Marine heatwaves and upwelling shape stress responses in a keystone predator.

Climate change increases the frequency and intensifies the magnitude and duration of extreme events in the sea, particularly so in coastal habitats. However, the interplay of multiple extremes and the consequences for species and ecosystems remain unknown. We experimentally tested the impacts of summer heatwaves of differing intensities and durations, and a subsequent upwelling event on a temperate keystone predator, the starfish Asterias rubens. We recorded mussel consumption throughout the experiment and assessed activity and growth at strategically chosen time points. The upwelling event overall impaired starfish feeding and activity, likely driven by the acidification and low oxygen concentrations in the upwelled seawater. Prior exposure to a present-day heatwave (+5°C above climatology) alleviated upwelling-induced stress, indicating cross-stress tolerance. Heatwaves of present-day intensity decreased starfish feeding and growth. While the imposed heatwaves of limited duration (9 days) caused slight impacts but allowed for recovery, the prolonged (13 days) heatwave impaired overall growth. Projected future heatwaves (+8°C above climatology) caused 100% mortality of starfish. Our findings indicate a positive ecological memory imposed by successive stress events. Yet, starfish populations may still suffer extensive mortality during intensified end-of-century heatwave conditions.

Role of hydrodynamics in shaping chemical habitats and modulating the responses of coastal benthic systems to ocean global change.

Marine coastal zones are highly productive, and dominated by engineer species (e.g. macrophytes, molluscs, corals) that modify the chemistry of their surrounding seawater via their metabolism, causing substantial fluctuations in oxygen, dissolved inorganic carbon, pH, and nutrients. The magnitude of these biologically driven chemical fluctuations is regulated by hydrodynamics, can exceed values predicted for the future open ocean, and creates chemical patchiness in subtidal areas at various spatial (µm to meters) and temporal (minutes to months) scales. Although the role of hydrodynamics is well explored for planktonic communities, its influence as a crucial driver of benthic organism and community functioning is poorly addressed, particularly in the context of ocean global change. Hydrodynamics can directly modulate organismal physiological activity or indirectly influence an organism's performance by modifying its habitat. This review addresses recent developments in (i) the influence of hydrodynamics on the biological activity of engineer species, (ii) the description of chemical habitats resulting from the interaction between hydrodynamics and biological activity, (iii) the role of these chemical habitat as refugia against ocean acidification and deoxygenation, and (iv) how species living in such chemical habitats may respond to ocean global change. Recommendations are provided to integrate the effect of hydrodynamics and environmental fluctuations in future research, to better predict the responses of coastal benthic ecosystems to ongoing ocean global change.

Effects of first intermediate host density, host size and salinity on trematode infections in mussels of the south-western Baltic Sea.

Trematode prevalence and abundance in hosts are known to be affected by biotic drivers as well as by abiotic drivers. In this study, we used the unique salinity gradient found in the south-western Baltic Sea to: (i) investigate patterns of trematode infections in the first intermediate host, the periwinkle Littorina littorea and in the downstream host, the mussel Mytilus edulis, along a regional salinity gradient (from 13 to 22) and (ii) evaluate the effects of first intermediate host (periwinkle) density, host size and salinity on trematode infections in mussels. Two species dominated the trematode community, Renicola roscovita and Himasthla elongata. Salinity, mussel size and density of infected periwinkles were significantly correlated with R. roscovita, and salinity and density correlated with H. elongata abundance. These results suggest that salinity, first intermediate host density and host size play an important role in determining infection levels in mussels, with salinity being the main major driver. Under expected global change scenarios, the predicted freshening of the Baltic Sea might lead to reduced trematode transmission, which may be further enhanced by a potential decrease in periwinkle density and mussel size.

Warming and temperature variability determine the performance of two invertebrate predators.

