Gene regulatory response to hyposalinity in the brown seaweed Fucus vesiculosus.

BACKGROUND: Rockweeds are among the most important foundation species of temperate rocky littoral shores. In the Baltic Sea, the rockweed Fucus vesiculosus is distributed along a decreasing salinity gradient from the North Atlantic entrance to the low-salinity regions in the north-eastern margins, thus, demonstrating a remarkable tolerance to hyposalinity. The underlying mechanisms for this tolerance are still poorly understood. Here, we exposed F. vesiculosus from two range-margin populations to the hyposaline (2.5 PSU - practical salinity unit) conditions that are projected to occur in the region by the end of this century as a result of climate change. We used transcriptome analysis (RNA-seq) to determine the gene expression patterns associated with hyposalinity acclimation, and examined the variation in these patterns between the sampled populations. RESULTS: Hyposalinity induced different responses in the two populations: in one, only 26 genes were differentially expressed between salinity treatments, while the other population demonstrated up- or downregulation in 3072 genes. In the latter population, the projected future hyposalinity induced an acute response in terms of antioxidant production. Genes associated with membrane composition and structure were also heavily involved, with the upregulation of fatty acid and actin production, and the downregulation of ion channels and alginate pathways. Changes in gene expression patterns clearly indicated an inhibition of the photosynthetic machinery, with a consequent downregulation of carbohydrate production. Simultaneously, energy consumption increased, as revealed by the upregulation of genes associated with respiration and ATP synthesis. Overall, the genes that demonstrated the largest increase in expression were ribosomal proteins involved in translation pathways. The fixation rate of SNP:s was higher within genes responding to hyposalinity than elsewhere in the transcriptome. CONCLUSIONS: The high fixation rate in the genes coding for salinity acclimation mechanisms implies strong selection for them. The among-population differentiation that we observed in the transcriptomic response to hyposalinity stress suggests that populations of F. vesiculosus may differ in their tolerance to future desalination, possibly as a result of local adaptation to salinity conditions within the Baltic Sea. These results emphasise the importance of considering interspecific genetic variation when evaluating the consequences of environmental change.

Smooth or smothering? The self-cleaning potential and photosynthetic effects of oil spill on arctic macro-algae Fucus distichus.

Due to increased sea transport and offshore gas and oil exploration, the Arctic is facing an unprecedented risk of marine oil spills. Although beached oil spills can lead to acute and chronic impacts on intertidal ecosystems, the effects of oil spills on macro-algae in Arctic ecosystems is lacking. Here, we assessed the effect and response of the tidal macro-algae Fucus distichus to oiling, i.e. self-cleaning potential by seawater wash and photosynthetic activity. Oiling with four oil types (ANS, Grane, IFO30 and MGO) was simulated by exposing F. distichus tips to oil. Oil removal half-times ranged between 0.8 - 4.5 days, indicating that oiling of macro-algae with the tested oils was short-term. Further, Grane oil mostly inhibited photosynthetic activity whereas oil from ANS, IFO30 and MGO stimulated it. The photosynthetic activity of F. distichus continued to be affected (inhibited or stimulated), even after oil on the tip surface was washed off.

Sensitivities to global change drivers may correlate positively or negatively in a foundational marine macroalga.

Ecological impact of global change is generated by multiple synchronous or asynchronous drivers which interact with each other and with intraspecific variability of sensitivities. In three near-natural experiments, we explored response correlations of full-sibling germling families of the seaweed Fucus vesiculosus towards four global change drivers: elevated CO2 (ocean acidification, OA), ocean warming (OW), combined OA and warming (OAW), nutrient enrichment and hypoxic upwelling. Among families, performance responses to OA and OW as well as to OAW and nutrient enrichment correlated positively whereas performance responses to OAW and hypoxia anti-correlated. This indicates (i) that families robust to one of the three drivers (OA, OW, nutrients) will also not suffer from the two other shifts, and vice versa and (ii) families benefitting from OAW will more easily succumb to hypoxia. Our results may imply that selection under either OA, OW or eutrophication would enhance performance under the other two drivers but simultaneously render the population more susceptible to hypoxia. We conclude that intraspecific response correlations have a high potential to boost or hinder adaptation to multifactorial global change scenarios.

Tolerance of Fucus vesiculosus exposed to diesel water-accommodated fraction (WAF) and degradation of hydrocarbons by the associated bacteria.

