Topographic heterogeneity triggers complementary cascades that enhance ecosystem multifunctionality.

Topographic heterogeneity sets the stage for community assembly, but its effects on ecosystem functioning remain poorly understood. Here, we test the hypothesis that topographic heterogeneity underpins multiple cascading species interactions and functional pathways that indirectly control multifunctionality. To do so, we combined experimental manipulation of a form of topographic heterogeneity on rocky shores (holes of various sizes) with a comprehensive assessment of naturally assembled communities and multifunctionality. Structural equation modeling indicated that heterogeneity: (1) enhanced biodiversity by supporting filter feeder richness; (2) triggered a facilitation cascade via reef-forming (polychaete) and biomass-dominant (macroalga) foundation species, which in turn broadly supported functionally diverse epibiotic and understory assemblages; and (3) inhibited a key consumer (limpet). The model supported that these mechanisms exerted complementary positive effects on individual functions (e.g., water filtration, ecosystem metabolism, nutrient uptake) and, in turn, collectively enhanced multifunctionality. Topographic heterogeneity may therefore serve as a cornerstone physical attribute by initiating multiple cascades that propagate through ecological communities via foundation species, ultimately manifesting disproportionate effects on ecosystem multifunctionality.

Loss, resilience and recovery of kelp forests in a region of rapid ocean warming.

BACKGROUND AND AIMS: Changes in kelp abundances on regional scales have been highly variable over the past half-century owing to strong effects of local and regional drivers. Here, we assess patterns and dominant environmental variables causing spatial and interspecific variability in kelp persistence and resilience to change in Nova Scotia over the past 40 years. METHODS: We conducted a survey of macrophyte abundance at 251 sites spanning the Atlantic coast of Nova Scotia from 2019 to 2022. We use this dataset to describe spatial variability in kelp species abundances, compare species occurrences to surveys conducted in 1982 and assess changes in kelp abundance over the past 22 years. We then relate spatial and temporal patterns in abundance and resilience to environmental metrics. KEY RESULTS: Our results show losses of sea urchins and the cold-tolerant kelp species Alaria esculenta, Saccorhiza dermatodea and Agarum clathratum in Nova Scotia since 1982 in favour of the more warm-tolerant kelps Saccharina latissima and Laminaria digitata. Kelp abundances have increased slightly since 2000, and Saccharina latissima and L. digitata are widely abundant in the region today. The highest kelp cover occurs on wave-exposed shores and at sites where temperatures have remained below thresholds for growth (21 °C) and mortality (23 °C). Moreover, kelp has recovered from turf dominance following losses at some sites during a warm period from 2010 to 2012. CONCLUSIONS: Our results indicate that dramatic changes in kelp community composition and a loss of sea urchin herbivory as a dominant driver of change in the system have occurred in Nova Scotia over the past 40 years. However, a broad-scale shift to turf-dominance has not occurred, as predicted, and our results suggest that resilience and persistence are still a feature of kelp forests in the region despite rapid warming over the past several decades.

Fucoid Macroalgae Have Distinct Physiological Mechanisms to Face Emersion and Submersion Periods in Their Southern Limit of Distribution.

During high tide, macroalgae are submersed, facing adequate environmental conditions, however, at low tide, these species can be exposed to high UV radiation and desiccation, leading to an overproduction of reactive oxygen species, causing oxidative stress. Since intertidal organisms present differential sensitivity to abiotic fluctuations, this study aimed to evaluate the physiological responses [photosynthetic pigments, hydrogen peroxide (H2O2), lipid peroxidation (LP), and thiols and proline] of three macroalgae, from different intertidal levels, towards tidal regimes. Samples of Pelvetia canaliculata, Ascophyllum nodosum, and Fucus serratus were collected from beaches located on the southern limit of distribution in periods of potential stress (Summer and Spring), under low and high tide. The photosynthetic pigments of P. canaliculata and F. serratus were generally higher during low tide, and the oxidative damage evidenced by H2O2 and LP increased in the Summer, while A. nodosum showed greater oxidative damage in the Spring. While thiol content did not change, proline levels were species- and tidal-specific among sampling dates. P. canaliculata presented higher resilience to unfavorable conditions, while F. serratus was the most sensitive species. The physiological responses analyzed were species-specific, pointing to the high susceptibility of low intertidal organisms to expected extreme climatic events.

