Biological control of toxic cyanobacteria by mixotrophic predators: an experimental test of intraguild predation theory

Abstract

Intraguild predators both feed on and compete with their intraguild prey. In theory, intraguild predators can therefore be very effective as biological control agents of intraguild prey species, especially in productive environments. We investigated this hypothesis using the mixotrophic chrysophyte Ochromonas as intraguild predator and the harmful cyanobacterium Microcystis aeruginosa as its prey. Ochromonas can grow photoautotrophically, but can also graze efficiently on Microcystis. Hence, it competes with its prey for inorganic resources. We developed a mathematical model and parameterized it for our experimental food web. The model predicts dominance of Microcystis at low nutrient loads, coexistence of both species at intermediate nutrient loads, and dominance of Ochromonas but a strong decrease of Microcystis at high nutrient loads. We tested these theoretical predictions in chemostat experiments supplied with three different nitrogen concentrations. Ochromonas initially suppressed the Microcystis abundance by >97% compared to the Microcystis monocultures. Thereafter, however, Microcystis gradually recovered to ∼20% of its monoculture abundance at low nitrogen loads, but to 50–60% at high nitrogen loads. Hence, Ochromonas largely lost control over the Microcystis population at high nitrogen loads. We explored several mechanisms that might explain this deviation from theoretical predictions, and found that intraspecific interference at high Ochromonas densities reduced their grazing rates on Microcystis. These results illustrate the potential of intraguild predation to control pest species, but also show that the effectiveness of their biological control can be reduced in productive environments.

Intraguild predation enables coexistence of competing phytoplankton in a well‐mixed water column

“…Consistent with other forms of intraguild predation Polis 1997, Mylius et al 2001), mixotrophy permits the persistence of a weaker competitor for light that would otherwise be competitively excluded (Huisman and Weissing 1994). This is in keeping with other theoretical results that predict mixotroph dominance in high-resource environments (Wilken et al 2014a, Ptacnik et al 2016) such as eutrophic freshwater, estuarine, and coastal marine ecosystems. However, coexistence is not guaranteed: If the mixotroph has a high attack rate or conversion efficiency, or if surface light intensity is high, the mixotroph can exclude the phototroph.…”

The functional role of planktonic mixotrophs in altering seston stoichiometry

“…Several studies have investigated concentrations of particular nutrients in mixotrophic flagellates, but most of them focused more on the effect of light, temperature and dissolved nutrient conditions on phagotrophic feeding and its contribution to C and nutrient budgets (Caron et al 1993, Li et al 2000, Skovgaard et al 2000, Smalley et al 2003, Carvalho & Granéli 2010, Simonds et al 2010, Brutemark & Granéli 2011, Wilken et al 2014, Johnson 2015 or on the relationship of internal nutrient concentrations and toxin production in different harmful dinoflagel-lates (Johnsen et al 1999, John & Flynn 2000, Van de Waal et al 2013, Pérez Blanco et al 2015. We are aware of only 2 empirical studies that have specifically addressed the balance of intracellular nutrients in particular mixotrophs and its dependence on environmental factors and potential differences in their nutrient stoichiometry compared to purely phototrophic or heterotrophic organisms.…”

How to evaluate the potential occurrence of intraguild predation

“…This can only be evaluated in replicated, long-term population experiments and invasion experiments, of which there are not many around (Morin 1999; Diehl and Feissel 2000; Montserrat et al 2008, 2012; Hiltunen et al 2013; Wilken et al 2014). These experiments serve to discriminate between IGP, classical competition and predation (Table 1).…”

“…The importance and consequences of IGP for species coexistence ultimately need to be assessed in population-dynamical experiments or invasion experiments at various productivity levels (e.g. Morin 1999; Diehl and Feissel 2000, 2001; Montserrat et al 2008; Wilken et al 2014). Moreover, the effects of age or stage structure on the success of invasion of one species into a population of the other species should be studied experimentally (Montserrat et al 2012).…”