Temperature tolerance and biogeography of seaweeds: The marine algal flora of Helgoland (North Sea) as an example

Temperature tolerance (1 week exposure time) was determined at intervals during two successive years in 54 dominant marine benthic algae growing near Helgoland (North Sea). Seawater temperatures near Helgoland seasonally range between 3°C (in some years 0°) and 18°C. All algae survived 0°C, and none 33°C. Among the brown algae,Chorda tomentosa was the most sensitive species surviving only 18°C, followed by theLaminaria spp. surviving 20°, however not 23°C.Fucus spp. andCladostephus spongiosus were the most heat-tolerant brown algae, surviving 28°C. Among the red algae, species of the Delesseriaceae(Phycodrys rubens, Membranoptera alata) ranged on the lower end with a maximum survival temperature of 20°C, whereas the representatives of the Phyllophoraceae(Ahnfelitia plicata, Phyllophora truncata, P. pseudoceranoides) exhibited the maximum heat tolerance of the Helgoland marine algal flora with survival at 30°C. The latter value was also achieved byCodium fragile, Bryopsis hypnoides andEnteromorpha prolifera among the green algae, whereas theAcrosiphonia spp. survived only 20°C, andMonostroma undulatum only 10°C, not 15°C. Seasonal shifts of heat tolerance of up to 5°C were detected, especially inLaminaria spp. andDesmarestia aculeata. The majority of the dominant marine algal species of the Helgoland flora occurs in the Arctic, and it is hypothesized that also there the upper lethal limits of these species may hardly have changed even today. The data presented should provide a base for further analysis of the causes of geographical distribution of the North Atlantic algal species, but have still to be supplemented with similar investigations on other coasts, and supplemented with determinations of temperature requirements throughout the life cycle.Paper presented at the Seaweed Biogeography Workshop of the International Working Group on Seaweed Biogeography, held from 3–7 April 1984 at the Department of Marine Biology, University of Groningen (The Netherlands). Convenor: C. van den Hoek     

Some lower food web organisms in the nutrition of marine harpacticoid copepods: an experimental study

Some lower food web organisms from the marine littoral environment were studied as food for harpacticoid copepods. In laboratory experiments, it could be shown that, among the ciliates, the slow-movingUronema sp. was taken up while the fast-movingEuplotes sp. was not.Asterionella glacialis, a pennate diatom with spiny projections, was unsuitable as food. The centric diatomSkeletonema costatum was ingested by all harpacticoid species tested, includingTisbe holothuriae, Paramphiascella vararensis, Amphiascoides debilis andDactylopodia vulgaris. All are epibenthic and phytal species occurring in the shallow waters of Helgoland (North Sea). The amount of ciliate and algal carbon taken up was less than that provided by bacteria under laboratory conditions. However, some diatom food may be essential for the development ofD. vulgaris.     

Untersuchungen zum Vorkommen von Myxobakterien in von Meerwasser beeinflußten Substraten unter besonderer Berücksichtigung der Insel Helgoland

Representatives of the family Myxococcaceae,Myxococcus fulvus andM. virescens as well asArchangium gephyra could be isolated from marine sediments (depth range 5–58 m), collected near the island of Helgoland (North Sea); dunes and rudiments of salt marshes additionally yieldedM. coralloides and the rare speciesMelittangium licenicola andM. boletus (Cystobacteriaceae). In soil samples from the island,M. fulvus, M. virescens, M. coralloides, A. gephyra, Cystobacter fuscus andStigmatella erecta were found. These results were confirmed by data, obtained from the coastal zone of the island of Amrum and marine sediments from various regions. On the other hand samples from shallow fresh water (depth range 0.3–1 m) proved to be richer in species. It is assumed that the myxobacteria found in marine sediments occur as resting cells.     

Changing expression patterns of TonB-dependent transporters suggest shifts in polysaccharide consumption over the course of a spring phytoplankton bloom