A regime shift in intertidal assemblages triggered by loss of algal canopies: A multidecadal survey.

Canopy-forming macroalgae recently experienced a worldwide decline. This is relevant, because canopies sustain complex food webs in temperate coasts. We assessed the die-back of the canopy-forming alga Fucus serratus in N Spain, at its warm distributional range boundary, and its effects on associated assemblages. We combined long-term descriptive surveys with canopy-removal experiments. Results showed that rapid shifts to turf-forming communities were mostly the direct consequence of the canopy loss, rather than a concurrent process directly triggered by climate change. The switch alters the whole food web, as the prominent role of F.serratus and other cold-temperate intertidal fucoids is not being replaced by functionally equivalent species. Canopy loss caused a rapid biotic homogenization at regional scale which is spreading towards the west, from the edge to the central part of the former distributional range of F.serratus in N Spain. The most obvious effect is the ecological and functional impoverishment of the coastal system.

Estimating intertidal seaweed biomass at larger scales from quadrat surveys.

The amount of macroalgal biomass is an important ecosystem variable. Estimates can be made for a sampled area or values can be extrapolated to represent biomass over a larger region. Typically biomass is scaled-up using the area multiplied by the mean: a non-spatial method. Where algal biomass is patchy or shows gradients, non-spatial estimates for an area may be improved by spatial interpolation. A separate issue with scaling-up biomass estimates is that conventional confidence intervals based on the standard error (SE) of the sample may not be appropriate. The issues around interpolation and confidence intervals were examined for three fucoid species using data from 40 × 0.25 m-2 quadrats thrown in a 0.717 ha sampling plot on the shore of Galway Bay. Despite evidence of spatial autocorrelation, interpolation did not appear to improve estimates of the total plot biomass of Fucus serratus and F. vesiculosus. In contrast, interpolated estimates for Ascophyllum nodosum had less error than those based on the non-spatial method. Bootstrapped confidence intervals had several benefits over those based on the SE. These benefits include the avoidance of negative confidence limits at low sample sizes and no assumptions of normality in the data. If there is reason to expect strong patchiness or a gradient of biomass in the area of interest, interpolation is likely to produce more accurate estimates of biomass than non-spatial methods. Development of methodologies for biomass would benefit from more definition of local and regional gradients in biomass and their associated covariates.

Marine macroalgae as food for earthworms: growth and selection experiments across ecotypes.

Historically, subsistence farmers around the Atlantic coast of NW Europe utilized marine algae as a fertilizer in agroecosystems, a practice that continued in small areas and is now considered to have real potential for re-establishing sustainable food production systems on marginal soils. Earthworms form a significant component of soil fauna, and their ecosystem services are well-documented. Therefore, palatability of marine organic amendments to faunal detritivores of terrestrial systems is of interest. This work aimed to assess the potential for growth of Aporrectodea caliginosa, Lumbricus rubellus and Aporrectodea longa fed with two common macroalgae (seaweeds), Laminaria digitata and Fucus serratus. In addition, choice chambers were constructed to permit earthworm selection of these macroalgae with more conventional organic materials, horse manure (HM) and birch leaves (BL). Over a period of 2 months, earthworm species showed significantly greater mass gain with conventional food (p < 0.05). Laminaria outperformed Fucus, which in turn was superior to soil alone. Similarly, when given a choice, a significant preference (p < 0.001) was shown for the more nitrogen-rich HM and BL over the seaweeds. No removal was recorded for A. caliginosa when offered seaweeds only. By contrast, L. rubellus and A. longa showed significant preferences (p < 0.001) for Laminaria over Fucus and fresh material over degraded. These results underline an interest to profit from natural resources (seaweeds) to maintain or improve soil biological quality in marginal coastal areas.

