Increased resistance towards generalist herbivory in the new range of a habitat-forming seaweed. Ecosphere 3 (12): 125 (original) (raw)
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Geographic variation in seaweed induced responses to herbivory
Marine Ecology Progress Series, 2007
Recent work on European (Swedish and English) populations of Ascophyllum nodosum has detected inducible defenses in response to snail grazing that include a decrease in algal palatability and an increase in phlorotannin concentration, a class of potential chemical defenses. However, tests of induced responses in other A. nodosum populations are lacking and we thus have a limited understanding of how widespread such responses are in fucoid algae. We exposed a North American (Massachusetts) A. nodosum population to Littorina obtusata, the same snail species used in previous studies, and tested for the presence of inducible responses during 2 experiments. In contrast to European populations, the North American population of A. nodosum did not develop any such responses. Exposure to either direct grazing or just waterborne cues associated with grazing for 26 d failed to suppress the palatability of artificial foods made from seaweed tissues exposed to these treatments. In addition, exposure to grazer cues did not increase seaweed phlorotannin levels compared to controls. The lack of induced responses in the North American population cannot be attributed to tissue type or potential seasonal variation in inducibility because each of our 2 independent experiments tested for responses in 2 tissue types (apical tips and basal shoots) in both the winter and spring. Furthermore, consistent with European work, the North American population lacked obvious grazing damage at the time of collection, suggesting that the differences we observed were unrelated to recent history with grazers. Thus, our work and that of others indicates that A. nodosum displays considerable inter-population variability in its response to a single herbivore species.
Increased chemical resistance explains low herbivore colonization of introduced seaweed
Oecologia, 2006
The success of introduced species is often attributed to release from co-evolved enemies in the new range and a subsequent decreased allocation to defense (EICA), but these hypotheses have rarely been evaluated for systems with low host-specificity of enemies. Here, we compare herbivore utilization of the brown seaweed, Fucus evanescens, and its coexisting competitors both in its native and new ranges, to test certain predictions derived from these hypotheses in a system dominated by generalist herbivores. While F. evanescens was shown to be a preferred host in its native range, invading populations supported a less diverse herbivore fauna and it was less preferred in laboratory choice experiments with important herbivores, when compared to co-occurring seaweeds. These results are consistent with the enemy release hypothesis, despite the fact that the herbivore communities in both regions were mainly composed of generalist species. However, in contrast to the prediction of EICA, analysis of anti-grazing compounds indicated a higher allocation to defense in introduced compared to native F. evanescens. The results suggest that the invader is subjected to less intense enemy control in the new range, but that this is due to an increased allocation to defense rather than release from specialized herbivores. This indicates that increased resistance to herbivory might be an important strategy for invasion success in systems dominated by generalist herbivores.
Higher resistance to herbivory in introduced compared to native populations of a seaweed
Oecologia, 2010
Non-indigenous species (NIS) are important components of global change, and in order to manage such species it is important to understand which factors aVect their success. Interactions with enemies in the new range have been shown to be important for the outcome of introductions, but thus far most studies on NIS-enemy interactions have considered only specialist herbivores in terrestrial systems. Here we present the results from the Wrst biogeographic study that compares herbivore resistance between populations in the native and new region of a non-indigenous seaweed. We show that low consumption of the non-indigenous seaweed by a generalist herbivore is caused by higher chemical defence levels and herbivore resistance in the new range-and not by the failure of the herbivore to recognise the non-indigenous seaweed as a suitable host. Since most seaweed-herbivore interactions are dominated by generalist herbivores, this pattern could be common in marine communities. Our results also reveal that traits used to predict the invasive potential of species, such as their resistance to enemies, can change during the invasion process, but not always in the way predicted by dominant theories.
Oecologia, 2010
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.
INDUCIBLE AND CONSTITUTIVE DEFENSES OF VALUABLE SEAWEED TISSUES: CONSEQUENCES FOR HERBIVORE FITNESS
Ecology, 2005
Optimal Defense Theory predicts that plants exposed to herbivory should allocate more resources to produce costly secondary metabolites in tissues with higher fitness values. To increase plant resistance, the secondary metabolites must have a negative impact on the preference and/or performance of herbivores. We tested the hypotheses that induction of secondary metabolites (phlorotannins) in a brown seaweed in response to grazing by herbivorous gastropods will differ between seaweed tissues with different fitness values (basal stipes and annual shoots), and that the subsequent change in food value will affect the fitness (growth and fecundity) of the gastropods. Induction of phlorotannins was significant in both tissue types but was more pronounced in basal stipes, which have a higher fitness value. Basal tissues also had significantly higher constitutive defense levels than did apical tissues. No effects of algal tissue type or grazing history on the growth rate of the gastropods were detected. However, the number of viable eggs was significantly lower for gastropods feeding on basal shoots, and there was a significantly lower proportion of viable eggs produced by gastropods that were offered previously grazed seaweed tissues. The results show that induced resistance, and its variation among different plant parts, can have significant negative effects on herbivore performance that may reduce future herbivore pressure and thus enhance plant fitness.
