Aschwin H. Engelen

Polyunsaturated Fatty acids of marine macroalgae: potential for nutritional and pharmaceutical applications.

As mammals are unable to synthesize essential polyunsaturated fatty acids (PUFA), these compounds need to be taken in through diet. Nowadays, obtaining essential PUFA in diet is becoming increasingly difficult; therefore this work investigated the suitability of using macroalgae as novel dietary sources of PUFA. Hence, 17 macroalgal species from three different phyla (Chlorophyta, Phaeophyta and Rhodophyta) were analyzed and their fatty acid methyl esters (FAME) profile was assessed. Each phylum presented a characteristic fatty acid signature as evidenced by clustering of PUFA profiles of algae belonging to the same phylum in a Principal Components Analysis. The major PUFA detected in all phyla were C18 and C20, namely linoleic, arachidonic and eicosapentaenoic acids. The obtained data showed that rhodophytes and phaeophytes have higher concentrations of PUFA, particularly from the n-3 series, thereby being a better source of these compounds. Moreover, rhodophytes and phaeophytes presented “healthier” ∑n-6/∑n-3 and PUFA/saturated fatty acid ratios than chlorophytes. Ulva was an exception within the Chlorophyta, as it presented high concentrations of n-3 PUFA, α-linolenic acid in particular. In conclusion, macroalgae can be considered as a potential source for large-scale production of essential PUFA with wide applications in the nutraceutical and pharmacological industries.

Identity of the Qingdao algal bloom.

In early July 2008, news agencies worldwide reported on a vast algal bloom that was threatening the upcoming Olympic sailing events in Qingdao, China. The identity of the culpable alga, however, remained undiscussed. We have identified the alga that caused the bloom by means of morphological and molecular data, including sequence data of the plastid encoded large subunit ribulose 1,5‐bisphosphate carboxylase gene (rbcL) and the nuclear encoded rDNA internal transcribed spacer (ITS) region. The bloom‐forming alga falls within the morphological limits of the green seaweed Ulva prolifera O.F. Müller (‘Enteromorpha prolifera (O.F. Müller) J. Agardh’) but our phylogenetic analyses show that it forms a clade with representatives of the Ulva linza‐procera‐prolifera (LPP) complex. The Chinese rbcL sequences are identical to those of specimens collected from Japan, New Zealand, Finland and Portugal, suggesting that the taxon is widely distributed. rDNA ITS sequences showed a close affinity with Japanese isolates of the species complex. The Qingdao bloom is a typical illustration of a green tide, which occurs increasingly along several coasts worldwide.

Biodiversity mediates top–down control in eelgrass ecosystems: a global comparative‐experimental approach

Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom-up and top-down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass (Zostera marina) to quantify how top-down and bottom-up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top-down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross-site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large-scale patterns corresponded strikingly with prior small-scale experiments. Our results link global and local evidence that biodiversity and top-down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.

A meta-analysis of seaweed impacts on seagrasses: Generalities and knowledge gaps

Seagrasses are important habitat-formers and ecosystem engineers that are under threat from bloom-forming seaweeds. These seaweeds have been suggested to outcompete the seagrasses, particularly when facilitated by eutrophication, causing regime shifts where green meadows and clear waters are replaced with unstable sediments, turbid waters, hypoxia, and poor habitat conditions for fishes and invertebrates. Understanding the situations under which seaweeds impact seagrasses on local patch scales can help proactive management and prevent losses at greater scales. Here, we provide a quantitative review of available published manipulative experiments (all conducted at the patch-scale), to test which attributes of seaweeds and seagrasses (e.g., their abundances, sizes, morphology, taxonomy, attachment type, or origin) influence impacts. Weighted and unweighted meta-analyses (Hedges d metric) of 59 experiments showed generally high variability in attribute-impact relationships. Our main significant findings were that (a) abundant seaweeds had stronger negative impacts on seagrasses than sparse seaweeds, (b) unattached and epiphytic seaweeds had stronger impacts than ‘rooted’ seaweeds, and (c) small seagrass species were more susceptible than larger species. Findings (a) and (c) were rather intuitive. It was more surprising that ‘rooted’ seaweeds had comparatively small impacts, particularly given that this category included the infamous invasive Caulerpa species. This result may reflect that seaweed biomass and/or shading and metabolic by-products like anoxia and sulphides could be lower for rooted seaweeds. In conclusion, our results represent simple and robust first-order generalities about seaweed impacts on seagrasses. This review also documented a limited number of primary studies. We therefore identified major knowledge gaps that need to be addressed before general predictive models on seaweed-seagrass interactions can be build, in order to effectively protect seagrass habitats from detrimental competition from seaweeds.