Algal blooms produce large quantities of organic matter that is subsequently remineralised by bacterial heterotrophs. Polysaccharide is a primary component of algal biomass. It has been hypothesised that individual bacterial heterotrophic niches during algal blooms are in part determined by the available polysaccharide substrates present. Measurement of the expression of TonB-dependent transporters, often specific for polysaccharide uptake, might serve as a proxy for assessing bacterial polysaccharide consumption over time. To investigate this, we present here high-resolution metaproteomic and metagenomic datasets from bacterioplankton of the 2016 spring phytoplankton bloom at Helgoland island in the southern North Sea, and expression profiles of TonB-dependent transporters during the bloom, which demonstrate the importance of both the Gammaproteobacteria and the Bacteroidetes as degraders of algal polysaccharide. TonB-dependent transporters were the most highly expressed protein class, split approximately evenly between the Gammaproteobacteria and Bacteroidetes, and totalling on average 16.7% of all detected proteins during the bloom. About 93% of these were predicted to take up organic matter, and for about 12% of the TonB-dependent transporters, we predicted a specific target polysaccharide class. Most significantly, we observed a change in substrate specificities of the expressed transporters over time, which was not reflected in the corresponding metagenomic data. From this, we conclude that algal cell wall-related compounds containing fucose, mannose, and xylose were mostly utilised in later bloom stages, whereas glucose-based algal and bacterial storage molecules including laminarin, glycogen, and starch were used throughout. Quantification of transporters could therefore be key for understanding marine carbon cycling.Subject terms: Water microbiology, Molecular ecology, Proteomics     

Guest research facilities at the Biologische Anstalt Helgoland: Past and present

The Biologische Anstalt Helgoland (BAH) offers unique possibilities for research and education in marine sciences in the southern part of the North Sea. Besides its own research duties, the Institute provides research facilities and technical assistance for guest scientists, assists in the teaching and education of university student groups, and conducts its own courses. The Institute further supplies universities and research institutions on the mainland with marine organisms. The marine station on Helgoland has 14 laboratories, with a total of 32 working places available for guest scientists. The Wadden Sea Institute in List on the island of Sylt offers 6 laboratories with a total of 18 working places. Furthermore, laboratory classrooms are located on Helgoland and in List for 50 and 20 participants, respectively. For the convenience of the guest researchers staying at the BAH, guest-houses are run on Helgoland (Arthur-Hagmeier-Haus, Wilhelm-Mielk-Haus) und in List (Adolf-Bückmann-Haus). Guest researchers have been welcome since the founding of the Institute in 1892. Heincke gave a brief report on the activities of the first visitors from 1892 to 1897. Only sporadic reports are available for the first 60 years of this century. Guest scientists and their activities have only been recorded in detail in the annual reports of the BAH since 1962. The number of researchers and the length of their visits have increased continuously since 1962. The research facilities on Helgoland, in List and Hamburg have been modernized during the last 20 years. In 1971, four modern laboratories for guest researchers could be opened on Helgoland with financial support of the German Research Foundation (DFG). The number, of guest researchers in List and Hamburg increased after the completion of new buildings in 1979 and 1982. The recent increase in research activities by guest scientists is due to numerous students, from many different universities, using the superb research facilities to do their Masters thesis, or Ph.D. Guest researchers and students either perform their own research or cooperate with scientists of the BAH.     

The marine macroalgae of Helgoland (North Sea): an annotated list of records between 1845 and 1999

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. Received in revised form: 22 May 2000 Electronic Publication     

Candidatus Prosiliicoccus vernus,a spring phytoplankton bloom associated member of the Flavobacteriaceae

Microbial degradation of algal biomass following spring phytoplankton blooms has been characterised as a concerted effort among multiple clades of heterotrophic bacteria. Despite their significance to overall carbon turnover, many of these clades have resisted cultivation. One clade known from 16S rRNA gene sequencing surveys at Helgoland in the North Sea, was formerly identified as belonging to the genus Ulvibacter. This clade rapidly responds to algal blooms, transiently making up as much as 20% of the free-living bacterioplankton. Sequence similarity below 95% between the 16S rRNA genes of described Ulvibacter species and those from Helgoland suggest this is a novel genus. Analysis of 40 metagenome assembled genomes (MAGs) derived from samples collected during spring blooms at Helgoland support this conclusion. These MAGs represent three species, only one of which appears to bloom in response to phytoplankton. MAGs with estimated completeness greater than 90% could only be recovered for this abundant species. Additional, less complete, MAGs belonging to all three species were recovered from a mini-metagenome of cells sorted via flow cytometry using the genus specific ULV995 fluorescent rRNA probe. Metabolic reconstruction indicates this highly abundant species most likely degrades proteins and the polysaccharide laminarin. Fluorescence in situ hybridisation showed coccoid cells, with a mean diameter of 0.78 mm, with standard deviation of 0.12 μm. Based on the phylogenetic and genomic characteristics of this clade, we propose the novel candidate genus Candidatus Prosiliicoccus, and for the most abundant and well characterised of the three species the name Candidatus Prosiliicoccus vernus.     

