Interaction between isopod grazing and wave action: a structuring force in macroalgal communities in the southern Baltic Sea

The macroalgal belt in the southern Baltic Sea may be partly structured by the interaction of physical and biological factors. A field study, spanning the 1990s, describes a rapid decline of the Fucus spp. stands along the wave-exposed Swedish southeast coast. During this period, a relative dominance of Fucus vesiculosus L. shifted to a relative dominance of Fucus serratus L. The decline of F. vesiculosus coincided with observations of large numbers of the grazing isopods Idotea baltica (Pallas) and Idotea granulosa Rathke, or with field observations of frequent grazing marks on Fucus fronds. I. baltica, but not I. granulosa, tended to aggregate in the declining Fucus spp. stands, indicating a strong preference for Fucus spp. In a mesocosm experiment I. baltica, when given a choice, grazed both Fucus species at weak water motion. At strong water motion grazing was concentrated on F. vesiculosus. It is hypothesized that one of the reasons I. baltica preferred F. vesiculosus to F. serratus at strong water motion may have been differences in habitat quality, like width of thallus, influencing the ability to cling to the plant. Smaller thallus, as in F. vesiculosus, thus is the preferred habitat for grazing of I. blatica. We postulate that the existence of F. serratus in the area may be favoured by strong wave action and moderate but not strong grazing by I. baltica, relaxing the interspecific competition from F. vesiculosus.     

Food and habitat choice of the isopod Idotea baltica in the northeastern Baltic Sea

The isopod Idotea baltica is the most important benthic herbivore in the Baltic Sea. There exists a significant correlation between the distribution of the adult isopod and the belts of bladder wrack Fucus vesiculosus. However, following the eutrophication induced blooms of the filamentous macroalga Pilayella littoralis and the disappearance of F. vesiculosus a notable increase in idoteid abundances has been observed. The aim of this paper was (1) to evaluate experimentally whether F. vesiculosus provides either food, shelter or both to the isopods and (2) to estimate the role of associated filamentous algae in the habitat selection process. Amongst six abundant macroalgal species, about 50% of isopod population was attracted to F. vesiculosuscovered with the filamentous algae P. littoralis. The majority of the remaining part of the population was either swimming freely or attracted to non-epiphytic P. littoralis. When both live algae and artificial substrata were provided, P. littoralis growing on artificial substrata was clearly preferred by the isopods over epiphyte-free F. vesiculosus. In the grazing experiment where I. baltica was allowed to choose between F. vesiculosus and P. littoralis the latter contributed practically 100% of the diet of the isopod. The results indicate the importance of P. littoralis as a food item and F. vesiculosus as a shelter for I. baltica.     

Despite marine traits,the endemic Fucus radicans (Phaeophyceae) is restricted to the brackish Baltic Sea

Many of the marine species that were introduced to the Baltic Sea during the Littorina stage (c. 8500–3000 years BP), e.g. Fucus vesiculosus and F. serratus, have adapted to the present low salinity. These marine species have gone from marine conditions into lower salinity environments. In this paper we ask why the recently discovered endemic brown alga Fucus radicans shows the opposite pattern. Fucus radicans is only present in the northern parts of the Baltic Sea, the low salinity Bothnian Sea (4–6 psu). Potentially, the fitness of F. radicans might be reduced in higher salinities if it is better adapted to brackish conditions. We hypothesize, however, that the southern distribution limit of F. radicans is set by biotic factors, e.g. competition with F. vesiculosus and higher grazing pressure by Idotea balthica and not by salinity. Our results show that the reproductive output of F. radicans is limited by low salinity (4 psu) but increases in higher salinities. However, the southern distribution limit, i.e. the northern Baltic Proper, is regulated by biotic factors, where the additive effects from shading by taller F. vesiculosus thalli and grazing on F. radicans by the isopod I. balthica limit the biomass production of F. radicans. We suggest that F. radicans still maintains marine traits due to its ability to propagate clonally and is restricted to the Bothnian Sea by interactions with F. vesiculosus and I. balthica. We also propose that increased precipitation due to climate change might affect the northern range limit and that the distribution of F. radicans could be expected to shift further south into the Baltic Proper.     

