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Molecular analysis of Ulva compressa (Chlorophyta, Ulvales) reveals its morphological plasticity, distribution and potential invasiveness on German North Sea and Baltic Sea coasts
Abstract
To resolve historical misinterpretations of species descriptions and to comprehend the morphological diversity together with the distribution of Ulva compressa Linnaeus in northern Germany, a morphological and molecular study was undertaken of recently collected specimens and herbarium vouchers. Phylogenetic analyses from sequences of the plastid encoded tufA gene confirmed that U. compressa is abundant along the German Baltic Sea and North Sea coasts. We were able to genetically confirm the presence of U. compressa in the Baltic Sea below salinities of 15 PSU. However, we detected morphologies agreeing with the attached and branched tubular type material only in the North Sea, while U. compressa on Baltic Sea coasts indiscriminately exhibited a very distinct morphology of sheet-like thalli that were always unattached, with the exception of one collection site. Drifting forms were also frequently detected in the Wadden Sea, but not on the island of Helgoland. The tufA sequences of attached and tubular forms of U. compressa from the German Wadden Sea were identical to the drifting sheets found in the Wadden and Baltic Seas and the sequence divergence was extremely small at ≤0.9%. The proliferating, blade-like thalli of U. compressa appear as a nuisance ecotype that is able to form massive accumulations associated with oxygen depletion. Mass accumulations were observed to cause severe damage and increased mortality of habitat forming Zostera and Ruppia populations.
... Nevertheless, Ulva is known for its capacity to change between different morphologies. This has been observed and studied both under laboratory conditions (Provasoli and Pintner 1980;Matsuo et al. 2005;Spoerner et al. 2012;Wichard 2015;Wichard et al. 2015) and under natural conditions in New England, the German North Sea, and the Baltic Sea (Hofmann et al 2010;Steinhagen et al. 2019b). Tan et al. (1999) also discovered the presence of foliose Ulva compressa Linnaeus (usually found in its tubular form) in brackish water in Scotland. ...
... Moreover, similar specimens were found in the Wadden Sea in areas with a salinity range between 30 and 33.5 PSU and in environments with drastic changes in temperature and salinity (e.g., basins and drain channels). Tubular specimens, however, were rare in such conditions (Steinhagen et al. 2019b). In Steinhagen et al. (2019b) it was suggested that the foliose morphotype of U. compressa was not as limited by salinity as its tubular morphotype. ...
... Tubular specimens, however, were rare in such conditions (Steinhagen et al. 2019b). In Steinhagen et al. (2019b) it was suggested that the foliose morphotype of U. compressa was not as limited by salinity as its tubular morphotype. In another work, it was suggested that the reduced RGR of germlings of Ulva fasciata Delile (a foliose species) in low salinities could be related to a reduced cell viability. ...
The genus Ulva is globally distributed and has been thoroughly studied because of its functional biochemical composition, rapid growth rates and opportunistic features, and interest in Ulva cultivation is growing worldwide. In Europe, mostly near- and on-shore flow-through cultivation systems are used and land-based recirculating aquaculture systems (RAS) using fresh water or artificial seawater have not been developed for Ulva. While RAS provides quality control and can be located inland, maintenance costs are high. Using selected strains adapted to low-salinity could reduce seawater production costs and improve the economic feasibility. Therefore, our study assessed how salinity can be used as a tool for strain selection and optimization of functional traits. Growth rates and antioxidant activity of three species (four strains) of tubular and foliose Ulva from the NE-Atlantic and Mediterranean (foliose: Ulva lacinulata – two geographical strains, tubular: Ulva linza and Ulva flexuosa) were followed for three weeks at salinities ranging from 10 to 30 PSU. The tubular strains achieved optimal growth at a lower salinity than U. lacinulata. However, growth rates of both foliose strains were higher than of tubular strains, even at sub-optimal salinity. Therefore, U. lacinulata is a good candidate for RAS with artificial seawater, and the cost of salt can be reduced by up to 33.3% (20 PSU) without significantly reducing the growth rate of U. lacinulata. Higher antioxidant activity was achieved by reducing the salinity to 10 PSU for 10 days, suggesting that the functional traits of cultivated Ulva lacinulata can be optimized prior to harvest.
... Recently, green macroalgae of the genus Ulva attracted interest from the growing aquaculture industry [11][12][13][14][15][16] due to their fast growth and high nutrition value [13,[17][18][19][20]. However, these traits also make them prone to introduction to new ecosystems by human dispersal [21][22][23], and combined with the fact that some opportunistic species can form green tides under suitable nutrient conditions [24][25][26][27], correct species identification and phylogeographic assessments of this taxonomic group is crucial before development as aquaculture species. ...
... [36][37][38][39][40][41][42][43][44][45]). New species are being constantly described [13,14,25,[46][47][48][49] and allegedly well-defined species are revised [27,[49][50][51][52][53][54][55]. A striking example is the genus Ulva (e.g. ...
... [56]), which currently comprises 85 taxonomically accepted species, >550 historic species names, and several entities with unclear taxonomic status [57]. Ulva species exhibit a variety of complex morphologies [25,27,36,53,[58][59][60][61], and therefore, morphologically based species identification often lead to mis-identification [25,27,50,52,53,56,61]. ...
Correct species identification is fundamental for assessment and understanding of biodiversity. Erroneous species
identification may impede conservation management and may delay detection of invasive species. The ubiqui-
tous green algal genus Ulva is known for its wide environmental tolerance, plastic morphology, occurrence of
cryptic species and ambiguous species concepts that hinder clear identification. We used molecular monitoring to
assess species diversity and distribution of Ulva along the full Atlantic-Baltic Sea salinity gradient (> 10,000 km).
Ulva specimens were collected from Denmark, Finland, Germany, Norway, and Sweden. DNA barcoding analysis
of the tufA gene revealed 20 genetic entities in total, of which 11 could be identified to species level
(U. californica, U. flexuosa, U. torta, U. linza, U. prolifera, U. fenestrata, U. australis, U. intestinalis, U. compressa,
U. gigantea, U. lacinulata). Nine entities (Ulva sp. 1–9; [Ulva capillata]) yielded novel sequence reads that
belonged to either unidentified species, species complexes, or singletons. At least 3 of the discovered species
(U. australis, U. californica, U. gigantea) are considered non-native and potentially invasive. Furthermore,
considerable differences between the observed and the historically estimated species distributions were found.
The highest diversity was recorded in the Atlantic and Skagerrak region whereas only two entities of taxo-
nomically accepted species where found north-east the Blekinge coast. Our study shows that the species diversity
of Ulva in the study area is diverging from previous reports, and that molecular methods are imperative for
species identification in this morphologically plastic genus. Furthermore, the presence of non-native species
indicates a necessity for further fine-scale monitoring in specific areas to e.g. mitigate formation of green tides.
... In terms of Ulva, the issue of species concept itself has been added to a problem relating to species identification, because of high phenotypic plasticity of many members of Ulvales which resulting in a "historical misinterpretation" in species level of Ulva (Steinhagen et al., 2019b). ...
... To show the plasticity of Ulva species' morphogenesis which might result from environmental drivers or symbiont-dependent development, we can refer to morphological plasticity of U. compressa in northern Germany, North Sea and Baltic Sea besides misidentification of U. compressa and U. mutabilis (Steinhagen et al., 2019a, Steinhagen et al., 2019b. ...
... Typically, the thallus's unique tubular shape and its branching pattern were considered a distinguishing factor for the taxonomic identification of U. compressa, but this is now deemed controversial (see references in Steinhagen et al., 2019b). As it has been noted earlier, many researchers believed that branching patterns cannot be a solid parameter for taxonomic classifications as branching can be affected by external factors such as salinity (Blomster et al., 2002, Steinhagen et al., 2019b. ...
The results of this thesis highlight: (i) Specific Ulva-associated bacterial functions (promoting cell division, or cell differentiation) that cannot be assigned to a specific genus/taxonomic group of bacteria, (ii) an integrated multitrophic aquaculture system (IMTA) system ensuring an adequate supply of nutrients and a sufficient chemical mixture of algal growth- and morphogenesis-promoting factors (AGPFs) for reliable Ulva cultivation and (iii) the first-characterised mechanisms to date by which Ulva extract can impact germination and growth in Arabidopsis.
... This publication provides an update to an earlier article by Schramm (1998), who already gave a detailed description of the macroalgal species distribution and diversity along SE North Sea and Baltic Sea coasts. During the last two decades several species introductions into the region have been recorded [for example, approximately 10 on German coasts (Lackschewitz et al. 2014, Steinhagen et al. 2018 and also range shifts of species were observed within the area (Kovtun et al. 2009, Steinhagen et al. 2018. Nonetheless, the general distribution patterns outlined by Schramm (1998) still remain valid. ...
... This publication provides an update to an earlier article by Schramm (1998), who already gave a detailed description of the macroalgal species distribution and diversity along SE North Sea and Baltic Sea coasts. During the last two decades several species introductions into the region have been recorded [for example, approximately 10 on German coasts (Lackschewitz et al. 2014, Steinhagen et al. 2018 and also range shifts of species were observed within the area (Kovtun et al. 2009, Steinhagen et al. 2018. Nonetheless, the general distribution patterns outlined by Schramm (1998) still remain valid. ...
... Drifting algae can provide ecological services to the coastal environment (Salovius et al. 2005, Nyberg et al. 2009). On the other hand, dense blooms or mats of unattached opportunistic seaweeds that typically develop as a result of eutrophication, such as Ceramium tenuicorne, Vertebrata fucoides, Chaetomorpha linum, Cladophora species or Ulva species (Norkko and Bonsdorff 1996a,b, Schramm 1998, Steinhagen et al. 2018, also have negative impact on the Baltic Sea and Wadden Sea environment. They very often cause anoxia and environmental deterioration (Norkko and Bonsdorff 1996a,b, Osterling and Pihl 2001, Lauringson and Kotta 2006, Holmer and Nielsen 2007, Arroyo et al. 2012, Quillien et al. 2016, Steinhagen et al. 2018) and in the short term their removal could be a countermeasure against these negative effects. ...
Due to low salinity and lack of hard substrata, the Baltic Sea and Kattegat area and German and Danish North Sea coasts are characterized by a relatively low diversity of seaweeds. At the same time the areas are severely eutrophicated, which has caused extensive shifts in macroalgal communities toward opportunistic species. Unattached seaweed communities dominated by Furcellaria lumbricalis , which have been a resource for hydrocolloid production since the 1940s, have been severely reduced due to eutrophication and unsustainable harvesting and are nowadays only exploited commercially in Estonia. On the other hand, the biomass of opportunistic seaweeds of various red, green and brown algal genera has increased. They cause ecological problems, are a nuisance on many tourist beaches and constitute at the same time a potential bioresource that is so far only exploited to a limited extent for production of energy and fertilizer. Commercial seaweed cultivation is largely focused on Saccharina latissima and still very limited, but is currently being expanded as a compensation measure for sea-based fish aquaculture. Also land-based seaweed cultivation is primarily employed for recycling of nutrients in tank animal aquaculture, but in most cases so far only on an experimental scale.
... The microand macromorphological characters of the vouchers were assessed using the above-mentioned criteria. When possible, small thallus pieces of the historical voucher specimens were sampled for molecular verification of species identity, as described in Steinhagen et al. (2018a). ...
... One morphotype was only observed on North Sea coasts and corresponded to the morphology of the tubular and branched type material (Linnaeus, 1753). However, as already discussed elsewhere (Steinhagen et al., 2018a), genetically indistinguishable specimens from the Baltic and Wadden Seas exhibited a completely different morphology that was consistently distromatic and sheet-like. Evidently, the distromatic morphology of U. compressa strongly overlaps with the allegedly unique morphology of U. lactuca, thereby causing a considerable amount of historical taxonomic confusion (Steinhagen et al., 2018a). ...
... However, as already discussed elsewhere (Steinhagen et al., 2018a), genetically indistinguishable specimens from the Baltic and Wadden Seas exhibited a completely different morphology that was consistently distromatic and sheet-like. Evidently, the distromatic morphology of U. compressa strongly overlaps with the allegedly unique morphology of U. lactuca, thereby causing a considerable amount of historical taxonomic confusion (Steinhagen et al., 2018a). Based on the results of the present study, U. lactuca in northern Germany is only present on Helgoland (Table 2, Supplementary table 2), whereas historical records from the Baltic Sea (Schories et al., 2009) are misidentified U. compressa specimens (Steinhagen et al., 2018a). ...
DNA barcoding analysis, using tufA, revealed considerable differences between the expected and observed species inventory of
Ulva sensu lato in the Baltic and North Sea areas of the German state of Schleswig-Holstein. Of 20 observed genetic entities, at
least four (U. australis, U. californica, U. gigantea and Umbraulva dangeardii) had been introduced recently, whereas three
others (one Ulva sp. and two Blidingia spp.) could not be identified at the species level and could also represent recently
introduced species. In addition, the observed distributions of Kornmannia leptoderma and U. rigida were much more
extensive than indicated by historical records, whereas Blidingia minima and Gayralia oxysperma were absent or much less
common than expected. Barcoding analysis also revealed that both U. tenera (type material) and U. pseudocurvata (historical
vouchers) from Helgoland, an off-shore island in the North Sea, actually belong to U. lactuca, a species that appears to be
restricted to this island. Furthermore, past morphological descriptions of U. intestinalis and U. compressa have apparently
been too restrictive and have been responsible for numerous misidentifications. The same is true for U. linza, which, in
northern Germany, clusters into two genetically closely related but morphologically indistinguishable entities. One of these
entities is present on Helgoland, while the second is present on North Sea and Baltic Sea mainland coasts.
