Prey morphotype and abundance controls plastid retention and bloom dynamics for a mixotrophic dinoflagellate

Dinophysis is an obligate mixotroph that relies on consumption of the ciliate, Mesodinium rubrum, to grow and form harmful algal blooms (HABs). In this study, blooms of Dinophysis acuminata in two NY, USA, estuaries were studied over the course of 3 yr (2019–2021) using discrete samples and an Imaging FlowCytobot (IFCB) to capture images of plankton 20–150 μm. The darkness of Dinophysis images on the IFCB was used to quantify the “fullness” or feeding state of Dinophysis cells. Culture experiments performed to ground truth this approach revealed a highly significant correlation (R = 0.98; p < 0.001) between the darkness of Dinophysis cells and the abundance of Mesodinium. With a quantitative scale developed to track the fullness of Dinophysis cells, ecosystem observations revealed the percentage of “full” Dinophysis cells increased during blooms of a large-morphotype Mesodinium that preceded the initiation of Dinophysis blooms. A smaller morphotype Mesodinium appeared during Dinophysis bloom peaks suggesting they supported bloom maintenance. While the relative abundance of diatoms was elevated before Dinophysis blooms, other dinoflagellates and tintinnids increased in abundance during these HABs indicating they emerged within a consortium of heterotrophs and mixotrophs that may have collectively filled the same open niche as Dinophysis. This study reveals the manner in which different Mesodinium populations co-bloom with Dinophysis to support plastid acquisition, bloom initiation, and bloom maintenance and contextualizes these changes within the larger plankton community succession associated with these HABs.