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Stress physiology and reproductive phenology of Arctic endemic kelp Laminaria solidungula J. Agardh

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Abstract

The reproductive phenology and the responses of the early life history stages of the Arctic endemic kelp Laminaria solidungula to global climate change stressors were investigated. This species inhabits low-light areas at depths up to 18 m and under the canopy of other large kelps in shallower depths. Around Svalbard, fertile sporophytes had been collected in late spring to early autumn. This observation suggests that sporogenesis starts in late autumn, continuing throughout the winter and ending in early spring, or that reproduction may occur throughout the year, especially among deepwater population where diel fluctuating low light may be perceived as short days to induce sporogenesis. Fertile sporophytes were induced to release spores that were subsequently exposed to different temperatures (2, 7, 12, 17 °C) in isolation and in interaction with ultraviolet radiation (UVR). Results showed a high temperature affinity up to 12 °C for meiospore germination and growth, but its photosynthesis was low-light-adapted and susceptible to UVR. After 16 days of cultivation, germlings died under 17 °C and gametophyte size was largest at 12 °C. After 48-day cultivation under continuous daylight, gametogenesis was not observed. The projected ocean warming will unlikely negatively affect photosynthesis and growth of micro- and macrostages of L. solidungula. Conversely, the susceptibility of meiospores and gametophytes to high PAR and UVR can disrupt the completion of the life cycle. However, sporogenesis and gametogenesis, which are the key processes for the survival of this Arctic endemic species that requires low temperature and short days, can still occur in deepwater habitats.

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References

  • Amsler CD, Neushul M (1989) Diel periodicity of spore release from kelp Nereocystis luetkeana (Mertens) Postels et Ruprecht. J Exp Mar Biol Ecol 134:117–127

    Article  Google Scholar 

  • Bartsch I, Vogt J, Pehlke C, Hanelt D (2013) Prevailing sea surface temperatures inhibit summer reproduction of the kelp Laminaria digitata at Helgoland (North Sea). J Phycol 49:1061–1073

    Article  PubMed  Google Scholar 

  • Bartsch I, Paar M, Fredriksen S, Schwanitz M, Daniel C, Wiencke C (in review) Changes in kelp forest biomass and depth distribution in Kongsfjorden (Spitsbergen) between 1996–1998 and 2012–2014 reflect Arctic warming. Polar Biol

  • Belseth E (2012) Eco-physiology of the Arctic kelp Laminaria solidungula- using divers, remotely operated vehicle and pulse amplitude modulated fluorometry. MSc thesis, Norwegian University of Science and Technology, Trondheim, Norway

  • Bischof K, Hanelt D, Wiencke C (2000) Effects of ultraviolet radiation on photosynthesis and related enzyme reactions of marine macroalgae. Planta 211:555–562

    Article  CAS  PubMed  Google Scholar 

  • Bischof K, Hanelt D, Aguilera J, Karsten U, Vogele B, Sawall T, Wiencke C (2002) Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. I. Sensitivity of photosynthesis to ultraviolet radiation. Mar Biol 140:1097–1106

    Article  CAS  Google Scholar 

  • Breeman AM, Guiry MD (1989) Tidal influences on the photoperiodic induction of tetrasporogenesis in Bonnemaisonia hamifera (Rhodophyta). Mar Biol 102:5–14

    Article  Google Scholar 

  • Carney LT, Edwards MS (2010) Role of nutrient fluctuations and delayed development in gametophyte reproduction by Macrocystis pyrifera (Phaeophyceae) in Southern California. J Phycol 46:987–996

    Article  Google Scholar 

  • Carney LT, Bohonak AJ, Edwards MS, Alberto F (2013) Genetic and experimental evidence for a mixed-age, mixed-origin bank of kelp microscopic stages in southern California. Ecology 94:1955–1965

    Article  PubMed  Google Scholar 

  • Dring MJ, Makarov V, Schoschina E, Lorenz M, Lüning K (1996) Influence of ultraviolet-radiation on chlorophyll fluorescence and growth in different life-history stages of three species of Laminaria (Phaeophyta). Mar Biol 126:183–191

    Article  CAS  Google Scholar 

  • Edwards MS (2000) The role of alternate life-history stages of a marine macroalga: a seed bank analogue? Ecology 81:2404–2415

    Article  Google Scholar 

  • Edwards MS, Hernandez-Carmona G (2005) Delayed recovery of giant kelp near its southern range limit in the North Pacific following El Niño. Mar Biol 147:273–279