... %). Specimens belonging to this cluster had a broad distribution and were found in all three main study areas at remote and protected sites, as well as in highly trafficked waters (see also Steinhagen et al. [2018b] and Chapter II). ...
... Howeverand as also observed by others )tubular branched individuals occasionally occur in our study area and this divergent morphology is promoted by low salinities (Steinhagen et al., 2018b; see also Chapter II). ...
... One of them was only found on North Sea coasts and is in full agreement with the tubular and branched type material . However -and as discussed elsewhere in detail (Steinhagen et al., 2018a; see also Chapter IV) -all Baltic Sea and many Wadden Sea specimens of this entity exhibited a completely different morphology that was always distromatic and sheet-like. Yet, both morphologies are genetically indistinguishable. ...
In this doctoral project, I investigated the recent inventory, distribution and phylogenetic relationships of Ulva sensu lato in northern Germany, including sampling sites at the Baltic Sea, Wadden Sea and on Helgoland. Furthermore, I compared the recent results with historic findings. Therfore, this thesis constitutes a complete revision of the species inventory of Ulva sensu lato in northern Germany. Assessments of biodiversity were based on both the analysis of classical morphological characters and DNA barcoding. Phylogenetic analysis of more than 370 sequences of the tufA marker gene revealed the presence of 20 different species in German waters.
... Crossing strains with different mating types is well-described (Føyn, 1959(Føyn, , 1960Hoxmark, 1976). Such crossing experiments have demonstrated that U. mutabilis and U. compressa are fully interfertile (Steinhagen et al., 2018), with the latter being a morphologically variable species that has a global distribution and is involved in green tide formation (Steinhagen et al., 2018(Steinhagen et al., , 2019. To remain consistent with the existing literature and avoid confusion with older literature in which natural isolates were solely identified based on morphological characteristics, we will keep the distinction between U. mutabilis (lab strains) and U. compressa (natural populations) throughout this perspective. ...
... Individuals can form blades, tubes, or branched thalli ( Figure 2a). Populations thrive in broad irradiance, temperature, or salinity gradients (Steinhagen et al., 2019;Taylor et al., 2001) and show high resistance to both heavy metal contamination (Ratkevicius et al., 2003) and organic micro-pollutants (Hardegen et al., 2023). The power of population genomics should therefore be harnessed to explore genomic diversity using a pan-genome to associate genetic regions to specific phenotypes. ...
Green seaweeds exhibit a wide range of morphologies and occupy various ecological niches, spanning from freshwater to marine and terrestrial habitats. These organisms, which predominantly belong to the class Ulvophyceae, showcase a remarkable instance of parallel evolution toward complex multicellularity and macroscopic thalli in the Viridiplantae lineage. Within the green seaweeds, several Ulva species ("sea lettuce") are model organisms for studying carbon assimilation, interactions with bacteria, life cycle progression, and morphogenesis. Ulva species are also notorious for their fast growth and capacity to dominate nutrient-rich, anthropogenically disturbed coastal ecosystems during "green tide" blooms. From an economic perspective, Ulva has garnered increasing attention as a promising feedstock for the production of food, feed, and biobased products, also as a means of removing excess nutrients from the environment. We propose that Ulva is poised to further develop as a model in green seaweed research. In this perspective, we focus explicitly on Ulva mutabilis/compressa as a model species and highlight the molecular data and tools that are currently available or in development. We discuss several areas that will benefit from future research or where exciting new developments have been reported in other Ulva species.
... The use of molecular markers (e.g., ITS, rbcL, and tufA) for species identification has become the mainstream method to ensure the accuracy and credibility of identification results (e.g. Hofmann et al., 2010;Hughey et al., 2019;Steinhagen et al., 2019). However, due to the limited differentiation signals of these marker sequences, their resolution is inadequate for identifying closely related Ulva species. ...
... Our results of phylogenomic analysis well supported taxonomic revisions of some species names at the genomic level (Figures 10, 11), e.g. U. mutabilis Föyn, U. pertusa Kjellman and U. fasciata Delile are taxonomic synonyms of U. compressa Linnaeus (Steinhagen et al., 2019), U. australis Areschoug (Couceiro et al., 2011) and U. lactuca Linnaeus (Hughey et al., 2019), respectively. It is worth emphasizing that our results show that eight of 40 Ulva plastomes were assigned wrong species names reported at first Wang et al., 2020;Fort et al., 2021;Hughey et al., 2021). ...
To understand the evolutionary driving forces of chloroplast (or plastid) genomes
(plastomes) in the green macroalgal genus Ulva (Ulvophyceae, Chlorophyta), in
this study, we sequenced and constructed seven complete chloroplast genomes
from five Ulva species, and conducted comparative genomic analysis of Ulva
plastomes in Ulvophyceae. Ulva plastome evolution reflects the strong selection
pressure driving the compactness of genome organization and the decrease of
overall GC composition. The overall plastome sequences including canonical
genes, introns, derived foreign sequences and non-coding regions show a
synergetic decrease in GC content at varying degrees. Fast degeneration of
plastome sequences including non-core genes (minD and trnR3), derived foreign
sequences, and noncoding spacer regions was accompanied by the marked
decrease of their GC composition. Plastome introns preferentially resided in
conserved housekeeping genes with high GC content and long length, as might
be related to high GC content of target site sequences recognized by intronencoded
proteins (IEPs), and to more target sites contained by long GC-rich
genes. Many foreign DNA sequences integrated into different intergenic regions
contain some homologous specific orfs with high similarity, indicating that they
could have been derived from the same origin. The invasion of foreign sequences
seems to be an important driving force for plastome rearrangement in these IRlacking
Ulva cpDNAs. Gene partitioning pattern has changed and distribution
range of gene clusters has expanded after the loss of IR, indicating that genome
rearrangement was more extensive and more frequent in Ulva plastomes, which
was markedly different from that in IR-containing ulvophycean plastomes. These
new insights greatly enhance our understanding of plastome evolution in
ecologically important Ulva seaweeds.
... In selected sub-regions of the Wadden Sea 60% of the tidal flats were completely covered by algal mats made up of Ulva species (Kolbe et al., 1995). Despite some reduction and regulation of nutrient discharges since, all inner coastal waters of the German Bight, thus including the Wadden Sea, have recently been classed as a 'problem area', indicating substantial eutrophication effects (Brockmann et al., 2018), and Ulva is still noted across Wadden Sea areas (Geertz-Hansen et al., 1993;Kamermans et al., 1998;Rossi, 2006;Steinhagen et al., 2019b). Once algal detritus is buried into sediment it can cause disjunct distributions of small enriched patches (Kamermans et al., 1998), directly impacting the habitat of any infauna. ...
... Thalli of the green macroalga Ulva compressa (Linnaeus, 1753) were collected from an intertidal mudflat in List on the island of Sylt (55 • 01 ′ 08.2"N 8 • 26 ′ 22.5 ′′ E). The species classification of U. compressa E.M. Farrell et al. was not genetically determined, as a large population of U. compressa is knowingly present at the collection site (Steinhagen et al., 2019a) and within the Wadden Sea there is strong interconnectivity between Ulva populations (Steinhagen et al., 2019a;Steinhagen et al., 2019b). The algae used in this study were thus assumed to be U. compressa (hereafter referred to as "Ulva"). ...
Bioturbation is a central transport process for ecosystem functioning, especially in large soft sediment habitats like the Wadden Sea. The amphipod C. volutator is a dominant bioturbator in the Wadden Sea, due to its great abundance and almost continuous particle movement. Expedition or loss of its bioturbation activity could thus hold ramifications for ecosystem functioning within sediments, like carbon sequestration and nutrient recycling. Here we test the effect that temperature and organic enrichment have on the bioturbation of C. volutator; two prevalent abiotic factors in the Corophiid's habitat that have fluctuated over recent decades, and are expected to change in the future. In-situ experiments were conducted under 8 and 15 °C, with varying levels (0 g, 0.1 g, and 0.2 g) of powdered Ulva compressa enriching cores containing C. volutator. We found a significant interaction effect of temperature and organic enrichment on the bioturbation rate of the amphipod, with bioturbation only increasing with added organic enrichment at 15 °C. Further, a threshold within our experiments was also reached under 15 °C, where the amphipod ceased to expedite bioturbation under higher organic enrichment. This upper limit on this dominant bioturbation imposed with organic enrichment emphasizes the sensitivity of C. volutator. Our findings reveal bioturbation can be limited by temperature in colder months, and opposingly, limited by organic enrichment under warmer conditions. In future Wadden Sea scenarios where temperature is predicted to be warmer and winters milder, enhanced bioturbation activity by C. volutator could prove crucial in continued ecosystem functions.
... In the Baltic Sea, the first study using DNA barcoding for biodiversity assessments was published in 2008 and since then the method has been increasingly used in ecological studies (Figure 1.1.2). Studies include the taxonomic identification of diverse species, including Bryoazoa (Nikulina 2008), Gammarus (Costa et al. 2009), diatoms (Pniewski et al. 2010), Ulva (Steinhagen et al. 2019b), nematodes (Phelan et al. 2016), or the shipworm Teredo (Weigelt et al. 2016). Biodiversity observations using metabarcoding revealed that bacterial communities changed along the 2000 km salinity gradient from the northern freshwater to the southern marine region with no decline at brackish conditions, in contrast to multicellular organisms (Herlemann et al. 2011). ...
... Metabarcoding including eDNA is also increasingly used as a useful tool for the detection of invasive species in the Baltic Sea, including amphipods (Grabowski et al. 2012, Rewicz et al. 2020, Gammarus tigrinus (Rewicz et al. 2019(Rewicz et al. , 2020, the seaweed Ulva (Steinhagen et al. 2019b(Steinhagen et al. , 2019a, plankton species (Grabowski et al. 2012, Sukhikh et al. 2013, the soft bottom clam Mya (Ardura and Zaiko 2018), crab species (Forsström and Vasemägi 2016) and bivalves (Ardura et al. , 2017. Since the detection of novel species in an area is essentially a presence/absence survey, such studies suffer the least from other problems associated with barcoding, such as DNA degeneration and difficulties of abundance quantification. ...
This meta-data collection is based on 164 peer-reviewed stable isotope articles published in the Baltic Sea ecology field. The studies that have been published cover searches from 1992 to 2021 (July 10). The meta-data collection is a resource for both experienced isotope ecologists and newcomers to grasp and access all published Baltic Sea SIA work on any fundamental or applied research topic, sub-region, taxon, or trophic group of interest. It also represents an ideal foundation for an envisioned "Baltic Isobank" database of primary stable isotope data, following the vision outlined in Eglite et al. (2022).
Baltic Sea stable isotope ecology meta-data collection is available on Dryad: https://doi.org/10.5061/dryad.sj3tx966d
... In addition to morphology-based taxonomy, crossing experiments have been used to test the biological species concept and refine species boundaries, perhaps more in Ulva than in any other group of seaweeds (Føyn 1955;Bliding 1963;Larsen 1981). More recent studies have used mating experiments in combination with DNA and morpho-anatomical data to describe new species, such as U. ohnoi and U. limnetica (Hiraoka et al. 2004;Ichihara et al. 2009), or to elucidate species boundaries in taxonomically challenging complexes such as U. flexuosa, U. mediterranea (now U. aragoënsis) and U. californica (Hiraoka et al. 2017), U. reticulata and U. ohnoi , U. prolifera and U. linza (Cui et al. 2018), and U. compressa and U. mutabilis (Steinhagen et al. 2018b) (all taxon names with authorities are listed in Supplementary Table S1). ...
... In recent years, combining DNA sequences and morphoanatomy has become a standard approach in Ulva diversity studies Hayden and Waaland 2004;Loughnane et al. 2008;Shimada et al. 2008;Heesch et al. 2009;Kraft et al. 2010;Mares et al. 2011;Guidone et al. 2013;Kirkendale et al. 2013;Ogawa et al. 2013;Kiana et al. 2016;Hanyuda and Kawai 2018;Krupnik et al. 2018;Steinhagen et al. 2018b;Kang et al. 2019;Tonatiuh et al. 2019;Fort et al. 2020a;2022;Xie et al. 2020;Melton III and Lopez-Bautista 2021;Tran et al. 2021). Markers that are frequently used include the nuclear ribosomal internal transcribed spacer (nrDNA ITS), the plastid encoded gene ribulose-bisphosphate carboxylase (rbcL), and more recently the plastid translation elongation factor Tu (tufA). ...
The green seaweed Ulva is important from ecological and economic perspectives, but the identification of species is often problematic. Here we assessed and discussed different perspectives to establish a stable taxonomic framework for Ulva, which will benefit both ecological and applied research. We evaluated (1) the performance of commonly used DNA-barcode markers (ITS rDNA, rbcL, and tufA) using species delimitation methods (PTP and GMYC), (2) the usage of species names in the literature, and (3) the geographic coverage of genetic data to identify poorly sampled regions. Species delimitation employing the tufA gene was the most consistent across methods. Not surprisingly, DNA-based species delimitation was often in disagreement with traditional morphology-based species definitions. Biological species concepts, where tested, proved to be generally narrower than DNA-based species delimitation. Although the use of molecular markers has greatly improved our view of Ulva diversity, the names associated with DNA sequences in public databases are often unreliable, complicating species identification. Recently, sequencing type materials has considerably reduced the gap between DNA sequence data and Linnaean names, but our knowledge on Ulva diversity remains inadequate, especially in tropical regions. Perspectives for Ulva taxonomy include the consistent use of multiple DNA-barcode markers assisted by species delimitation methods, applications of genomic data, and crossing experiments. To arrive at a stable nomenclature, we outline the benefits and shortcomings of adhering to the rules and practices of the International Code of Nomenclature for algae, fungi, and plants, for example, by sequencing name-bearing types and discuss alternative approaches.
