Inka Bartsch

The genus Laminaria sensu lato : recent insights and developments

This review about the genus Laminaria sensu lato summarizes the extensive literature that has been published since the overview of the genus given by Kain in 1979. The recent proposal to divide the genus into the two genera Laminaria and Saccharina is acknowledged, but the published data are discussed under a ‘sensu lato’ concept, introduced here. This includes all species which have been considered to be ‘Laminaria’ before the division of the genus. In detail, after an introduction the review covers recent insights into phylogeny and taxonomy, and discusses morphotypes, ecotypes, population genetics and demography. It describes growth and photosynthetic performance of sporophytes with special paragraphs on the regulation of sporogenesis, regulation by endogenous rhythms, nutrient metabolism, storage products, and salinity tolerance. The biology of microstages is discussed separately. The ecology of these kelps is described with a focus on stress defence against abiotic and biotic factors and the role of Laminaria as habitat, its trophic interactions and its competition is discussed. Finally, recent developments in aquaculture are summarized. In conclusion to each section, as a perspective and guide to future research, we draw attention to the remaining gaps in the knowledge about the genus and kelps in general.

Impact of oceanic warming on the distribution of seaweeds in polar and cold-temperate waters

Temperature is one of the most important factors controlling the biogeographic distribution of seaweeds and is expected to increase due to the rise in anthropogenic greenhouse gas concentrations, especially in polar and cold-temperate regions. To estimate prospective distributional shifts in cold-water key structural seaweeds from both hemispheres, we related temperature requirements and recent distributions of seaweeds to observed mean sea surface temperature (SST) isotherms for the periods 1980–1999 (Meteorological Office Hadley Centre’s SST data set; HadISST) and to modelled temperatures for 2080–2099 wCoupled Model Intercomparison Project 3 (CMIP3) database prepared for the Intergovernmental Panel on Climate Change Fourth Assessment Report (IPCC AR4) reportx based on moderate greenhouse gas emissions Special Report on Emission Scenarios – Scenario B1 (SRESA1B). Under this scenario, North Atlantic polar to cold-temperate seaweeds investigated will extend their distribution into the High Arctic until the end of the 21st century, but retreat along the northeastern Atlantic coastline. In contrast, selected Antarctic seaweeds will probably not significantly alter their latitudinal distributions, as deduced from our presently incomplete knowledge of their temperature requirements. We identified several cold-temperate regions where seaweed composition and abundance will certainly change with elevated temperatures. The results are discussed in the context of local temperature conditions, effects of multifactorial abiotic and biotic interactions and expected ecological consequences for seaweed-dominated ecosystems.

TEMPERATURE REQUIREMENTS AND BIOGEOGRAPHY OF ANTARCTIC, ARCTIC AND AMPHIEQUATORIAL SEAWEEDS

The temperature requirements for growth and survival of cold water seaweeds from both Hemispheres are compared and discussed in relation to the climatic history of the various regions and in relation to the origin of amphiequatorial distribution patterns. Endemic Antarctic species are most strongly adapted to low temperatures. In contrast, endemic Arctic macroalgae show higher temperature demands and correspond in their temperature responses to many Antarctic cold-temperate species. Arctic cold-temperate species show similar temperature requirements to cold-temperate species from southernmost South America. The temperature requirements of cold-temperate N. Atlantic species are somewhat higher than those of cold-temperate N. E. Pacific species. These differences are the result of the different times of exposure of these groups to low temperatures. The first steps in the adaptation of macroalgae to low temperatures are an increase in cold tolerance and an increase of growth and reproduction rates at low temperatures. Later, the ability to grow and reproduce at greater-than-or-equal-to 15 to 20-degrees-C and to survive temperatures greater-than-or-equal-to 20-degrees-C is lost. This temperature response type is exemplified in endemic Arctic and Arctic cold-temperate seaweeds exposed to low temperatures since about 3 My. The last steps in the adaptation to low temperatures include the loss of ability to grow and reproduce at greater-than-or-equal-to 5 or 10-degrees-C and a strong reduction in the upper survival temperatures (UST) down to 10-13-degrees-C. This temperature response type is typical for endemic Antarctic species exposed to cold waters for at least 14 My. Amphiequatorial filamentous green and brown algal taxa and microthalli of amphiequatorial brown algae mostly show USTs of 23 to 28.5-degrees-C, significantly higher compared to single Hemisphere taxa from the same regions. These findings strongly favour a migrationist jump across the equator to the other Hemisphere during Pleistocene lowering of the water temperatures in the tropics. Reproduction and growth during the passage across the equator would not have been possible in all species except Ectocarpus siliculosus due to the narrow temperature-reproduction and temperature-growth windows.

