Flexibility in macroalgal response to herbivory: The influence of grazing pressure on the induction of chemical defences in seaweeds

Herbivores have major impacts on the abundance and distribution of seaweeds and have an important role in structuring benthic communities. To counteract this top-down control, macroalgae developed various adaptations to tolerate, avoid or defend herbivory. An induced resistance, triggered by the presence of grazers, should be an effective strategy against consumers, especially in temperate systems where herbivores` abundances fluctuate in time. In contrast to terrestrial systems little is known about mechanisms of inducible defences in marine macroalgae. Due to the fact that previous studies in marine systems mainly focused only on the presence or absence of induced resistance to herbivory, the temporal dynamics in and the flexibility of the defence induction in seaweeds remained poorly investigated. In the study at hand it was investigated in a pilot study whether different species of marine macroalgae, collected on the island of Anglesey, in North Wales, are able to evoke defences against herbivory. In the main experiment it was examined whether the speed at which defences are up-regulated is a function of grazing pressure. For this, living algal material of Asophyllum nodosum and Fucus vesiculosus was exposed to two different density levels of the periwinkle Littorina littorea for a time span up to 28 days, while algae material of the same macroalgal species was kept in the absence of grazers to serve as controls. To assess the effect of herbivory, fragments were taken from moderately/ intensively grazed as well as from the control algal tissue and two-way choice feeding assays were conducted subsequently. Differences in palatability were measured using naive individuals of the same gastropod species. In contrast to previous studies, feeding assays were conducted every second day to ensure a high temporal resolution and to find out more about the dynamics iv and the temporal profile of inducible defences. It was also investigated how fast a defence is relaxed after the removal of grazers. Additionally, a high performance liquid chromatography and a colorimetric Folin–Ciocalteu assay was conducted to determine if the difference in palatability of algae tissue was based on chemical compounds that acted as grazer deterrents and hence caused the in the feeding assays observed changes in algal palatability. Furthermore, growth rates of grazed and control algal fragments were measured as an indicator of metabolic costs of defence induction. A faster response to herbivory in the higher density level in comparison to the lower density level was not observed. Consequently the hypothesis that a higher grazing pressure leads to a faster defence induction could not be confirmed for either grazer-algae combination. However, it was detected that defences fluctuated in their effectiveness, interestingly as well in the presence as in the absence of grazers. In marine systems temporal oscillations in grazer resistance have not been reported so far. Additionally, a stronger defence induction was observed in the pilot study conducted in summer than in the main experiment in autumn, indicating a seasonal variation in response to grazing. Nevertheless, it can not be confirmed, that flexible defences are costly in terms of metabolic energy, because a reduced growth rate correlating with grazer resistance was not found. Furthermore, there was no evidence that the defence was chemically mediated. The data pronounce the importance of subsequent high temporal resolution sampling. Temporal differences on a small scale between days and on a large scale between seasons were found. Therefore, the results propose that macroalgal resistance to herbivory shows a high degree of variability in contrast to an on/off mechanism in the presence/absence of grazers. Especially, a defence induced in pulses could serve the purpose to create variability in the macroalgae serving as food source and, therefore hinder herbivores` cov evolution.This has important implications for the interpretation of previous studies on inducible defences in marine benthic systems that failed to find a flexible antiherbivory resistance, which was maybe only due to the low number of sampling events. Consequently the results give new insight in the variability that can be inherent in resistances, what presumably influences the proposition of nearshore food webs and therefore would have important ecological implications.