... Even though less than 0.1% of the total seaweed production is accounted for by green seaweeds [2,16], the green seaweed Ulva-generally known as Sea Lettuce-has received a lot of attention by the aquaculture sector due to its compelling traits [17][18][19]. Combining the characteristics of being ubiquitously distributed [20], having a high environmental tolerance and being resistant towards changing abiotic factors [21][22][23], Ulva spp. exhibit high and fast growth rates [18,24] and are capable of thriving under high stocking densities [25,26], which makes them excellent aspirants for large-scale aquacultures. ...
... N 11 • 6 42.84 E). Because the genus Ulva exhibits several species with extraordinary phenotypic plasticity [20][21][22][23], adequate identification of the used biomass can, in most of the cases, only be obtained by applying modern molecular identification techniques such as DNA barcoding. Detailed information on applied cultivation conditions as well as molecular identification of the parental biomass of U. fenestrata can be found in [40]. ...
The growing world population demands an increase in sustainable resources for biorefining. The opening of new farm grounds and the cultivation of extractive species, such as marine seaweeds, increases worldwide, aiming to provide renewable biomass for food and non-food applications. The potential for European large-scale open ocean farming of the commercial green seaweed crop Ulva is not yet fully realized. Here we conducted manipulative cultivation experiments in order to investigate the effects of hatchery temperature (10 and 15 °C), nutrient addition (PES and 3xPES) and swarmer density (500 and 10,000 swarmers ml−1) on the biomass yield and biochemical composition (fatty acid, protein, carbohydrate, pigment and phenolic content) of off-shore cultivated Ulva fenestrata in a Swedish seafarm. High seedling densities were optimal for the growth of this northern hemisphere crop strain and significantly increased the mean biomass yield by ~84% compared to low seedling densities. Variations of nutrients or changes in temperature levels during the hatchery phase were not necessary to increase the subsequent growth in an open-water seafarm, however effects of the factors on the thallus habitus (thallus length/width) were observed. We found no significant effect of the environmental factors applied in the hatchery on the total fatty acid or crude protein content in the off-shore cultivated Ulva. However, low seedling density and low temperature increased the total carbohydrate content and furthermore, high temperature in combination with high nutrient levels decreased the pigment content (chlorophyll a, b, carotenoids). Low temperature in combination with high nutrient levels increased the phenolic content. Our study confirms the successful and sustainable potential for large-scale off-shore cultivation of the Scandinavian crop U. fenestrata. We conclude that high seedling density in the hatchery is most important for increasing the total biomass yield of sea-farmed U. fenestrata, and that changing temperature or addition of nutrients overall does not have a large effect on the biochemical composition. To summarize, our study contributes novel insights into the large-scale off-shore cultivation potential of northern hemisphere U. fenestrata and underpins suitable pre-treatments during the hatchery phase of seedlings to facilitate a successful and cost-efficient large-scale rope cultivation.
... This alga is known for its rapid, proliferous growth in eutrophic conditions, even forming green tides (Blomster et al., 2002;Liu et al., 2013). U. compressa usually displays great morphological plasticity due to temperature, salinity, irradiance, wave exposure, and nutrient content (Steinhagen et al., 2019). Previously, two mitochondrial genomes of U. compressa, one complete mitogenome (GenBank accession number KX595276) from Southern Yellow Sea, China (Cai et al., 2018a), and another nearly complete mitogenome (MK069586) from China, had been sequenced. ...
... Uco2 Uco3 Uco4 Uco5 information among these five samples of U. compressa, new DNA markers could be designed to study the population diversity and phylogeography of the green-tide forming alga (Steinhagen et al., 2019). Considering the marked intraspecific variations in genome size, intron content, genome architecture and gene mutations in U. compressa, the mitogenome will be a valuable tool to help us understand the native or non-indigenous nature of the cosmopolitan Ulva species. ...
To gain further insights into intraspecific evolution of Ulva mitochondrial genomes, the mitogenomes of three morphotypes of the green-tide forming alga, Ulva compressa Linnaeus from China and United States, were sequenced and compared with the available data from Ulvophyceae. The U. compressa mitogenomes displayed substantial genome size variation at intraspecific level ranging from 61,700 to > 66,587 bp, due to different acquisitions of foreign DNA fragments, gain or loss of both group I and II introns, and non-coding intergenic spacer regions. The U. compressa mitogenomes harbored variable gene content ranging from 69 genes (including orfs) in Uco1 to 76 in Uco5, and contained different intron content from 4 introns in Uco3 and Uco4 to 7 in Uco1. A total of 63 genes and only two group IB introns (intron cox1-1107 and cox1-1125) were shared by these five mitogenomes. The U. compressa mitogenomes accumulated many more inverted repeat (IR) elements, ranging from 45 in Uco1 to 88 in Uco2, than that of the other Ulva species (3–34). A locally collinear block of eight genes (rps11-rps19-rps4-rpl16-trnR-trnQ-trnE-trnS) with the size of 3,631 bp has been inverted only in Uco1 indicating that the rearrangement event happened after its divergence from Uco2–5 and might be related to a specific IR element. The majority of the common genes (~76%) displayed high identity (>98%) among these five mitogenomes, while some low values were observed in six genes mainly due to duplication and insertion/deletion mutations of small DNA fragments. Our study presented the first case of multiple intraspecific variations in ulvophycean mitogenomes, and indicated that the mitogenome will be a valuable tool for understanding the native or non-indigenous nature of the cosmopolitan Ulva species.
... As previously shown in U. mutabilis (Føyn 1958, 1959, Fjeld and Borresen 1975, Børresen and Fjeld 1977) also in U. compressa different shapes and morphologies have been observed (Tan et al. 1999, Steinhagen 2018. These led to suggestions that various forms of environmental stressors or the absence or presence of certain bacteria may influence the morphogenetic switch between so-called "leafy" and "cylindrical" morphologies of U. compressa (Tan et al. 1999, Wichard 2015. ...
... Some of the added and peer reviewed reference organisms corresponded to the morphological species concept of Linnaeus (1753) and represented the authentic U. compressa morphotype. Due to the strong morphological variability in 2 U. compressa certain morphotypes were only recently revealed by molecular techniques in more recent studies (Steinhagen 2018). ...
As one of the most abundant and ubiquitous representatives of marine and brackish coastal macrophytobenthos communities, the genus Ulva is not only an important primary producer but also of ecological and morphogenetic interest to many scientists. Ulva mutabilis became an important model organism to study morphogenesis and mutualistic interactions of macroalgae and microorganisms. Here we report that our collections of Ulva compressa Linnaeus (1753) from Germany are conspecific with the type strains of the model organism Ulva mutabilis Føyn (1958), which were originally collected at Olhão on the south coast of Portugal and have from that time on been maintained in culture as gametophytic and parthenogenetic lab strains. Different approaches were used to test conspecificity: (1) comparisons of vegetative and reproductive features of cultured material of U. mutabilis and German U. compressa demonstrated a shared morphological pattern; (2) gametes of U. compressa and U. mutabilis successfully mated and developed into fertile sporophytic first‐generation offspring; (3) molecular phylogenetics and species delimitation analyses based on the Generalized Mixed Yule‐Coalescent method showed that U. mutabilis isolates (sl‐G[mt+]) and (wt‐G[mt‐]) and U. compressa belong to a unique Molecular Operational Taxonomic Unit. According to these findings, there is sufficient evidence that U. mutabilis and U. compressa should be regarded as conspecific.
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... It occupies the first 5 m of the marine areas' surfaces and can be found either in shallow water or in eutrophic zones. It is distinguished by a very thin thallus with a leaf-shaped, ribbon-like, or tubular form and green color that can be transparent under stress (Steinhagen et al., 2019). Currently, 102 species (accepted taxonomically) have been identified worldwide (Guiry and Guiry, 2022). ...
Seaweed surfaces harbor diverse epibiotic bacterial communities with functions related to morphogenesis, host health, and defense. Among seaweed holobionts, culturable strains can represent innovative sources of bioactive compounds and enzymes. The global industrial demand for microbial enzymes is continually growing in order to improve certain manufacturing processes with new perspectives of industrial exploitation. In this regard, the present study focuses on the enzymatic production and the antimicrobial activities of culturable epibiotic bacteria of Ulva from the Tunisian coast. Culturable associated bacteria were isolated and molecular identification was realized by 16S rRNA gene sequencing. For each strain, eight enzymatic activities were investigated: amylase, hemolysis, DNase, cellulase, lecithinase, lipase, gelatinase, and chitinase. The antimicrobial activity of Ulva-associated bacteria was evaluated against seven pathogenic bacteria, Escherichia coli, Vibrio anguillarum, Vibrio alginoliticus, Pseudomonas aeruginosa, Aeromonas hydrophila, Salmonella typhymurium, and Staphylococcus aureus, and one yeast, Candida albicans. The antibiotic resistance of isolated strains was determined for 15 commonly used antibiotics. The phylogenetic analysis revealed that the isolates belonged to Alphaproteobacteria (3), Gammaproteobacteria (5), Actinobacteria (3), and Firmicutes (4) phyllum. The majority of the isolates (66%) produced simultaneously more than one enzyme. Hemolysis was produced by 46.6% of isolates, while DNase was produced by 33% of strains. On the other hand, 13% of strains produced lecithinase, gelatinase, cellulase, and lipase. No chitinase was produced by the isolated bacteria. In addition, 60% of isolates displayed antimicrobial activity against at least one pathogenic strain. All Ulva ohnoi-associated bacteria were resistant to at least seven commonly used antibiotics. These results highlighted the occurrence of several enzymatic activities within Ulva-associated bacteria that can have potential uses in the industrial sector.
... The new species U. vietnamensis (=VN sp1) can be distinguished morphologically from other tubular Ulva species by the narrow thallus, and the high number of pyrenoids. Ulva tepida, U. meridionalis, U. compressa Linnaeus, U. linza, U. limnetica and U. intestinalis Linnaeus have broader thalli (Bliding 1963;Blomster et al. 1998;Ichihara et al. 2009;Horimoto et al. 2011;Masakiyo and Shimada 2014;Steinhagen et al. 2018b), while U. ralfsii (Harvey) Le Jolis is narrower (filiform). Ulva clathrata (Roth) C. Agardh has short spine-like branchlets throughout the thallus (Bliding 1963), which were not observed in U. vietnamensis. ...
Species diversity of Ulva in Vietnam was investigated using three commonly used genetic markers, the nuclear encoded rDNA ITS region and the plastid encoded rbcL and tufA genes. Single locus species delimitation methods, complemented with morphological and ecological information resulted in the delimitation of 19 species. This diversity is largely incongruent with the traditional understanding of Ulva diversity in Vietnam. Only four species identified in this study, U. lactuca, U. reticulata, U. spinulosa, and U. flexuosa, have been previously reported, and seven species, U. ohnoi, U. tepida, U. chaugulii, U. kraftiorum, U. meridionalis, U. limnetica, and U. aragoënsis, are recorded for the first time from Vietnam. Seven genetic clusters could not be associated with species names with certainty. A new species, U. vietnamensis, is described from marine to brackish coastal areas from southern Vietnam based on its morphological and molecular distinctiveness from the currently known Ulva species. A comparison with recent molecular‐based studies of Ulva diversity showed that species composition in Vietnam is similar to that of adjacent countries, including Japan, China, as well as Australia. Our study emphasizes the importance of molecular data in the assessment of Ulva diversity, and indicates that a lot of diversity may still remain to be discovered, especially in tropical regions.
... Ulva comprises diverse species which present two main morphologies, either tubular monostromatic (single cell layer) or foliose distromatic (two cell layers) [2,3]. Some species also present both morphotypes, such as U. compressa [4,5]. Thus, this morphological diversity is not solely explained by genetic variability, but also by considerable morphological plasticity in response to environmental conditions and variations in the associated microbiome [1,6,7]. ...
Sea lettuce (Ulva spp.), with its worldwide distribution and remarkable ability to grow rapidly under various conditions, represents an important natural resource that is still under-exploited. Its biomass can be used for a wide range of applications in the food/feed, pharmaceutical, nutraceutical, biofuel, and bioremediation industries. However, knowledge of the factors affecting Ulva biomass yield and composition is far from complete. Indeed, the respective contributions of the microbiome, natural genetic variation in Ulva species, environmental conditions and importantly, the interactions between these three factors on the Ulva biomass, have been only partially elucidated. Further investigation is important for the implementation of large-scale Ulva aquaculture, which requires stable and controlled biomass composition and yields. In this review, we document Ulva biomass composition, describe the uses of Ulva biomass and we propose different strategies for developing a sustainable and profitable Ulva aquaculture industry.
... The species-rich macroalgal genus Ulva currently contains at least 99 taxonomically accepted species worldwide (Guiry and Guiry, 2022), as well as some unconfirmed cryptic species (Steinhagen et al., 2019a,b). Ulva species have high morphological diversity and plasticity at the intraspecific level (Gao et al., 2016;Steinhagen et al., 2019c), so accurate and reliable species identification often requires the use of common DNA markers (e.g., ITS, rbcL, tuf A, etc.) (Blomster et al., 2002;Liu et al., 2013;Fort et al., 2020). Organelle genome as a molecular marker can make us more accurately understand the concept of Ulva species and more comprehensively understand their genetic diversity and evolutionary relationships, which could not be done by a single or several DNA markers. ...
