Limited predatory effects on infaunal macrobenthos community patterns in intertidal soft-bottom of Arctic coasts.

Predation shapes marine benthic communities and affects prey species population dynamics in tropic and temperate coastal systems. However, information on its magnitude in systematically understudied Arctic coastal habitats is scarce. To test predation effects on the diversity and structure of Arctic benthic communities, we conducted caging experiments in which consumers were excluded from plots at two intertidal sedimentary sites in Svalbard (Longyearbyen and Thiisbukta) for 2.5 months. Unmanipulated areas served as controls and partial (open) cages were used to estimate potential cage effects. At the end of the experiment, we took one sediment core from each plot and quantified total biomass and the number of each encountered taxon. At both sites, the experimental exclusion of predators slightly changed the species composition of communities and had negligible effects on biomass, total abundance, species richness, evenness, and Shannon Index. In addition, we found evidence for cage effects, and spatial variability in the intensity of the predation effects was identified. Our study suggests that predators have limited effects on the structure of the studied intertidal macrobenthic Arctic communities, which is different from coastal soft-bottom ecosystems at lower latitudes.

Geographic variation in fitness-related traits of the bladderwrack Fucus vesiculosus along the Baltic Sea-North Sea salinity gradient.

In the course of the ongoing global intensification and diversification of human pressures, the study of variation patterns of biological traits along environmental gradients can provide relevant information on the performance of species under shifting conditions. The pronounced salinity gradient, co-occurrence of multiple stressors, and accelerated rates of change make the Baltic Sea and its transition to North Sea a suitable region for this type of study. Focusing on the bladderwrack Fucus vesiculosus, one of the main foundation species on hard-bottoms of the Baltic Sea, we analyzed the phenotypic variation among populations occurring along 2,000 km of coasts subjected to salinities from 4 to >30 and a variety of other stressors. Morphological and biochemical traits, including palatability for grazers, were recorded at 20 stations along the Baltic Sea and four stations in the North Sea. We evaluated in a common modeling framework the relative contribution of multiple environmental drivers to the observed trait patterns. Salinity was the main and, in some cases, the only environmental driver of the geographic trait variation in F. vesiculosus. The decrease in salinity from North Sea to Baltic Sea stations was accompanied by a decline in thallus size, photosynthetic pigments, and energy storage compounds, and affected the interaction of the alga with herbivores and epibiota. For some traits, drivers that vary locally such as wave exposure, light availability or nutrient enrichment were also important. The strong genetic population structure in this macroalgae might play a role in the generation and maintenance of phenotypic patterns across geographic scales. In light of our results, the desalination process projected for the Baltic Sea could have detrimental impacts on F. vesiculosus in areas close to its tolerance limit, affecting ecosystem functions such as habitat formation, primary production, and food supply.

Adult Prey Neutralizes Predator Nonconsumptive Limitation of Prey Recruitment.

Recent studies have shown that predator chemical cues can limit prey demographic rates such as recruitment. For instance, barnacle pelagic larvae reduce settlement where predatory dogwhelk cues are detected, thereby limiting benthic recruitment. However, adult barnacles attract conspecific larvae through chemical and visual cues, aiding larvae to find suitable habitat for development. Thus, we tested the hypothesis that the presence of adult barnacles (Semibalanus balanoides) can neutralize dogwhelk (Nucella lapillus) nonconsumptive effects on barnacle recruitment. We did a field experiment in Atlantic Canada during the 2012 and 2013 barnacle recruitment seasons (May-June). We manipulated the presence of dogwhelks (without allowing them to physically contact barnacles) and adult barnacles in cages established in rocky intertidal habitats. At the end of both recruitment seasons, we measured barnacle recruit density on tiles kept inside the cages. Without adult barnacles, the nearby presence of dogwhelks limited barnacle recruitment by 51%. However, the presence of adult barnacles increased barnacle recruitment by 44% and neutralized dogwhelk nonconsumptive effects on barnacle recruitment, as recruit density was unaffected by dogwhelk presence. For species from several invertebrate phyla, benthic adult organisms attract conspecific pelagic larvae. Thus, adult prey might commonly constitute a key factor preventing negative predator nonconsumptive effects on prey recruitment.