    Article  Google Scholar 

  • Fredersdorf J, Muller R, Becker S, Wiencke C, Bischof K (2009) Interactive effects of radiation, temperature and salinity on different life history stages of the Arctic kelp Alaria esculenta (Phaeophyceae). Oecologia 160:483–492

    Article  PubMed  Google Scholar 

  • Gruber A, Roleda MY, Bartsch I, Hanelt D, Wiencke C (2011) Sporogenesis under UVR in Laminaria digitata (Phaeophyceae) reveals protection of photosensitive meiospores within soral tissue: physiological and anatomical evidence. J Phycol 47:603–614

    Article  PubMed  Google Scholar 

  • Hanelt D, Roleda MY (2009) Acclimation to UV-B radiation may induce a reduction in photoinhibitory stress on some Caribbean marine macrophytes. Aquat Bot 91:6–12

    Article  CAS  Google Scholar 

  • Hanelt D, Wiencke C, Karsten U, Nultsch W (1997) Photoinhibition and recovery after high light stress in different developmental and life-history stages of Laminaria saccharina (Phaeophyta). J Phycol 33:387–395

    Article  Google Scholar 

  • Hanelt D, Tüg H, Bischof K, Groß C, Lippert H, Sawall T, Wiencke C (2001) Light regime in an arctic fjord: a study related to stratospheric ozone depletion as a basis for determination of UV effects on algal growth. Mar Biol 138:649–658

    Article  CAS  Google Scholar 

  • Henley WJ, Dunton KH (1997) Effects of nitrogen supply and continuous darkness on growth and photosynthesis of the arctic kelp Laminaria solidungula. Limnol Oceanogr 42:209–216

    Article  CAS  Google Scholar 

  • Holzinger A, Di Piazza L, Lütz C, Roleda MY (2011) Sporogenic and vegetative tissues of Saccharina latissima (Laminariales, Phaeophyceae) exhibit distinctive sensitivity to experimentally enhanced ultraviolet radiation: photosynthetically active radiation ratio. Phycol Res 59:221–235

    Article  Google Scholar 

  • Hooper RG (1984) Functional adaptations to the polar environment by the Arctic kelp, Laminaria solidungula. Brit Phycol J 19:194

    Google Scholar 

  • IPCC (2013) Climate Change 2013: The Physical Science Basis. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Contribution of working group I to the fifth assessment report (AR5) of the intergovern-mental panel on climate change. Cambridge University Press, Cambridge, p 1535

    Google Scholar 

  • Iversen KR, Seuthe L (2011) Seasonal microbial processes in a high-latitude fjord (Kongsfjorden, Svalbard): I. Heterotrophic bacteria, picoplankton and nanoflagellates. Polar Biol 34:731–749

    Article  Google Scholar 

  • Kain JM (1989) The seasons in the subtidal. Br Phycol J 24:201–215

    Article  Google Scholar 

  • Karsten U, Bischof K, Wiencke C (2001) Photosynthetic performance of Arctic macroalgae after transplantation from deep to shallow waters. Oecologia 127:11–20

    Article  Google Scholar 

  • Krause-Jensen D, Duarte CM (2014) Expansion of vegetated coastal ecosystems in the future Arctic. Front Mar Sci 1:77. doi:10.3389/fmars.2014.00077

    Article  Google Scholar 

  • Leal PP, Hurd CL, Roleda MY (2014) Meiospores produced in sori of nonsporophyllous laminae of Macrocystis pyrifera (Laminariales, Phaeophyceae) may enhance reproductive output. J Phycol 50:400–405

    Article  PubMed  Google Scholar 

  • Lewis RJ, Green MK, Afzal ME (2013) Effects of chelated iron on oogenesis and vegetative growth of kelp gametophytes (Phaeophyceae). Phycol Res 61:46–51

    Article  CAS  Google Scholar 

  • Manney GL, Santee ML, Rex M et al (2011) Unprecedented Arctic ozone loss in 2011. Nature 478:469–475

    Article  CAS  PubMed  Google Scholar 

  • Maturilli M, Herber A, König-Langlo G (2013) Climatology and time series of surface meteorology in Ny-Ålesund, Svalbard. Earth Syst Sci Data 5:155–163. doi:10.5194/essd-5-155-2013

    Article  Google Scholar 

  • Maturilli M, Herber A, König-Langlo G (2015) Surface radiation climatology for Ny-Ålesund, Svalbard (78.9°N), basic observations for trend detection. Theor Appl Climatol 120:331–339

    Article  Google Scholar 

  • McDonald JH (2014) Handbook of biological statistics, 3rd edn. Sparky House Publishing, Baltimore, p 305

