Among the thousands of unicellular phytoplankton species described in the sea, some frequently occurring and bloom-forming marine dinoflagellates are known to produce the potent neurotoxins causing paralytic shellfish poisoning. The natural function of these toxins is not clear, although they have been hypothesized to act as a chemical defence towards grazers. Here, we show that waterborne cues from the copepod Acartia tonsa induce paralytic shellfish toxin (PST) production in the harmful algal bloom-forming dinoflagellate Alexandrium minutum. Induced A. minutum contained up to 2.5 times more toxins than controls and was more resistant to further copepod grazing. Ingestion of non-toxic alternative prey was not affected by the presence of induced A. minutum. The ability of A. minutum to sense and respond to the presence of grazers by increased PST production and increased resistance to grazing may facilitate the formation of harmful algal blooms in the sea.
Physical damage caused by herbivores or artificial clipping is known to induce responses in secondary chemistry as well as increased resistance to further grazing in a large number of terrestrial vascular plants, but this has only rarely been described for marine algae. In the present study, it was found that a few weeks of grazing by the gastropod Littorina obtusata can induce substantially increased concentrations of phlorotannins in the intertidal brown seaweed Ascophyllum nodosum. In contrast, grazing by the isopod Idotea granulosa and simulations of herbivory through momentary and continuous clipping caused no significant changes in phlorotannin levels. This indicates a high degree of specificity in the elicitation of chemical responses to physical damage, something which previously has been shown for terrestrial vascular plants but not for marine algae. Ascophyllum plants that had been grazed by L. obtusata were also less susceptible than undamaged plants to further grazing by gastropods, but no such induced resistance was found in the experiments with I. granulosa. Feeding experiments with undamaged Ascophyllum plants and artificial food containing different levels of phlorotannins provided further support for the sensitivity of the feeding behavior of L. obtusata, and the insensitivity of I. granulosa, to intraspecific variation in the phlorotannin content of Ascophyllum. Since L. obtusata is specialized to live and feed on a few fucoid species, including A. nodosum, the results imply that phlorotannins have an important mediating role in the interactions between these macroalgae and L. obtusata. The experimentally induced increase of phlorotannins was consistent with results from phlorotannin analyses of Ascophyllum individuals from natural populations, where plants that had been heavily grazed by L. obtusata contained significantly higher levels of phlorotannins compared to undamaged plants. A field survey of the distribution and abundance of L. obtusata revealed that the density of the gastropod is highly variable at the same spatial scale as the phlorotannin content of Ascophyllum in the study area. These results suggest that grazing by L. obtusata can be an important factor in explaining natural phenotypic variation in the phlorotannin content of Ascophyllum.Together with the results from a few other studies on the interactions between mesoherbivores and marine algae, the results of this study support the previously proposed hypothesis that it is feeding by relatively small, less mobile herbivores that is most likely to cue for induced production of defense chemicals in seaweeds. More studies on such interactions may reveal that the apparent rarity of inducible chemical defenses in seaweeds is misleading.
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...
The demand for vegetable proteins increases globally and seaweeds are considered novel and promising protein sources. However, the tough polysaccharide-rich cell walls and the abundance of polyphenols reduce the extractability and digestibility of seaweed proteins. Therefore, food grade, scalable, and environmentally friendly protein extraction techniques are required. To date, little work has been carried out on developing such methods taking into consideration the structural differences between seaweed species. In this work, three different protein extraction methods were applied to three Swedish seaweeds (Porphyra umbilicalis, Ulva lactuca, and Saccharina latissima). These methods included (I) a traditional method using sonication in water and subsequent ammonium sulfate-induced protein precipitation, (II) the pH-shift protein extraction method using alkaline protein solubilization followed by isoelectric precipitation, and (III) the accelerated solvent extraction (ASE®) method where proteins are extracted after pre-removal of lipids and phlorotannins. The highest protein yields were achieved using the pH-shift method applied to P. umbilicalis (22.6 ± 7.3%) and S. latissima (25.1 ± 0.9%). The traditional method resulted in the greatest protein yield when applied to U. lactuca (19.6 ± 0.8%). However, the protein concentration in the produced extracts was highest for all three species using the pH-shift method (71.0 ± 3.7%, 51.2 ± 2.1%, and 40.7 ± 0.5% for P. umbilicalis, U. lactuca, and S. latissima, respectively). In addition, the pH-shift method was found to concentrate the fatty acids in U. lactuca and S. latissima by 2.2 and 1.6 times, respectively. The pH-shift method can therefore be considered a promising strategy for producing seaweed protein ingredients for use in food and feed.
Summary 1Terrestrial plants can sense and respond to herbivory, which may lead to increased resistance towards further grazing if the responses have negative effects on the preference and/or performance of the herbivores. Marine plants (seaweeds) are exposed to a considerable grazing pressure by herbivores ranging from large, mobile fishes and sea urchins to small, sedentary crustaceans and molluscs. The number of investigations studying induced resistance in seaweeds has increased during the last decade, but empirical results are conflicting. 2 We performed a categorical meta-analysis to evaluate statistically the overall seaweed responses to damage or damage-related cues, and factors that may explain the observed variation in inducible seaweed resistance to herbivores. 3 We found a highly significant overall effect of damage on induced seaweed resistance to further herbivory. Division of the studies into different categories showed that brown and green, but not red, seaweeds induce significant resistance to further grazing in response to grazing by small crustaceans and gastropods, but not in response to large gastropods and sea urchins. The seaweeds showed stronger responses when exposed to damage for 11-20 days than in shorter or longer experiments. 4 Seaweeds are very important both as habitat and food for a wide range of marine animals. Our findings contribute importantly to the general ecological understanding of marine plant-herbivore interactions by showing that induced resistance in seaweeds is more common than previously assumed. Many recent marine investigations included in this study have not put emphasis on the ecological relevance and underlying mechanisms of the investigated plant-herbivore interactions. We suggest that the scientific value of future investigations concerning induced defences in marine algae would benefit from formulating more advanced and/or complex hypotheses including the genetic and biochemical mechanisms, cost and constraints of damage-induced civilian and defensive seaweed responses, as well as the effects of these responses on herbivores and other organisms/trophic levels, and on community structure and functioning.
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