Formation of harmful algal blooms cannot be explained by allelopathic interactions

Abstract

Many planktonic microalgae produce a range of toxins and may form harmful algal blooms. One hypothesis is that some toxins are allelopathic, suppressing the growth of competitors, and it has been suggested that allelopathy may be one important mechanism causing algal blooms. In a metaanalysis of recent experimental work, we looked for evidence that allelopathy may explain the initiation of algal blooms. With few exceptions, allelopathic effects were only significant at very high cell densities typical of blooms. We conclude that there is no experimental support for allelopathy at prebloom densities, throwing doubts on allelopathy as a mechanism in bloom formation. Most studies tested allelopathy using cell-free manipulations. With simple models we show that cell-free manipulations may underestimate allelopathy at low cell densities if effects are transmitted during cell-cell interactions. However, we suggest that the evolution of allelopathy under field conditions may be unlikely even if based on cell-cell interactions. The spatial dispersion of cells in turbulent flow will make it difficult for an allelopathic cell to receive an exclusive benefit, and a dispersion model shows that dividing cells are rapidly separated constraining clone selection. Instead, we propose that reported allelopathic effects may be nonadaptive side effects of predator-prey or casual parasitic cell-cell interactions.cell-cell interactions ͉ chemical ecology ͉ evolution ͉ hydrodynamics T here is a growing awareness that harmful blooms of cyanobacteria and planktonic protists, known as harmful algal blooms (HABs), have increased globally with serious implications for human health and economy (1). The severe socioeconomic impacts of HABs call for a better understanding of the factors and mechanisms causing blooms. Harmful effects by HAB species are largely mediated through the production of highly toxic compounds (1). The adaptive significance is still unclear, but it has been suggested that toxins confer some advantage that allows HAB species to reach the very high cell densities characterizing plankton blooms (2). One possible mechanism is that toxic compounds defend a plankter against pathogens, parasites, or predators. This mechanism is supported by recent work showing that toxin-producing species can be less preferred by predators, and that a predator presence may induce toxin production (3). A second mechanism is that the active release of toxins may inhibit the growth or survival of competing species. Such chemically mediated interference competition is known as allelopathy and is common among terrestrial plants (4-5). Many laboratory experiments have also revealed allelopathic effects for limnic and marine plankton (see Results), although most studies suggest that allelopathic effects are caused by compounds other than known toxins characterizing HAB species (6-8). It has been proposed that allelopathy might explain a competitive advantage among planktonic cyanobacteria and protists and the initiation and/or continuation of plankto...

Distinctly different behavioral responses of a copepod, Temora longicornis , to different strains of toxic dinoflagellates, Alexandrium spp.

“…Algal blooms occur when algal growth exceeds zooplankton grazing. Thus, harmful algal blooms are thought to be facilitated by reduced grazing due to the algae producing toxic substances (Jonsson et al, 2009) that, in turn, are believed mainly to function as grazer deterrents. Reported grazer responses to harmful algae are diverse.…”

The effect of costs associated with toxin production in a competitive system

“…Sole et al [36] modified the allelopathic interaction term and proved that the role of allelopathy appears to be important only for high concentrations of the toxic algae. Recently, using simple models, Jonsson et al [19] supported the previous observation and confirmed that allelopathic (hereafter called a toxin) effect does not play any role to the initiation of algal blooms.…”

“…We have allocated a cost for producing toxic chemicals and toxin concentrations by separate equations. We have assumed that allelopathic effects become significantly important when the amount of toxin present in the system becomes very high (it has been reported by Sole et al [36]; Jonsson [19]). For numerical simulations, parameter values are taken from various literature sources.…”

“…Recent studies have revealed that allelopathic interactions among plankton become important only at the high cell concentrations typical for well-developed plankton blooms [12,19,33,36]. In 2005, Sole et al, modelled allelopathic effects among marine microalgae and quantified the importance of this interaction using experimental data.…”

Bioactive compounds of marine dinoflagellate isolates from western Greenland and their phylogenetic association within the genus Alexandrium

“…Smayda, 1997;Cembella, 2003;Tillmann, 2004;Jonsson et al, 2009), particularly for known toxigenic species. Among Alexandrium species, interspecific competition and antipredation defense mechanisms are most frequently invoked.…”