A REAPPRAISAL OF PORPHYRA AND BANGIA (BANGIOPHYCIDAE, RHODOPHYTA) IN THE NORTHEAST ATLANTIC BASED ON THE rbcL–rbcS INTERGENIC SPACER

Sequence data of the rbcL–rbcS noncoding intergenic spacer of the plastid genome for 47 specimens of Porphyra and Bangia from the northeast Atlantic reveal that they fall into 11 distinct sequences: P. purpurea, P. dioica (includes a sample of P. “ochotensis” from Helgoland), P. amplissima (includes P. thulaea and British records of P. “miniata”), P. linearis, P. umbilicalis, P. “miniata”, B. atropurpurea s.l. from Denmark and B. atropurpurea s.l. from Wales, P. drachii, P. leucosticta (includes a British record of P. “miniata var. abyssicola”), and P. “insolita” (includes P. “yezoensis” from Helgoland). Of these, data obtained for P. purpurea, P. dioica, P. amplissima, P. linearis, P. umbilicalis, P. drachii, and P. leucosticta were based on type specimens or material compared with types. Comparison of sequence data for Porphyra spp. and Bangia atropurpurea s.l. (including B. fuscopurpurea, the type species of Bangia) confirms that the species are congeneric. The data also confirm that the number of layers that make up the Porphyra thallus are not taxonomically significant. Comparison of sequence data for species from the northeast Atlantic with those for material of two species from the Pacific reveals that the species fall into two distinct groupings: an Atlantic group, containing P. purpurea, P. dioica, P. amplissima, P. linearis, P. umbilicalis, P. “miniata”, and B. atropurpurea, and a Pacific group, containing P. “pseudolinearis”, P. drachii, P. leucosticta, P. “yezoensis” (including a sample of P. “tenera”), and P. “insolita” (including P. “yezoensis” from Helgoland). The possibility of alien species in the northeast Atlantic is discussed.

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

Abstract. 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.

Global Seaweed Biogeography Under a Changing Climate: The Prospected Effects of Temperature

Temperature is one of the most important factors controlling the biogeography of seaweeds. To identify worldwide prospective distributional shifts of major biogeographical regions under a global change scenario, we applied a macroecological modeling approach. We compared the borders of biogeographical regions between present and end of the century sea surface temperatures (SST) taken from global climate model simulations and drew conclusions for distributional changes. All regions will extend towards the poles. As a consequence, the tropical region will widen considerably. However, there will be almost no change in the northern extent of the Antarctic region. According to the model data, the annual SST gradient will change along extensive coastlines creating broad transitional regions, some of which contain high seaweed genus diversity. As a consequence, the structure of the seaweed assemblages in these biogeographical regions will probably be reorganized.

Combined effects of CO2, temperature, irradiance and time on the physiological performance of Chondrus chrispus (Rhodophyta)

Abstract In natural environments, marine biotas are exposed to a variety of simultaneously acting abiotic factors. Among these, temperature, irradiance and CO2 availability are major factors influencing the physiological performance of marine macroalgae. To test whether elevated levels of CO2 may remediate the otherwise reduced performance of uncalcified seaweeds under the influence of other stressful abiotic factors, we performed multi-factorial experiments with the red alga Chondrus crispus from Helgoland (North Sea) with two levels of CO2, temperature and irradiance: low and high pCO2 levels were tested in combination with either (1) optimal and low irradiances or (2) optimal and sub-lethal high temperatures for growth. Performance of C. crispus was evaluated as biomass increase and relative growth rates (RGR), gross photosynthesis and pigment content. Acclimations of growth and photosynthesis were measured after 4 and 8 days. Acclimation time was crucial for elucidating single or combined CO2 effects on growth and photosynthesis. Significant CO2 effects became evident only in combination with either elevated temperature or reduced irradiance. Growth and photosynthesis had divergent patterns: RGR and biomass significantly increased only under a combination of high pCO2 and elevated temperature; gross photosynthesis was significantly reduced under high pCO2 conditions at low irradiance. Pigment content varied in response to irradiance and temperature, but was independent of pCO2.

