In situ tests on inducible defenses in Dictyota kunthii and Macrocystis integrifolia (Phaeophyceae) from the Chilean coast

Numerous experimental studies have reported inducible defenses in macroalgae, but most of them have been conducted in laboratory environments where algae were maintained detached from the substratum and in artificial flow regimes. The results of those experiments might not reflect the natural situation, which can only be studied in situ. We examined whether the brown macroalgae Dictyota kunthii (C. Agardh) Greville and Macrocystis integrifolia (Bory) show inducible defenses following exposure to different grazing levels (direct, water-borne cues from nearby grazed conspecifics, presence of a non-grazing herbivore and natural grazing) in field experiments, striving to maintain natural conditions as much as possible. We measured palatability of algae after exposure to different grazing levels by using live algae and agar-based food containing non-polar extracts. M. integrifolia showed no induction of defenses (at least not of non-polar compounds), suggesting constitutive defenses, absence of defenses (tolerance) or use of another strategy to avoid herbivory. These results are similar to those from previous laboratory experiments. In D. kunthii, defense was induced after two weeks of direct grazing by amphipods under field conditions. Water-borne cues from nearby grazed conspecifics, presence of a non-grazing herbivore and natural grazing did not induce defenses. Induction of defense in response to direct grazing agrees with results from a previous laboratory study, but while indirect cues induced defenses in the laboratory, there was no measurable induced defense in the field. Probably chemical cues from grazers are diluted quickly in the field, not reaching concentrations that cause induction of defenses. This might be the reason why in some algae induction by direct grazing is a more important defensive strategy than induction by water-borne cues. The results from our study also suggest that laboratory experiments showing induced defenses in response to grazed neighbours or mere grazer presence need to be interpreted with caution.     

Differential toxic effects of Ulva lactuca (Chlorophyta) on the herbivorous gastropods,Littorina littorea and L. obtusata (Mollusca)

Members of the genus Ulva are widespread and abundant in intertidal and shallow subtidal areas but there are conflicting data regarding susceptibility to herbivory. While some studies have documented that Ulva spp. were favored by a diversity of marine herbivores, other work has revealed herbivore deterrence. We investigated grazing and growth rates of the littorinid species, Littorina littorea and L. obtusata, when offered Fucus vesiculosus, Ascophyllum nodosum, Ulva lactuca, and Chondrus crispus, highlighting distinctive vulnerabilities to toxic effects of U. lactuca. Ulva lactuca was the preferred food of L. littorea, while L. obtusata showed no grazing on this ephemeral algal species. In contrast, F. vesiculosus was highly preferred by L. obtusata. Although L. littorea demonstrated a grazing preference for U. lactuca, growth rate of this gastropod species was nearly 3× greater when fed F. vesiculosus, suggesting a non‐lethal, negative effect of U. lactuca on L. littorea with long‐term exposure. Mortality of L. obtusata ranged from 0% to 100% when held in the presence of various Ulva densities for 1 week, and Ulva exudate depressed herbivory of this gastropod. We conclude that the water‐soluble, toxic exudate produced by U. lactuca in response to herbivory had allelochemical properties, and may contain a cleavage product (acrylic acid) of dimethylsulfoniopropionate or reactive oxygen species (i.e., H₂O₂). Observed differences in susceptibility to Ulva toxicity by the littorinid species may be related to generalist versus specialist feeding and habitat strategies.     

Floating seaweed and the influences of temperature, grazing and clump size on raft longevity — A microcosm study

Laboratory experiments were conducted to evaluate the longevity, and consequently also the rafting capacity of the brown seaweeds Fucus vesiculosus and Ascophyllum nodosum. The seaweed degradation process and the activity of the grazer Idotea baltica were strongly influenced by temperature: only at 5 °C, the seaweed growth exceeded the weight loss. At higher temperatures, seaweed fragments sank quickly (within 100 days at temperatures higher than 15 °C). This process was significantly accelerated in the presence of I. baltica, resulting in a decrease of raft longevity of 60-70%. At a constant temperature of 15 °C and in the absence of grazers, fragments of A. nodosum floated longer (mean 45 weeks) than fragments of F. vesiculosus (mean 15 weeks). The results indicate that floating seaweeds have the potential to stay afloat for a long time, but that their longevity is temperature-dependent and can be strongly reduced by grazing activity of associated herbivores.     

