Temperature dependence of parasitoid infection and abundance of a diatom revealed by automated imaging and classification

Abstract

Diatoms are a group of phytoplankton that contribute disproportionately to global primary production. Traditional paradigms that suggest diatoms are consumed primarily by larger zooplankton are challenged by sporadic parasitic "epidemics" within diatom populations. However, our understanding of diatom parasitism is limited by difficulties in quantifying these interactions. Here, we observe the dynamics of Cryothecomonas aestivalis (a protist) infection of an important diatom on the Northeast U.S. Shelf (NES), Guinardia delicatula, with a combination of automated imaging-in-flow cytometry and a convolutional neural network image classifier. Application of the classifier to >1 billion images from a nearshore time series and >20 survey cruises across the broader NES reveals the spatiotemporal gradients and temperature dependence of G. delicatula abundance and infection dynamics. Suppression of parasitoid infection at temperatures <4 °C drives annual cycles in both G. delicatula infection and abundance, with an annual maximum in infection observed in the fall-winter preceding an annual maximum in host abundance in the winter-spring. This annual cycle likely varies spatially across the NES in response to variable annual cycles in water temperature. We show that infection remains suppressed for ~2 mo following cold periods, possibly due to temperature-induced local extinctions of the C. aestivalis strain(s) that infect G. delicatula. These findings have implications for predicting impacts of a warming NES surface ocean on G. delicatula abundance and infection dynamics and demonstrate the potential of automated plankton imaging and classification to quantify phytoplankton parasitism in nature across unprecedented spatiotemporal scales.