Meeresalgen von Helgoland: Ergänzung

Complementary to a previous publication (Kornmann & Sahling, 1977), this investigation deals mainly with microscopic algae occurring in the rocky littoral of Helgoland island (North Sea). Based on the results obtained from cultivation experiments, the heterogeneousUlvella-complex of Dangeard has been rearranged and partly included in a new genusStromatella, andPlanophila respectively. The life history ofChlorocystis cohnii proved to be heteromorphic, the zygotes developing into a Codiolum-sporophyte. Also inHalochlorococcum marinum, some of the biflagellate swarmers give rise to Codiolum-like cells.Chlorocystis andHalochlorococcum, up to now members of the Chlorococcales, are incorporated into the new Codiolophycean order, Chlorocystidales. Three newHalochlorococcum species are described, the epiphytic“Chlorochytrium” moorei also being combined with this genus. Supplementary observations on some crustose red algae from transparent substrates are included in this study, as well as findings of some species not previously reported for the Helgoland area.     

Helgoland und die Erforschung der marinen Benthosalgen

Early phycological research on the island of Helgoland was performed by amateur phycologists from the adjacent coastal regions of Germany (Bremen, Hamburg, Lower Saxony and Schleswig-Holstein). These pioneers were followed by professionals, and by collectors from the mainland universities, particularly from Berlin. This second phase group includes the naturalist Christian Gottfried Ehrenberg, the zoologists Johannes Müller, Ernst Haeckel and Anton Dohrn, and the botanists Alexander Braun, Nathanael Pringsheim, and Ferdinand Cohn. The leading marine phycologist in Germany, towards the end of the 19th century, was Johannes Reinke, who finally worked at the University of Kiel. Paul Kuckuck's doctoral thesis had been supervised by Reinke who recommended him for the post of the first curator of botany at the Biological Station of Helgoland, which was founded in 1892. Kuckuck worked on the island from 1892 to 1914. After World War I, and after Kuckuck's untimely death, Wilhelm Nienburg became the second curator of botany on Helgoland, from 1921 to 1923. The next permanent phycologist on the island, from 1925 to 1936, was Ernst Schreiber. He was followed in 1936 by Peter Kornmann, who retired in 1972 but still continues as a research worker, together with Paul-Heinz Sahling, who started to work as a technical assistant under the guidance of Ernst Schreiber in 1927.

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Herrn Dr. Dr. h. c. Peter Kornmann zum 80. Geburtstag gewidmet.     

Long-term changes in the macrozoobenthos around the rocky island of Helgoland (German Bight,North Sea)

The paper briefly summarizes what is known about long-term changes (facts, causes, consequences) in the macrozoobenthos of intertidal and subtidal hard-bottom communities around the island of Helgoland (German Bight, North Sea). There is increasing observational evidence that these communities (spectrum and abundances of species) are changing on a long-term temporal scale. The reasons are diverse and mainly anthropogenic. A shift in North Sea climate towards more oceanic conditions may be among the most important factors driving the recent changes in species spectrum. Many of the species which have been recorded as new to the Helgoland area during the past decade are southern (oceanic) species which may be considered as indicators of a warming trend.Communicated by K. Wiltshire     

Genetic covariation of the marine fungal symbiont Haloguignardia irritans (Ascomycota, Pezizomycotina) with its algal hosts Cystoseira and Halidrys (Phaeophyceae, Fucales) along the west coast of North America

The fungal endophyte Haloguignardia irritans induces gall formation on the brown algal genera Cystoseira and Halidrys occurring from Oregon to Baja California, Mexico. Here we examine genetic covariation and compare rDNA phylogenies to investigate the coevolutionary histories of H. irritans and its algal hosts. Despite recognition of H. irritans as a single morphological species, internal transcribed spacer rDNA sequences representative of its geographic range are characterized by sequence variation at the intraspecific to intrageneric levels. An assessment of parallel cladogenesis between endophyte and host phylogenies provides evidence for a combination of independent fungal divergence and host jumping, similar to that observed in terrestrial lichens. Our results suggest that reduced gene flow due to geographic isolation is a major contributing factor to more concerted covariation observed at one island site, rather than to differences among algal host species alone. Because geography and its effects on gene flow can create heterogeneous mosaics of coevolution for symbioses in terrestrial environments, our results support the notion that conservation efforts toward the maintenance of genetic diversity in marine environments should likewise consider geographic complexity and its effects on coevolving marine species.     