Comparing the Relative Importance of Water-Borne Cues and Direct Grazing for the Induction of Defenses in the Brown Seaweed Fucus vesiculosus

Some seaweed species have been shown to release water-borne cues after herbivore attack, for example, to attract natural enemies of the herbivore. These cues may also be sensed by neighboring seaweeds and used to adjust their defenses in anticipation of a possible herbivore attack. Several studies indicated information transfer between seaweed individuals in the past, including the brown seaweed Fucus vesiculosus. Previous work showed induction of defenses in F. vesiculosus in response to water-borne cues released by isopod-grazed conspecifics. In contrast, another study on induced responses after exposure to cues from isopod-grazed neighbors using the same seaweed species yielded contradictory results. This study reassessed the ability of F. vesiculosus individuals to sense water-borne cues released by isopod-grazed neighbors in a series of experiments that monitored F. vesiculosus palatability in response to direct grazing by Idotea baltica and water-borne cues from isopod-grazed neighbors relative to unmanipulated seaweed pieces. Two-choice feeding assays were conducted with both fresh and reconstituted seaweed pieces. Direct grazing by I. baltica induced a chemical defense in F. vesiculosus, confirming results of previous studies. In contrast, evidence for increased herbivore resistance in seaweed pieces that were located downstream of isopod-grazed F. vesiculosus could not be provided. The lack of defense induction in response to grazing of conspecific neighbors may be explained by the environmental conditions and the scattered distribution of F. vesiculosus individuals in the intertidal zone of Helgoland, which may render resource investment in the emission and/or response to water-borne cues at this site unprofitable.     

Water-borne cues of a non-indigenous seaweed mediate grazer-deterrent responses in native seaweeds, but not vice versa

Plants optimise their resistance to herbivores by regulating deterrent responses on demand. Induction of anti-herbivory defences can occur directly in grazed plants or from emission of risk cues to the environment, which modifies interactions of adjacent plants with, for instance, their consumers. This study confirmed the induction of anti-herbivory responses by water-borne risk cues between adjoining con-specific seaweeds and firstly examined whether plant-plant signalling also exists among adjacent hetero-specific seaweeds. Furthermore, differential abilities and geographic variation in plant-plant signalling by a non-indigenous seaweed as well as native seaweeds were assessed. Twelve-day induction experiments using the non-indigenous seaweed Sargassum muticum were conducted in the laboratory in Portugal and Germany with one local con-familiar (Portugal: Cystoseira humilis, Germany: Halidrys siliquosa) and hetero-familiar native species (Portugal: Fucus spiralis, Germany: F. vesiculosus). All seaweeds were grazed by a local isopod species (Portugal: Stenosoma nadejda, Germany: Idotea baltica) and were positioned upstream of con- and hetero-specific seaweeds. Grazing-induced modification in seaweed traits were tested in three-day feeding assays between cue-exposed and cue-free (?=?control) pieces of both fresh and reconstituted seaweeds. Both Fucus species reduced their palatability when positioned downstream of isopod-grazed con-specifics. Yet, the palatability of non-indigenous S. muticum remained constant in the presence of upstream grazed con-specifics and native hetero-specifics. In contrast, both con-familiar (but neither hetero-familiar) native species reduced palatability when located downstream of grazed S. muticum. Similar patterns of grazer-deterrent responses to water-borne cues were observed on both European shores, and were almost identical between assays using fresh and reconstituted seaweeds. Hence, seaweeds may use plant-plant signalling to optimise chemical resistance to consumers, though this ability appeared to be species-specific. Furthermore, this study suggests that native species may benefit more than a non-indigenous species from water-borne cue mediated reduction in consumption as only natives responded to signals emitted by hetero-specifics.     