Comparative mitogenomics of Ulva species have revealed remarkable variations in genome size due to the integration of exogenous DNA fragments, the proliferation of group I/II introns, and the change of repeat sequences. The genus Ulva is a species-rich taxonomic group, containing a variety of green-tide forming algae. In this study, five complete mitogenomes of the green-tide forming macroalga, Ulva meridionalis R.Horimoto & S.Shimada, were assembled and compared with the available ulvophycean mtDNAs. The main circular mitogenomes of U. meridionalis ranged from 82.94 kb to 111.49 kb in size, and its 111.49-kb mitogenome was the largest Ulva mitogenome sequenced so far. The expansion of U. meridionalis mitogenomes is mainly due to the tandem integration of a 5.36-kb mitochondrial circular plasmid (pUme), as well as the proliferation of introns. An intact DNA-directed RNA polymerase gene (rpo) was present in pUme of U. meridionalis and were then detected in two putative plasmids (pUmu1 and pUmu2) found in Ulva mutabilis. The observed integration of the circular plasmid into U. meridionalis mitogenomes seems to occur via homologous recombination, and is a more recent evolutionary event. Many highly homologous sequences of these three putative plasmids can be detected in the other Ulva mtDNAs sequenced thus far, indicating the integration of different mitochondrial plasmid DNA into the mitogenomes is a common phenomenon in the evolution of Ulva mitogenomes. The random incidence of destruction of plasmid-derived rpos and open reading frames (orfs) suggests that their existence is not the original characteristic of Ulva mitogenomes and there is no selective pressure to maintain their integrity. The frequent integration and rapid divergence of plasmid-derived sequences is one of the most important evolutionary forces to shape the diversity of Ulva mitogenomes.
... A recent study on the vegetative and reproductive features of U. mutabilis (collected from the Ria Formosa in Portugal, locus typicus [48]) and U. compressa (collected from the Baltic Sea in Germany and the Yellow Sea in China) revealed that gametes from both species could combine and develop into fertile sporophytes [40,[49][50][51]. Following phylogenetic analyses, it was discovered that these species are conspecific. ...
The marine green macroalga Ulva (Chlorophyta, Ulvales), also known as sea lettuce, coexists with a diverse microbiome. Many Ulva species proliferate in nature and form green algal blooms (“green tides”), which can occur when nutrient-rich wastewater from agricultural or densely populated areas is flushed into the sea. Bacteria are necessary for the adhesion of Ulva to its substrate, its growth, and the development of its blade morphology. In the absence of certain bacteria, Ulva mutabilis develops into a callus-like morphotype. However, with the addition of the necessary marine bacteria, the entire morphogenesis can be restored. Surprisingly, just two bacteria isolated from U. mutabilis are sufficient for inducing morphogenesis and establishing the reductionist system of a tripartite community. While one bacterial strain causes algal blade cell division, another causes the differentiation of basal cells into a rhizoid and supports cell wall formation because of a low concentration of the morphogen thallusin (below 10⁻¹⁰ mol/L). This review focuses on the research conducted on this topic since 2015, discusses how U. mutabilis has developed into a model organism in chemical ecology, and explores the questions that have already been addressed and the perspectives that a reductionist model system allows. In particular, the field of systems biology will achieve a comprehensive, quantitative understanding of the dynamic interactions between Ulva and its associated bacteria to better predict the behavior of the system as a whole. The reductionist approach has enabled the study of the bacteria-induced morphogenesis of Ulva. Specific questions regarding the optimization of cultivation conditions as well as the yield of raw materials for the food and animal feed industries can be answered in the laboratory and through applied science. Genome sequencing, the improvement of genetic engineering tools, and the first promising attempts to leverage macroalgae–microbe interactions in aquaculture make this model organism, which has a comparatively short parthenogenetic life cycle, attractive for both fundamental and applied research. The reviewed research paves the way for the synthetic biology of macroalgae-associated microbiomes in sustainable aquacultures.
... One exception is Blidingietum minimae den Hartog 1959, which appears to be a cluster of multiple distinct communities that are adapted to similar, but still different, environments. Another possible exception could be past Baltic Sea records of Ulvetum compressae (Berner 1931) Giaccone 1993, given that U. compressa virtually never exhibits its type morphology in the Baltic Sea (Steinhagen et al. 2019b). We did not encounter Ulvetum compressae (Berner 1931) Giaccone 1993. ...
Supralittoral and shallow water seaweed communities are particularly exposed to impacts such as climate change and disturbance by humans. Therefore, their classification, the study of composition, and the monitoring of their structural changes are particularly important. A phytosociological survey of the supralittoral and upper sublittoral vegetation of the South West Baltic Sea revealed eight phytobenthos communities with two variants comprising 35 taxa of macrophytes (18 taxa of Chlorophyta, 13 taxa of Rhodophyta and four taxa of Phaeophyceae, Ochrophyta). Five of the eight communities were dominated by Ulvales (Ulva intestinalis, Kornmannia leptoderma, and three Blidingia species), the other three by Fucus vesiculosus. Most Fucus vesiculosus-dominated communities contained U. intestinalis and U. linza as subdominants. Only one of the communities had until now been described as an association ( Ulvetum intestinalis Feldman 1937). The syntaxonomic composition of the investigated vegetation includes both phytocenoses with the domination of green algae ( Ulvetum intestinalis Feldman 1937 and communities of Blidingia marginata, unidentified Blidingia spp. and Kornmannia leptoderma), as well as a number of communities dominated by Fucus vesiculosus. Mainly boreal Atlantic species and cosmopolitans make up the bulk of the species in these associations.
... S1 to S3 in appendix), which confirms earlier reports of increasing standing stocks of Ceramium tenuicorne in the area (Schramm and Nienhuis 1996). Interestingly, the genus Ulva was much less abundant, although it is by far the most abundant nuisance seaweed on a global scale (Smetacek and Zingone 2013) and ecological impact of Ulva blooms in the region has been observed on a local scale (Steinhagen et al. 2018). Taken together, the total amount of "other algae", consisting primarily of ephemeral species today, increased from less than 0.225 kg per m in 1977 (Grave and Moeller 1982) to 1.4 kg per m in 2012/2013 (Tab S3 in appendix). ...
Beach visitors rate beach quality in large part by its appearance. Removal of natural beach litter (called beach wrack) has, therefore, high priority for beach managers in coastal areas dependent on revenues from tourism. Focusing on the German Baltic Sea coast, the amount of beach wrack has increased by a factor of approximately 3.4 between 1977 and 2012/2013. At the same time, the composition of macrophyte communities underwent a severe change from late successional stages (eelgrass and bladder wrack) toward more ephemeral communities. Correspondingly, the contribution of bladder wrack to seaweed litter alone dropped from 75% in 1977 to 18.1% today, while the contribution of ephemeral and nutrient-opportunistic seaweeds increased by a factor larger than 6.2 to approximately 44%. Such seaweed opportunists could have a higher potential for olfactorial nuisance than late successional macrophytes. To test this hypothesis, odors extracted from equal amounts of nutrient-opportunistic and non-opportunistic species that had been partially degraded under equal conditions were compared in a public survey. Participants graded the smell of opportunistic species, in particular Ceramium tenuicorne, consistently as more intense and less pleasant than the odor of non-opportunistic species. The particularly high potential of Ceramium litter and the relatively lower potential of eelgrass litter for deterrence were confirmed in field experiments. We conclude that the documented compositional shift in macrophyte communities at German Baltic Sea coasts since the onset of eutrophication has caused a shift of beach wrack composition toward species with a higher potential for olfactorial deterrence, which could explain recent concerns of beach managers about beach wrack despite the limited increase of biomass in the study area.
... While research on Ulva is spread across multiple species, U. mutabilis [now also including conspecific Ulva compressa (140,141)] is a promising candidate model organism for the genus Ulva (156) and related groups of ulvophytes. U. mutabilis has several key advantages, including a relatively high rate of spontaneous mutability to produce stable morphotypes such as Slender, a life cycle that can be easily controlled (146,156), and a sequenced haploid genome (37) ( Table 1). ...
The repeated evolution of multicellularity across the tree of life has profoundly affected the ecology and evolution of nearly all life on Earth. Many of these origins were in different groups of photosynthetic eukaryotes, or algae. Here, we review the evolution and genetics of multicellularity in several groups of green algae, which include the closest relatives of land plants. These include millimeter-scale, motile spheroids of up to 50,000 cells in the volvocine algae; decimeter-scale seaweeds in the genus Ulva (sea lettuce); and very plantlike, meter-scale freshwater algae in the genus Chara (stoneworts). We also describe algae in the genus Caulerpa, which are giant, multinucleate, morphologically complex single cells. In each case, we review the life cycle, phylogeny, and genetics of traits relevant to the evolution of multicellularity, and genetic and genomic resources available for the group in question. Finally, we suggest routes toward developing these groups as model organisms for the evolution of multicellularity.
Expected final online publication date for the Annual Review of Genetics, Volume 55 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... While many Ulva species have been shown to display subtle morphological differences [1,2], the plasticity of those morphological characteristics in response to environmental changes render species identification based solely on morphological characters uncertain. For example, some Ulva species can display both foliose and tubular morphotypes [3,4]. Hence, molecular identification is the method of choice for Ulva species determination. ...
Sea Lettuce (Ulva spp. Ulvophyceae, Ulvaceae) has tremendous ecological and industrial impacts, from the negative effects of green tide events to the industrial production of food, feed, and value-added products. Due to the morphological similarities between Ulva species, their identification requires the use of “barcoding”, which relies on the sequencing of short fragments of DNA and the comparison of the obtained sequence to that of sequences present in public repositories. However, Sanger sequencing can be costly when hundreds of samples need to be analysed. In addition, “barcoding”, which uses Sanger sequencing, cannot be applied directly on bulk biomass, and requires independent assessment of the individuals within, which is often not possible in commercial products. Here, we describe a novel “sequencing-free” method for species identification of foliose Ulva species that by-passes the drawbacks associated with Sanger sequencing. The assay uses restriction digestion enzymes which target species-specific Single Nucleotide Polymorphisms (SNPs) present within the ITS1 sequence. Digestion of the ITS1 PCR product with two enzyme mixtures allows for the discrimination of the main foliose Ulva species, as well as U. compressa, which can have a foliose morphotype. Of the species tested, only U. pseudorotundata and U. arasakii show the same digestion pattern. Since those two Ulva species are allopatric, we expect this issue to be of limited impact for the users. In addition to species identification, we demonstrate that the assay can be used for hybrid detection, which can have interests for Ulva breeding and species delimitation. Importantly, the assay can be used to detect at once the different Ulva species present within a bulk of Ulva biomass, which could allow for traceability and characterisation of the purity of Ulva commercial products. This study provides a new quick and cost-effective method for foliose Ulva species identification that could readily be extended to other species.
The ubiquitous and species rich genus Ulva comprises entities of green macroalgae with variable morphologies. Ulva species are important from ecological and economic perspectives, but their identification is often problematic. Current knowledge on Ulva diversity has focused mainly on foliose individuals of temperate regions, but genetic and morphological data on tubular species are often insufficient and the species richness is ambiguous due to the lack of molecularly identified type vouchers. Together with a previous study, our study demonstrates that due to the crypticity of tubular entities of the genus Ulva present in the Atlantic-Baltic Sea transect, certain species remained undetected until recently whereas molecular evidence of other historically identified species is missing. An entity which appears to be a relatively frequent species in the Atlantic-Baltic Sea transect and which was probably mis-identified with other species in the past is here described as Ulva capillata sp. nov.. The description is based on molecular identification using tuf A and rbcL sequences, and by comparing the species´ phylogenetic relationships, distribution and range margins in the Atlantic-Baltic Sea transect, as well as on morpho-anatomical characters, and early ontogenetic development. By comparisons with closely related and potentially morphologically overlapping species concepts we were able to identify the uniqueness of U. capillata . Therefore, the description of U. capillata as a new species within the genus Ulva is supported by a combination of molecular, morphological, and ontogentic evidence which confirm their uniqueness in comparison to other species concepts.
Furthermore, our results strongly emphasize the importance and necessity to molecularly investigate especially tubular historic type vouchers within the genus Ulva to facilitate a clear species identification to omit continuing with taxonomic confusion and ongoing misapplication of names of e.g. cryptic species concepts within this important green algal genus.
To understand the evolution of Ulva chloroplast genomes at intraspecific and interspecific levels, in this study, three complete chloroplast genomes of Ulva compressa Linnaeus were sequenced and compared with the available Ulva cpDNA data. Our comparative analyses unveiled many noticeable findings. First, genome size variations of Ulva cpDNAs at intraspecific and interspecific levels were mainly caused by differences in gain or loss of group I/II introns, integration of foreign DNA fragments, and content of non-coding intergenic spacer regions. Second, chloroplast genomes of U. compressa shared the same 100 conserved genes as other Ulva cpDNA, whereas Ulva flexuosa appears to be the only Ulva species with the minD gene retained in its cpDNA. Third, five types of group I introns, most of which carry a LAGLIDADG or GIY-YIG homing endonuclease, and three of group II introns, usually encoding a reverse transcriptase/maturase, were detected at 26 insertion sites of 14 host genes in the 23 Ulva chloroplast genomes, and many intron insertion-sites have been found for the first time in Chlorophyta. Fourth, one degenerate group II intron previously ignored has been detected in the infA genes of all Ulva species, but not in the closest neighbor, Pseudoneochloris marina, and the other chlorophycean taxa, indicating that it should be the result of an independent invasion event that occurred in a common ancestor of Ulva species. Finally, the seven U. compressa cpDNAs represented a novel gene order which was different from that of other Ulva cpDNAs. The structure of Ulva chloroplast genomes is not conserved, but remarkably plastic, due to multiple rearrangement events.