Specificity in Mesograzer-Induced Defences in Seagrasses.

Grazing-induced plant defences that reduce palatability to herbivores are widespread in terrestrial plants and seaweeds, but they have not yet been reported in seagrasses. We investigated the ability of two seagrass species to induce defences in response to direct grazing by three associated mesograzers. Specifically, we conducted feeding-assayed induction experiments to examine how mesograzer-specific grazing impact affects seagrass induction of defences within the context of the optimal defence theory. We found that the amphipod Gammarus insensibilis and the isopod Idotea chelipes exerted a low-intensity grazing on older blades of the seagrass Cymodocea nodosa, which reflects a weak grazing impact that may explain the lack of inducible defences. The isopod Synischia hectica exerted the strongest grazing impact on C. nodosa via high-intensity feeding on young blades with a higher fitness value. This isopod grazing induced defences in C. nodosa as indicated by a consistently lower consumption of blades previously grazed for 5, 12 and 16 days. The lower consumption was maintained when offered tissues with no plant structure (agar-reconstituted food), but showing a reduced size of the previous grazing effect. This indicates that structural traits act in combination with chemical traits to reduce seagrass palatability to the isopod. Increase in total phenolics but not in C:N ratio and total nitrogen of grazed C. nodosa suggests chemical defences rather than a modified nutritional quality as primarily induced chemical traits. We detected no induction of defences in Zostera noltei, which showed the ability to replace moderate losses of young biomass to mesograzers via compensatory growth. Our study provides the first experimental evidence of induction of defences against meso-herbivory that reduce further consumption in seagrasses. It also emphasizes the relevance of grazer identity in determining the level of grazing impact triggering resistance and compensatory responses of different seagrass species.

Predator nonconsumptive effects on prey recruitment weaken with recruit density.

We investigated the nonconsumptive effects (NCEs) of predatory dogwhelks (Nucella lapillus) on intertidal barnacle (Semibalanus balanoides) recruitment through field experiments on the Gulf of St. Lawrence coast and the Atlantic coast of Nova Scotia, Canada. We studied the recruitment seasons (May-June) of 2011 and 2013. In 2011, the Gulf coast had five times more nearshore phytoplankton (food for barnacle larvae and recruits) during the recruitment season and yielded a 58% higher barnacle recruit density than the Atlantic coast at the end of the recruitment season. In 2013, phytoplankton levels and barnacle recruit density were similar on both coasts and also lower than for the Gulf coast in 2011. Using the comparative-experimental method, the manipulation of dogwhelk presence (without allowing physical contact with prey) revealed that dogwhelk cues limited barnacle recruitment under moderate recruit densities (Atlantic 2011/2013 and Gulf 2013) but had no effect under a high recruit density (Gulf 2011). Barnacle recruits attract settling larvae through chemical cues. Thus, the highest recruit density appears to have neutralized dogwhelk effects. This study suggests that the predation risk perceived by settling larvae may decrease with increasing recruit density and that prey food supply may indirectly influence predator NCEs on prey recruitment.

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.

Induced resistance to periwinkle grazing in the brown seaweed Fucus vesiculosus (Phaeophyceae): molecular insights and seaweed-mediated effects on herbivore interactions.