Effects of ocean acidification on growth and physiology of Ulva lactuca (Chlorophyta) in a rockpool-scenario

Rising atmospheric CO2‐concentrations will have severe consequences for a variety of biological processes. We investigated the responses of the green alga Ulva lactuca (Linnaeus) to rising CO2‐concentrations in a rockpool scenario. U. lactuca was cultured under aeration with air containing either preindustrial pCO2 (280 μatm) or the pCO2 predicted by the end of the 21st century (700 μatm) for 31 days. We addressed the following question: Will elevated CO2‐concentrations affect photosynthesis (net photosynthesis, maximum relative electron transport rate (rETR(max)), maximum quantum yield (Fv/Fm), pigment composition) and growth of U. lactuca in rockpools with limited water exchange? Two phases of the experiment were distinguished: In the initial phase (day 1–4) the Seawater Carbonate System (SWCS) of the culture medium could be adjusted to the selected atmospheric pCO2 condition by continuous aeration with target pCO2 values. In the second phase (day 4–31) the SWCS was largely determined by the metabolism of the growing U. lactuca biomass. In the initial phase, Fv/Fm and rETR(max) were only slightly elevated at high CO2‐concentrations, whereas growth was significantly enhanced. After 31 days the Chl a content of the thalli was significantly lower under future conditions and the photosynthesis of thalli grown under preindustrial conditions was not dependent on external carbonic anhydrase. Biomass increased significantly at high CO2‐concentrations. At low CO2‐concentrations most adult thalli disintegrated between day 14 and 21, whereas at high CO2‐concentrations most thalli remained integer until day 31. Thallus disintegration at low CO2‐concentrations was mirrored by a drastic decline in seawater dissolved inorganic carbon and HCO3−. Accordingly, the SWCS differed significantly between the treatments. Our results indicated a slight enhancement of photosynthetic performance and significantly elevated growth of U. lactuca at future CO2‐concentrations. The accelerated thallus disintegration at high CO2‐concentrations under conditions of limited water exchange indicates additional CO2 effects on the life cycle of U. lactuca when living in rockpools.

Effects of ocean acidification on different life-cycle stages of the kelp Laminaria hyperborea (Phaeophyceae)

Abstract Our objective for this study was to evaluate the influence of preindustrial and expected future atmospheric CO2 concentrations (280 μatm and 700 μatm pCO2, respectively) on different life-cycle stages of the kelp Laminaria hyperborea from Helgoland (Germany, North Sea). Zoospore germination, gametogenesis, vegetative growth, sorus formation and photosynthetic performance of vegetative and fertile tissue were examined. The contribution of external carbonic anhydrase (exCA) to C-supply for net-photosynthesis (net-PS) and the Chla- and phlorotannin content were investigated. Female gametogenesis and vegetative growth of sporophytes were significantly enhanced under the expected future pCO2. rETR(max) and net-PS of young vegetative sporophytes tended to increase performance at higher pCO2. The trend towards elevated net-PS vanished after inhibition of exCA. In vegetative sporophytes, phlorotannin content and Chla content were not significantly affected by pCO2.

Prevailing sea surface temperatures inhibit summer reproduction of the kelp Laminaria digitata at Helgoland (North Sea)

The impact of abiotic factors on kelp sporophyte reproduction has rarely been investigated. Laminaria digitata (Hudson) J.V. Lamouroux is one of the few summer fertile Laminaria species worldwide and reproduction is subjected to relatively high water temperatures. We investigated the impact of prevailing summer temperatures (~18°C in August) on the induction of sporangia, meiospore release, and germination at the island of Helgoland (North Sea). At Helgoland, fertile sporophytes are found between April and December with a maximum in late summer. While released meiospore numbers were constant between June and October, germination rates decreased significantly in summer. Short‐term exposure of mature sori to 17°C–22°C induced a significantly higher meiospore release indicating enhancement of sporulation by elevated temperatures. Induction of sporangia on vegetative blade disks was not possible at 20°C, and fertility was only 20% at 18°C–19°C, but it was 100% in cool temperatures of 1°C–10°C. It was shown for the first time in a kelp species that “sporogenesis” is the life‐cycle process with the narrowest temperature window compared to growth or survival of the sporophyte or reproduction, growth, and survival of the gametophyte. We incorporated several parameters (induction time, fertile area, and relative fertility) into a “Reproductive efficiency index.” This indicates that sporogenesis of L. digitata is a cold‐adapted process with an optimum at (5)–10°C. The results show that the population at Helgoland is at its reproduction limit despite the existence of other geographically more southerly located populations.