Ecological processes and intra-specific genetic diversity reciprocally affect each other. While the importance of uniting ecological variables and genetic variation to understand species' plasticity, adaptation, and evolution is increasingly recognized, only few studies have attempted to address the intersection of population ecology and genetics using marine macrophyte as models. Representative empirical case studies on genetic diversity are reviewed that explore ecological and evolutionary processes in marine macrophytes. These include studies on environment-induced phenotypic plasticity and associated ecological adaptation; population genetic variation and structuring driven by ecological variation; and ecological consequences mediated by intraspecific and interspecific diversity. Knowledge gaps are also discussed that impede the connection of ecology and genetics in macrophytes and possible approaches to address these issues. Finally, an eco-evolutionary perspective is advocated, by incorporating structural-to-functional genomics and life cycle complexity, to increase the understanding of the adaptation and evolution of macrophytes in response to environmental heterogeneity.
Ulva is a ubiquitous macroalgal genus of commercial interest. Integrated Multi-Trophic Aquaculture (IMTA) systems promise large-scale production of macroalgae due to their high productivity and environmental sustainability. Complex host–microbiome interactions play a decisive role in macroalgal development, especially in Ulva spp. due to algal growth- and morphogenesis-promoting factors released by associated bacteria. However, our current understanding of the microbial community assembly and structure in cultivated macroalgae is scant. We aimed to determine (i) to what extent IMTA settings influence the microbiome associated with U. rigida and its rearing water, (ii) to explore the dynamics of beneficial microbes to algal growth and development under IMTA settings, and (iii) to improve current knowledge of host–microbiome interactions. We examined the diversity and taxonomic composition of the prokaryotic communities associated with wild versus IMTA-grown Ulva rigida and surrounding seawater by using 16S rRNA gene amplicon sequencing. With 3141 Amplicon Sequence Variants (ASVs), the prokaryotic richness was, overall, higher in water than in association with U. rigida. Bacterial ASVs were more abundant in aquaculture water samples than water collected from the lagoon. The beta diversity analysis revealed distinct prokaryotic communities associated with Ulva collected in both aquacultures and coastal waters. Aquaculture samples (water and algae) shared 22% of ASVs, whereas natural, coastal lagoon samples only 9%. While cultivated Ulva selected 239 (8%) host-specific ASVs, wild specimens possessed more than twice host-specific ASVs (17%). Cultivated U. rigida specimens enriched the phyla Cyanobacteria, Planctomycetes, Verrucomicrobia, and Proteobacteria. Within the Gammaproteobacteria, while Glaciecola mostly dominated the microbiome in cultivated algae, the genus Granulosicoccus characterized both Ulva microbiomes. In both wild and IMTA settings, the phylum Bacteroidetes was more abundant in the bacterioplankton than in direct association with U. rigida. However, we observed that the Saprospiraceae family within this phylum was barely present in lagoon water but very abundant in aquaculture water. Aquaculture promoted the presence of known morphogenesis-inducing bacteria in water samples. Our study suggests that IMTA significantly shaped the structure and composition of the microbial community of the rearing water and cultivated U. rigida. Detailed analysis revealed the presence of previously undetected taxa associated with Ulva, possessing potentially unknown functional traits.
Macroalgal microbiomes have core functions related to biofilm formation, growth, and morphogenesis of seaweeds. In particular, the growth and development of the sea lettuce Ulva spp. (Chlorophyta) depends on bacteria releasing morphogenetic compounds. Under axenic conditions, the macroalga Ulva mutabilis develops a callus-like phenotype with cell wall protrusions. However, coculturing with Roseovarius sp. (MS2) and Maribacter sp. (MS6), which produce various stimulatory chemical mediators, completely recovers morphogenesis. This ecological reconstruction forms a tripartite community which can be further studied for its role in cross-kingdom interactions. Hence, our study sought to identify algal growth- and morphogenesis-promoting factors (AGMPFs) capable of phenocopying the activity of Maribacter spp. We performed bioassay-guided solid-phase extraction in water samples collected from U. mutabilis aquaculture systems. We uncovered novel ecophysiological functions of thallusin, a sesquiterpenoid morphogen, identified for the first time in algal aquaculture. Thallusin, released by Maribacter sp., induced rhizoid and cell wall formation at a concentration of 11 pmol L-1. We further demonstrated that gametes acquired the iron complex of thallusin, thereby linking morphogenetic processes with intracellular iron homeostasis. Understanding macroalgae-bacteria interactions permits further elucidation of the evolution of multicellularity and cellular differentiation and development of new applications in microbiome-mediated aquaculture systems.
Green macroalgae, mostly represented by the Ulvophyceae, the main multicellular branch of the Chlorophyceae, constitute important primary producers of marine and brackish coastal ecosystems. Ulva or sea lettuce species are some of the most abundant representatives, being ubiquitous in coastal benthic communities around the world. Nonetheless the genus also remains largely understudied. This review highlights Ulva as an exciting novel model organism for studies of algal growth, development and morphogenesis as well as mutualistic interactions. The key reasons that Ulva is potentially such a good model system are: (i) patterns of Ulva development can drive ecologically important events, such as the increasing number of green tides observed worldwide as a result of eutrophication of coastal waters, (ii) Ulva growth is symbiotic, with proper development requiring close association with bacterial epiphytes, (iii) Ulva is extremely developmentally plastic, which can shed light on the transition from simple to complex multicellularity and (iv) Ulva will provide additional information about the evolution of the green lineage.
Ulva, one of the first Linnaean genera, was later circumscribed to consist of green seaweeds with distromatic blades, and Enteromorpha Link was established for tubular forms. Although several lines of evidence suggest that these generic constructs are artificial, Ulva and Enteromorpha have been maintained as separate genera. Our aims were to determine phylogenetic relationships among taxa currently attributed to Ulva, Enteromorpha, Umbraulva Bae et I.K. Lee and the monotypic genus Chloropelta C.E. Tanner, and to make any nomenclatural changes justified by our findings. Analyses of nuclear ribosomal internal transcribed spacer DNA (ITS nrONA) (29 ingroup taxa including the type species of Ulva and Enteromorphat, the chloroplast-encoded rbcL gene (for a subset of taxa) and a combined data set were carried out. All trees had a strongly supported clade consisting of all Ulva, Enteromorpha and Chloropelta species, but Ulva and Enteromorpha were not monophyletic. The recent removal of Vmbraulva olivascens (PJ.L. Dangeard) Bae et I.K. Lee from Ulvu is supported, although the relationship of the segregate genus Umhraulva to Ulvaria requires further investigation. These results, combined with earlier molecular and culture data, provide strong evidence that Ulva, Enteromorpha and Chloropelta are not distinct evolutionary entities and should not be recognized as separate genera. A comparison of traits for surveyed species revealed few synapomorphies. Because Ulva is the oldest name, Enteromorpha and Chloropclta are here reduced to synonymy with Ulva, and new combinations are made where necessary.
Phylogenies are increasingly used in all fields of medical and biological research. Moreover, because of the next generation sequencing revolution, datasets used for conducting phylogenetic analyses grow at an unprecedented pace. RAxML (Randomized Axelerated Maximum Likelihood) is a popular program for phylogenetic analyses of large datasets under maximum likelihood. Since the last RAxML paper in 2006, it has been continuously maintained and extended to accommodate the increasingly growing input datasets and to serve the needs of the user community.
I present some of the most notable new features and extensions of RAxML, such as, a substantial extension of substitution models and supported data types, the introduction of SSE3, AVX, and AVX2 vector intrinsics, techniques for reducing the memory requirements of the code and a plethora of operations for conducting post-analyses on sets of trees. In addition, an up-to-date, 50 page user manual covering all new RAxML options is available.
The code is available under GNU GPL at https://github.com/stamatak/standard-RAxML.
Alexandros.Stamatakis@h-its.org.
Productivity of seagrasses can be controlled by physiological processes, as well as various biotic and abiotic factors that influence plant metabolism. Light, temperature, and inorganic nutrients affect biochemical processes of organisms, and are considered as major factors controlling seagrass growth. Minimum light requirements for seagrass growth vary among species due to unique physiological and morphological adaptations of each species, and within species due to photo-acclimation to local light regimes. Seagrasses can enhance light harvesting efficiencies through photo-acclimation during low light conditions, and thus plants growing near their depth limit may have higher photosynthetic efficiencies. Annual temperatures, which are highly predictable in aquatic systems, play an important role in controlling site specific seasonal seagrass growth. Furthermore, both thermal adaptation and thermal tolerance contribute greatly to seagrass global distributions. The optimal growth temperature for temperate species range between 11.5 °C and 26 °C, whereas the optimal growth temperature for tropical/subtropical species is between 23 °C and 32 °C. However, productivity in persistent seagrasses is likely controlled by nutrient availability, including both water column and sediment nutrients. It has been demonstrated that seagrasses can assimilate nutrients through both leaf and root tissues, often with equal uptake contributions from water column and sediment nutrients. Seagrasses use HCO3− inefficiently as a carbon source, thus photosynthesis is not always saturated with respect to DIC at natural seawater concentrations leading to carbon limitation for seagrass growth. Our understanding of growth dynamics in seagrasses, as it relates to main environmental factors such as light, temperature, and nutrient availability, is critical for effective conservation and management of seagrass habitats.
In the large archipelago area of the northern Baltic Sea, increasing occurrences of drifting benthic macroalgae have been recorded in the subtidal zone. Their role as a structuring factor on the zoobenthic community has been altered from inducing occasional small-scale disturbances to inducing large-scale mortality of macrobenthic populations. A controlled field experiment was conducted on a sandy bottom in order to test for temporal responses of benthic invertebrate populations to severe stress imposed by the algal mats. Algae corresponding to amounts recorded in the field were enclosed in net- bags and attached to the bottom. Population abundance of the zoobenthic species under algae were compared with control plots for 5 wk with weekly sampling. Massive die-offs of benthic populations were recorded in both the experiment and under natural occurrences of drift algal mats. The commu- nity dominants in abundance (mudsnails Hydrobia spp.) and biomass (bivalve Macoma balthica) ex- hibited strong population reductions after 9 d of algal stress. Within 5 wk, population crashes were recorded for the sedentary polychaetes Manayunkia aestuarina and Pygospio elegans, while popula- tions of the errant polychaete Nereis diversicolor and tubificid oligochaetes remained stable under the algal mats. Initial short-term recovery after the algae were removed was rapid and dominated by Hydrobia spp. The strong negative effects on key species such as M. balthica may have severe effects on entire food-web dynamics in Baltic coastal ecosystems.
Marine primary productivity is an important agent in the global cycling of carbon dioxide, a major 'greenhouse gas', and variations in the concentration of the ocean's phytoplankton biomass can therefore explain trends in the global carbon budget. Since the launch of satellite-mounted sensors globe-wide monitoring of chlorophyll, a phytoplankton biomass proxy, became feasible. Just as satellites, the Forel-Ule (FU) scale record (a hardly explored database of ocean colour) has covered all seas and oceans - but already since 1889. We provide evidence that changes of ocean surface chlorophyll can be reconstructed with confidence from this record. The EcoLight radiative transfer numerical model indicates that the FU index is closely related to chlorophyll concentrations in open ocean regions. The most complete FU record is that of the North Atlantic in terms of coverage over space and in time; this dataset has been used to test the validity of colour changes that can be translated to chlorophyll. The FU and FU-derived chlorophyll data were analysed for monotonously increasing or decreasing trends with the non-parametric Mann-Kendall test, a method to establish the presence of a consistent trend. Our analysis has not revealed a globe-wide trend of increase or decrease in chlorophyll concentration during the past century; ocean regions have apparently responded differentially to changes in meteorological, hydrological and biological conditions at the surface, including potential long-term trends related to global warming. Since 1889, chlorophyll concentrations have decreased in the Indian Ocean and in the Pacific; increased in the Atlantic Ocean, the Mediterranean, the Chinese Sea, and in the seas west and north-west of Japan. This suggests that explanations of chlorophyll changes over long periods should focus on hydrographical and biological characteristics typical of single ocean regions, not on those of 'the' ocean.
In the northern Baltic Sea, occurrences of benthic drifting macroalgal mats have become an increasing problem. Accumulations of algae induce hypoxia and anoxia in zoobenthos above the halocline on shallow sandy bottoms. The immediate and temporal responses of a macrozoobenthic community to accumulations of drifting algal mats were studied in a field experiment on an exposed shallow sandy bottom (7.5 m depth) in the northern Baltic Sea. Experimental algal plots (50 x 50 cm) corresponding to amounts recorded in the field (440 g dwt m(-2)) were enclosed in net-bags and attached to the bottom. Changes in zoobenthic community structure under the algae were compared with ambient control plots for a period of 5 wk with sampling every seventh day. Community parameters (species, abundance and biomass) in the control community remained stable. Structural differences were recorded after 9 d, and community breakdown after 16 to 21 d of algal cover. Only opportunists and species tolerant to hypoxia remained under the algae. High particulate organic C/N ratios in the sediment under algal plots were recorded after 4 wk, indicating deposition of organic material from the algae to the sediment. Initial recovery (5 d) after terminated algal stress was rapid and dominated by a mass invasion of hydrobiid snails, possibly attracted by enrichment of the sediment. Laboratory tests on algal degradation showed a 10-fold increase in phosphorus in the water due to nutrient leakage during hypoxia (20% O-2). Algal cover, and the induction of hypoxia through degradation of the algae, exhibited severe effects on zoobenthic community structure and a potential to accelerate local eutrophication. We therefore feel that the escalating amounts of drifting algae recorded in the field are a significant threat to the coastal biota.
