Defense mechanisms in phytoplankton: traits and trade–offs

Abstract

In aquatic ecosystems, phytoplankton form the base of the food webs. They generate nearly half of the global primary productivity and consequently play a vital role in regulating Earth’s climate via carbon cycling. In addition, phytoplankton community composition impacts the biogeochemical cycles of inorganic elements since different functional groups of phytoplankton have different requirements and acquisition modes for nutrients. Therefore, since phytoplankton community composition impacts the global climate and the functioning of aquatic ecosystems, it is important to understand what mechanisms in turn determine the community composition. Evidently, one such mechanism is predation and the subsequent employment of defensive strategies, which promotes coexistence and species diversity. However, the promotion of species diversity requires trade–offs. This implies that the advantage of a defense mechanism must come at a cost, otherwise all species would evolve towards a state of equal defense and the community composition would no longer be promoted by predation. Based on the available evidence, it appears that the function of many proposed defensive traits in phytoplankton remains unclear and the trade–offs undocumented or unquantified. In many cases, experimental evidence even suggests that defenses are costless. Here, we propose that some costs may materialize only under natural conditions, while other may become evident under resource–deficient conditions when a rivalry for limiting resources between growth and defense occurs. For that reason, a mechanistic understanding of the hypothesized component processes is required for evaluation of costs that are realized under natural conditions, while the magnitude of the costs must be assessed under conditions of resource limitation. As stated above, the role of many proposed defenses remains elusive including the protective role of silicified cell walls in diatoms. While it seems intuitive that the siliceous wall may have evolved as a mechanical protection against grazing, many other roles of a siliceous shell have been proposed and direct evidence of defense is limited. In addition, the anticipated benefits must be traded off against the costs; since deposition of silica in diatoms is determined by their growth rates, this dependency can be regarded as one of the costs of silicification. We experimentally demonstrate the protective role of silicified cell walls against adult copepods and nauplii, with near inversely proportional relationship between predation risk and silica wall thickness. On the other hand, our empirical data reveal that the increased cell wall thickness is inconsequential to protozoan grazers that engulf their prey. Additionally, we demonstrate that the deposition of silica in diatoms decreases with increasing growth rates, suggesting a possible cost to silicification. Overall, it appears that the silica wall is an efficient defense mechanism against copepods, implying that the plasticity of silicification in diatoms has likely evolved as a response to copepod grazing whose specialized tools to break open silicified walls have co–evolved with their prey. Another common trait observed in phytoplankton is the production of chemical compounds, yet often the evolution and the function of such compounds remain unclear. Often, a defensive role of toxin production is anticipated, and this interpretation is supported by observations of increased toxin synthesis in the presence of grazers, which in some cases leads to reduced predation mortality. On the other hand, experiments have consistently failed to observe any costs of toxin production, but a mechanistic understanding of the underlying processes may allow their quantification — i.e. that the production of nitrogen–rich compounds likely depends on ambient nitrogen levels. We demonstrate with a simple fitness optimization model that the cost of toxin production is indeed negligible when nitrogen and light are plentiful. However, when nitrogen or light is limiting cell growth and when grazers are abundant, the model predicts substantial costs that lead to a significant reduction in cell division rates. Our results indicate that the investment in toxin production pays–off since defended cells experience reduced grazing mortality, which consequently leads to the net growth rates that are twice as high as of undefended cells. In this PhD work, I provided an overview of defense mechanisms in phytoplankton and associated trade–offs. In search for defense trade–offs, I identified which traits lack experimental evidence supporting their defensive function (e.g. silicified cell walls), and proposed ways to assess the costs in future experimental or theoretical studies (e.g. toxin production).