The viability and physiological state of brown macroalgae Fucus vesiculosus and its associated epiphytic bacteria exposed to diesel water-accommodated fraction (WAF), as well as the capacity of this association to deplete petroleum hydrocarbons (HCs) were experimentally tested. After a 6-day exposure treatment, the algal-surface associated bacteria were identified as primarily hydrocarbon-oxidising bacteria (HOB), and the algal-HOB association was able to deplete petroleum hydrocarbons from the diesel WAF by 80%. The HOB density on the algal surface exposed to diesel WAF was 350% higher compared to the control (i.e. HOB density on the algal surface exposed to ambient seawater), which suggest that they actively proliferated in the presence of hydrocarbons and most likely consumed hydrocarbons as their primary organic substrate. Exposure to diesel WAF did not affect the metabolic activity of F. vesiculosus. Higher lipid peroxidation was observed in F. vesiculosus exposed to diesel WAF while catalase concentration decreased only during the first day of exposure. Results suggest F. vesiculosus is tolerant to oil pollution and the algal-HOB association can efficiently deplete petroleum hydrocarbons in oil-contaminated seas.

Integrating experimental and distribution data to predict future species patterns.

Predictive species distribution models are mostly based on statistical dependence between environmental and distributional data and therefore may fail to account for physiological limits and biological interactions that are fundamental when modelling species distributions under future climate conditions. Here, we developed a state-of-the-art method integrating biological theory with survey and experimental data in a way that allows us to explicitly model both physical tolerance limits of species and inherent natural variability in regional conditions and thereby improve the reliability of species distribution predictions under future climate conditions. By using a macroalga-herbivore association (Fucus vesiculosus - Idotea balthica) as a case study, we illustrated how salinity reduction and temperature increase under future climate conditions may significantly reduce the occurrence and biomass of these important coastal species. Moreover, we showed that the reduction of herbivore occurrence is linked to reduction of their host macroalgae. Spatial predictive modelling and experimental biology have been traditionally seen as separate fields but stronger interlinkages between these disciplines can improve species distribution projections under climate change. Experiments enable qualitative prior knowledge to be defined and identify cause-effect relationships, and thereby better foresee alterations in ecosystem structure and functioning under future climate conditions that are not necessarily seen in projections based on non-causal statistical relationships alone.

Tolerance to climate change of the clonally reproducing endemic Baltic seaweed, Fucus radicans: is phenotypic plasticity enough?

To predict the effects of climate change, we first need information on both the current tolerance ranges of species and their future adaptive potential. Adaptive responses may originate either in genetic variation or in phenotypic plasticity, but the relative importance of these factors is poorly understood. Here, we tested the tolerance of Fucus radicans to the combination of hyposalinity and warming projected by climate models for 2070-2099. We measured the growth and survival responses of thalli in both current and future conditions, focusing on variations in tolerance among and within different clonal lineages. Survival was 32% lower in future than in current conditions, but the weight and length of the thalli which survived was respectively 267% and 178% higher when exposed to future conditions. The relatively high tolerance to the future conditions suggests that F. radicans is likely to persist in its current distributional range, which is limited to the Gulf of Bothia and Estonian coast in the Baltic Sea. Furthermore, this species may be able to expand its distribution southward and replace its congener F. vesiculosus, which, in previous studies, has not tolerated the future conditions as well. In addition, we discovered variation in tolerance to future conditions within one of the clonal lineages, which have been hitherto presumed to lack adaptive variation. The discovery of intra-clonal phenotypic plasticity means that this alga has the potential for adaptive responses to climate change, which may be the key to the future persistence of F. radicans in the Baltic Sea.

Living apart-together: Microhabitat differentiation of cryptic nematode species in a saltmarsh habitat.

Coexistence of highly similar species is at odds with ecological theory of competition; coexistence, then, requires stabilizing mechanisms such as differences in ecological niche. In the bacterivore nematode Litoditis marina species complex, which occurs associated with macro-algae, four cryptic lineages (Pm I-IV) co-occur in the field along the south-western coast and estuaries of The Netherlands. Here we investigate the temporal and/or spatial niche differentiation in their natural environment using a qPCR-based detection and relative quantification method. We collected different algal species (i.e. two Fucus species and Ulva sp.) and separated algal structures (i.e. receptacula, thalli, non-fertile tips and bladders) at different sampling months and times (i.e. twice per sampling month), to examine differences in microhabitat use between coexisting L. marina species. Results demonstrate that the cryptic species composition varied among different algal species and algal structures, which was also subject to temporal shifts. Pm I dominated on Fucus spp., Pm II showed dominance on Ulva sp., while Pm III overall had the lowest frequencies. Microhabitat partitioning was most pronounced between the two cryptic species which had similar microbiomes (Pm I and Pm II), and less so between the two species which had significantly different microbiomes (Pm I and Pm III), suggesting that species which share the same microhabitats may avoid competition through resource partitioning. The interplay of microhabitat differentiation and temporal dynamics among the cryptic species of L. marina implies that there is a complex interaction between biotic components and abiotic factors which contributes to their coexistence in the field.