A long-term comparison of the benthic algal flora of Clare Island, County Mayo, western Ireland

The marine benthic algal flora of Clare Island, off County Mayo, western shore of Ireland, was investigated; collections of intertidal and subtidal marine algae were made at 16 sites along the eastern and southern shores in the years 1990, 1993 and 2000–2002. The data and observations obtained were compared with the results of a similar survey conducted by Arthur Disbrowe Cotton in 1910–1911. Considering the results of the original survey and the new survey together, the marine algal flora of the island currently totals 293 species; 224 species were recorded by Cotton in the original survey, whereas 223 species were identified in the present study. Most species are common to the original and the new list and the main differences are easily explainable; the new survey used SCUBA diving, which allowed the collection of several subtidal species not collected in 1910, and Cotton reported several microscopic green and brown algae, usually difficult to recognise in the field, which were not rediscovered. The most remarkable differences consist in the current presence of some large intertidal brown algae (Bifurcaria bifurcata, Cystoseira foeniculacea and Cystoseira nodicaulis) that were not reported in the survey of 1910. Two algae, Codium fragile subsp. tomentosoides and Asparagopsis armata, were introduced in Europe after the original survey. At present, the benthic algal assemblages of Clare Island still have basically the same structure and distribution as in 1910 and, if compared with other coastal areas of Europe, the intertidal marine environment of Clare Island appears remarkably well conserved.     

Ökologische Untersuchungen an einem marinen Pilz aus der Umgebung von Helgoland

Zusammenfassung 1. Der aus dem Gezeitenstrom zwischen Insel und Düne Helgoland erstmalig isolierte PilzThraustochytrium kinnei n. sp. zeichnet sich durch besonderen Habitus und Entwicklungsgang von den bisher beschriebenen Arten des gleichen Formenkreises ab.2. Hierdurch bot er sich als leicht zu identifizierendes Objekt für die mitgeteilten Untersuchungen zur Ökologie mariner Niederer Pilze an.3. Wir verfolgen die Vorkommen Niederer Pilze der GattungenThraustochytrium, Schizochytrium und Dermocystidium an fünf Dauerstationen in der Wesermündung und der Deutschen Bucht. Hier zeigte sich, daßT. kinnei nur bei Helgoland in den Monaten Juli bis Dezember mit einiger Sicherheit aufzufinden war, während er im April bis Juni 1965 fehlte.4. Aus dem Verhalten vonT. kinnei und dem Fehlen einer typischen Gradation müssen wir schließen, daß es sich hierbei um einen Uferbewohner handelt, der in Zoosporenform im Gezeitenstrom mitgeführt wird.5. Weitere Untersuchungen zur Physiologie des Pilzes sind im Gange und sollen Aufschluß über seine spezifischen Ansprüche geben.

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Ecological investigations on a marine fungus from the area near Helgoland

A new fungusThraustochytrium kinnei n. sp. was isolated for the first time from tidal currents between the island Helgoland and its nearby dune. It is characterized by a habitus and life cycle different from those of related species previously described. These differences allow for an easy identification and thus make the new species a suitable object for ecological studies on lower marine fungi. The presence of lower fungi from the generaThraustochytrium, Schizochytrium andDermocystidum was recorded at 5 permanent stations in the Weser estuary and the German Bight.T. kinnei was found during the period from July to December and only near Helgoland. Its restricted distribution seems to indicate that the new species is a littoral form which is transported in the form of zoospores in the tidal currents. Further investigations on the physiology ofT. kinnei are presently being carried out.

     

Feasibility of assessing the community composition of prasinophytes at the Helgoland Roads sampling site with a DNA microarray

The microalgal class Prasinophyceae (Chlorophyta) contains several picoeukaryotic species, which are known to be common in temperate and cold waters and have been observed to constitute major fractions of marine picoplankton. However, reliable detection and classification of prasinophytes are mainly hampered by their small size and few morphological markers. Consequently, very little is known about the abundance and ecology of the members of this class. In order to facilitate the assessment of the abundance of the Prasinophyceae, we have designed and evaluated an 18S rRNA gene-targeted oligonucleotide microarray consisting of 21 probes targeting different taxonomic levels of prasinophytes. The microarray contains both previously published probes from other hybridization methods and new probes, which were designed for novel prasinophyte groups. The evaluation of the probe set was done under stringent conditions with 18S PCR fragments from 20 unialgal reference cultures used as positive targets. This microarray has been applied to assess the community composition of prasinophytes at Helgoland, an island in the North Sea where time series data are collected and analyzed daily but only for the nano- and microplankton-size fractions. There is no identification of prasinophytes other than to record them numerically in the flagellate fraction. The samples were collected every 2 weeks between February 2004 and December 2006. The study here demonstrates the potential of DNA microarrays to be applied as a tool for quick general monitoring of this important picoplanktonic algal group.     

Predation hazard during migratory stopover: are light or heavy birds under risk?

