Ocean acidification reduces thallus strength in a non-calcifying foundation seaweed.

Climate change is causing unprecedented changes in terrestrial and aquatic ecosystems through the emission of greenhouse gases, including carbon dioxide (CO2). Approximately 30% of CO2 is taken up by the ocean ('ocean acidification', OA)1, which has profound effects on foundation seaweed species. Negative physical effects on calcifying algae are clear2, but studies on habitat-forming fleshy seaweeds have mainly focused on growth and less on thallus strength3,4. We exposed the habitat-forming brown seaweed Fucus vesiculosus to OA corresponding to projected climate change effects for the year 2100, and observed reduced apical thallus strength and greater loss of exposed individuals in the field. The tissue contained less calcium and magnesium, both of which are important for creating structural alginate matrices. Scanning electron microscopy (SEM) revealed tissue voids in the OA samples that were not present in seaweeds grown under ambient pCO2. We conclude that under OA, weakened F. vesiculosus will be at a significantly higher risk of physical damage and detachment.

Salinity and host drive Ulva-associated bacterial communities across the Atlantic-Baltic Sea gradient.

The green seaweed Ulva is a model system to study seaweed-bacteria interactions, but the impact of environmental drivers on the dynamics of these interactions is little understood. In this study, we investigated the stability and variability of the seaweed-associated bacteria across the Atlantic-Baltic Sea salinity gradient. We characterized the bacterial communities of 15 Ulva sensu lato species along 2,000 km of coastline in a total of 481 samples. Our results demonstrate that the Ulva-associated bacterial composition was strongly structured by both salinity and host species (together explaining between 34% and 91% of the variation in the abundance of the different bacterial genera). The largest shift in the bacterial consortia coincided with the horohalinicum (5-8 PSU, known as the transition zone from freshwater to marine conditions). Low-salinity communities especially contained high relative abundances of Luteolibacter, Cyanobium, Pirellula, Lacihabitans and an uncultured Spirosomaceae, whereas high-salinity communities were predominantly enriched in Litorimonas, Leucothrix, Sulfurovum, Algibacter and Dokdonia. We identified a small taxonomic core community (consisting of Paracoccus, Sulfitobacter and an uncultured Rhodobacteraceae), which together contributed to 14% of the reads per sample, on average. Additional core taxa followed a gradient model, as more core taxa were shared between neighbouring salinity ranges than between ranges at opposite ends of the Atlantic-Baltic Sea gradient. Our results contradict earlier statements that Ulva-associated bacterial communities are taxonomically highly variable across individuals and largely stochastically defined. Characteristic bacterial communities associated with distinct salinity regions may therefore facilitate the host's adaptation across the environmental gradient.

In vitro digestibility and Caco-2 cell bioavailability of sea lettuce (Ulva fenestrata) proteins extracted using pH-shift processing.

Seaweed is a promising sustainable source of vegan protein as its farming does not require arable land, pesticides/insecticides, nor freshwater supply. However, to be explored as a novel protein source the content and nutritional quality of protein in seaweed need to be improved. We assessed the influence of pH-shift processing on protein degree of hydrolysis (%DH), protein/peptide size distribution, accessibility, and cell bioavailability of Ulva fenestrata proteins after in vitro gastrointestinal digestion. pH-shift processing of Ulva, which concentrated its proteins 3.5-times, significantly improved the %DH from 27.7±2.6% to 35.7±2.1% and the amino acid accessibility from 56.9±4.1% to 72.7±0.6%. Due to the higher amino acid accessibility, the amount of most amino acids transported across the cell monolayers was higher in the protein extracts. Regarding bioavailability, both Ulva and protein extracts were as bioavailable as casein. The protein/peptide molecular size distribution after digestion did not disclose a clear association with bioavailability.

Ocean acidification decreases grazing pressure but alters morphological structure in a dominant coastal seaweed.

Ocean acidification driven by anthropogenic climate change is causing a global decrease in pH, which is projected to be 0.4 units lower in coastal shallow waters by the year 2100. Previous studies have shown that seaweeds grown under such conditions may alter their growth and photosynthetic capacity. It is not clear how such alterations might impact interactions between seaweed and herbivores, e.g. through changes in feeding rates, nutritional value, or defense levels. Changes in seaweeds are particularly important for coastal food webs, as they are key primary producers and often habitat-forming species. We cultured the habitat-forming brown seaweed Fucus vesiculosus for 30 days in projected future pCO2 (1100 µatm) with genetically identical controls in ambient pCO2 (400 µatm). Thereafter the macroalgae were exposed to grazing by Littorina littorea, acclimated to the relevant pCO2-treatment. We found increased growth (measured as surface area increase), decreased tissue strength in a tensile strength test, and decreased chemical defense (phlorotannins) levels in seaweeds exposed to high pCO2-levels. The herbivores exposed to elevated pCO2-levels showed improved condition index, decreased consumption, but no significant change in feeding preference. Fucoid seaweeds such as F. vesiculosus play important ecological roles in coastal habitats and are often foundation species, with a key role for ecosystem structure and function. The change in surface area and associated decrease in breaking force, as demonstrated by our results, indicate that F. vesiculosus grown under elevated levels of pCO2 may acquire an altered morphology and reduced tissue strength. This, together with increased wave energy in coastal ecosystems due to climate change, could have detrimental effects by reducing both habitat and food availability for herbivores.