Physiological responses to variations in grazing and light conditions in native and invasive fucoids.

Poor physiological acclimatization to climate change has led to shifts in the distributional ranges of various species and to biodiversity loss. However, evidence also suggests the relevance of non-climatic physical factors, such as light, and biotic factors, which may act in interactive or additive way. We used a mechanistic approach to evaluate the ecophysiological responses of four seaweed species (three dominant intertidal fucoids, Fucus serratus, Ascophyllum nodosum, Bifurcaria bifurcata, and the invasive Sargassum muticum) to different conditions of grazing, light irradiance and ultraviolet (UV) radiation. We performed a large-scale mesocosm experiment with a total of 800 individual thalli of macroalgae. The factorial experimental design included major algal traits, photoacclimation, nutrient stoichiometry and chemical defence as response variables. Few significant effects of the factors acting alone or in combination were observed, suggesting a good capacity for acclimatization in all four species. The significant effects were generally additive and there were no potentially deleterious synergistic effects between factors. Fucus serratus, a species currently undergoing a drastic contraction of its southern distribution limit in Europe, was the most strongly affected species, showing overall lower photosynthetic efficiency than the other species. The growth rate of F. serratus decreased when UV radiation was filtered out, but only in the presence of grazers. Moreover, more individuals of this species tended to reach maturity in the absence of grazers, and the nitrogen content of tissues decreased under full-spectrum light. Only the phlorotannin content of tissues of B. bifurcata and of exudates of A. nodosum, both slow-growing species, were positively affected by respectively removal of UVB radiation and the presence of grazers. The findings for S. muticum, a well-established invasive seaweed across European coasts, suggested similar physiological response of this fast-growing species to different levels of grazing activity and light quality/intensity. As expected, this species grew faster than the other species. Bifurcaria bifurcata and A. nodosum only showed minor effects of light quality and grazing on phlorotannins content, which suggests good resistance of these two long-lived species to the experimental conditions. Mechanistic approaches that are designed to analyse interactive effects of physical and biotic factors provide an understanding of physiological responses of species and help to improve the confidence of predictive distribution models.

Environmental and phenotypic heterogeneity of populations at the trailing range-edge of the habitat-forming macroalga Fucus serratus.

Empirical work on the dynamics of range limits of species distributions often lack replications of edge populations. We compared the local environment and performance of two groups of geographically peripheral populations of the foundation intertidal alga Fucus serratus L. at its southern range boundary in the NW Iberian Peninsula. Two populations were located on the Western Galician coast in large embayments or rias, and the other two on a Northern open coastal stretch in Lugo province. Sharp differences were detected in the local environment and performance of the two groups of populations. While recruitment was quite consistent throughout the year in rias, it was very limited and variable in Lugo. Furthermore, thalli from rias were severely damaged following their transplantation in Lugo, and poor conditions of local adult plants were detected there in subsequent years. These results suggest a higher vulnerability of Lugo populations under new climate conditions, while western rias, strongly influenced by upwelling events, feasibly act as contemporary refugia for this species. If sustained over time, these refugia may mitigate the retreat of the seaweed' rear-edge predicted by large spatial scale models.

Tolerance and potential for adaptation of a Baltic Sea rockweed under predicted climate change conditions.

Climate change is threating species' persistence worldwide. To predict species responses to climate change we need information not just on their environmental tolerance but also on its adaptive potential. We tested how the foundation species of rocky littoral habitats, Fucus vesiculosus, responds to combined hyposalinity and warming projected to the Baltic Sea by 2070-2099. We quantified responses of replicated populations originating from the entrance, central, and marginal Baltic regions. Using replicated individuals, we tested for the presence of within-population tolerance variation. Future conditions hampered growth and survival of the central and marginal populations whereas the entrance populations fared well. Further, both the among- and within-population variation in responses to climate change indicated existence of genetic variation in tolerance. Such standing genetic variation provides the raw material necessary for adaptation to a changing environment, which may eventually ensure the persistence of the species in the inner Baltic Sea.