Comparison of the Effects of Fucoidans on the Cell Viability of Tumor and Non-Tumor Cell Lines.

Fucoidans extracted from brown algae exert manifold biological activities paving the way for the development of numerous applications including treatments outside tumor therapy such as age-related macular degeneration or tissue engineering. In this study, we investigated the antiproliferative effects of fucoidans extracted from six different algae (Fucus vesiculosus, F. serratus, F. distichus subsp. evanescens, Dictyosiphon foeniculaceus, Laminaria digitata, Saccharina latissima) as well as three reference compounds (Sigma fucoidan, heparin, enoxaparin) on tumor (HL-60, Raji, HeLa, OMM-1, A-375, HCT-116, Hep G2) and non-tumor (ARPE-19, HaCaT) cell lines. All fucoidans were extracted according to a standardized procedure and tested in a commercially available MTS assay. Cell viability was measured after 24 h incubation with test compounds (1-100 µg/mL). Apart from few exceptions, fucoidans and heparins did not impair cell viability. In contrast, fucoidans significantly increased cell viability of suspension cell lines, but not of adherent cells. Fucoidans slightly increased viability of tumor cells and had no impact on the viability of non-tumor cells. The cell viability of HeLa and ARPE-19 cells negatively correlated with protein content and total phenolic content (TPC) of fucoidans, respectively. In summary, none of the tested fucoidans turned out to be anti-proliferative, rendering them interesting for future studies and applications.

Effects of Fucoidans from Five Different Brown Algae on Oxidative Stress and VEGF Interference in Ocular Cells.

BACKGROUND: Fucoidans are interesting for potential usage in ophthalmology, and especially age-related macular degeneration. However, fucoidans from different species may vary in their effects. Here, we compare fucoidans from five algal species in terms of oxidative stress protection and vascular endothelial growth factor (VEGF) interference in ocular cells. METHODS: Brown algae (Fucus vesiculosus, Fucus distichus subsp. evanescens, Fucus serratus, Laminaria digitata, Saccharina latissima) were harvested and fucoidans isolated by hot-water extraction. Fucoidans were tested in several concentrations (1, 10, 50, and 100 µg/mL). Effects were measured on a uveal melanoma cell line (OMM-1) (oxidative stress), retinal pigment epithelium (RPE) cell line ARPE19 (oxidative stress and VEGF), and primary RPE cells (VEGF). Oxidative stress was induced by H2O2 or tert-Butyl hydroperoxide (TBHP). Cell viability was investigated with methyl thiazolyl tetrazolium (MTT or MTS) assay, and VEGF secretion with ELISA. Affinity to VEGF was determined by a competitive binding assay. RESULTS: All fucoidans protected OMM-1 from oxidative stress. However, in ARPE19, only fucoidan from Saccharina latissima was protective. The affinity to VEGF of all fucoidans was stronger than that of heparin, and all reduced VEGF secretion in ARPE19. In primary RPE, only the fucoidan from Saccharina latissima was effective. CONCLUSION: Among the fucoidans from five different species, Saccharina latissima displayed the most promising results concerning oxidative stress protection and reduction of VEGF secretion.

In vivo uptake of iodine from a Fucus serratus Linnaeus seaweed bath: does volatile iodine contribute?

Seaweed baths containing Fucus serratus Linnaeus are a rich source of iodine which has the potential to increase the urinary iodide concentration (UIC) of the bather. In this study, the range of total iodine concentration in seawater (22-105 µg L-1) and seaweed baths (808-13,734 µg L-1) was measured over 1 year. The seasonal trend shows minimum levels in summer (May-July) and maximum in winter (November-January). The bathwater pH was found to be acidic, average pH 5.9 ± 0.3. An in vivo study with 30 volunteers was undertaken to measure the UIC of 15 bathers immersed in the bath and 15 non-bathers sitting adjacent to the bath. Their UIC was analysed pre- and post-seaweed bath and corrected for creatinine concentration. The corrected UIC of the population shows an increase following the seaweed bath from a pre-treatment median of 76 µg L-1 to a post-treatment median of 95 µg L-1. The pre-treatment UIC for both groups did not indicate significant difference (p = 0.479); however, the post-treatment UIC for both did (p = 0.015) where the median bather test UIC was 86 µg L-1 and the non-bather UIC test was 105 µg L-1. Results indicate the bath has the potential to increase the UIC by a significant amount and that inhalation of volatile iodine is a more significant contributor to UIC than previously documented.