    Google Scholar 

  • Michler T, Aguilera J, Hanelt D, Bischof K, Wiencke C (2002) Long-term effects of ultraviolet radiation on growth and photosynthetic performance of polar and cold-temperate macroalgae. Mar Biol 140:1117–1127

    Article  CAS  Google Scholar 

  • Moy FE, Christie H (2012) Large-scale shift from sugar kelp (Saccharina latissima) to ephemeral algae along the south and west coast of Norway. Mar Biol Res 8:309–321

    Article  Google Scholar 

  • Müller R, Wiencke C, Bischof K (2008) Interactive effects of UV radiation and temperature on microstages of Laminariales (Phaeophyceae) from the Arctic and North Sea. Clim Res 37:203–213

    Article  Google Scholar 

  • Müller R, Laepple T, Bartsch B, Wiencke C (2009) Impact of oceanic warming on the distribution of seaweeds in polar and cold-temperate waters. Bot Mar 52:617–638

    Article  Google Scholar 

  • Müller R, Desel C, Steinhoff FS, Wiencke C, Bischof K (2012) UV-radiation and elevated temperatures induce formation of reactive oxygen species in gametophytes of cold-temperate/Arctic kelps (Laminariales, Phaeophyceae). Phycol Res 60:27–36

    Article  Google Scholar 

  • Olischläger M, Wiencke C (2013) Seasonal fertility and combined effects of temperature and UV radiation on Alaria esculenta and Laminaria digitata (Phaeophyceae) from Spitsbergen. Polar Biol 36:1018–1029

    Article  Google Scholar 

  • Parages ML, Heinrich S, Wiencke C, Jimenez C (2013) Rapid phosphorylation of MAP kinase-like proteins in two species of Arctic kelps in response to temperature and UV radiation stress. Environ Exp Bot 91:30–37

    Article  CAS  Google Scholar 

  • Piquet AM-T, van de Poll WH, Visser RJW, Wiencke C, Bolhuis H, Buma AGJ (2014) Springtime phytoplankton dynamics in Arctic Krossfjorden and Kongsfjorden (Spitsbergen) as a function of glacier proximity. Biogeosciences 11:2263–2279

    Article  Google Scholar 

  • Roleda MY (2009) Photosynthetic response of Arctic kelp zoospores exposed to radiation and thermal stress. Photochem Photobiol Sci 8:1302–1312

    Article  CAS  PubMed  Google Scholar 

  • Roleda MY, Wiencke C, Hanelt D (2006a) Thallus morphology and optical characteristics affect growth and DNA damage by UV radiation in juvenile Arctic Laminaria sporophytes. Planta 223:407–417

    Article  CAS  PubMed  Google Scholar 

  • Roleda MY, Clayton MN, Wiencke C (2006b) Screening capacity of UV-absorbing compounds in spores of Arctic Laminariales. J Exp Mar Biol Ecol 338:123–133

    Article  CAS  Google Scholar 

  • Roleda MY, Hanelt D, Wiencke C (2006c) Exposure to ultraviolet radiation delays photosynthetic recovery in Arctic kelp zoospores. Photosynth Res 88:311–322

    Article  CAS  PubMed  Google Scholar 

  • Roleda MY, Zacher K, Wulff A, Hanelt D, Wiencke C (2007) Photosynthetic performance, DNA damage and repair in gametes of the endemic Antarctic brown alga Ascoseira mirabilis exposed to ultraviolet radiation. Austral Ecol 32:917–926

    Article  Google Scholar 

  • Roleda MY, Lüder UH, Wiencke C (2010) UV-susceptibility of zoospores of the brown macroalga Laminaria digitata from Spitsbergen. Polar Biol 33:577–588

    Article  Google Scholar 

  • Roleda MY, Morris JN, McGraw CM, Hurd CL (2012) Ocean acidification and seaweed reproduction: increased CO2 ameliorates the negative effect of lowered pH on meiospore germination in the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae). Glob Chang Biol 18:854–864

    Article  Google Scholar 

  • Sevilgen DS, de Beer D, Al-Handal AY, Brey T, Polerecky L (2014) Oxygen budgets in subtidal arctic (Kongsfjorden, Svalbard) and temperate (Helgoland, North Sea) microphytobenthic communities. Mar Ecol Prog Ser 504:27–42

    Article  CAS  Google Scholar 

  • Staehelin J, Harris NRP, Appenzeller C, Eberhard J (2001) Ozone trends: a review. Rev Geophys 39:231–290

    Article  CAS  Google Scholar 

  • Steinhoff FS, Wiencke C, Wuttke S, Bischof K (2011) Effects of water temperatures, UV radiation and low vs high PAR on phlorotannin content and germination in zoospores of Saccorhiza dermatodea (Tilopteridales, Phaeophyceae). Phycologia 50:256–263