Herbivory is a key factor for controlling seaweed biomass and community structure. To cope with grazers, constitutive and inducible defenses have evolved in macroalgae. Inducible chemical defenses show grazer-specificity and, at the same time, have the potential to mediate interactions among different herbivores. Furthermore, temporal variations in defense patterns, which may adjust antiherbivory responses to grazing pressure, were reported in two brown seaweeds. However, underlying cellular processes are only rudimentarily characterized. To investigate the response of Fucus vesiculosus (L.) to periwinkle (Littorina obtusata) grazing, feeding assays were conducted at several times during a 33 d induction experiment. Underlying cellular processes were analyzed through gene expression profiling. Furthermore, direct processes driving the antiherbivory response to periwinkle grazing and indirect effects on another herbivore, the isopod Idotea baltica, were elucidated. F. vesiculosus showed multiple defense pulses in response to periwinkle grazing, suggesting a high level of temporal variability in antiherbivory traits. Defense induction was accompanied by extensive transcriptome changes. Approximately 400 genes were significantly up-/down-regulated relative to controls, including genes relevant for translation and the cytoskeleton. Genes involved in photosynthesis were mostly down-regulated, while genes related to the respiratory chain were up-regulated, indicating alterations in resource allocation. The comparison of genes regulated in response to isopod (previous study) and periwinkle grazing suggests specific induction of several genes by each herbivore. However, grazing by both herbivores induced similar metabolic processes in F. vesiculosus. These common defense-related processes reflected in strong indirect effects as isopods were also repelled after previous grazing by L. obtusata.

Large-scale variation in combined impacts of canopy loss and disturbance on community structure and ecosystem functioning.

Ecosystems are under pressure from multiple human disturbances whose impact may vary depending on environmental context. We experimentally evaluated variation in the separate and combined effects of the loss of a key functional group (canopy algae) and physical disturbance on rocky shore ecosystems at nine locations across Europe. Multivariate community structure was initially affected (during the first three to six months) at six locations but after 18 months, effects were apparent at only three. Loss of canopy caused increases in cover of non-canopy algae in the three locations in southern Europe and decreases in some northern locations. Measures of ecosystem functioning (community respiration, gross primary productivity, net primary productivity) were affected by loss of canopy at five of the six locations for which data were available. Short-term effects on community respiration were widespread, but effects were rare after 18 months. Functional changes corresponded with changes in community structure and/or species richness at most locations and times sampled, but no single aspect of biodiversity was an effective predictor of longer-term functional changes. Most ecosystems studied were able to compensate in functional terms for impacts caused by indiscriminate physical disturbance. The only consistent effect of disturbance was to increase cover of non-canopy species. Loss of canopy algae temporarily reduced community resistance to disturbance at only two locations and at two locations actually increased resistance. Resistance to disturbance-induced changes in gross primary productivity was reduced by loss of canopy algae at four locations. Location-specific variation in the effects of the same stressors argues for flexible frameworks for the management of marine environments. These results also highlight the need to analyse how species loss and other stressors combine and interact in different environmental contexts.

Temporal dynamics of inducible anti-herbivory defenses in the brown seaweed Ascophyllum nodosum (Phaeophyceae)(1).

Anti-herbivory defenses support persistence of seaweeds. Little is known, however, about temporal dynamics in the induction of grazer-deterrent seaweed traits. In two induction experiments, consumption rates of the periwinkle Littorina obtusata (L.) on the brown seaweed Ascophyllum nodosum (L.) Le Jolis were measured in 3-d intervals. Changes in palatability of directly grazed A. nodosum were tested every 3 d with feeding assays using fresh and reconstituted seaweed pieces. Likewise, assays with fresh A. nodosum assessed changes in seaweed palatability in response to water-borne cues from nearby grazed conspecifics. Consumption rates of L. obtusata varied significantly during the 27-d induction phase of each experiment. Direct grazing by L. obtusata lowered palatability of fresh and reconstituted A. nodosum pieces to conspecific grazers after 15 d as well as after 6 and 12 d, respectively. After 12, 18, and 24 d, fresh A. nodosum located downstream of L. obtusata-grazed conspecifics was significantly less palatable than A. nodosum located downstream of ungrazed conspecifics. Changes in L. obtusata consumption rates and A. nodosum palatability during both induction experiments suggest temporal variation of grazer-deterrent responses, which may complicate experimental detection of inducible anti-herbivory defenses.

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.