Long-term decline and recent recovery of Fucus populations along the rocky shores of southeast Sweden, Baltic Sea

The Fucus populations on rocky shores along 300 km of the coastal waters of southeast Sweden in the Baltic proper have been studied since 1984 at a number of fixed sites as part of monitoring programmes. This paper describes changes in distribution and abundance of F. vesiculosus and F. serratus during the period 1984–2001. Sheltered sites showed a consistent temporal and spatial pattern of Fucus spp. distribution over a coastline of 300 kilometres. The depth penetration and abundance of Fucus spp. increased during the 1980s. Around 1990 the development reversed as a consequence of grazing and in 1997 many sites were almost devoid of Fucus spp. Since 1998 both abundance and depth penetration have increased again, possibly as a result of local measures against eutrophication. Exposed sites, on the other hand, lost their Fucus populations at the beginning of the 1990s, and they have not recovered. Extended field studies lead us to deduce that the fixed sites referred to above were representative of the Fucus populations in the area investigated. Major declines, both at sheltered and exposed sites, are attributed to grazing by the isopod Idotea baltica. The populations of I. baltica may have been favoured by the continuing eutrophication of the Baltic, a series of mild winters in the 1990s, and a contemporary decline in some potential predators.     

Seasonal changes in situ grazing of the mesoherbivores Idotea baltica and Gammarus oceanicus on the brown algae Fucus vesiculosus and Pylaiella littoralis in the central Gulf of Finland, Baltic Sea

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 Segerstråle 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.     

Seasonal variation in invertebrate grazing on Chara connivens and C. tomentosa in Kõiguste Bay, NE Baltic Sea

Charophytes are a highly endangered group of algae. In the Baltic Sea, the number of species, distribution area and biomass of charophytes have significantly decreased in recent decades. Although eutrophication triggers their initial decline, the mechanism of the final extinction of charophyte populations is not fully understood. An in situ experiment was performed to study the role of the mesoherbivores Idotea baltica, Gammarus oceanicus and Palaemon adspersus in the decline of charophytes in the north-eastern Baltic Sea. Invertebrate grazing showed a clear seasonality: grazing pressure was low in April, moderate in July, and high in October. Grazing on charophytes by P. adspersus was negligible, whereas I. baltica and G. oceanicus significantly reduced the biomass of charophytes in the field. Low photosynthetic activity (high decomposition rate) of the charophytes favoured grazing. The invertebrates studied preferred Chara tomentosa to C. connivens. Low consumption of C. connivens may reflect its non-native origin. The experiment suggests that, under moderately eutrophic conditions, grazers are not likely to control charophyte populations. However, grazers have the potential to eliminate charophytes in severely eutrophic systems under the stress of filamentous algae.Communicated by H.D. Franke     

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

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.     

Temporal dynamics of induced resistance in a marine macroalga: Time lag of induction and reduction in Fucus vesiculosus

In recent years several studies have shown that inducible resistance is ubiquitous in brown algae. However, while many studies on terrestrial plants identified eliciting signals and the response cascade to resistance, the knowledge on inducible marine macroalgal defense is lagging far behind and is often restricted to the mere recognition of its presence. This study is the first to accurately quantify the temporal dynamics, i.e. the time lag of induction and relaxation, of antifeeding defense in a marine macroalga, Fucus vesiculosus, from the Baltic Sea. Time lag of induction and reduction of induced feeding resistance were assessed via feeding assays, because the identities of defensive compounds are still unknown. Our results demonstrate that F. vesiculosus induced defense 10-14 days after the onset of grazing by the isopod Idotea baltica. Defenses were relaxed within 2-4 days after cessation of grazing. Thus, defense seems to be deployed sparingly and just long enough to avoid substantial loss of tissue.     