The genetic diversity of the green algal genus Ulva sensu lato in the New Zealand region was surveyed, examining rbcL sequences of 581 samples from a wide geographical range. Twenty-four genetically distinct taxa were discovered in New Zealand waters, belonging to three genera–Ulva (19 species), Umbraulva (four species) and Gemina (one species). Of the 19 species of Ulva reported here, 13 could be identified to the species level based on morphological and genetic data. The remaining six species cannot currently be assigned to known species groups due to a lack of close homology with sequences in GenBank. These species may include undescribed endemic taxa, recognised taxa for which rbcL sequences are not yet available, or may represent cryptogenic species. The genus Umbraulva is recorded for the first time for the New Zealand region and for the Southern Hemisphere. Of the four species distinguished, one is considered to be introduced to the region and the other three are undescribed indigenous taxa. Subantarctic samples provide the first evidence of the genus Gemina since its description in 1952: sequence data confirmed that Gemina is distinct from Ulva and Umbraulva. A number of the species identified in this study can be distinguished through a combination of growth form, morphological, ecological and distributional characters. However there remain considerable problems in distinguishing a number of other species by morphological characters alone. Based on information such as distribution in New Zealand (percentage of samples occurring in highly modified environments and/or areas with frequent vessel traffic), as well as the genetic similarity of New Zealand samples to material from overseas, we have concluded that at least five species have been introduced to the New Zealand region: Ulva armoricana, U. californica, U. flexuosa, U. lactuca and Umbraulva olivascens.
The development of proliferous (“bottle brush”) forms of Enteromorpha intestinalis (L.) Link has been studied in relation to salinity changes and also in media of extreme salinity. Two distinct patterns of development may produce similar morphologies; (A) the in situ germination of swarmers and (B) outgrowths from isolated, swollen cells present in the thallus. “Bottle brush” morphogenesis may be initiated by salinity changes and also by prolonged immersion in media of extreme salinity.
Receiving coastal waters and estuaries are among the most nutrient-enriched environments on earth, and one of the symptoms of the resulting eutrophication is the proliferation of opportunistic, fast-growing marine seaweeds. Here, we used a widespread macroalga often involved in blooms, Ulva spp., to investigate how supply of nitrogen (N) and phosphorus (P), the two main potential growth-limiting nutrients, influence macroalgal growth in temperate and tropical coastal waters ranging from low- to high-nutrient supplies. We carried out N and P enrichment field experiments on Ulva spp. in seven coastal systems, with one of these systems represented by three different subestuaries, for a total of nine sites. We showed that rate of growth of Ulva spp. was directly correlated to annual dissolved inorganic nitrogen (DIN) concentrations, where growth increased with increasing DIN concentration. Internal N pools of macroalgal fronds were also linked to increased DIN supply, and algal growth rates were tightly coupled to these internal N pools. The increases in DIN appeared to be related to greater inputs of wastewater to these coastal waters as indicated by high δ15N signatures of the algae as DIN increased. N and P enrichment experiments showed that rate of macroalgal growth was controlled by supply of DIN where ambient DIN concentrations were low, and by P where DIN concentrations were higher, regardless of latitude or geographic setting. These results suggest that understanding the basis for macroalgal blooms, and management of these harmful phenomena, will require information as to nutrient sources, and actions to reduce supply of N and P in coastal waters concerned.
The genus Caulerpa consists of about 75 species of tropical to subtropical siphonous green algae. To better understand the evolutionary history of the genus, a molecular phylogeny was inferred from chloroplast tufA sequences of 23 taxa. A sequence of Caulerpella ambigua was included as a potential outgroup. Results reveal that the latter taxon is, indeed, sister to all ingroup sequences. Caulerpa itself consists of a series of relatively ancient and species-poor lineages and a relatively modern and rapidly diversifying clade, containing most of the diversity. The molecular phylogeny conflicts with the intrageneric sectional classification based on morphological characters and an evolutionary scheme based on chloroplast ultrastructure. High bootstrap values support monophyly of C. mexicana, C. sertularioides, C. taxifolia, C. webbiana, and C. prolifera, whereas most other Caulerpa species show para- or polyphyly.
Measurements of oxygen variability and transport in seagrasses and other submerged plants are difficult to conduct and interpret
due to the existence of several sources and sinks of oxygen driving internal transport at different rates depending on conditions
in the water column and sediment. Oxygen release and transport in seagrasses have mostly been assessed by measuring oxygen
changes in incubation chambers, but oxygen variability within the plants can be assessed at much higher spatial and temporal
resolution using microelectrodes. Also planar optodes could be applied to describe oxygen release to the rhizosphere at higher
spatial and temporal resolution.
Quantitatively, photosynthetic oxygen evolution is the most important source of oxygen for internal transport and aerobic
metabolism, but passive diffusion of oxygen from the water column to leaves and below-ground tissues during darkness is also
important, and this source is necessary for maintaining the oxygen supply to roots and rhizomes during dark periods of more
than 1–2 h. The largest loss of oxygen from seagrasses is from leaves to water column during periods of high light and photosynthesis,
but the continuous leakage of oxygen from roots and rhizomes to the anoxic sediment both during light and dark periods also
represents a major sink to plant oxygen. During high photosynthesis and active plant growth, the respiratory oxygen consumption
is much lower than oxygen release to the external media. However, the relative importance of respiration increases markedly
with increasing temperature or at times of low photosynthetic rates. The internal transport of oxygen between leaves and below-ground
tissues is most likely to be primarily driven by passive diffusion within the air-filled lacunae. Pressurization, however,
does occur and may account for some internal oxygen transport especially during transient shifts between light and darkness.
There is a need for more direct measurements of oxygen traveling velocities to elucidate the roles of passive diffusion vs.
pressurization under different environmental conditions, and the possible coupling between internal oxygen dynamics and seagrass
dieoffs deserves further investigation.
Seagrasses develop extensive beds at the interface between the water column and sediment in tidal or subtidal environments.
The height of seagrass canopy ranges from a few centimetres to more than a meter (Koch et al., Chapter 8), and seagrass rhizospheres
may penetrate from centimetres (e.g. Halophila sp; Duarte et al., 1998) to a few meters (e.g. Posidonia oceanica; Mateo et al., 1997) into the sediment, depending on the species. Seagrass beds may support large above- and below-ground
biomasses (Fig. 1), and they rank amongst the most productive marine primary producers (Duarte and Chiscano, 1999; Mateo et
al., Chapter 7).
The earliest known records of marine macroalgae from Helgoland (German Bight, North Sea) date from the mid-19th century.
Since then, 274 marine macroalgal species have been reported: 77 species of Chlorophycota, 100 species of Phaeophycota and
97 species of Rhodophycota. Additionally 11 species were only recorded as drift and 51 species as doubtful for Helgoland.
The remains of the herbarium of Paul Kuckuck, the first curator for botany at the Helgoland Biological Station between 1892
and 1914, are still located there and consist of 173 macroalgal species from Helgoland. On comparing this 100-year-old herbarium
and other old sources with recent macroalgal records, it became clear that changes in species composition have occurred. After
World War II, several species such as Arthrocladia villosa, Corynophlaea crispa, Cutleria multifida, Eudesme virescens, Mesogloia vermiculata, Sporochnus pedunculatus,
Antithamnion cruciatum, Apoglossum ruscifolium, Chondria dasyphylla, Helminthora divaricata, Jania rubens and Osmundea ramosissima were not found again. Other species such as Dictyota dichotoma, Leathesia difformis, Stictyosiphon soriferus, Helminthocladia calvadosii and Scinaia furcellata became very rare. Significantly, perhaps, most of these species have a heteromorphic life history with the appearance of the macroscopic phase
restricted to (spring and) summer. Many new species of green algae were recorded for Helgoland after 1959, due to new substrata
and the research activities of Peter Kornmann, curator for botany after 1959, and Paul-Heinz Sahling his technical assistant.
Introductions of species during the considered time period were: Bonnemaisonia hamifera, Codium fragile, Mastocarpus stellatus and Sargassum muticum. Type material of the following species is located at the Marine Biological Station at Helgoland: Mikrosyphar porphyrae, Porphyra insolita and Ulva tenera.
Introductions of non-indigenous species to new ecosystems are one of the major threats to biodiversity, ecosystem functions and services. Globally, species introductions may lead to biotic homogenisation, in synergy with other anthropogenic disturbances such as climate change and coastal pollution. Successful marine introductions depend on (1) presence of a transport vector, uptake of propagules and journey survival of the species; (2) suitable environmental conditions in the receiving habitat; and (3) biological traits of the invader to facilitate establishment. Knowledge has improved of the distribution, biology and ecology of high profile seaweed invaders, e.g. Caulerpa
taxifolia, Codium fragile ssp. tomentosoides, Sargassum
muticum, and Undaria
pinnatifida. Limited, regional information is available for less conspicuous species. The mechanisms of seaweed introductions are little understood as research on introduced seaweeds has been mostly reactive, following discoveries of introductions. Sources of introductions mostly cannot be determined with certainty apart from those directly associated with aquaculture activities and few studies have addressed the sometimes serious ecological and economic impacts of seaweed introductions. Future research needs to elucidate the invasion process, interactions between invaders, and impacts of introductions to support prevention and management of seaweed introductions.
Since its introduction in 2001, MrBayes has grown in popularity as a software package for Bayesian phylogenetic inference using Markov chain Monte Carlo (MCMC) methods. With this note, we announce the release of version 3.2, a major upgrade to the latest official release presented in 2003. The new version provides convergence diagnostics and allows multiple analyses to be run in parallel with convergence progress monitored on the fly. The introduction of new proposals and automatic optimization of tuning parameters has improved convergence for many problems. The new version also sports significantly faster likelihood calculations through streaming single-instruction-multiple-data extensions (SSE) and support of the BEAGLE library, allowing likelihood calculations to be delegated to graphics processing units (GPUs) on compatible hardware. Speedup factors range from around 2 with SSE code to more than 50 with BEAGLE for codon problems. Checkpointing across all models allows long runs to be completed even when an analysis is prematurely terminated. New models include relaxed clocks, dating, model averaging across time-reversible substitution models, and support for hard, negative, and partial (backbone) tree constraints. Inference of species trees from gene trees is supported by full incorporation of the Bayesian estimation of species trees (BEST) algorithms. Marginal model likelihoods for Bayes factor tests can be estimated accurately across the entire model space using the stepping stone method. The new version provides more output options than previously, including samples of ancestral states, site rates, site d(N)/d(S) rations, branch rates, and node dates. A wide range of statistics on tree parameters can also be output for visualization in FigTree and compatible software.
"Green tides" are vast accumulations of unattached green macroalgae associated with eutrophicated marine environments. They have major ecological and economic impacts globally, so an understanding of their origin and persistence is required in order to make management decisions. Blooms predominantly consist of two common fouling genera of the Ulvales, Ulva (distromatic sheets) and Enteromorpha (monostromatic tubes). In the Baltic Sea and elsewhere green tides have increased over the last few decades. On the west coast of Finland, summer blooms consist of monostromatic sheets resembling Monostroma (Codiolales). We identified these as Enteromorpha intestinalis by comparative analyses of rDNA internal transcribed spacer 1 (ITS1), 5.8S, and ITS2 sequences, the first time monostromatic sheets have been found in the genus Enteromorpha. Ordinary attached E. intestinalis sporulated freely in culture, but the sheets reproduced only by cell regeneration into typical tubular thalli. The ITS sequences were identical to those of attached E. intestinalis populations in southwestern Finland, but differed by two substitutions from other Baltic sequences. We infer that this bloom originated from local attached populations and now reproduces clonally by fragmentation. This study provides further evidence of radical changes in gross morphology of green algae under eutrophicated conditions and the need for molecular identification.
Comparative analysis of molecular sequence data is essential for reconstructing the evolutionary histories of species and inferring the nature and extent of selective forces shaping the evolution of genes and species. Here, we announce the release of Molecular Evolutionary Genetics Analysis version 5 (MEGA5), which is a user-friendly software for mining online databases, building sequence alignments and phylogenetic trees, and using methods of evolutionary bioinformatics in basic biology, biomedicine, and evolution. The newest addition in MEGA5 is a collection of maximum likelihood (ML) analyses for inferring evolutionary trees, selecting best-fit substitution models (nucleotide or amino acid), inferring ancestral states and sequences (along with probabilities), and estimating evolutionary rates site-by-site. In computer simulation analyses, ML tree inference algorithms in MEGA5 compared favorably with other software packages in terms of computational efficiency and the accuracy of the estimates of phylogenetic trees, substitution parameters, and rate variation among sites. The MEGA user interface has now been enhanced to be activity driven to make it easier for the use of both beginners and experienced scientists. This version of MEGA is intended for the Windows platform, and it has been configured for effective use on Mac OS X and Linux desktops. It is available free of charge from http://www.megasoftware.net.