Stressed but stable: canopy loss decreased species synchrony and metabolic variability in an intertidal hard-bottom community.

The temporal stability of aggregate community properties depends on the dynamics of the component species. Since species growth can compensate for the decline of other species, synchronous species dynamics can maintain stability (i.e. invariability) in aggregate properties such as community abundance and metabolism. In field experiments we tested the separate and interactive effects of two stressors associated with storminess--loss of a canopy-forming species and mechanical disturbances--on species synchrony and community respiration of intertidal hard-bottom communities on Helgoland Island, NE Atlantic. Treatments consisted of regular removal of the canopy-forming seaweed Fucus serratus and a mechanical disturbance applied once at the onset of the experiment in March 2006. The level of synchrony in species abundances was assessed from estimates of species percentage cover every three months until September 2007. Experiments at two sites consistently showed that canopy loss significantly reduced species synchrony. Mechanical disturbance had neither separate nor interactive effects on species synchrony. Accordingly, in situ measurements of CO(2)-fluxes showed that canopy loss, but not mechanical disturbances, significantly reduced net primary productivity and temporal variation in community respiration during emersion periods. Our results support the idea that compensatory dynamics may stabilise aggregate properties. They further suggest that the ecological consequences of the loss of a single structurally important species may be stronger than those derived from smaller-scale mechanical disturbances in natural ecosystems.

Variation in community structure across vertical intertidal stress gradients: how does it compare with horizontal variation at different scales?

In rocky intertidal habitats, the pronounced increase in environmental stress from low to high elevations greatly affects community structure, that is, the combined measure of species identity and their relative abundance. Recent studies have shown that ecological variation also occurs along the coastline at a variety of spatial scales. Little is known, however, on how vertical variation compares with horizontal variation measured at increasing spatial scales (in terms of sampling interval). Because broad-scale processes can generate geographical patterns in community structure, we tested the hypothesis that vertical ecological variation is higher than fine-scale horizontal variation but lower than broad-scale horizontal variation. To test this prediction, we compared the variation in community structure across intertidal elevations on rocky shores of Helgoland Island with independent estimates of horizontal variation measured at the scale of patches (quadrats separated by 10s of cm), sites (quadrats separated by a few m), and shores (quadrats separated by 100s to 1000s of m). The multivariate analyses done on community structure supported our prediction. Specifically, vertical variation was significantly higher than patch- and site-scale horizontal variation but lower than shore-scale horizontal variation. Similar patterns were found for the variation in abundance of foundation taxa such as Fucus spp. and Mastocarpus stellatus, suggesting that the effects of these canopy-forming algae, known to function as ecosystem engineers, may explain part of the observed variability in community structure. Our findings suggest that broad-scale processes affecting species performance increase ecological variability relative to the pervasive fine-scale patchiness already described for marine coasts and the well known variation caused by vertical stress gradients. Our results also indicate that experimental research aiming to understand community structure on marine shores should benefit from applying a multi-scale approach.

Stress ecology in fucus: abiotic, biotic and genetic interactions.

Stress regimes defined as the synchronous or sequential action of abiotic and biotic stresses determine the performance and distribution of species. The natural patterns of stress to which species are more or less well adapted have recently started to shift and alter under the influence of global change. This was the motivation to review our knowledge on the stress ecology of a benthic key player, the macroalgal genus Fucus. We first provide a comprehensive review of the genus as an ecological model including what is currently known about the major lineages of Fucus species with respect to hybridization, ecotypic differentiation and speciation; as well as life history, population structure and geographic distribution. We then review our current understanding of both extrinsic (abiotic/biotic) and intrinsic (genetic) stress(es) on Fucus species and how they interact with each other. It is concluded that (i) interactive stress effects appear to be equally distributed over additive, antagonistic and synergistic categories at the level of single experiments, but are predominantly additive when averaged over all studies in a meta-analysis of 41 experiments; (ii) juvenile and adult responses to stress frequently differ and (iii) several species or particular populations of Fucus may be relatively unaffected by climate change as a consequence of pre-adapted ecotypes that collectively express wide physiological tolerences. Future research on Fucus should (i) include additional species, (ii) include marginal populations as models for responses to environmental stress; (iii) assess a wider range of stress combinations, including their temporal fluctuations; (iv) better differentiate between stress sensitivity of juvenile versus adult stages; (v) include a functional genomic component in order to better integrate Fucus' ecological and evolutionary responses to stress regimes and (vi) utilize a multivariate modelling approach in order to develop and understand interaction networks.

