Responsibility of microzooplankton and parasite pressure for the demise of toxic dinoflagellate blooms

Abstract

Two mechanisms proposed to control dinoflagellate blooms -parasitism by eukaryotes (e.g. Amoebophrya sp.) and grazing by microzooplankton -have been explored through previous laboratory and field studies but lack quantitative assessment. We modelled the relative effect of these mechanisms. We used literature values to embed an Anderson-May host-microparasite model into a microbial food web model (nano-and microphytoplankton, nano-and microzooplankton, a toxic dinoflagellate, a dinoflagellate parasite). Three scenarios were examined to simulate the introduction of a toxic dinoflagellate and its parasite into an environment: (1) a food web, including autotrophic nanoand microplankton, heterotrophic flagellates, and ciliates; (2) as for Case 1 but with a toxic dinoflagellate; (3) as for Case 2 but with a dinoparasite. This mimics observations in a French estuary, where a toxic dinoflagellate began blooming in 1988; since 1998, blooms appear to have become regulated, and numerous parasitic infections by Amoebophrya sp. occurred from 2004 to 2006. After supporting parasite control of dinoflagellate blooms, we assessed the effects of observed ranges of key variables associated with the parasite and other components of the food web on parasite control of the dinoflagellate population. Population dynamics were examined over 50 d. In Case 1, all taxa had 10 to 20 d blooms. In Case 2, the toxic dinoflagellate population dynamics mimicked that of the microphytoplankton, and this dinoflagellate was reduced in numbers but not extirpated by microzooplankton grazing. In Case 3 population blooms occurred, and the parasite virtually eliminated the dinoflagellate over ~10 d. Sensitivity analysis indicated that our assessment was robust. We propose that the decline in toxic dinoflagellates in the French estuary may have been due to an introduced dinoparasite. In general, we suggest that parasites may have greater impact on toxic dinoflagellate blooms than microzooplankton grazers; the parasites have the potential to eliminate the toxic dinoflagellates. We recommend that such parasites be incorporated into more complex food web models.

Distribution and host diversity of Amoebophryidae parasites across oligotrophic waters of the Mediterranean Sea

“…were found to infect up to 46% of dinoflagellate host cells, particularly the toxic species Alexandrium minutum . Models based on these results showed that the parasite was able to eliminate the host population over a 10 days period (Montagnes et al, 2008). Alternatively, other studies considered Amoebophrya parasitism as a minor factor causing host mortality.…”

Infection dynamics of Amoebophryidae parasitoids on harmful dinoflagellates in a southern Chilean fjord dominated by diatoms

“…Due to the strong vertical stratification usually observed in Reloncaví Fjord, correlations were established separately for each depth (n = 24) to minimize the interference of light and salinity related to the vertical variability of these variables. Similarly, because a time-delay is also expected to occur in hostparasitoid dynamics (Montagnes et al 2008, Salomon & Stolte 2010), short-term interactions be tween Prorocentrum micans and parasitoids be longing to the Amoebophryidae were evaluated by correlating depth-integrated P. micans abundances from each sampling with depth-integrated numbers of dinospores and infected P. micans observed on the previous sampling date (n = 24). Infected P. micans abundances were based on the prevalence estimated by FISH and the total P. micans enumerated in Lugol- …”

“…This was adjusted to 2.85 d considering the average ambient temperature (15°C) observed during this study and a Q 10 of 2 (Montagnes et al 2008).…”

“…Within a few hours, the vermiform stage fragments and releases hundreds of new infective dinospores (Coats & Bockstahler 1994, Coats & Park 2002, each potentially capable of infecting a novel host. Both field observations and model predictions indicate that these parasitoids have the capacity to efficiently control their dinoflagellate host populations (Cachon 1964, Coats et al 1996, Montagnes et al 2008, Salomon & Stolte 2010.…”

“…Calbet et al 2003, Montagnes et al 2008. It has recently been postulated that dinoflagellate blooms may also result from the absence of efficient pathogens in newly invaded areas (Salomon et al 2003), a theory known as the 'enemy release hypothesis' in terrestrial ecology (Keane & Crawley 2002).…”