Assessment of the spatial variability of phenolic contents and associated bioactivities in the invasive alga Sargassum muticum sampled along its European range from Norway to Portugal

Sargassum muticum, an invasive brown macroalga presently distributed along European Atlantic coasts from southern Portugal to the south coast of Norway, was studied on a large geographical scale for its production of phenolic compounds with potential industrial applications and their chemical and biological activities. S. muticum can produce high biomass in Europe, which could be exploited to supply such compounds. S. muticum was collected in Portugal, Spain, France, Ireland and Norway (three sites/country) to examine the effect of the latitudinal cline and related environmental factors. Assays focused particularly on polyphenols and their activities. Crude acetone–water extracts were purified using solid phase extraction (SPE) and antioxidant and antimicrobial activities of crude extracts and semi-purified fractions measured. Total phenolic content was assessed by colorimetric Folin–Ciocalteu assay and reactive oxygen species activities by 2,2-diphenyl-1-picrylhydrazyl, reducing power, β-carotene bleaching method and xanthine oxidase assay. Antibacterial activities were tested on terrestrial and marine strains to evaluate potential use in biomedical and aquaculture fields. Purified active phlorotannins, isolated by SPE, were identified using NMR. Phenolic contents differ clearly among countries and among sites within countries. Quality did not change between countries, however, although there were some slight differences in phlorethol type. Additionally, some fractions, especially from the extreme north and south, were very active. We discuss this in relation to environmental conditions and the interest of these compounds. S. muticum represents a potential natural source of bioactive compounds and its collection could offer an interesting opportunity for the future management of this species in Europe.

Effects of wave exposure and depth on biomass, density and fertility of the fucoid seaweed Sargassum polyceratium (Phaeophyta, Sargassaceae)

Sargassum polyceratium is widely distributed around the island of Curaçao (Netherlands Antilles) where it inhabits strongly contrasting habitats. Changes in population structure have been followed in three bays with increasing levels of wave exposure at two depths: shallow (0 m) and deep (18 m). The effects of increasing wave exposure were investigated by studying three deep-water populations; and the effects of depth by studying shallow- and deep-water populations in the two calmer bays. Total density and stage density (reproductive thalli, juvenile thalli) were determined and total and individual thallus biomass was estimated non-destructively. In the most wave-exposed deep-water population thalli were twice as long with more than twice the biomass than in the calmest deep-water population. Total density and juvenile density were highest in the bay with intermediate wave exposure. Depth was an important factor at both the individual and population level. Shallow-water thalli had basal holdfast areas that were four times larger than those from deep water, and thallus biomass was positively correlated with holdfast area. Shallow-water juveniles invested more in the development of a holdfast and lateral growth than deep-water juveniles. Total biomass per quadrat was up to 10-fold higher in shallow- than in deep-water populations. In shallow-water populations reproductive thalli were present throughout the year whereas in deep-water populations they were present only during autumn and winter. We conclude that both wave exposure and depth affect population structure. Thalli were generally bigger and total biomass higher in the more exposed bay(s) and in shallower water, contradicting the general pattern in macroalgae of reduced size and biomass with increasing wave exposure.

Rhizosphere Microbiomes of European + Seagrasses Are Selected by the Plant, But Are Not Species Specific.

Seagrasses are marine flowering plants growing in soft-body sediments of intertidal and shallow sub-tidal zones. They play an important role in coastal ecosystems by stabilizing sediments, providing food and shelter for animals, and recycling nutrients. Like other plants, seagrasses live intimately with both beneficial and unfavorable microorganisms. Although much is known about the microbiomes of terrestrial plants, little is known about the microbiomes of seagrasses. Here we present the results of a detailed study on the rhizosphere microbiome of seagrass species across the North-eastern Atlantic Ocean: Zostera marina, Zostera noltii, and Cymodocea nodosa. High-resolution amplicon sequencing of 16S rRNA genes showed that the rhizobiomes were significantly different from the bacterial communities of surrounding bulk sediment and seawater. Although we found no significant differences between the rhizobiomes of different seagrass species within the same region, those of seagrasses in different geographical locations differed strongly. These results strongly suggest that the seagrass rhizobiomes are shaped by plant metabolism, but not coevolved with their host. The core rhizobiome of seagrasses includes mostly bacteria involved in the sulfur cycle, thereby highlighting the importance of sulfur-related processes in seagrass ecosystems.

