Trait trade-offs in phagotrophic microalgae: the mixoplankton conundrum

Analysis of trait trade-offs, through which physiological traits requiring common resources are ‘traded’ to optimize competitive advantage, provides a route to simplify and more readily understand the complexities of ecology. The concept of trait trade-offs has found favour in plankton research, especially directed at phytoplankton, defined here as phototrophs incapable of phagotrophy. Mixoplankton, defined as protists that combine phototrophy and phagotrophy, are now recognized as being widespread and significant members of the protist plankton community; many photoflagellate ‘phytoplankton’ are actually mixoplankton, as are many ‘(microbial) zooplankton’. Mixoplankton might be expected to be dominant, being able to exploit different trophic strategies while simultaneously eliminating competitors. That mixoplankton are not dominant suggests that physiological trait trade-offs erode their apparent competitive edge. We present a systematic analysis of potential trait trade-offs in phototrophic protists focused on mixoplankton. We find no clear evidence to support trait trade-off arguments in plankton research, except perhaps for acquired phototrophy in mixoplanktonic ciliates versus zooplanktonic ciliates. Our findings suggest that the presence of various mixoplankton throughout the surface ocean waters is most likely explained by factors other than trait trade-offs. Diversities in mixoplankton form and function thus reflect that evolution of these organisms from very different lineages, provide them with advantages to function competitively in mature ecosystems with complex trophic interplay. Indeed, the complexity of those lineages is inconsistent with core trait trade-off definitions; there is no single ancestral mixoplankton nor a common environment supporting trait-trade-off-directed evolution. HIGHLIGHTS ● Trait trade-offs do not explain the breadth of mixoplankton ecophysiological capabilities. ● Diversity of mixoplankton form and function reflects phylogenetic diversity. ● Only one potential trait trade-off was identified which was for ciliates that steal chloroplasts.