On the offshore island Helgoland, passerine birds killed by predators (feral cats Felis catus and raptors, mainly sparrowhawks Accipiter nisus ) during stopover were measured and weighed when found freshly killed and still intact. Supplemented by data of migrating birds ringed on Helgoland and predated on the island later on, age and body mass of victims were compared to live birds trapped on Helgoland during ringing operations. In the eleven species considered, most predator kills fell within the lightest 20% of birds measured during ringing, regardless of which type of predator was involved. It seems that the risk of being heavy due to fuel loads with respect to reduced escape performance is overestimated. The higher exposure of light birds due to more intense foraging and displacement to suboptimal habitats is probably of higher biological significance by offering conspicuous prey for predators. The lower risk of heavy birds when prey of different body condition is available for predators has implications for modelling optimal migration behaviour, and predation risk is perhaps not an important factor for migrants when deciding on site use.     

The survival of <Emphasis Type="Italic">Sicyopterus stimpsoni</Emphasis>, an endemic amphidromous Hawaiian gobiid fish,relies on the hydrological cycles of streams: evidence from changes in algal composition of diet through growth stages fish

Gut contents of larval, juvenile, and adult specimens of the Hawaiian gobiid fish Sicyopterus stimpsoni were examined to catalog the algal flora ingested by this species. The developmental stages of S. stimpsoni examined represented hallmark points in the fish’s life cycle corresponding with major migratory and metamorphic transitions. The algal flora was dominated by diatom species and shifted from taxa representative of a marine, planktonic community in larval fish to a freshwater, benthic community in juvenile and adult fish. This change in diet corresponds with the migration of larval fish to freshwater streams just prior to juvenile development in which rapid modification in mouth anatomy makes ingestion of planktonic algal species difficult. Benthic diatoms from juvenile and adult fish assemblages represented multiple genera that live in a narrow set of environmental conditions. These algae grow during a specific period in the development of the benthic algal community in Hawaiian streams. This suggests a highly specialized dietary behavior that depends heavily on continually restarting the benthic algal successional pattern, which appears to be regulated by the hydrological cycles of streams on the island.     

Contribution to the taxonomy and ecology of the Azorean benthic marine algae

Algal zonation patterns were studied in two sites (Caloura, south coast and Ribeirinha, north coast) of the island of Sao Miguel, Azores. At each site two stations were studied and the transects revealed the occurrence of two distinct and well established algal zones. In the first zone, daily immersed and emersed by the tide, the algae were growing in a dense and short tangle forming a mat, referred to as algal turf. In the second zone, which was wet most of the time, the algae were larger and frondose. A list of the species of benthic marine algae occurring on the algal turf of each station is given. Of the total of 47 species found, eight are new for the Azores and another 13 species are recorded for the first time for Sao Miguel. Gigartina acicularis (Roth) Lamouroux and articulate coralline algae (Corallina oficinalis Linnaeus and Jania spp.) were the more common species. Seasonal variation of the algal turf was studied and related to mean monthly values of air and sea water temperatures, insolation and hours of light. The zonation patterns and composition of algal species were compared with those from other open rocky shores.     

Extraordinary high natal philopatry in a migratory passerine

Natal dispersal is a key component of population dynamics in birds. It guarantees the genetic exchange of populations, favours range expansions and reduces intraspecific competition. In general, natal philopatry of migratory passerines is quite low (0–13.5%). In this study, we give evidence that, under specific conditions, migratory populations of passerine birds may show a considerably elevated natal philopatry. In a Linnet Carduelis cannabina population on the remote island of Helgoland in the North Sea, we found an extraordinary high return rate of yearlings (38%), which corresponds exactly to the annual survival rate of the species. Despite being completely migratory, the Linnets of Helgoland apparently return to a large extent to their native area and consequently might support the population maintenance on the island. Further studies are needed to reveal if this high natal philopatry is only an unusual 1-year event or a general characteristic of this partially isolated island population.     

Five scientists on excursion — a picture of marine biology on Helgoland before 1892

Five scientists on excursion — a picture of marine biology on Helgoland before 1892. The picture, of which several variant poses with minor differences exist, is a photograph taken on Helgoland in September, 1865. The original is to be found in the collections of the Ernst-Haeckel-Haus in Jena. The photograph shows only a few objects and fewer persons, but they are arranged like a bouquet: in front, collecting vessels; behind, grouped around a table, five scientists, Dohrn, Greeff, Haeckel, Salverda, Marchi. They hold up their catching nets like insignia, identifying their basic activity. This photograph is a unique document for the marine biological research on Helgoland before 1892. Furthermore, it illustrates a time and place for the birth of the idea of establishing the world's most famous marine biological station, the Stazione Zoologica di Napoli.