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, Emilia- nia 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 asso- ciated 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.