Diatom defence: Grazer induction and cost of shell‐thickening

Abstract

Diatoms account for 40% of the ocean primary production and play a key role in the oceans’ ability to sequester carbon. The evolutionary success of diatoms and their role in ocean biogeochemistry are related to the siliceous shell that provide partial protection against grazing. The structure and function of phytoplankton communities are governed by environmental constraints and organismal trade‐offs. Defence mechanisms may help explain the high diversity of phytoplankton (incl. diatoms) in the ocean, but only if the defence comes at a cost. Defence costs have been notoriously difficult to demonstrate and quantify in marine phytoplankton. Here, we demonstrate for seven species of planktonic diatoms that their shell thickens and their growth rate declines when cells are exposed to chemical cues from copepods, important predators of diatoms. The responses are proportional to the concentration of grazer cues, but are also highly variable, both between and within species. At our standard experimental condition, the typical decline in growth rate is 10%, and the typical increase in cellular biogenic silica is 16%. The latter value corresponds to a decline in grazing mortality due to small copepods of 11%. Thus, silification in response to grazers is exactly warranted. The similar magnitude of the costs and benefits of silification suggests a flat fitness landscape along the competition‐defence axis. This may help explain the high diversity of coexisting diatoms in the ocean. The significant but variable contribution of diatoms to the downward flux of organic carbon in the ocean depends to a large extent on the silica content of the cells. This is due less to the ballasting effect of silica, but mainly to the different life histories of more or less defended cells that are governed by evolutionary adaptations and—as demonstrated here—plastic responses to grazers. A free Plain Language Summary can be found within the Supporting Information of this article.

Predator-induced defence in a dinoflagellate generates benefits without direct costs

“…It is reasonable to assume that the copepods respond to the concentration rather than the contents of toxins, and the shrinking of the cells may therefore be adaptive and part of the defence. A similar consistent response in cell size to grazer cues has been found in four species of diatoms [24].…”

“…According to optimal defence theory, inducible defences are favoured when predation risks vary in time and defence costs are significant [19,20]. While these costs have likely been reduced through evolution, the wide variety of inducible defences found in both marine and terrestrial organisms suggests the presence of influential trade-offs to any beneficial defensive trait [21][22][23][24].…”

Diatoms Versus Copepods: Could Frustule Traits Have a Role in Avoiding Predation?

“…Although cells of T. pseudonana exposed to copepods changed in morphology and elemental composition (Figures 1A,C and Supplementary Tables 1, 2, 4), these alterations were insufficient to counter the decrease of the predated populations. In diatoms, increasing Si content is a known strategy to rise mechanical strength and to reduce predation pressure (Pančić et al, 2019;Grønning and Kiørboe, 2020). However, a higher Si deposition corresponds to a higher cost of shell thickening (Friedrichs et al, 2013;Pančić et al, 2019;Grønning and Kiørboe, 2020) and thus, this extra cost may also have contributed to the lower growth rate shown in Figures 1A,D for T. pseudonana.…”

“…The morphological shift is still in progress and probably linked to a continuous balance between an effective response to different selective pressures including predation and the cost of shell thickening (Martin-Jezequel et al, 2000;Hildebrand et al, 2018;Grønning and Kiørboe, 2020). Phytoplankton has evolved multiple strategies to avoid predation (Pančić and Kiørboe, 2018;Lürling, 2020), those may involve not only morphological defences (e.g., colony formation, thick silica shell) but also behavioural defences (e.g., motility) or physiological defences (e.g., toxicity).…”

Ecology of Fear: Spines, Armor and Noxious Chemicals Deter Predators in Cancer and in Nature

“…Diatoms have frustules, silicified cell walls (Hamm et al, 2003), which allow them to survive passage through a predator's gut (Fowler and Fisher, 1983). Diatoms thicken their frustule walls in response to copepod grazing (Pondaven et al, 2007;Grønning and Kiørboe, 2020). Coccolithophore phytoplankton are named for their calcium carbonate plates, or coccoliths, which surround their cell walls (Figure 1D).…”