Periodicity of propagule expulsion and settlement in the competing native and invasive brown seaweeds, Cystoseira humilis and Sargassum muticum (Phaeophyta)

Dense stands of the invasive species Sargassum muticum (Yendo) Fensholt develop in tidal pools close to its southern distributional limit in Europe, the southwest coast of Portugal. Along this coast, sheltered tidal pools form a specific habitat in which colonization occurs. Invaded pools are originally inhabited by Cystoseira humilis Kützing. Differences in gamete release between the competing native and alien species might be important for the initial settlement and further spread of the invader. Therefore, we tested whether egg expulsion and embryo settlement in both species had the same timing with respect to lunar and tidal cycles. For more than 2 months during the reproductive season egg expulsion and embryo release were monitored daily for each species. Egg expulsion in S. muticum showed a broadly semilunar periodicity peaking around full and new moon (spring tides), when low tides take place in the morning/evening. In contrast, C. humilis egg expulsion showed an asymmetric semilunar-to-lunar periodicity peaking around waning quarter moon, when low tides occur around midday. Embryo settlement detected in pools was low for both species and less periodic. Phase differences in expulsion events between the two species with respect to the semilunar cycle suggest that cues other than the moon are involved in their timing. Our observations suggest that variations in physiological mechanisms and/or environmental conditions result in different patterns of egg expulsion between the two species. This might have consequences for fertilization success, gamete dispersal and survival. It was further found that peaks in egg expulsion and embryo release (i.e. settlement) in S. muticum were much more synchronous at a site in northern Portugal compared with a site close to the current southern distributional limit in south-west Portugal, possibly as a consequence of thermal stress experienced in the south.

Faunal differences between the invasive brown macroalga Sargassum muticum and competing native macroalgae

Interactions between macroalgae and their associated fauna are of great interest for marine invasions, because fauna may increase the biotic resistance of a system and macroalgal invasions may cause shifts in faunal composition. We tested for differences in faunal community structure between a macroalgal invader, Sargassummuticum, and several native macroalgae in intertidal pools on both the west and south coast of Portugal. On each coast, we compared the faunal diversity and composition associated with the invader with that of the competing native macroalga(e). On the west coast, the diversity of the fauna associated with S. muticum was equal to or lower than with the native competitor, Cystoseira humilis. Fauna composition differed between S. muticum and C. humilis at both locations, but within each species, no differences between locations were detected. In contrast, the fauna diversity on S. muticum of the south coast varied among locations. S. muticum fauna differed from the fauna of all native macroalgae at one location, but only from three out of seven native macroalgae at the other location. Discriminating fauna species did not show a consistent pattern towards higher or lower abundances in S. muticum compared to most native macroalgae, and species-specific contributions were small. Differences in fauna community also depended on the identity of the native macroalga. In conclusion, the fauna associated with S. muticum differs from many native brown macroalgae, but these differences were not consistent as they depend both on the native macroalgal species and on location. This invader does not seem to have a severe negative impact on local macroalgae-associated fauna.

Temperature effects on gametophyte life-history traits and geographic distribution of two cryptic kelp species.

A major determinant of the geographic distribution of a species is expected to be its physiological response to changing abiotic variables over its range. The range of a species often corresponds to the geographic extent of temperature regimes the organism can physiologically tolerate. Many species have very distinct life history stages that may exhibit different responses to environmental factors. In this study we emphasized the critical role of the haploid microscopic stage (gametophyte) of the life cycle to explain the difference of edge distribution of two related kelp species. Lessonia nigrescens was recently identified as two cryptic species occurring in parapatry along the Chilean coast: one located north and the other south of a biogeographic boundary at latitude 29–30°S. Six life history traits from microscopic stages were identified and estimated under five treatments of temperature in eight locations distributed along the Chilean coast in order to (1) estimate the role of temperature in the present distribution of the two cryptic L. nigrescens species, (2) compare marginal populations to central populations of the two cryptic species. In addition, we created a periodic matrix model to estimate the population growth rate (λ) at the five temperature treatments. Differential tolerance to temperature was demonstrated between the two species, with the gametophytes of the Northern species being more tolerant to higher temperatures than gametophytes from the south. Second, the two species exhibited different life history strategies with a shorter haploid phase in the Northern species contrasted with considerable vegetative growth in the Southern species haploid stage. These results provide strong ecological evidence for the differentiation process of the two cryptic species and show local adaptation of the life cycle at the range limits of the distribution. Ecological and evolutionary implications of these findings are discussed.