    Article  Google Scholar 

  • Suzuki S, Furuya K, Kawai T, Takeuchi I (2008) Effect of seawater temperature on the productivity of Laminaria japonica in the Uwe Sea, southern Japan. J Appl Phycol 20:833–844

    Article  Google Scholar 

  • Svendsen H, Beszczynska-Møller A, Hagen JO, Lefauconnier B, Tverberg V, Gerland S et al (2002) The physical environment of Kongsfjorden–Krossfjorden, an Arctic fjord system in Svalbard. Polar Res 21:133–166

    Article  Google Scholar 

  • Swanson AK, Druehl LD (2000) Differential meiospore size and tolerance of ultraviolet light stress within and among kelp species along a depth gradient. Mar Biol 136:657–664

    Article  Google Scholar 

  • tom Dieck I (1989) Vergleichende Untersuchungen zur Ökophysiologie und Kreuzbarkeit innerhalb der digitaten Sektion der Gattung Laminaria. PhD thesis, University of Hamburg, Hamburg, Germany

  • tom Dieck I (1992) North Pacific and North Atlantic digitate Laminaria species (Phaeophyta): hybridization experiments and temperature responses. Phycologia 31:147–163

  • tom Dieck I (1993) Temperature tolerance and survival in darkness of kelp gametophytes (Laminariales, Phaeophyta)- ecological and biogeographic implications. Mar Ecol Prog Ser 100:253–264

  • von Hobe M, Bekki S, Borrmann S, Cairo F, D’Amato F, Di Donfrancesco G et al (2013) Reconciliation of essential process parameters for an enhanced predictability of Arctic stratospheric ozone loss and its climate interactions (RECONCILE): activities and results. Atmos Chem Phys 13:9233–9268

    Article  Google Scholar 

  • Wiencke C, Fischer G (1990) Growth and stable carbon isotope composition of cold-water macroalgae in relation to light and temperature. Mar Ecol Prog Ser 65:283–292

    Article  Google Scholar 

  • Wiencke C, Clayton MN, Schoenwaelder M (2004) Sensitivity and acclimation to UV radiation of zoospores from five species of Laminariales from the Arctic. Mar Biol 145:31–39

    Article  Google Scholar 

  • Wiencke C, Roleda MY, Gruber A, Clayton MN, Bischof K (2006) Susceptibility of zoospores to UV radiation determines upper depth distribution limit of Arctic kelps: evidence through field experiments. J Ecol 94:455–463

    Article  Google Scholar 

  • Wiencke C, Lüder UH, Roleda MY (2007) Impact of ultraviolet radiation on physiology and development of zoospores of the brown alga Alaria esculenta from Spitzbergen. Physiol Plant 130:601–612

    Article  CAS  Google Scholar 

  • Zacher K, Roleda MY, Hanelt D, Wiencke C (2007) UV effects on photosynthesis and DNA in propagules of three different Antarctic seaweeds (Adenocystis utricularis, Monostroma hariotii and Porphyra endiviifolium). Planta 225:1505–1516

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by Christian Wiencke, financed by Alfred Wegener Institute for Polar and Marine Research (AWI) and performed at the Kings Bay Marine Laboratory in Ny Ålesund, Svalbard. Thanks to Max Schwanitz and the AWI-SCUBA diving team for sample collection and Pablo Leal for the image analysis. The author is grateful to three anonymous reviewers, Inka Bartsch, and Michael Greenacre for providing helpful comments. Thanks to Christopher Cornwall for proof reading.

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Authors and Affiliations

  1. Institute for Polar Ecology, Christian-Albrechts-University Kiel, Wischhofstr. 1-3, 24148, Kiel, Germany

    Michael Y. Roleda

  2. Alfred Wegener Institute for Polar and Marine Research, Biologische Anstalt Helgoland, 27498, Helgoland, Germany

    Michael Y. Roleda

  3. Norwegian Institute for Bioeconomy Research, Kudalsveien 6, 8049, Bodø, Norway

    Michael Y. Roleda

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Correspondence to Michael Y. Roleda.

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“This article belongs to the special issue on the ‘Kongsfjorden ecosystem—new views after more than a decade of research,’ coordinated by Christian Wiencke and Haakon Hop”.

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Roleda, M.Y. Stress physiology and reproductive phenology of Arctic endemic kelp Laminaria solidungula J. Agardh. Polar Biol 39, 1967–1977 (2016). https://doi.org/10.1007/s00300-015-1813-x

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