Habitat heterogeneity, predation and gene flow: colour polymorphism in the isopod, Idotea baltica

The colour polymorphic isopod Idotea baltica inhabits the brown alga Fucus vesiculosus which is often colonised by the white epizoite Electra crustulenta (Bryozoa). In an experiment the predation risk for the different colour morphs of I. baltica was highly dependent on background colouration. Morph frequencies and Electra density varied substantially among 10 collecting sites but correlated poorly with each other, suggesting that local selection for cryptic colouration may be counteracted by gene flow. Indeed, estimates based on four polymorphic allozymes suggested rate of gene flow to be high. These results support the hypothesis that locally varying selection for cryptic colouration counteracted by gene flow contributes to the maintenance of colour polymorphism in I. baltica. The visual differences between the microhabitats and the differential microhabitat use between males and females seem to result in different patterns of selection on males and females for cryptic colouration. Also this is likely to play an important role for the polymorphism.     

Responses of growth and phlorotannins in <Emphasis Type="Italic">Fucus vesiculosus</Emphasis> to nutrient enrichment and herbivory

Discharge from anthropogenic sources may modify both macroalgal growth patterns and resource allocation to carbon based secondary compounds, thereby affecting their susceptibility for herbivory. We tested the effect of eutrophication in terms of nutrient enhancement on growth and phlorotannin concentration of Fucus vesiculosus by conducting manipulative experiments in the field and mesocosms. In the field experiment we utilised fish farms as nutrient sources and in the mesocosm-experiment we manipulated ambient nutrient levels and occurrence of the herbivorous isopod Idotea baltica. Vicinity of a fish farm affected neither growth nor the phlorotannin concentration of Fucus but increased the amount of epiphytes growing on Fucus. Other organisms such as epiphytic filamentous algae and periphyton, which are more capable of quickly utilizing excess nutrients, may restrain the direct effects of nutrient enhancement on Fucus. In a manipulative mesocosm experiment, neither nutrient enrichment nor occurrence of herbivores affected phlorotannin concentration implying lack of induced defences, at least in terms of increasing phlorotannin concentration. Feeding of thallus decreased the growth rate of algae, but the number of reproductive organs, receptacles, was not affected by herbivory. The negative effect of herbivory on the amount of apical tips tended to be stronger under nutrient enriched conditions. We conclude that eutrophication processes, in terms of nutrient enrichment, does not have strong direct effect on growth or phlorotannin production of F. vesiculosus. However, there may be important indirect consequences. First, herbivory may be targeted more to apical parts of the thallus under eutrophicated conditions. Second, the result that Fucus growing close to nutrient sources were smaller than those in control areas may reflect differences in mortality schedules of algae between eutrophicated and control areas.     

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.     

Polar extracts of the brown alga Fucus vesiculosus (L.) reduce assimilation efficiency but do not deter the herbivorous isopod Idotea baltica (Pallas)

Plant secondary metabolites provide resistance against herbivory if they are capable of decreasing herbivore performance or deterring feeding. Here we test the effects of phlorotannin-containing polar extracts from the brown alga Fucus vesiculosus on the assimilation efficiency and feeding preferences of the herbivorous isopod Idotea baltica. We test the effects separately for each sex of the isopod to test the hypothesis that the digestive efficiencies of the sexes may have diverged. Phlorotannin-containing polar extracts were incorporated into an agar-based artificial food in varying amounts. We also varied the quality of the food, using high-quality food containing animal proteins and low-quality food containing only algal material. The total assimilation efficiency as well as the assimilation efficiencies of carbon and nitrogen decreased with an increasing concentration of phlorotannin-containing extracts. The negative effects on carbon and nitrogen assimilation were higher when extracts were incorporated in the high-quality food. Females were consistently more efficient than males in all assimilation measures; there were no interactions between sex and food quality or phlorotannin concentration, suggesting that the digestive efficiency of the sexes had diverged but that the two sexes responded similarly to phlorotannin enriched artificial food. Although phlorotannin-containing extracts were harmful to performance, they did not deter feeding in preference tests. On the contrary: the isopods preferred the food containing more phlorotannins, suggesting that phlorotannins may act as cues in host recognition. Thus phlorotannins were inefficient deterrents, and I. baltica seems to be adapted to utilizing phlorotannin-containing foods despite their detrimental effects on assimilation. We suggest that F. vesiculosus provides a predation refuge and temporal constancy in availability for I. baltica, both of which select for the ability to utilize it as a food. Phlorotannin-containing polar extracts from F. vesiculosus are still harmful digestibility reducers, and may thereby prevent complete specialization and generate selection for utilization of a wider host range.     

