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The Interactive Effects of Elevated CO2 and Ammonium Enrichment on the Physiological Performances of Saccharina japonica (Laminariales, Phaeophyta)

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Abstract

Environmental challenges such as ocean acidification and eutrophication influence the physiology of kelp species. We investigated their interactive effects on Saccharina japonica (Laminariales, Phaeophyta) under two pH conditions [Low, 7.50; High (control), 8.10] and three NH +4 concentrations (Low, 4; Medium, 60; High, 120 μM). The degree of variation of pH values in the culture medium and inhibition rate of photosynthetic oxygen evolution by acetazolamide were affected by pH treatments. Relative growth rates, carbon, nitrogen, and the C:N ratio in tissue samples were influenced by higher concentrations of NH +4 . Rates of photosynthetic oxygen evolution were enhanced under elevated CO2 or NH +4 conditions, independently, but these two factors did not show an interactive effect. However, rates of NH +4 uptake were influenced by the interactive effect of increased CO2 under elevated NH +4 treatment. Although ocean acidification and eutrophication states had an impact on physiological performance, chlorophyll fluorescence was not affected by those conditions. Our results indicated that the physiological reactions by this alga were influenced to some extent by a rise in the levels of CO2 and NH +4 . Therefore, we expect that the biomass accumulation of S. japonica may well increase under future scenarios of ocean acidification and eutrophication.

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References

  • Abreu MH, Pereira R, Yarish C, Buschmann AH, Sousa-Pinto I (2011) IMTA with Gracilaria vermiculophylla: productivity and nutrient removal performance of the seaweed in a landbased pilot scale system. Aquaculture 312:77–87

    Article  Google Scholar 

  • Agatsuma Y, Endo H, Yoshida S, Ikemori C, Takeuchi Y, Fujishima H, Nakajima N, Sano M, Kanezaki N, Imai H, Yamamoto N, Kanahama H, Matsubara T, Takahashi S, Isogai T, Taniguchi K (2014) Enhancement of Saccharina kelp production by nutrient supply in the Sea of Japan off southwestern Hokkaido, Japan. J Appl Phycol 26:1845–1852

    Article  Google Scholar 

  • Andria J, Vergara J, Perez-Llorens JL (1999) Biochemical responses and photosynthetic performance of Gracilaria sp. (Rhodophyta) from Cádiz, Spain, cultured under different inorganic carbon and nitrogen levels. Eur J Phycol 34:497–504

    Article  Google Scholar 

  • Axelsson L, Mercado JM, Figueroa FL (2000) Utilization of HCO3 at high pH by the brown macroalga Laminaria saccharina. Eur J Phycol 35:53–59

    Article  Google Scholar 

  • Beardall J, Giordano M (2002) Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms, and their regulation. Funct Plant Biol 29:335–347

    Article  Google Scholar 

  • Boderskov T, Schmedes PS, Bruhn A, Rasmussen MB, Nielsen MM, Pedersen MF (2016) The effect of light and nutrient availability on growth, nitrogen, and pigment contents of Saccharina latissima (Phaeophyceae) grown in outdoor tanks, under natural variation of sunlight and temperature, during autumn and early winter in Denmark. J Appl Phycol 28:1153–1165

    Article  Google Scholar 

  • Bricker SB, Longstaff B, Dennison W, Jones A, Boicourt K, Wicks C, Woerner J (2008) Effects of nutrient enrichment in the nation’s estuaries: a decade of change. Harmful Algae 8:21–32

    Article  Google Scholar 

  • Cai WJ, Hu X, Huang WJ, Murrell MC, Lehrter JC, Lohrenz SE, Chou WC, Zhai W, Hollibaugh JT, Wang Y, Zhao P, Guo X, Gundersen K, Dai M, Gong GC (2011) Acidification of subsurface coastal waters enhanced by eutrophication. Nat Geosci 4:766–770

    Article  Google Scholar 

  • Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:C09S04

    Article  Google Scholar 

  • Chen B, Zou D, Ma J (2016) Interactive effects of elevated CO2 and nitrogen–phosphorus supply on the physiological properties of Pyropia haitanensis (Bangiales, Rhodophyta). J Appl Phycol 28:1235–1243

    Article  Google Scholar 

  • Christie H, Norderhaug KM, Fredriksen S (2009) Macrophytes as habitat for fauna. Mar Ecol-Prog Ser 396:221–233

    Article  Google Scholar 

  • Chung IK, Oak JH, Lee JA, Shin JA, Kim JG, Park KS (2013) Installing kelp forests/seaweed beds for mitigation and adaptation against global warming: Korean Project Overview. ICES J Mar Sci 70:1038–1044

