A Quantitative Assessment of the Role of the Parasite Amoebophrya in the Termination of Alexandrium fundyense Blooms within a Small Coastal Embayment

Abstract

Parasitic dinoflagellates of the genus Amoebophrya infect free-living dinoflagellates, some of which can cause harmful algal blooms (HABs). High prevalence of Amoebophrya spp. has been linked to the decline of some HABs in marine systems. The objective of this study was to evaluate the impact of Amoebophrya spp. on the dynamics of dinoflagellate blooms in Salt Pond (MA, USA), particularly the harmful species Alexandrium fundyense. The abundance of Amoebophrya life stages was estimated 3–7 days per week through the full duration of an annual A. fundyense bloom using fluorescence in situ hybridization coupled with tyramide signal amplification (FISH- TSA). More than 20 potential hosts were recorded including Dinophysis spp., Protoperidinium spp. and Gonyaulax spp., but the only dinoflagellate cells infected by Amoebophrya spp. during the sampling period were A. fundyense. Maximum A. fundyense concentration co-occurred with an increase of infected hosts, followed by a massive release of Amoebophrya dinospores in the water column. On average, Amoebophrya spp. infected and killed ∼30% of the A. fundyense population per day in the end phase of the bloom. The decline of the host A. fundyense population coincided with a dramatic life-cycle transition from vegetative division to sexual fusion. This transition occurred after maximum infected host concentrations and before peak infection percentages were observed, suggesting that most A. fundyense escaped parasite infection through sexual fusion. The results of this work highlight the importance of high frequency sampling of both parasite and host populations to accurately assess the impact of parasites on natural plankton assemblages.

Zooplankton community grazing impact on a toxic bloom of Alexandrium fundyense in the Nauset Marsh System, Cape Cod, Massachusetts, USA

“…Observations of A. fundyense abundances and development of the spring 2012 toxic bloom in the Nauset Marsh System were generally consistent with three other concurrent studies in the NMS (Velo-Suárez et al, 2013; Ralston et al, 2014; Brosnahan et al, submitted). Ralston et al (2014) correlated the anomalously early onset of the A. fundyense bloom in the NMS with unusually warm winter and spring temperatures.…”

“…Concurrent with this study, Velo-Suárez et al (2013) examined the role of Amoebophrya infection as a loss factor for A. fundyense populations in Salt Pond and found that, while infection killed < 1% d −1 in the early bloom phases (until 17 April 2012), at the end phase of the bloom Amoebophrya infected and killed ~30% of the A. fundyense population per day. Maximum A. fundyense mortality due to Amoebophrya infection occurred on 24 April 2012, which coincided with the only incubation experiment in this study that resulted in significant losses between Initial and Incubated A. fundyense abundances (Table 1; Fig.…”

“…For each experiment 15 l of water were collected from 5 m depth with three casts of a 5-l Niskin bottle. Samples were collected from 5 m depth because the maximum concentration of A. fundyense cells in the NMS tends to reside in that depth stratum due to the diel vertical migration behavior of A. fundyense in this system (Anderson and Stolzenbach, 1985; Crespo et al, 2011; Velo-Suárez et al, 2013). The three casts were combined in a 20-l carboy, and in order to keep the sample as close as possible to ambient pond temperatures, during the return to shore the carboy was placed in a cooler and submerged in a jacket of water collected at the station with a bucket.…”

Temperature and Residence Time Controls on an Estuarine Harmful Algal Bloom: Modeling Hydrodynamics and Alexandrium fundyense in Nauset Estuary

“…Instead of depending on water temperature, the decline tended to occur at a consistent phase of the bloom that could be described by a degree-day calculation (Ralston et al, 2014). The mechanisms behind the bloom decline in Nauset remain unresolved, as it may represent loss due to encystment, parasitism by Amoebophrya (Velo-Suárez et al, 2013), or some other process. In the results presented here, the mortality rate increased from 0 to the maximum value over degree days 500 to 550.…”

Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics

“…Approximately 75-80% of the toxic eukaryotic phytoplankton species are dinoflagellates, and they cause shellfish poisoning and harmful algal blooms of global importance. Symbiotic genera like Symbiodinium participate in interactions with metazoans and are essential for the formation of reef ecosystems, and parasitic forms play a central role in the collapse of harmful algal blooms, including those caused by dinoflagellates themselves (3). Dinoflagellates synthesize important secondary metabolites including sterols, polyketides, toxins, and dimethylsulfide, and several of them have evolved bioluminescence.…”