Diatom defence: Grazer induction and cost of shell-thickening

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.

1. 硅藻（diatoms）约占海洋初级生产力的40%，在海洋固碳过程中发挥关键作用。硅藻的演化成功及其在海洋生物地球化学中的核心功能，与其具有部分抗牧食保护作用的硅质外壳密切相关。
2. 浮游植物（phytoplankton）群落的结构与功能受环境限制与生物权衡机制调控。防御机制或可解释海洋中浮游植物（包括硅藻）的高度多样性，但前提是防御行为需付出相应代价。然而，在海洋浮游植物中，防御代价的证实与量化一直是公认的难题。
3. 本研究针对7种浮游硅藻展开实验，证实当硅藻细胞暴露于桡足类（copepods，硅藻的重要捕食者）释放的化学信号时，其硅质外壳会增厚，生长速率随之下降。上述响应随牧食者信号浓度升高而增强，但在不同物种及同一物种不同个体间均存在显著差异。
4. 在本研究的标准实验条件下，硅藻的生长速率平均下降10%，细胞内生源硅（biogenic silica）含量平均提升16%。后者对应小型桡足类导致的牧食死亡率降低11%。由此可见，针对牧食者的硅化响应完全具有生态学合理性。
5. 硅化作用的代价与收益规模相近，表明在竞争-防御轴上存在平坦的适合度景观（fitness landscape）。这一发现或可解释海洋中共存硅藻的高度多样性。
6. 硅藻对海洋有机碳向下通量的贡献显著但存在差异，这在很大程度上取决于细胞的硅质含量。这一现象并非源于硅的球化效应，而主要与不同防御程度的细胞具有各异的生活史有关——这些生活史由演化适应以及本研究证实的、针对牧食者的表型可塑性响应（plastic responses）共同调控。