Marine Ecology Progress Series, vol. 131, 143-157 In the northern Baltic Sea, occurrences of benthic drifting macroalgal mats have become an increasing problem. Accumulations of algae induce hypoxia and anoxia in zoobenthos above the halocline on shallow sandy bottoms. The immediate and temporal response of macrozoobenthic community of accumulations of drifting algal mats were studied in a field experiment on an exposed shallow sandy bottom (7.5 m depht) in the northern Baltic Sea. Experimental algal plots (50 ' 50 cm) corresponding to amounts recorded in the field (440 g dwt m-2) were enclosed in net-bags and attached to the bottom. Changes in zoobenthic community structure under the algae were compared with ambient control plots for a period of 5 wk with sampling every seventh day. Community parameters (species, abundance and biomass) in the control community remained stable. Structural differences were recorded after 9 d, and community breakdown after 16 to 21 d of algal cover. Only opportunists and species tolerant to hypoxia remained under the alga. High particulate organic C/N ratios in the sediment under algal plots were recorded after 4 wk, indicating deposition of organic material from the algae to the sediment. Initial recovery (5 d) after terminated algal stress was rapid and dominated by a mass invasion of hydropiid snails, possibly attracted by enrichment of the sediment. Laboratory tests on algal degradation showed a 10-fold increase in phosphorous in the water due to nutrient leakage during hypoxia (20% O2). Algal cover, and the induction of hypoxia through degradation of the algae, exhipited severe effects on zoobenthic community structure and a potential to accelerate local eutrophication. We therefore feel that the escalating amounts of drifting algae recorded in the field are a significant threat to the coastal biota.
Coastal ecosystems and the services they provide are adversely affected by a wide variety of human activities. In particular, seagrass meadows are negatively affected by impacts accruing from the billion or more people who live within 50 km of them. Seagrass meadows provide important ecosystem services, including an estimated $1.9 trillion per year in the form of nutrient cycling; an order of magnitude enhancement of coral reef fish productivity; a habitat for thousands of fish, bird, and invertebrate species; and a major food source for endangered dugong, manatee, and green turtle. Although individual impacts from coastal development, degraded water quality, and climate change have been documented, there has been no quantitative global assessment of seagrass loss until now. Our comprehensive global assessment of 215 studies found that seagrasses have been disappearing at a rate of 110 km(2) yr(-1) since 1980 and that 29% of the known areal extent has disappeared since seagrass areas were initially recorded in 1879. Furthermore, rates of decline have accelerated from a median of 0.9% yr(-1) before 1940 to 7% yr(-1) since 1990. Seagrass loss rates are comparable to those reported for mangroves, coral reefs, and tropical rainforests and place seagrass meadows among the most threatened ecosystems on earth.
The marine benthic algae (Bangiophyceae, Fucophyceae, Tribophyceae, Charophyceae and Chlorophyceae) of the Baltic Sea area have been registered and the distribution for each taxon in 22 districts has been reported. The number of species decreases through the districts from c. 325 in the northern part of Kattegat to less than 100 in the Gulf of Bothnia, along the declining salinity gradient. -from Editors
Summer mass blooms of macroalgae have been occurring increasingly for two decades along the French Atlantic coastline (Fig. 9.1). The coasts of Brittany are the most affected, considering the nearly 100 000 m3 of green seaweeds collected yearly from the beaches. One member of the genus Ulva is particularly involved in these mass blooms, although some ectocarpales, for example Pilayella littoralis, recently appeared in some localities.
Blooms of opportunistic macroalgae are an increasing feature of shallow-water marine areas. By virtue of their simple morphology and broad physiological tolerances, species within the genera Enteromorpha, Ulva, Chaetomorpha and Cladophora are able to utilize enhanced nutrients (nitrogen and phosphorus) and outcompete other seaweeds as well as seagrasses, and sometimes phytoplankton. High biomasses of bloom-forming macroalgae provide a refuge for small fishes, crustaceans and gastropods but generate a hostile physico-chemical environment in the underlying sediment. The associated sediment infauna responds dramatically: burrowing bivalves are forced to the surface and surface deposit feeders may be excluded. Blooms directly reduce the abundance of the invertebrate prey of fishes and shorebirds and also physically interfere with the feeding behaviour of some predators. Only a small proportion of the organic matter fixed by blooms is consumed by grazers and most of this material enters the local decomposer cycle or subsidizes more distant areas.
The universality and species discriminatory power of the plastid rubisco large subunit (rbcL) (considering 5′ and 3′ fragments independently), elongation factor tufA, and universal amplicon (UPA), and the nuclear D2/D3 region of the large ribosomal subunit (LSU) and the internal transcribed spacer of the ribosomal cistron (ITS) were evaluated for their utility as DNA barcode markers for green macroalgae. Excepting low success for ITS, all of these markers failed for the Cladophoraceae. For the remaining taxa, the 3′ region of the rbcL (rbcL-SP) and tufA had the largest barcode gaps (difference between maximum intra- and minimum inter-specific divergence). Unfortunately, moderate amplification success (80 % excluding Cladophoracae) caused, at least in part, by the presence of introns within the rbcL-3P for some taxa reduced the utility of this marker as a universal barcode system. The tufA marker, on the other hand, had strong amplification success (95% excluding the Cladophoraceae) and no introns were uncovered. We thus recommend that tufA be adopted as the standard marker for the routine barcoding of green marine macroalgae (excluding the Cladophoraceae). During this survey we discovered cryptic species in Acrosiphonia, Monostroma, and Ulva indicating that significant taxonomic work remains for green macroalgae.
The eutrophication, or nutrient enrichment, of coastal waters as a result of man’s activities is now widely recognized as a major, world-wide pollution threat. Essentially, the increased anthropogenic source of inorganic plant nutrients interferes with the natural annual nutrient cycles and can artifically enhance primary production during periods when activity is normally low. This can have quite considerable ecological consequences for both pelagic and benthic organisms. For example, phytoplankton activity will be increased (Hoogweg et al. 1991) and, although this can be generally beneficial by increasing fisheries (Raymont 1947; Fonselius 1978; Elmgren 1989), there is some evidence that it has resulted in the occurrence of some phytoplankton blooms, both toxic and non-toxic, which have had serious effects on local fisheries and leisure activities (Braarud 1945; Ruud 1968; O’Sullivan 1971; Zou and Dong 1983; Rosenberg 1985; Kimor 1991). One such bloom occurred in the northern Adriatic in 1988 when large quantities of mucilaginous material was washed up on many tourist beaches (Degobbis 1989; Vukadin 1991). A number of authors have similarly speculated on the possible relationship between eutrophication and the occurrence of toxic blooms of microalgae in the North Sea (Cole 1972).
A multiple sequence alignment program, MAFFT, has been developed. The CPU time is drastically reduced as compared with existing
methods. MAFFT includes two novel techniques. (i) Homo logous regions are rapidly identified by the fast Fourier transform
(FFT), in which an amino acid sequence is converted to a sequence composed of volume and polarity values of each amino acid
residue. (ii) We propose a simplified scoring system that performs well for reducing CPU time and increasing the accuracy
of alignments even for sequences having large insertions or extensions as well as distantly related sequences of similar length.
Two different heuristics, the progressive method (FFT‐NS‐2) and the iterative refinement method (FFT‐NS‐i), are implemented
in MAFFT. The performances of FFT‐NS‐2 and FFT‐NS‐i were compared with other methods by computer simulations and benchmark
tests; the CPU time of FFT‐NS‐2 is drastically reduced as compared with CLUSTALW with comparable accuracy. FFT‐NS‐i is over
100 times faster than T‐COFFEE, when the number of input sequences exceeds 60, without sacrificing the accuracy.
We conducted a laboratory experiment to investigate the effects of drifting algal conglomerates on meiofauna and how its response to the presence of various macrobenthic species was modified by them. We mimicked a situation which is common in the archipelago area of the Baltic Sea, where algal mats become stagnant in shallow embayments, covering wide areas in whose centre hypoxic and even anoxic conditions develop rapidly. We used three macrobenthic species: Macoma balthica, Hediste diversicolor and Marenzelleria spp., which have shown different tolerance degrees to the drifting algae. In our experiment, drifting algae caused a major decline in sediment meiofaunal abundance and changes in the community structure, both with and without the three macrobenthic species under analysis. Of the three macrobenthic species, Marenzelleria spp. seemed to have a higher tolerance to low oxygen levels induced by the algal mats, while M. balthica and H. diversicolor mortality increased after 6 days under the algae. Both Hediste and Macoma seemed to exert a double facilitating effect: into the sediment, probably by increasing oxygen levels in deeper layers and through sediment reworking; and into the algae, via disturbance of surface layers, enhancing meiofaunal escape to the algal mass and probably their survival from the hypoxia induced below. Hediste also caused a decrease in harpacticoid copepod abundance, presumably through predation, and this was also the case for Marenzelleria in whose presence the abundance of copepods, but also turbellarians, was drastically reduced. The so far undocumented dramatic effect caused by drifting algae on meiofauna populations in our experiment shows how the negative impact of hypoxia induced by drifting algal mats (eutrophication) is propagated to almost all levels of the trophic and functional chain, influencing species interactions even at the lowest levels. This might be especially important in low diversity systems such as the Baltic Sea, were species and functional diversity are already depauperated.
A molecular phylogeny was reconstructed from a culture collection of >150 isolates of epi‐endophytic and endophytic green algae, based on nucleotide sequences of the plastid tufA and nuclear ITS2 loci. The cultures were isolated from a variety of algal hosts, notably the red algae Chondrus crispus, Mastocarpus stellatus, and Osmundea species, and the brown algae Chorda filum and Fucus serratus. The phylogeny revealed that in the Ulvales the majority of isolates fell into Acrochaete (Ulvellaceae), Ulva (Ulvaceae), Bolbocoleon (Bolbocoleaceae), and at least two unknown genera provisionally assigned to the Kornmanniaceae. Acrochaete was monophyletic. The genus was also more specious than previously described with 12 species, including up to six new species awaiting formal description. Isolates identified as Acrochaete repens, the type species of the genus, were polyphyletic. The remainder of the isolates were placed in the Ulotrichales. The results confirm that the endophytic habit supports a broad diversity of algal taxa and suggest that blade formation is a relatively recent innovation within the green algae.
Macroalgal bloom‐forming species occur in coastal systems worldwide. However, due to overlapping morphologies in some taxa, accurate taxonomic assessment and classification of these species can be quite challenging. We investigated the molecular and morphological characteristics of 153 specimens of bloom‐forming Ulva located in and around Narragansett Bay, RI, USA. We analyzed sequences of the nuclear internal transcribed spacer 1 region (ITS1) and the chloroplast‐encoded rbcL; based on the ITS1 data, we grouped the specimens into nine operational taxonomic units (OTUs). Eight of these OTUs have been previously reported to exist, while one is novel. Of the eight OTUs, all shared sequence identity with previously published sequences or differed by less than 1.5% sequence divergence for two molecular markers. Previously, 10 species names were reported for Ulva in Rhode Island (one blade and nine tube‐forming species) based upon morphological classification alone. Of our nine OTUs, three contained blade‐forming specimens (U. lactuca, U. compressa, U. rigida), one OTU had a blade with a tubular stipe, and six contained unbranched and/or branched tubular morphologies (one of these six, U. compressa, had both a blade and a tube morphology). While the three blade‐forming OTUs in Narragansett Bay can frequently be distinguished by careful observations of morphological characteristics, and spatial/temporal distribution, it is much more difficult to distinguish among the tube‐forming specimens based upon morphology or distribution alone. Our data support the molecular species concept for Ulva, and indicate that molecular‐based classifications of Ulva species are critical for proper species identification, and subsequent ecological assessment or mitigation of Ulva blooms.
Sudden beaching of huge seaweed masses smother the coastline and form rotting piles on the shore. The number of reports of these events in previously unaffected areas has increased worldwide in recent years. These 'seaweed tides' can harm tourism-based economies, smother aquaculture operations or disrupt traditional artisanal fisheries. Coastal eutrophication is the obvious, ultimate explanation for the increase in seaweed biomass, but the proximate processes that are responsible for individual beaching events are complex and require dedicated study to develop effective mitigation strategies. Harvesting the macroalgae, a valuable raw material, before they beach could well be developed into an effective solution.
Abstract This investigation complements two previous publications by Kornmann & Sahling [1977, 1983]. The paper summarizes floristic
changes that have taken place in the marine macroalgal flora of Helgoland, North Sea, over the past 100 years. Moreover, taxonomical
and, partly, life history data are given on 5 genera of green algae, e.g.Ulva, including the description of a new species,Ulva tenera; 5 genera of brown algae, e.g.Fucus ceranoides, Sargassum muticum, both species being new records for Helgoland; and 6 genera of red algae, e.g.Porphyra; Mastocarpus stellatus, which is also a new record for Helgoland.)