Effects of filamentous algae and deposited matter on the survival of Fucus vesiculosus L. germlings in the Baltic Sea

As a result of increased nutrient levels in the Baltic Sea during thepast 50 years, mass developments of filamentous algae have become a commonfeature along the Swedish east coast and deposition of organic matter has alsoincreased. To test whether these two factors have any effects on the early lifestages of Fucus vesiculosus a number of laboratory andfield studies were conducted. The amount of epilithic and epiphytic filamentousalgae on F. vesiculosus and the amount of deposited matterin the littoral zone were quantified during the two reproductive periods ofF. vesiculosus, early summer (May–June) and lateautumn (September–October). Both filamentous algae (Cladophoraglomerata) and deposited matter (introduced either before or aftersettlement of fertilized eggs) were shown to significantly decrease the numberof surviving germlings. The survival of germlings seeded on stones withfilamentous algae, or seeded on culture dishes concurrently with the lowestconcentration of deposited matter (0.1 g dm^–2),was 5% or less. In the field, the amount of filamentous algae was significantlyhigher during F. vesiculosus summer reproduction, whereasthe amount of deposited matter collected in traps was significantly higherduring the period of autumn reproduction. The greatest biomass of filamentousalgae was observed at sheltered sites. Based on the negative effects offilamentous algae and deposited matter on Fucusrecruitmentand the observation of local and seasonal differences in abundance offilamentous algae and deposition, we suggest that the prerequisites for thesurvival of either summer or autumn-reproducing populations of F.vesiculosus in the Baltic Sea may differ locally.     

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.     

Genetic and environmental variation in performance of a marine isopod: effects of eutrophication

Environmental variation in food resources modifies performance of herbivores, in addition to genetic variation and maternal effects. In marine benthic habitats, eutrophication may modify herbivores diets by changing host species composition or nutritional quality of algae for herbivores. We studied experimentally the effects of diet breadth and nutrient availability for the host algae on fitness components of the herbivorous isopod Idotea baltica. We fed the adult isopods with the brown algae Fucus vesiculosus and Pilayella littoralis and juveniles with the green alga Cladophora glomerata. By using half-sib families, we were able to separate the genetic, environmental and maternal effects on intermolt duration and size of the juveniles. The mothers confined to the diet consisting of both Fucus and Pilayella grew better and produced larger egg mass than those having consumed Fucus alone. Nutrient enhancement of algae did not influence the performance of the adult herbivores. However, the juveniles achieved twice the weight as well as shorter intermolt duration when consuming nutrient-treated C. glomerata. Mothers nutrition, either nutrient enrichment of her food algae or diet breadth, did not affect juvenile survival or growth as such, but we found evidence that the broader diet consumed by the mother mediated offspring performance by further accelerating growth rate of the offspring that fed on nutrient-treated alga. Intermolt duration was a highly heritable trait, but size showed very low heritability. Instead, maternal effects on size were substantial, suggesting that differences among mothers in their egg-provisioning ability strongly affect weight gain of their offspring. A high amount of additive genetic variance in intermolt duration implies potential for quick evolutionary responses in the growth schedule in the face of changes in the selective environment. We conclude that eutrophication, in addition to improving growth and reproduction of I. baltica by enhancing food quality and by providing opportunity for broader, more profitable diets, may act as a selective agent on life-history traits. Eutrophication of coastal waters is thus likely to reflect in herbivore density, population dynamics and eventually, grazing pressure of littoral macroalgae.     

