Induced resistance in a brown alga: phlorotannins, genotypic variation and fitness costs for the crustacean herbivore

Abstract

In the marine littoral, strong grazing pressure selects for macroalgal defenses such as the constitutive and inductive production of defense metabolites. Induced defenses are expected under spatiotemporally varying grazing pressure and should be triggered by a reliable cue from herbivory, thereby reducing grazing pressure via decreased herbivore preference and/or performance. Although induced resistance has frequently been demonstrated in brown macroalgae, it is yet to be investigated whether induced macroalgal resistance shows genetic variation, a prerequisite for evolutionary responses to selection. In addition, consequences of induced resistance on herbivore performance have rarely been tested while the role of brown algal phlorotannins as inducible defense metabolites remains ambiguous. Using preference bioassays, we tested various cues, e.g., natural grazing, waterborne cues or simulated grazing to induce resistance in the brown alga Fucus vesiculosus. Further, we investigated whether there are induced responses in phlorotannin content, genetic variation in induced resistance or incurred performance costs to the mesoherbivore isopod, Idotea baltica. We found that both direct grazing and waterborne grazing cues decreased the palatability of F. vesiculosus, while increasing the total phlorotannin content. Since the sole presence of the herbivore also increased the total soluble phlorotannins, yet failed to stimulate deterrence, we concluded that phlorotannins alone do not explain increased resistance. Induced resistance varied between algal genotypes and thus showed potential for evolutionary responses to variation in grazing pressure. Induced resistance also incurred performance costs for female I. baltica via reduced egg production. Our results show that the induced resistance of F. vesiculosus decreases grazing pressure by deterring herbivores as well as impairing their performance. Resistance may be induced in advance by waterborne cues and spread effectively throughout the F. vesiculosus belt. Through lowering herbivore performance, induced resistance may also reduce future grazing pressure by decreasing the population growth rate of I. baltica.

Waterborne Signaling Primes the Expression of Elicitor-Induced Genes and Buffers the Oxidative Responses in the Brown Alga Laminaria digitata

“…Previous studies on the A. nodosum algal model have shown that waterborne signaling affects the population dynamics of herbivores and predators in controlled laboratory conditions [21] [53]. It has also recently been suggested that resistance to herbivores may be induced in advance by waterborne cues and spread effectively throughout a F. vesiculosus belt [23]. In diatoms, perception of sublethal levels of aldehydes such as (2E,4E/Z)-decadienal by cells close to damaged cells could sensitize resistance to successive aldehyde exposure, providing an early-warning protective mechanism, as shown by Vardi et al [54].…”

“…This phenomenon is especially well documented in freshwater ecosystems [18] [19]. In marine benthic communities, this type of communication has been reported in rockweed ( Ascophyllum nodosum ) — a common brown alga of North Atlantic rocky shores — when it interacts with an herbivorous snail [20] [21] as well as in other species of fucoids challenged with crustacean grazers [22] [23]. Little is known about the chemical structure of these waterborne cues and the steps that lead from their perception to the actual defense response [20], which may express its features only after a secondary attack.…”

Water-Borne Cues of a Non-Indigenous Seaweed Mediate Grazer-Deterrent Responses in Native Seaweeds, but Not Vice Versa

“…These patterns were observed at both European shores and were almost identical between assays using fresh and reconstituted seaweeds. Although the nature of the water-borne risk cues mediating trophic interactions between grazers and seaweeds is still unknown, several other studies working on seaweed-seaweed interactions assumed water-borne cues to evolve as signals in aquatic environments [18], [29], [30].…”

Spatial and temporal variation in DMSP content in the invasive seaweed Codium fragile ssp. fragile: effects of temperature, light and grazing

“…Quantitative variation in the concentration of secondary metabolites is common, and occurs over a range of spatial and temporal scales (Van Alstyne et al 2001a). This variation can be generated by heritable differences between individuals (Wright et al 2004, Haavisto et al 2010 or by environmental factors, such as nutrient concentrations, herbivory, light, and temperature (Karsten et al 1992, Yates & Peckol 1993.…”