Do native herbivores provide resistance to Mediterranean marine bioinvasions? A seaweed example
Biological Invasions, 2011
Generalist herbivores in marine ecosystems are poorly examined for their potential to serve as a source of biotic resistance against algal invasion. We assessed how one of the main generalist herbivores in Mediterranean rocky reefs (the sea urchin Paracentrotus lividus) affects Lophocladia lallemandii and Caulerpa racemosa, two algal invaders with strong detrimental effects on native benthic communities. In a comparison of sea urchin gut contents to algal community composition, strong preferences were exhibited, leading to no relationship between con-sumption and availability. Both C. racemosa and L. lallemandi were abundant in algal assemblages ([60% occurrence), but C. racemosa (20% of diet) was consumed more than L. lallemandi (3.5%). Experimental enclosures of sea urchins (12 sea urchins * m -2 ) were carried out in locations where L. lallemandii was already established and C. racemosa was rare (new invasion) or abundant (established invasion). C. racemosa was negatively affected by sea urchins only when it was rare, and no effect was detected when the alga was already abundant. Results for L. lallemandi were exactly opposite: urchins limited seasonal increases in L. lallemandi in highly-invaded areas. Because of the small amount of direct consumption of L. lallemandi, its decrease in abundance may be related to the grazing of native algae where L. lallemandii is attached. Overall, our results show that high densities of native herbivores may reduce invasive algae at low densities, due to a combination of direct and indirect effects, but it has no significant effect in highly-invaded areas.
Marine Biology, 2004
Environmental and/or genetic among-site variation in plant quality may influence growth and fecundity of specialized herbivores inhabiting a particular site. Such variation is important as it generates spatial variation in selection for traits related to plant–herbivore interaction. Littoral macroalgae are known to respond plastically to environmental variation by modifying their chemistry or morphology. We studied geographic variation in phlorotannin, nitrogen, protein, and sugar (fucose, mannitol, and melibiose) concentrations of the brown alga Fucus vesiculosus at 12 sites separated by 0.5 to 40 km in the naturally fragmented Archipelago Sea in the northern Baltic Sea. By this regional variation in algal chemistry we attempted to explain among-population variation in size and fecundity of the crustacean herbivore Idotea baltica. We observed high spatial variation in all the measured chemical characteristics of F. vesiculosus, as well as in female size and the number of eggs produced by the herbivores. Spatial variation in nitrogen or protein contents of the alga did not explain the variation of herbivore traits. However, egg size positively covaried with spatial variation in the concentration of mannitol, the major storage carbohydrate of the alga. Such a positive relationship may arise if I. baltica can utilize the nutritive value of a mannitol-rich diet thereby being better able to provision the developing eggs with energy-rich metabolites. Unexpectedly, the concentration of phlorotannins, secondary metabolites having a putative role in defense against herbivory, positively covaried with the size of the herbivore. Among-population variation in host plant chemistry and covariation of that with herbivore growth and reproduction imply that herbivores respond to the local quality of their host plants, and that geographical structuring of populations has to be taken into account in studies of plant–herbivore interactions.
Induced herbivore resistance in seaweeds: a meta-analysis
Journal of Ecology, 2007
1 Terrestrial 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.
Hydrobiologia, 2006
The in situ grazing experiments were performed in the shallow water rocky habitat of the northern Baltic Sea during ice-free season 2002. In the experiments the effects of algal species and choice on the grazing of the mesoherbivores Idotea baltica (Pallas) and Gammarus oceanicus Segerstra˚le were tested. Salinity, temperature, concentration of nutrients in water and macroalgae and net production of macroalgae were considered as random effects in the analysis. The invertebrate feeding rate was mainly a function of the net photosynthetic activity of Pylaiella littoralis (L.) Kjellman and Fucus vesiculosus L. Feeding rate increased significantly with decreasing algal photosynthetic activity. When the two algal species were incubated together invertebrates fed primarily on P. littoralis. Low selectivity towards P. littoralis coincided with its high photosynthetic activity. The presence of F. vesiculosus did not modify the invertebrate feeding on P. littoralis. The results indicated that (1) the grazing on F. vesiculosus depended on the availability of P. littoralis, (2) the photosynthetic activity of algae explained the best the variation in grazing rate and (3) the grazers are not likely to control the early outbreak of filamentous algae in the northern Baltic Sea by avoiding young and photosynthetically active algae. The likely mechanism behind the relationship is that the increased photosynthetic activity of macroalgae coincides with their higher resistance to herbivory.