Interactions of plant stress and herbivory: intraspecific variation in the susceptibility of a palatable versus an unpalatable seaweed to sea urchin grazing

Summary Interactions among environmental stresses, plant defensive characteristics, and plant nutrient status may significantly affect an alga's susceptibility to herbivores. Following desiccation, the palatable seaweed Gracilaria tikvahiae was less susceptible to grazing by the sea urchin Arbacia punctulata while the unpalatable alga Padina gymnospora became more susceptible. Increased grazing on desiccated Padina appeared to result from a loss of chemical defenses following desiccation. Palatable plants treated with organic extracts from desiccated Padina plants were consumed at more than twice the rate of plants treated with extracts from undesiccated plants. Increased susceptibility of Padina did not correlate with changes in protein content of the alga; reduced grazing on desiccated Gracilaria was associated with a decrease in protein content. When Padina was grazed by Arbacia or mechanically damaged to mimic urchin grazing, its susceptibility to Arbacia decreased within 1 to 5 days. These results demonstrate that history of physical or biological stress may affect a plant's susceptibility to herbivory. We hypothesize that urchins cue primarily on attractiveness features (e.g. nutrient content) of highpreference algae and deterrent features (e.g. chemical defenses) of low-preference algae. Stresses may therefore increase, decrease, or not affect a plant's susceptibility to herbivory depending upon the primary feeding cues used by the herbivore, the defensive mechanisms used by the plant, and the way these are altered by various environmental stresses.     

TRANSPORT AND DEFENSIVE ROLE OF ELATOL AT THE SURFACE OF THE RED SEAWEED LAURENCIA OBTUSA (CERAMIALES,RHODOPHYTA)1

Natural within‐thallus concentrations of elatol produced by Laurencia obtusa (Huds.) J. V. Lamour. inhibit herbivory and prevent fouling. However, elatol occurs in larger amounts within the thallus compared with the quantities from the surface of this alga. We evaluated whether the surface elatol concentrations inhibit both herbivory and fouling and whether the content of corps en cerise can be transferred to the external cell walls. Surface elatol concentrations did not inhibit herbivory by sea urchins, settlement of barnacle larvae, or mussel attachment. Evidence of a connection between the corps en cerise, where elatol is probably stored, and the cell wall of L. obtusa was based on channel‐like membranous connections that transport vesicles from the corps to the cell wall region. Therefore, L. obtusa presents a specific process of chemical transport between the cell storage structures and the plant surface. We hypothesized that if high amounts of elatol are capable of inhibiting herbivory and fouling, if the tested organisms are ecologically relevant, and if elatol really occurs on the surface of L. obtusa and this seaweed can transport this compound to its surface, the low natural concentration of defensive chemicals on the surface of L. obtusa is probably not absolute but may be variable according to environmental conditions. We also hypothesized that herbivory and fouling would not exert the same selective force for the production of defensive chemicals on L. obtusa’s surface since the low concentrations of elatol were inefficient to inhibit either processes or distinguish selective pressures.     

INDUCTION AND REDUCTION OF ANTI‐HERBIVORE DEFENSES IN BROWN AND RED MACROALGAE OFF THE KENYAN COAST1

Herbivory is particularly intense in tropical benthic communities, suggesting preference of constitutive, rather than inducible, anti‐herbivory defense. The objective of the study was to examine whether anti‐herbivore defenses in the red alga Hypnea pannosa J. Agardh and the brown algae Sargassum asperifolium Hering and G. Martens ex J. Agardh and Cystoseira myrica (S.G. Gmelin) C. Agardh could be induced and subsequently reduced in response to grazing by the amphipod Cymadusa filosa Savigny. During a 14‐day treatment phase, algae were exposed to amphipod grazing or were left ungrazed (control). Subsequently, one subset of algae was used in feeding assays, whereas another was cultivated for additional 14 days without consumers (recovery phase). At the end of each phase, bioassays were conducted to detect defensive traits in terms of differences in consumption rates of grazed and control pieces of live algae and agar‐based food containing nonpolar algal extracts. Consumption of grazed live S. asperifolium and H. pannosa specimens was lower than of control algae. Furthermore, nonpolar extracts of grazed S. asperifolium and C. myrica were less preferred than those from control algae. Defensive responses were exclusively detected after the treatment phase, although strong preference of ungrazed H. pannosa and C. myrica over grazed conspecifics continued throughout the recovery phase. These findings suggest that phenotypic plasticity in anti‐herbivory defense of marine macroalgae 1) might be more common than previously shown, 2) could be switched on and off within 2 weeks, and 3) can be found in nonpolar algal extracts.