Harmful algal blooms of Heterosigma akashiwo and environmental features regulate Mesodinium cf. rubrum abundance in eutrophic conditions

Abstract

Functional drivers of phytoplankton that can potentially form harmful algal blooms (HABs) are important to understand given the increased prevalence of anthropogenic modification and pressure on coastal habitats. However, teasing these drivers apart from other influences is problematic in natural systems, while laboratory assessments often fail to replicate relevant natural conditions. One such potential bloom-forming species complex highlighted globally is Mesodinium cf. rubrum, a planktonic ciliate. This species occurs persistently in the Sundays Estuary in South Africa yet has never been observed to “bloom” (> 1,000 cell.ml ⁻¹). Modified by artificial nutrient-rich baseflow conditions, the Sundays Estuary provides a unique Southern Hemisphere case study to identify the autecological drivers of this ciliate due to artificial seasonally “controlled” abiotic environmental conditions. This study utilised a three-year monitoring dataset (899 samples) to assess the drivers of M. cf. rubrum using a generalised modelling approach. Key abiotic variables that influenced population abundance were season and salinity, with M. cf. rubrum populations peaking in summer and spring and preferring polyhaline salinity regions (>18) with pronounced water column salinity stratification, especially in warmer months. This was reflected in the diel vertical migration (DVM) behaviour of this species, demonstrating its ability to utilise the optimal daylight photosynthetic surface conditions and high-nutrient bottom waters at night. The only phytoplankton groups clearly associated with M. cf. rubrum were Raphidophyceae and Cryptophyceae. Although M. cf. rubrum reflects a niche overlap with the dominant HAB-forming phytoplankton in the estuary (the raphidophyte, Heterosigma akashiwo), its reduced competitive abilities restrict its abundance. In contrast, the mixotrophic foraging behaviour of M. cf. rubrum exerts a top-down control on cryptophyte prey abundance, yet, the limited availability of these prey resources (mean < 300 cells ml ⁻¹) seemingly inhibits the formation of red-water accumulations. Hydrodynamic variability is necessary to ensure that no single phytoplankton HAB-forming taxa outcompetes the rest. These results confirm aspects of the autecology of M. cf. rubrum related to salinity associations and DVM behaviour and contribute to a global understanding of managing HABs in estuaries.

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