Isolation of Fucus serratus Gametes and Cultivation of the Zygotes.

Zygotes of the Fucale species are a powerful model system to study cell polarization and asymmetrical cell division (Bisgrove and Kropf, 2008). The Fucale species of brown algae grow in the intertidal zone where they reproduce by releasing large female eggs and mobile sperm in the surrounding seawater. The gamete release can be induced from sexually mature fronds in the laboratory and thousands of synchronously developing zygotes are easily obtained. In contrast to other eukaryotic models, such as land plants (Brownlee and Berger, 1995), the embryo is free of maternal tissues and therefore readily amenable to pharmacological approaches. The zygotes are relatively large (up to 100 µm in diameter), facilitating manipulations and imaging studies. During the first hours of zygote development, the alignment of the axis to external cues such as light is labile and can be reversed by light gradients from different directions. A few hours before rhizoid emergence, the alignment of the axis and the polarity are fixed and the cells germinate accordingly. At this stage the zygotes are naturally attached to the substratum through the secretion of cell wall adhesive materials ( Kropf et al., 1988 ; Hervé et al., 2016 ). The first cell division occurs about 24 h after fertilisation and the early embryo is composed of only two cell types that differ in size, shape and developmental fates (i.e., thallus cells and rhizoid cells) ( Bouget et al., 1998 ). The embryo can be successfully cultivated in the laboratory for a few more days (4 weeks maximum) and has an invariant division pattern during the early stages, which allows cell lineages to be traced histologically.

Dynamics of cell wall assembly during early embryogenesis in the brown alga Fucus.

Zygotes from Fucus species have been used extensively to study cell polarization and rhizoid outgrowth, and in this model system cell wall deposition aligns with the establishment of polarity. Monoclonal antibodies are essential tools for the in situ analysis of cell wall glycans, and here we report the characteristics of six monoclonal antibodies to alginates (BAM6-BAM11). The use of these, in conjunction with monoclonal antibodies to brown algal sulfated fucans, has enabled the study of the developmental dynamics of the Fucus zygote cell walls. Young zygotes are spherical and all alginate epitopes are deposited uniformly following cellulose deposition. At germination, sulfated fucans are secreted in the growing rhizoid wall. The redistribution of cell wall epitopes was investigated during treatments that cause reorientation of the growth axis (change in light direction) or disrupt rhizoid development (arabinogalactan-protein-reactive Yariv reagent). Alginate modeling was drastically impaired in the latter, and both treatments cause a redistribution of highly sulfated fucan epitopes. The dynamics of cell wall glycans in this system have been visualized in situ for the first time, leading to an enhanced understanding of the early developmental mechanisms of Fucus species. These sets of monoclonal antibodies significantly extend the available molecular tools for brown algal cell wall studies.

Pronounced gradients of light, photosynthesis and O2 consumption in the tissue of the brown alga Fucus serratus.

Macroalgae live in an ever-changing light environment affected by wave motion, self-shading and light-scattering effects, and on the thallus scale, gradients of light and chemical parameters influence algal photosynthesis. However, the thallus microenvironment and internal gradients remain underexplored. In this study, microsensors were used to quantify gradients of light, O2 concentration, variable chlorophyll fluorescence, photosynthesis and O2 consumption as a function of irradiance in the cortex and medulla layers of Fucus serratus. The two cortex layers showed more efficient light utilization compared to the medulla, calculated both from electron transport rates through photosystem II and from photosynthesis-irradiance curves. At moderate irradiance, the upper cortex exhibited onset of photosynthetic saturation, whereas lower thallus layers exhibited net O2 consumption. O2 consumption rates in light varied with depth and irradiance and were more than two-fold higher than dark respiration. We show that the thallus microenvironment of F. serratus exhibits a highly stratified balance of production and consumption of O2 , and when the frond was held in a fixed position, high incident irradiance levels on the upper cortex did not saturate photosynthesis in the lower thallus layers. We discuss possible photoadaptive responses and consequences for optimizing photosynthetic activity on the basis of vertical differences in light attenuation coefficients.