Macroalgal blooms arc produced by nutrient enrichment of estuaries in which the sea floor lies within the photic zone. We review fcaturcs of macroalgal blooms pointed out in recent literature and summarize work done in the Waquoit Bay Land Margin Ecosystems Research project which suggests that nutrient loads, water residcncc times, presence of fringing salt marshes, and grazing affect macroalgal blooms. Increases in nitrogen supply raise macroalgal N uptake rates, N contents of tissues, photosynthesis-irradiance curves and P,,,.,, and accelerate growth of fronds. The resulting increase in macroalgal biomass is the macroalgal bloom, which can displace other estuarine producers, Fringing marshes and brief water residence impair the intensity of macroalgal blooms. Grazing pressure may control blooms of palatable macroalgac, but only at lower N loading rates. Macroalgal blooms end when growth of the phytoplankton attenuates irradiation reaching the bottom. In cstuarics with brief water rcsidencc times, phytoplankton may not have enough time to grow and shade macrophytcs. High phytoplankton division rates achieved at high nutrient concentrations may compensate for the brief time to divide before cells arc transported out of the estuary. Increased N loads and associated macroalgal blooms pervasively and fundamentally alter estuarinc ecosystems. Macroalgae intercept nutrients regenerated from sediments and thus uncoupIe biogeochemical sedimentary cycles from those in the water column. Macroalgae take up so much N that water quality seen:? high even where N loads are high. Macroalgal C moves more readily through microbial and consumer food webs than C derived from seagrasscs that were replaced by macroalgae. Macroalgae dominate 0, profiles of the water columns of shallow estuaries and thus alter the biogeochemistry of the sediments. Marc frequent hypoxia and habitat changes associated with macroalgal blooms also changes the abundance of bcnthic fauna in affected estuaries. Approaches to rcmediation of the many pervasive cffccts of macroalgal blooms riced to include interception of nutrients at their watcrshcd sources and perhaps removal by harvest of macroalgae or by increased flushing. Al- though we have much knowledge of macroalgal dynamics, all such management initiatives will require additional information.
Although the direct involvement of nitrogen and phosphorus has been shown, eutrophication remains poorly managed to this day. The excessive growth of some opportunist seaweeds is the consequence in coastal ecosystems close to agricultural or strongly urbanized and industrialized zones. In Brittany, a leading tourist region of France, green tides set down on the beaches big quantities of Ulva, of which some 100,000 m3 are harvested annually, with significant ecological and economic consequences. In Florida, although the macroalgae (notably Codium) drift about with the currents, they are of sufficient mass and spread over such areal extent to inhibit penetration of sunlight through the water column to the coral reef surface. They strand also on the beaches. Stabilization of algae by composting and methanization of hydrolyzed and pressed algae juice are two methods which have been studied in Brittany and can be used to enhance the value of the harvested seaweed, depending on local conditions and on evolution of needs in energy, basic materials or organic products. But the parallel made here between two very different ecosystems, both disturbed, leads above all to the question of what course to follow now to avoid a worldwide disaster.
This report represents a photographic documentation of the more
conspicuous species of the marine algal vegetation of the island
Helgoland (North Sea), based on collections and observations made since
1959. The catalogue is largely restricted to macroscopic forms, as
adequate knowledge of most of the microscopic ones is not yet available.
Remarks on some rare species are added in a special chapter; the list
includes some 150 species. With a few exceptions, the figures have been
obtained from living algae; they illustrate aspects of reproduction and
development and, occasionally, demonstrate different seasonal habits.
The simplified key may be useful for providing a guide both for
naturalists and students of marine phycology. In addition, this algal
flora enhances our knowledge of the distribution of benthic species
along the European coasts, as the rocky island of Helgoland intervenes
between southern Norway and the shores of the English Channel.
Distromatic foliose blades of the algal genus Ulva are notoriously difficult to identify due to their simple morphologies and few
diagnostic characteristics that often exhibit intraspecific variation and interspecific overlap. Hence, species differentiation is
difficult and diversity estimates are often inaccurate. Two major goals of this study were to assess the diversity of distromatic
Ulva spp. in the Great Bay Estuarine System (GBES) of New Hampshire and Maine, USA, and to compare historical and
present day records of these species. Molecular analysis (using ITS sequences) of field-collected specimens revealed four
distinct taxa: Ulva lactuca, U. rigida, U. compressa, and U. pertusa. Prior to molecular screening, Ulva lactuca was the only
distromatic Ulva species reported for the GBES. Ulva pertusa and the foliose form of U. compressa are newly recorded for the
Northwest Atlantic, and the range of U. rigida has been extended. Molecular analysis of historical herbarium voucher
specimens indicates that U. rigida, U. pertusa, and the foliose form of U. compressa have been present in the GBES since at
least 1966, 1967, and 1972, respectively. The distromatic morphotype of U. compressa is found only in low salinity areas, which
suggests that salinity may influence its morphological development. Molecular and morphological evaluations are critical if we
are to distinguish between cryptic taxa, accurately assess biodiversity, and effectively monitor the spread of non-indigenous
macroalgae.
The green algal genus Ulva includes a speciose group of marine macroalgae inhabiting shallow seas
worldwide. Although algal blooms in Asia highlight the opportunistic nature of several ‘nuisance’
species, recent research clearly reveals important positive benefits of Ulva. Applied research requires
accurate, reliable and rapid identification, however, identification of Ulva spp. has met with considerable
difficulty. Consequently, many have turned to molecular markers to aid in taxonomy. Previous studies of
plants and algae have relied heavily on ITS and rbcL. Recently, tufA has been presented as a suitable
barcoding gene to facilitate species-level identification of green macroalgae and it is used here to explore
the diversity of Ulva spp. in temperate Australia. Ninety Ulva specimens collected from 38 sites across
five states were sequenced for this gene region with exemplars from each genetic group also sequenced
for rbcL to test for congruence. Collections of Australian Ulva spp. were compared to samples from Asia
and North America and exhibited trends consistent with recent studies in terms of species relationships.
Results support an overwhelmingly cosmopolitan flora in temperate Australia that contrasts with other
Australasian surveys of Ulva that report a greater number of endemics and new species. Four new
records, as well as numerous range extensions for taxa already known from the country, are documented.
Evidence for three non-indigenous Ulva species in temperate Australia is discussed.
A multiple sequence alignment program, MAFFT, has been developed. The CPU time is drastically reduced as compared with existing methods. MAFFT includes two novel techniques. (i) Homo logous regions are rapidly identified by the fast Fourier transform (FFT), in which an amino acid sequence is converted to a sequence composed of volume and polarity values of each amino acid residue. (ii) We propose a simplified scoring system that performs well for reducing CPU time and increasing the accuracy of alignments even for sequences having large insertions or extensions as well as distantly related sequences of similar length. Two different heuristics, the progressive method (FFT-NS-2) and the iterative refinement method (FFT-NS-i), are implemented in MAFFT. The performances of FFT-NS-2 and FFT-NS-i were compared with other methods by computer simulations and benchmark tests; the CPU time of FFT-NS-2 is drastically reduced as compared with CLUSTALW with comparable accuracy. FFT-NS-i is over 100 times faster than T-COFFEE, when the number of input sequences exceeds 60, without sacrificing the accuracy.
On the basis of 160 living samples from 26 different stations five Ulva species were distinguished, and described for the Netherlands coast, namely U. pseudocurvata nov. spec., U. curvata (Kütz.) De Toni, U. lactuca L., U. rigida C.Ag. and U. scandinavica Bliding. Unialgal cultures were isolated from these samples in order to test the validity of the taxonomic criteria and to test the growth response of germlings and young blades to varying salinities. The following criteria appeared to be taxonomically valid, though most of them are subject to wide variation: (1) macroscopic morphology (including colour and texture); (2) form and arrangement of the cells in surface view; (3) the structure of the basal region (form and size of rhizoidal cells; the presence or absence of small-celled marginal wings; the presence or absence of longitudinal rhizoidal ribs; and the presence or absence of a flat central cavity in the lower basal region and the stipe); (4) the number of pyrenoids in a vegetative cell; (5) the appearance of the chloroplast in surface view; (6) the size of the cells; (7) the height-to-width ratio of the cells in cross-section; (8) thallus-thickness; (9) the morphology of young germlings; (10) the mode of reproduction. The results of this study largely confirm the taxonomic concepts of Bliding in Ulva. Diversity in Dutch Ulva appears to be greater than previously supposed. The five Ulva species have different distributions with regard to the estuarine gradients. Only U. lactuca and U. pseudocurvata grow attached to wave-exposed sea dikes and harbour moles of open coasts, but they also occur in more sheltered euhaline to polyhaline tidal waters. U. curvata, U. scandinavica and U. rigida are common in polyhaline man-made lakes in the south-western Netherlands, but also occur in tidal waters growing attached to shells and stones embedded in tidal sand- and mudflats. The latter three species were not found on open sea-coasts. Good growth of germlings and young blades occurs in a wide range of salinity (mainly 17–34%. S) and does not show a distinct correlation with differences in distribution in nature
Many workers have experienced difficulties in trying to identify species within the genus Enteromorpha . The difficulties arise from our lack of knowledge of the range of variation for the characters used to delimit the taxa and of the sources of the variation shown.
Enteromorpha intestinalis (L.) Link was originally described by Linnaeus (1753) under the name Ulva intestinalis as ‘Ulva tubulosa simplex’ and Enteromorpha compressa (L.) Grev., also by Linnaeus (1753) under the name Ulva compressa as ‘Ulva tubulosa ramosa compressa’. In their interpretations by later authors, the two species differ only in that the former is unbranched and the latter branched. In their cell size, in the unordered arrangement of the cells and in the single pyrenoid in the chloroplast, they seem to belong together. Whether or not a plant is branched would seem to be a straightforward character to use in practice, but for an alga of this kind this is not necessarily so. In its development the unbranched tube of the thallus begins life as a zoospore or zygote which at first divides transversely to form a short uniseriate filament and later by radial longitudinal divisions, the subsequent expansion of which leads to the formation of the hollow tube. In the formation of branches, individual cells, usually towards the base of the frond, divide by a single periclinal division. The outer cell of the pair thus formed then divides transversely forming a single-celled filament, later dividing by radial longitudinal divisions and repeating the structure of the main axis.
The very common green seaweeds Enteromorpha intestinalis (L.) Nees and E. compressa (L.) Nees are important fouling organisms and have commonly been used as indicators of eutrophication, but their taxonomic status is problematic. The genus presents extreme difficulties because there is wide intraspecific variation in morphology, but morphological differences between species are small and difficult to detect. In this study, molecular data were used in parallel with morphological characters to resolve the taxonomic problems. Phylogenetic analysis of sequences of the internal transcribed spacers ITS1 and ITS2 and the 5.8S gene distinguished two groups of samples, which were identified by morphological characters as E. compressa (branched) and E. intestinalis (normally unbranched). There was a low level of sequence divergence within each group of samples, but divergence between groups was as great as that between either of the two species and the outgroup E. prolifera. Clades representing E. compressa and E. intestinalis were also found in analyses of an independent molecular data set, chloroplast DNA restriction fragment length polymorphisms (RFLPs). Enteromorpha intestinalis and E. compressa represent two distinct, genetically divergent species. Reinterpretation of published studies shows that these species are reproductively isolated. However, E. compressa and E. intestinalis are sometimes very difficult to distinguish from each other and could be regarded as cryptic species. The presence or absence of branching was the most useful character distinguishing these two species, but there was an element of ambiguity because low salinity or salinity shock can induce branching in E. intestinalis. If environmental factors such as salinity are taken into account, branching can be used to identify the great majority of thalli correctly. This study therefore provides a basis for identifying the two most important marine fouling macroalgae and for their use in environmental monitoring and experimentation. Typification of these two Linnaean species showed that current usage of the names accords with the lectotype and protologue of both species. Samples that resembled E. usneoides did not form a clade in any of the trees, and constraining the data to support the monophyly of this group incurred a penalty. Enteromorpha usneoides appears to be an ecotype of E. compressa.
A large (about 10 ha), mixed bed of the seagrasses Zostera marina L. (narrow morph) and Zostera noltii Hornem. on the intertidal flats of Langstone Harbour, Hayling Island (Hampshire, UK), has been monitored annually since 1986. No noticeable changes took place in the period 1986–1990. In September 1991 this seagrass bed appeared to be largely destroyed by a thick blanket of the chlorophyte Enteromorpha radiata J. Agardh; most still living Zostera plants were in a bad condition. In August 1992 not a single specimen of Zostera was found growing in the area.
Appreciation of the true species diversity of the genus Ulva in Australian waters has been blinkered by the unproved assumption that its representatives there are largely cosmopolitan. As species of Ulva are some of the longest-standing and most widely reported taxa of macroalgae, the presumption that they are worldwide in distribution has led to most Australian members being equated with species originally described from extra-Australian type localities. Ulva species can be notoriously difficult to identify due to the few and often variable characters on which classical taxonomic studies focus so that names of specimens in hand, as well as names appearing in historical distribution records, are frequently difficult or impossible to verify. The combination of morphological and molecular analyses, the latter involving both nuclear (internal transcribed spacer [ITS]) and plastid (rbcL) markers, is critically important in taxonomic studies of the genus and has here been applied to selected Ulva populations from mostly cool-temperate southern Australian localities. It has been determined that habit- and anatomy-based keys of standard taxonomic literature are largely adequate for assigning species names based on classical concepts, but they often obscure a number of cryptic and pseudocryptic species that do not conform to extra-Australian populations of the same designation, as indicated by the corresponding molecular data. Here, we present six species (Ulva australis Aresch., U. compressa Forssk., U. fasciata Delile, U. intestinalis L., U. laetevirens Aresch., U. tanneri H. S. Hayden et J. R. Waaland) for which anatomical and molecular data were congruent with both classical concepts and GenBank accession data and confirm these as cosmopolitan taxa in Australia. We also present six putative species designations based on anatomy [U. clathrata (Roth) C. Agardh, U. flexuosa Wulfen, U. linza L., U. prolifera O. F. Müll., U. stenophylla Setch. et N. L. Gardner, U. brisbanensis sp. nov.] that are inconsistent with molecular data, suggesting novel or cryptic taxa not represented in GenBank.
Inaugural dissertation (doctoral)--Universität Greifswald. Includes bibliographical references (p. [vii]-viii).