Natural populations of shipworm larvae are attracted to wood by waterborne chemical cues.

The life cycle of many sessile marine invertebrates includes a dispersive planktonic larval stage whose ability to find a suitable habitat in which to settle and transform into benthic adults is crucial to maximize fitness. To facilitate this process, invertebrate larvae commonly respond to habitat-related chemical cues to guide the search for an appropriate environment. Furthermore, small-scale hydrodynamic conditions affect dispersal of chemical cues, as well as swimming behavior of invertebrate larvae and encounter with potential habitats. Shipworms within the family Teredinidae are dependent on terrestrially derived wood in order to complete their life cycle, but very little is known about the cues and processes that promote settlement. We investigated the potential for remote detection of settling substrate via waterborne chemical cues in teredinid larvae through a combination of empirical field and laboratory flume experiments. Natural populations of teredinid larvae were significantly more abundant close to wooden structures enclosed in plankton net compared to empty control nets, clearly showing that shipworm larvae can sense and respond to chemical cues associated with suitable settling substrate in the field. However, the flume experiments, using ecologically relevant flow velocities, showed that the boundary layer around experimental wooden panels was thin and that the mean flow velocity exceeded larval swimming velocity approximately 5 mm (≈ 25 larval body lengths) from the panel surface. Therefore, we conclude that the scope for remote detection of waterborne cues is limited and that the likely explanation for the higher abundance of shipworm larvae associated with the wooden panels in the field is a response to a cue during or after attachment on, or very near, the substrate. Waterborne cues probably guide the larva in its decision to remain attached and settle, or to detach and continue swimming and drifting until the next encounter with a solid substrate.

Acquired phototrophy through retention of functional chloroplasts increases growth efficiency of the sea slug Elysia viridis.

Photosynthesis is a fundamental process sustaining heterotrophic organisms at all trophic levels. Some mixotrophs can retain functional chloroplasts from food (kleptoplasty), and it is hypothesized that carbon acquired through kleptoplasty may enhance trophic energy transfer through increased host growth efficiency. Sacoglossan sea slugs are the only known metazoans capable of kleptoplasty, but the relative fitness contributions of heterotrophy through grazing, and phototrophy via kleptoplasts, are not well understood. Fitness benefits (i.e. increased survival or growth) of kleptoplasty in sacoglossans are commonly studied in ecologically unrealistic conditions under extended periods of complete darkness and/or starvation. We compared the growth efficiency of the sacoglossan Elysia viridis with access to algal diets providing kleptoplasts of differing functionality under ecologically relevant light conditions. Individuals fed Codium fragile, which provide highly functional kleptoplasts, nearly doubled their growth efficiency under high compared to low light. In contrast, individuals fed Cladophora rupestris, which provided kleptoplasts of limited functionality, showed no difference in growth efficiency between light treatments. Slugs feeding on Codium, but not on Cladophora, showed higher relative electron transport rates (rETR) in high compared to low light. Furthermore, there were no differences in the consumption rates of the slugs between different light treatments, and only small differences in nutritional traits of algal diets, indicating that the increased growth efficiency of E. viridis feeding on Codium was due to retention of functional kleptoplasts. Our results show that functional kleptoplasts from Codium can provide sacoglossan sea slugs with fitness advantages through photosynthesis.

Individual specialization to non-optimal hosts in a polyphagous marine invertebrate herbivore.

Factors determining the degree of dietary generalism versus specialism are central in ecology. Species that are generalists at the population level may in fact be composed of specialized individuals. The optimal diet theory assumes that individuals choose diets that maximize fitness, and individual specialization may occur if individuals' ability to locate, recognize, and handle different food types differ. We investigate if individuals of the marine herbivorous slug Elysia viridis, which co-occur at different densities on several green macroalgal species in the field, are specialized to different algal hosts. Individual slugs were collected from three original algal host species (Cladophora sericea, Cladophora rupestris and Codium fragile) in the field, and short-term habitat choice and consumption, as well as long-term growth (proxy for fitness), on four algal diet species (the original algal host species and Chaetomorpha melagonium) were studied in laboratory experiments. Nutritional (protein, nitrogen, and carbon content) and morphological (dry weight, and cell/utricle volume) algal traits were also measured to investigate if they correlated with the growth value of the different algal diets. E. viridis individuals tended to choose and consume algal species that were similar to their original algal host. Long-term growth of E. viridis, however, was mostly independent of original algal host, as all individuals reached a larger size on the non-host C. melagonium. E. viridis growth was positively correlated to algal cell/utricle volume but not to any of the other measured algal traits. Because E. viridis feeds by piercing individual algal cells, the results indicate that slugs may receive more cytoplasm, and thus more energy per unit time, on algal species with large cells/utricles. We conclude that E. viridis individuals are specialized on different hosts, but host choice in natural E. viridis populations is not determined by the energetic value of seaweed diets as predicted by the ODT.

