Influence of the Calcium Carbonate Shell of Coccolithophores on Ingestion and Growth of a Dinoflagellate Predator

Abstract

Coccolithophores are an important group of ∼200 marine phytoplankton species which cover themselves with a calcium carbonate shell called “coccosphere.” Coccolithophores are ecologically and biogeochemically important but the reason why they calcify remains elusive. One key function may be that the coccosphere offers protection against microzooplankton predation, which is one of the main causes of phytoplankton death in the ocean. Here, we investigated the effect of the coccosphere on ingestion and growth of the heterotrophic dinoflagellate Oxyrrhis marina. Calcified and decalcified cells of the coccolithophore species Emiliania huxleyi, Pleurochrysis carterae, and Gephyrocapsa oceanica were offered separately to the predator as well as in an initial ∼1:1 mixture. The decrease of the prey concentrations and predator abundances were monitored over a period of 48–72 h. We found that O. marina did not actively select against calcified cells, but rather showed a size selective feeding behavior. Thus, the coccosphere does not provide a direct protection against grazing by O. marina. However, O. marina showed slower growth when calcified coccolithophores were fed. This could be due to reduced digestion rates of calcified cells and/or increased swimming efforts when ballasted with heavy calcium carbonate. Furthermore, we show that the coccosphere reduces the ingestion capacity simply by occupying much of the intracellular space of the predator. We speculate that the slower growth of the grazer when feeding on calcified cells is of limited benefit to the coccolithophore population because other co-occurring phytoplankton species within the community that do not invest energy in the formation of a calcite shell could also benefit from the reduced growth of the predators. Altogether, these new insights constitute a step forward in our understanding of the ecological relevance of calcification in coccolithophores.

Nutritional response of a coccolithophore to changing pH and temperature

“…Coccoliths can diminish the nutritional value of coccolithophores in three ways. First, through mechanical protection, making it more difficult for grazers to access the protoplast (Haunost et al 2021). Second, through the need to counteract the increase in the pH of guts or food vacuoles due to carbonate dissolution (Harvey et al 2015).…”

“…Second, through the need to counteract the increase in the pH of guts or food vacuoles due to carbonate dissolution (Harvey et al 2015). Third, through reduction in the percentage of digestible material (Haunost et al 2021). While the first point hinges on morphology, the last two points center on the amount of calcite relative to organic material.…”

“…5F). Copepods do not need to destroy the coccosphere as they have to in the case of the diatom frustule (Langer et al 2007; Jansen 2008); however, dinoflagellates need to penetrate the coccosphere to digest the cell contents, and then egest the remaining indigestible calcium carbonate (Haunost et al 2021). This means that if the interlocking between coccoliths is reduced, dinoflagellates may be able to more readily access coccolithophore cell contents, potentially aiding in digestion.…”

“…Therefore, macrograzers such as copepods will likely benefit from the higher percentage of digestible material, and less so from both the reduced structural integrity of the coccosphere and the potentially negligible gut pH change (Harris 1994; Nejstgaard et al 1997; Langer et al 2007 b ; White et al 2018; Mayers et al 2020). Micrograzers such as dinoflagellates will likely benefit from all three aspects of coccolith‐related nutritional value change (Harvey et al 2015; Jaya et al 2016; Haunost et al 2021).…”

Resilience of Emiliania huxleyi to future changes in subantarctic waters

“…There is uncertainty regarding the primary function of calcification in coccolithophores, with protection from grazing, viral attack and UV radiation all considered as benefits [75][76][77][78]. Regardless, the consistency in the changes in cell volume, carbonate content and calcification (see Fig 5) infers that the benefits of calcification may remain largely unchanged in future subantarctic waters.…”