the high cost of grazing defense. The results suggest the existence of evolutionary tradeoffs between large cell size and grazing defenses (which decrease grazing mortality) and small size and minimal defenses (which promote growth and reproduction). Such tradeoffs could increase the species diversity of algal communities, which in turn promotes ecosystem stability.KEY WORDS: Ammonium · Phytoplankton · Nitrogen uptake · Growth rate · Grazing defense · Cell size · Evolutionary tradeoffs Resale or republication not permitted without written consent of the publisher

Isometric size-scaling of metabolic rate and the size abundance distribution of phytoplankton

“…Other processes such as size-differential grazing pressure by zooplankton [58] may affect the regular patterns in size abundance distribution of marine phytoplankton, by controlling phytoplankton abundances along the size spectrum and preventing the development of blooms of certain phytoplankton size groups. However, in marine ecosystems near to steady-state, grazing pressure is higher on small phytoplankton and the losses of smaller cells may be compensated by the higher sedimentation rates experienced by larger cells [11,46,59], resulting in a broad cell size-independence of loss processes. Furthermore, it has been hypothesized that resource competition between phytoplankton species of different size should lead to the dominance of phytoplankton community by the single size that requires the lowest resource concentration to grow [47,48].…”

“…Therefore, we hypothesize that other physiological and/or ecological strategies in addition to those proposed for respiratory rates in unicellular protists must be invoked to explain the isometric scaling relationship between phytoplankton carbon fixation rate and cell size. Microalgal species must maximize their resource acquisition and assimilation rates while minimizing loss rates in order to survive in aquatic pelagic ecosystems [46]. Thus, the size-scaling relationships in phytoplankton might have evolved, in part, as a consequence of adaptation processes that involved the acquisition of taxa-specific physiological strategies by species in certain size classes [47].…”

Increased cellular brevetoxins in the red tide dinoflagellate Karenia brevis under CO2 limitation of growth rate: Evolutionary implications and potential effects on bloom toxicity

“…Strains of the Center for Culture of Marine Phytoplankton (CCMP) 2228 and 2229 were obtained from the Provasoli-Guillard National Center for Marine Algae and Microbiota (East Boothbay Harbor, Maine Sunda et al 2005). It also contained 128 mmol L 21 NaNO 3 and 8 mmol L 21 NaH 2 PO 4 to generate a Redfield N : P of 16 : 1.…”

“…Cell concentrations, mean volume per cell, cell Chl a, cell C and N, and brevetoxins were measured for each sampling period as described below. Specific growth rates were determined from time-dependent changes in total cell volume (Sunda et al 2007).…”

Evolution of Nutrient Uptake Reveals a Trade‐Off in the Ecological Stoichiometry of Plant‐Herbivore Interactions

“…Although the grazing susceptibility of their species is not known, these results suggest that strong competitors would constitute more nutritious food for zooplankton and are likely to suffer more from grazing than weaker competitors. Sunda and Hardison (2010) reported considerable variation in the ammonium uptake rates of marine phytoplankton species. Four of their algal isolates are known to be poorly grazed by zooplankton, and only these four isolates had unusually low ammonium uptake rates and associated growth rates for their size.…”