Re-structuring of marine communities exposed to environmental change: a global study on the interactive effects of species and functional richness.

Species richness is the most commonly used but controversial biodiversity metric in studies on aspects of community stability such as structural composition or productivity. The apparent ambiguity of theoretical and experimental findings may in part be due to experimental shortcomings and/or heterogeneity of scales and methods in earlier studies. This has led to an urgent call for improved and more realistic experiments. In a series of experiments replicated at a global scale we translocated several hundred marine hard bottom communities to new environments simulating a rapid but moderate environmental change. Subsequently, we measured their rate of compositional change (re-structuring) which in the great majority of cases represented a compositional convergence towards local communities. Re-structuring is driven by mortality of community components (original species) and establishment of new species in the changed environmental context. The rate of this re-structuring was then related to various system properties. We show that availability of free substratum relates negatively while taxon richness relates positively to structural persistence (i.e., no or slow re-structuring). Thus, when faced with environmental change, taxon-rich communities retain their original composition longer than taxon-poor communities. The effect of taxon richness, however, interacts with another aspect of diversity, functional richness. Indeed, taxon richness relates positively to persistence in functionally depauperate communities, but not in functionally diverse communities. The interaction between taxonomic and functional diversity with regard to the behaviour of communities exposed to environmental stress may help understand some of the seemingly contrasting findings of past research.

The interaction between nutrient availability and disturbance frequency on the diversity of benthic marine communities on the north-east coast of England.

1. Several theoretical models predict under what conditions maximum species diversity can be maintained, and they are often used to develop effective ecosystem management plans. 2. Two models that are currently used to predict patterns of species diversity were empirically tested in marine subtidal benthic communities of different successional stages. 3. The two models were: the interactive effects of nutrient availability and disturbance frequency proposed by Kondoh (2001; Proceedings of the Royal Society London B, 268, 269-271), and the intermediate disturbance hypothesis (IDH) proposed by Connell (1978; Science, 199, 1302-1310). 4. Interactive effects were found to be transient and only occurred in the older communities, while the unimodal pattern suggested by the IDH was not supported in either successional stage. 5. It is concluded that these models are very general and thus lack sufficient explanatory power. Both models require a number of specific prerequisites for maximum diversity to be found, and though applicable in many different ecosystems they need to be refined as tools in order that they can be effectively used in habitat management plans.

Maximum species richness at intermediate frequencies of disturbance: consistency among levels of productivity.

Development of a mechanistic understanding and predictions of patterns of biodiversity is a central theme in ecology. One of the most influential theories, the intermediate disturbance hypothesis (IDH), predicts maximum diversity at intermediate levels of disturbance frequency. The dynamic equilibrium model (DEM), an extension of the IDH, predicts that the level of productivity determines at what frequency of disturbance maximum diversity occurs. To test, and contrast, the predictions of these two models, a field experiment on marine hard-substratum assemblages was conducted with seven levels of disturbance frequency and three levels of nutrient availability. Consistent with the IDH, maximum diversity, measured as species richness, was observed at an intermediate frequency of disturbance. Despite documented effects on productivity, the relationship between disturbance and diversity was not altered by the nutrient treatments. Thus, in this system the DEM did not improve the understanding of patterns of diversity compared to the IDH. Furthermore, it is suggested that careful consideration of measurements and practical definitions of productivity in natural assemblages is necessary for a rigorous test of the DEM.