In a warming ocean, temperature variability imposes intensified peak stress, but offers periods of stress release. While field observations on organismic responses to heatwaves are emerging, experimental evidence is rare and almost lacking for shorter-scale environmental variability. For two major invertebrate predators, we simulated sinusoidal temperature variability (±3 °C) around todays' warm summer temperatures and around a future warming scenario (+4 °C) over two months, based on high-resolution 15-year temperature data that allowed implementation of realistic seasonal temperature shifts peaking midpoint. Warming decreased sea stars' (Asterias rubens) energy uptake (Mytilus edulis consumption) and overall growth. Variability around the warming scenario imposed additional stress onto Asterias leading to an earlier collapse in feeding under sinusoidal fluctuations. High-peak temperatures prevented feeding, which was not compensated during phases of stress release (low-temperature peaks). In contrast, increased temperatures increased feeding on Mytilus but not growth rates of the recent invader Hemigrapsus takanoi, irrespective of the scale at which temperature variability was imposed. This study highlights species-specific impacts of warming and identifies temperature variability at the scale of days to weeks/months as important driver of thermal responses. When species' thermal limits are exceeded, temperature variability represents an additional source of stress as seen from future warming scenarios.

Response of foundation macrophytes to near-natural simulated marine heatwaves.

Marine heatwaves have been observed worldwide and are expected to increase in both frequency and intensity due to climate change. Such events may cause ecosystem reconfigurations arising from species range contraction or redistribution, with ecological, economic and social implications. Macrophytes such as the brown seaweed Fucus vesiculosus and the seagrass Zostera marina are foundation species in many coastal ecosystems of the temperate northern hemisphere. Hence, their response to extreme events can potentially determine the fate of associated ecosystems. Macrophyte functioning is intimately linked to the maintenance of photosynthesis, growth and reproduction, and resistance against pathogens, epibionts and grazers. We investigated morphological, physiological, pathological and chemical defence responses of western Baltic Sea F. vesiculosus and Z. marina populations to simulated near-natural marine heatwaves. Along with (a) the control, which constituted no heatwave but natural stochastic temperature variability (0HW), two treatments were applied: (b) two late-spring heatwaves (June, July) followed by a summer heatwave (August; 3HW) and (c) a summer heatwave only (1HW). The 3HW treatment was applied to test whether preconditioning events can modulate the potential sensitivity to the summer heatwave. Despite the variety of responses measured in both species, only Z. marina growth was impaired by the accumulative heat stress imposed by the 3HW treatment. Photosynthetic rate, however, remained high after the last heatwave indicating potential for recovery. Only epibacterial abundance was significantly affected in F. vesiculosus. Hence both macrophytes, and in particular F. vesiculosus, seem to be fairly tolerant to short-term marine heatwaves at least at the intensities applied in this experiment (up to 5°C above mean temperature over a period of 9 days). This may partly be due to the fact that F. vesiculosus grows in a highly variable environment, and may have a high phenotypic plasticity.

Impact of warming on biofouling communities in the northern Persian Gulf.

While the impact of ocean warming on single species is well described, the impact on marine biofouling communities is not well understood. Effluents of power plants have higher temperatures and can be used as natural large-scale test sites to investigate warming effects on marine ecosystems. In the present study, we evaluated the impact of elevated temperatures in the vicinity of a power plant on macro-biofouling communities in the northern coast of the Persian Gulf. The impact site was on average 2 °C warmer than the control site. Our results demonstrate a significantly different structure and composition of biofouling communities between control and impact sites. Warming led to a 1.5-fold increase in the mean coverage of biofouling communities and slightly decreased functional and species richness. Our results indicated that future warming will likely increase biofouling pressure, while decreasing diversity of communities, particularly in habitats where organisms exist at their upper tolerance limits of temperature.

Heat waves and their significance for a temperate benthic community: A near-natural experimental approach.