Invasion of a Habitat-Forming Seaweed: Effects on Associated Biota

Fucus evanescens is a brown alga of arctic origin that has invaded European coasts. The epiphytic community of F. evanescens in southern Sweden was compared with that of the native Fucus vesiculosus, to examine to what extent an invading seaweed can modify local biodiversity. F. evanescens was much less fouled than F. vesiculosus, supporting both less biomass and fewer species of epiphytes. Multivariate analysis of the most common epiphyte taxa showed that the epiphytic community composition of F. evanescens was not entirely separated from that of F. vesiculosus, but host species contributed significantly to explain the variation in community composition. The biomass of free-living invertebrates was also lower on F. evanescens, although the pattern differed between taxonomic groups. While the biomass of amphipods was lower on F. evanescens, there was no significant difference in biomass of isopods or gastropods between the Fucus species. The good correlation between biomass of epiphytes and free-living animals suggests that the epiphytes play an important role in providing a suitable habitat for many species of free-living epifauna. The study shows that the invasion of F. evanescens affects the environmental conditions for many species associated with the Fucus community but that the direct effect on biodiversity is probably low.     

ANTIFEEDING DEFENSE IN BALTIC MACROALGAE: INDUCTION BY DIRECT GRAZING VERSUS WATERBORNE CUES1

The prevalence of antigrazing defense induction and the cues triggering induction in marine macroalgae are generally not well understood. We examined the capacity of defense and the mechanisms of regulation in five common perennial macroalgal species from the Baltic Sea, Furcellaria lumbricalis (Huds.) J. V. Lamour., Delesseria sanguinea (Huds.) J. V. Lamour., Phyllophora pseudoceranoides (S. G. Gmel.) Newroth et A. R. A. Taylor, Fucus serratus L., and Fucus evanescens C. Agardh. Specifically, we investigated whether direct feeding and/or waterborne cues from feeding on neighboring conspecifics decreased the palatability of the tested algae. Direct feeding by the local isopod Idotea baltica triggered the induction of chemical defense in Fur. lumbricalis, D. sanguinea, P. pseudoceranoides, F. serratus, and F. evanescens. Conversely, we did not find any evidence for waterborne cues associated with feeding to trigger defense induction in neighboring conspecifics.     

Colour polymorphism and genetic variation in Idotea baltica populations from the Adriatic Sea and Baltic Sea

Phenotypic and genetic variation was studied in two of the four European subspecies of the marine isopod Idotea baltica; the Mediterranean I. b. basteri and the Baltic I. b. baltica. Spatial and temporal patterns of colour polymorphism were analysed in northern Adriatic and western Baltic Sea populations. Pronounced differences in phenotype composition were observed between populations of both subspecies as seen in the distribution of various colour variants bilineata, lineata, flavafusca and several combined forms). Compared with Adriatic samples, western Baltic Sea populations show higher phenotypic diversity. To obtain an estimate of the degree of genetic divergence between the subspecies, 12 gene-enzyme systems were investigated electrophoretically. The results obtained indicate a relatively high level of genetic variation; I. b. basteri from the nothern Adriatic tends to be more polymorphic and more heterozygous than I. b. baltica from the western Baltic. Both subspecies share identical electrophoretic mobilities of the homologous enzyme proteins examined; however, in allelic composition they exhibit significant differences at approximately half the number of loci scored. The genetic distance (Nei's D) measured at the subspecific level was 0.04. Amounts and geographical patterns of variation, observed both in colour phenotype and electrophoretic variation, are considered.