Abundance and size distribution of the sacoglossan Elysia viridis on co-occurring algal hosts on the Swedish west coast.

Sacoglossans are specialized marine herbivores that tend to have a close evolutionary relationship with their macroalgal hosts, but the widely distributed species Elysia viridis can associate with several algal species. However, most previous investigations on the field abundance and size distribution of E. viridis have focussed on Codium spp. in the British Isles, and algae from this genus are considered superior hosts for E. viridis. In the present study, we investigated the abundance and size distribution of E. viridis on 6 potential host algae with differing morphologies (the septate species Cladophora sericea, Cladophora rupestris, Chaetomorpha melagonium, and Ceramium virgatum, as well as the siphonaceous species Codium fragile and Bryopsis sp.) at 2 sites on the Swedish west coast over the course of a year. In spring, slugs were almost absent from all algal hosts. In summer and autumn, E. viridis consistently occurred on several of the algal species at both sites. The highest number of small E. viridis were found on C. sericea, intermediate numbers of significantly larger E. viridis were found on C. rupestris, while fewer, intermediate sized animals were found on C. fragile. Throughout the study period, only a few E. viridis individuals were found on C. melagonium, Bryopsis sp., and C. virgatum. Our results indicate that E. viridis is an annual species in Sweden, capable of exploiting co-occurring congeneric and intergeneric algal hosts with differing morphologies. These results corroborate previous findings that E. viridis can exploit several different algal species, but does not indicate that C. fragile is a superior host.

Mesoherbivores reduce net growth and induce chemical resistance in natural seaweed populations.

Herbivory on marine macroalgae (seaweeds) in temperate areas is often dominated by relatively small gastropods and crustaceans (mesoherbivores). The effects of these herbivores on the performance of adult seaweeds have so far been almost exclusively investigated under artificial laboratory conditions. Furthermore, several recent laboratory studies with mesoherbivores indicate that inducible chemical resistance may be as common in seaweeds as in vascular plants. However, in order to further explore and test the possible ecological significance of induced chemical resistance in temperate seaweeds, data are needed that address this issue in natural populations. We investigated the effect of grazing by littorinid herbivorous snails (Littorina spp.) on the individual net growth of the brown seaweed Ascophyllum nodosum in natural field populations. Furthermore, the capacity for induced resistance in the seaweeds was assessed by removing herbivores and assaying for relaxation of defences. We found that ambient densities of gastropod herbivores significantly reduced net growth by 45% in natural field populations of A. nodosum. Seaweeds previously exposed to grazing in the field were less consumed by gastropod herbivores in feeding bioassays. Furthermore, the concentration of phlorotannins (polyphenolics), which have been shown to deter gastropod herbivores, was higher in the seaweeds that were exposed to gastropod herbivores in the field. This field study corroborates earlier laboratory experiments and demonstrates that it is important to make sure that the lack of experimental field data on marine mesoherbivory does not lead to rash conclusions about the lack of significant effects of these herbivores on seaweed performance. The results strongly suggest that gastropods exert a significant selection pressure on the evolution of defensive traits in the seaweeds, and that brown seaweeds can respond to attacks by natural densities of these herbivores through increased chemical resistance to further grazing.

Marine dinoflagellates show induced life-history shifts to escape parasite infection in response to water-borne signals.

Many dinoflagellate species form dormant resting cysts as a part of their life cycle, and in some freshwater species, hatching of these cysts can be delayed by the presence of water-borne signals from grazing zooplankton. Some marine dinoflagellates can form temporary cysts, which may function to resist unfavourable short-term environmental conditions. We investigated whether the marine dinoflagellate Alexandrium ostenfeldii is able to induce an increased resistance to the parasitic flagellate Parvilucifera infectans by forming temporary cysts. We performed several laboratory experiments where dinoflagellates were exposed either to direct contact with parasites or to filtered water from cultures of parasite-infected conspecifics (parasite-derived signals). Infection by P. infectans is lethal to motile A. ostenfeldii cells, but temporary cysts were more resistant to parasite infection. Furthermore, A. ostenfeldii induced a shift in life-history stage (from motile cells to temporary cysts) when exposed to parasite-derived water-borne signals. The response was relaxed within a couple of hours, indicating that A. ostenfeldii may use this behaviour as a short-term escape mechanism to avoid parasite infection. The results suggest that intraspecies chemical communication evoked by biotic interactions can be an important mechanism controlling life-history shifts in marine dinoflagellates, which may have implications for the development of toxic algal blooms.