Climate change will not only shift environmental means but will also increase the intensity of extreme events, exerting additional stress on ecosystems. While field observations on the ecological consequences of heat waves are emerging, experimental evidence is rare, and lacking at the community level. Using a novel "near-natural" outdoor mesocosms approach, this study tested whether marine summer heat waves have detrimental consequences for macrofauna of a temperate coastal community, and whether sequential heat waves provoke an increase or decrease of sensitivity to thermal stress. Three treatments were applied, defined and characterized through a statistical analysis of 15 years of temperature records from the experimental site: (1) no heat wave, (2) two heat waves in June and July followed by a summer heat wave in August and (3) the summer heat wave only. Overall, 50% of the species showed positive, negative or positive/negative responses in either abundance and/or biomass. We highlight four possible ways in which single species responded to either three subsequent heat waves or one summer heat wave: (1) absence of a response (tolerance, 50% of species), (2) negative accumulative effects by three subsequent heat waves (tellinid bivalve), (3) buffering by proceeding heat waves due to acclimation and/or shifts in phenology (spionid polychaete) and (4) an accumulative positive effect by subsequent heat waves (amphipod). The differential responses to single or sequential heat waves at the species level entailed shifts at the community level. Community-level differences between single and triple heat waves were more pronounced than those between regimes with vs. without heat waves. Detritivory was reduced by the single heat wave while suspension feeding was less common in the triple heat wave regime. Critical extreme events occur already today and will occur more frequently in a changing climate, thus, leading to detrimental impacts on coastal marine systems.

Long-term exposure to acidification disrupts reproduction in a marine invertebrate.

Climate change research is advancing to more complex and more comprehensive studies that include long-term experiments, multiple life-history stages, multi-population, and multi-trait approaches. We used a population of the barnacle Balanus improvisus known to be sensitive to short-term acidification to determine its potential for long-term acclimation to acidification. We reared laboratory-bred individuals (as singles or pairs), and field-collected assemblages of barnacles, at pH 8.1 and 7.5 (≈ 400 and 1600 µatm pCO2 respectively) for up to 16 months. Acidification caused strong mortality and reduced growth rates. Acidification suppressed respiration rates and induced a higher feeding activity of barnacles after 6 months, but this suppression of respiration rate was absent after 15 months. Laboratory-bred barnacles developed mature gonads only when they were held in pairs, but nonetheless failed to produce fertilized embryos. Field-collected barnacles reared in the laboratory for 8 months at the same pH's developed mature gonads, but only those in pH 8.1 produced viable embryos and larvae. Because survivors of long-term acidification were not capable of reproducing, this demonstrates that B. improvisus can only partially acclimate to long-term acidification. This represents a clear and significant bottleneck in the ontogeny of this barnacle population that may limit its potential to persist in a future ocean.

A new flow-through bioassay for testing low-emission antifouling coatings.

Current antifouling (AF) technologies are based on the continuous release of biocides into the water, and consequently discharge into the environment. Major efforts to develop more environmentally friendly coatings require efficient testing in laboratory assays, followed by field studies. Barnacles are important fouling organisms worldwide, increasing hydrodynamic drag on ships and damaging coatings on underwater surfaces, and thus are extensively used as models in AF research, mostly in static, laboratory-based systems. Reliable flow-through test assays for the screening of biocide-containing AF paints, however, are rare. Herein, a flow-through bioassay was developed to screen for diverse low-release biocide paints, and to evaluate their effects on pre- and post-settlement traits in barnacles. The assay distinguishes between the effects from direct surface contact and bulk-water effects, which are crucial when developing low-emission AF coatings. This flow-through bioassay adds a new tool for rapid laboratory-based first-stage screening of candidate compounds and novel AF formulations.

Population and life-stage specific sensitivities to temperature and salinity stress in barnacles.

Temperature and salinity shape the distribution and genetic structure of marine communities. Future warming and freshening will exert an additional stress to coastal marine systems. The extent to which organisms respond to these shifts will, however, be mediated by the tolerances of all life-stages and populations of species and their potential to adapt. We investigated nauplius and cypris larvae of the barnacle Balanus (Amphibalanus) improvisus from the Swedish west coast with respect to temperature (12, 20, and 28 °C) and salinity (5, 15, and 30) tolerances. Warming accelerated larval development and increased overall survival and subsequent settlement success. Nauplii developed and metamorphosed best at intermediate salinity. This was also observed in cypris larvae when the preceding nauplii stages had been reared at a salinity of 30. Direct comparisons of the present findings with those on a population from the more brackish Baltic Sea demonstrate contrasting patterns. We conclude that i) B. improvisus larvae within the Baltic region will be favoured by near-future seawater warming and freshening, that ii) salinity tolerances of larvae from the two different populations reflect salinities in their native habitats, but are nonetheless suboptimal and that iii) this species is generally highly plastic with regard to salinity.