PHENOTYPIC DIFFERENTIATION AT SOUTHERN LIMIT BORDERS: THE CASE STUDY OF TWO FUCOID MACROALGAL SPECIES WITH DIFFERENT LIFE-HISTORY TRAITS1.

Marginal populations are often geographically isolated, smaller, and more fragmented than central populations and may frequently have to face suboptimal local environmental conditions. Persistence of these populations frequently involves the development of adaptive traits at phenotypic and genetic levels. We compared population structure and demographic variables in two fucoid macroalgal species contrasting in patterns of genetic diversity and phenotypic plasticity at their southern distribution limit with a more central location. Models were Ascophyllum nodosum (L.) Le Jol. (whose extreme longevity and generation overlap may buffer genetic loss by drift) and Fucus serratus L. (with low genetic diversity at southern margins). At edge locations, both species exhibited trends in life-history traits compatible with population persistence but by using different mechanisms. Marginal populations of A. nodosum had higher reproductive output in spite of similar mortality rates at all life stages, making edge populations denser and with smaller individuals. In F. serratus, rather than demographic changes, marginal populations differed in habitat, occurring restricted to a narrower vertical habitat range. We conclude that persistence of both A. nodosum and F. serratus at the southern-edge locations depends on different strategies. Marginal population persistence in A. nodosum relies on a differentiation in life-history traits, whereas F. serratus, putatively poorer in evolvability potential, is restricted to a narrower vertical range at border locations. These results contribute to the general understanding of mechanisms that lead to population persistence at distributional limits and to predict population resilience under a scenario of environmental change.

Feedback control of reactive oxygen and Ca signaling during brown algal embryogenesis.

In a recent paper in Planta, we combined novel confocal reflectance imaging of intracellular reactive oxygen species (ROS) with inhibition-of-growth experiments to show that ROS help to direct polarized growth in brown algal zygotes. Using confocal fluorescence imaging of intracellular Ca(2+) distributions, we were also able to show an interaction between ROS and Ca(2+) signaling. The modulation of intracellular Ca(2+) signals by reactive oxygen species (ROS) is a common motif in many plant and algal systems, but our Planta paper is its first demonstration during early development. We explain here how our findings complement a number of recent studies on polarized growth in plant and algal systems.

Inter-population differences in inherited copper tolerance involve photosynthetic adaptation and exclusion mechanisms in Fucus serratus.

• A comparative study of copper (Cu) toxicity and tolerance in three populations of Fucus serratus was conducted by examining Cu2+ effects on various physiological parameters. • Chlorophyll fluorescence, oxygen evolution, copper content, and relative growth rate of embryos and adults were measured on Cu2+ -exposed material. • Algae naturally exposed to elevated total Cu concentration (CuT ), were more Cu2+ resistant than those from clean sites, as indicated by higher embryo and adult growth rates and lower copper contents. The Cu2+ tolerance of F. serratus is at least partly inherited and relies partly on metal exclusion. • There were inhibitory effects of Cu2+ on oxygen exchange rates in both tolerant and non-tolerant algae. By contrast to sensitive algae, the maximum efficiency of photosystem II (Fv /Fm ), maximum fluorescence (Fm ) and zero fluorescence (Fo ) of resistant algae were unaffected by Cu2+ , whereas decreased quantum yield (ΦPSII) and increased nonphotochemical quenching (NPQ) were most pronounced in resistant algae. Inhibitory effects of Cu2+ on ΦPSII may result in the excitation energy being dissipated through xanthophyll-dependent quenching mechanisms in tolerant algae. In nontolerant algae, lower energy dissipation may result in chlorophyll degradation.