Habitat traits and food availability determine the response of marine invertebrates to ocean acidification.

Energy availability and local adaptation are major components in mediating the effects of ocean acidification (OA) on marine species. In a long-term study, we investigated the effects of food availability and elevated pCO2 (ca. 400, 1000 and 3000 µatm) on growth of newly settled Amphibalanus (Balanus) improvisus to reproduction, and on their offspring. We also compared two different populations, which were presumed to differ in their sensitivity to pCO2 due to differing habitat conditions: Kiel Fjord, Germany (Western Baltic Sea) with naturally strong pCO2 fluctuations, and the Tjärnö Archipelago, Sweden (Skagerrak) with far lower fluctuations. Over 20 weeks, survival, growth, reproduction and shell strength of Kiel barnacles were all unaffected by elevated pCO2 , regardless of food availability. Moulting frequency and shell corrosion increased with increasing pCO2 in adults. Larval development and juvenile growth of the F1 generation were tolerant to increased pCO2 , irrespective of parental treatment. In contrast, elevated pCO2 had a strong negative impact on survival of Tjärnö barnacles. Specimens from this population were able to withstand moderate levels of elevated pCO2 over 5 weeks when food was plentiful but showed reduced growth under food limitation. Severe levels of elevated pCO2 negatively impacted growth of Tjärnö barnacles in both food treatments. We demonstrate a conspicuously higher tolerance to elevated pCO2 in Kiel barnacles than in Tjärnö barnacles. This tolerance was carried over from adults to their offspring. Our findings indicate that populations from fluctuating pCO2 environments are more tolerant to elevated pCO2 than populations from more stable pCO2 habitats. We furthermore provide evidence that energy availability can mediate the ability of barnacles to withstand moderate CO2 stress. Considering the high tolerance of Kiel specimens and the possibility to adapt over many generations, near future OA alone does not seem to present a major threat for A. improvisus.

Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments.

Ocean acidification is expected to decrease calcification rates of bivalves. Nevertheless, in many coastal areas high pCO2 variability is encountered already today. Kiel Fjord (Western Baltic Sea) is a brackish (12-20 g kg(-1) ) and CO2 enriched habitat, but the blue mussel Mytilus edulis dominates the benthic community. In a coupled field and laboratory study we examined the annual pCO2 variability in this habitat and the combined effects of elevated pCO2 and food availability on juvenile M. edulis growth and calcification. In the laboratory experiment, mussel growth and calcification were found to chiefly depend on food supply, with only minor impacts of pCO2 up to 3350 µatm. Kiel Fjord was characterized by strong seasonal pCO2 variability. During summer, maximal pCO2 values of 2500 µatm were observed at the surface and >3000 µatm at the bottom. However, the field growth experiment revealed seven times higher growth and calcification rates of M. edulis at a high pCO2 inner fjord field station (mean pCO2 ca. 1000 µatm) in comparison to a low pCO2 outer fjord station (ca. 600 µatm). In addition, mussels were able to out-compete the barnacle Amphibalanus improvisus at the high pCO2 site. High mussel productivity at the inner fjord site was enabled by higher particulate organic carbon concentrations. Kiel Fjord is highly impacted by eutrophication, which causes bottom water hypoxia and consequently high seawater pCO2 . At the same time, elevated nutrient concentrations increase the energy availability for filter feeding organisms such as mussels. Thus, M. edulis can dominate over a seemingly more acidification resistant species such as A. improvisus. We conclude that benthic stages of M. edulis tolerate high ambient pCO2 when food supply is abundant and that important habitat characteristics such as species interactions and energy availability need to be considered to predict species vulnerability to ocean acidification.