    Article  Google Scholar 

  • Chung IK, Sondak CF, Beardall J (2017) The future of seaweed aquaculture in a rapidly changing world. Eur J Phycol 52:495–505

    Article  Google Scholar 

  • Cornwall CE, Comeau S, McCulloch MT (2017) Coralline algae elevate pH at the site of calcification under ocean acidification. Glob Change Biol 23:4245–4256

    Article  Google Scholar 

  • Cornwall CE, Hepburn CD, Pritchard D, Currie KI, McGraw CM, Hunter KA, Hurd CL (2012) Carbon-use strategies in macroalgae: differential responses to lowered pH and implications for ocean acidification. J Phycol 48:137–144

    Article  Google Scholar 

  • Cornwall CE, Revill AT, Hurd CL (2015) High prevalence of diffusive uptake of CO2 by macroalgae in a temperate subtidal ecosystem. Photosynth Res 124:181–190

    Article  Google Scholar 

  • Dawes CJ, Koch EW (1990) Physiological responses of the red algae Gracilaria verrucosa and G. tikvahiae before and after nutrient enrichment. B Mar Sci 46:335–344

    Google Scholar 

  • Dickson AG (1990) Standard potential of the reaction: AgCl(s)+ 12H2(g)=Ag (s)+HCl(aq), and and the standard acidity constant of the ion HSO4 in synthetic sea water from 273.15 to 318.15 K. J Chem Thermodyn 22:113–127

    Article  Google Scholar 

  • Drechsler Z, Sharkia R, Cabantchik ZI, Beer S (1993) Bicarbonate uptake in the marine macroalga Ulva sp. is inhibited by classical probes of anion exchange by red blood cells. Planta 191:34–40

    Article  Google Scholar 

  • Falkenberg LJ, Russell BD, Connell SD (2013) Contrasting resource limitations of marine primary producers: implications for competitive interactions under enriched CO2 and nutrient regimes. Oecologia 172:575–583

    Article  Google Scholar 

  • FAO (2017) The state of world fisheries and aquaculture. Food and Agriculture Organization of the United Nations. https://doi.org/www.fao.org/figis/servlet/TabSelector Accessed 7 Sep 2017

    Google Scholar 

  • Fredriksen S, Rueness J (1989) Culture studies of Gelidium latifolium (Grev.) Born et Thur. (Rhodophyta) from Norway. Growth and nitrogen storage in response to varying photon flux density, temperature and nitrogen availability. Bot Mar 32:539–546

    Article  Google Scholar 

  • Freitas Jr, JR, Morrondo JMS, Ugarte JC (2016) Saccharina latissima (Laminariales, Ochrophyta) farming in an industrial IMTA system in Galicia (Spain). J Appl Phycol 28:377–385

    Article  Google Scholar 

  • Gao K, Zheng Y (2010) Combined effects of ocean acidification and solar UV radiation on photosynthesis, growth, pigmentation and calcification of the coralline alga Corallina sessilis (Rhodophyta). Glob Change Biol 16:2388–2398

    Article  Google Scholar 

  • Gao X, Endo H, Agatsuma Y (2015) Effect of increased seawater temperature on biomass, growth, and maturation of Saccharina japonica near its southern limit in northern Japan. J Appl Phycol 27:1263–1270

    Article  Google Scholar 

  • Gao X, Endo H, Nagaki M, Agatsuma Y (2017) Interactive effects of nutrient availability and temperature on growth and survival of different size classes of Saccharina japonica (Laminariales, Phaeophyceae). Phycologia 56:253–260

    Article  Google Scholar 

  • Gattuso JP, Gao K, Lee K, Rost B, Schulz KG (2010) Guide to best practices for ocean acidification research and data reporting. In: Riebesell U, Fabry VJ, Hansson L, Gattuso JP (eds) Approaches and tools to manipulate the carbonate chemistry. Publications Office of the European Union, Luxembourg, pp 41–52

    Google Scholar 

  • Gattuso JP, Lavigne H (2009) Approaches and software tools to investigate the impact of ocean acidification. Biogeosciences 6:2121–2133

    Article  Google Scholar 

  • Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131

    Article  Google Scholar 

  • Go H, Hwang HJ, Nam TJ (2010) A glycoprotein from Laminaria japonica induces apoptosis in HT-29 colon cancer cells. Toxicol Vitro 24:1546–1553

    Article  Google Scholar 

  • Gómez-Pinchetti JL, del Campo Fernández E, Díez PM, Reina GG (1998) Nitrogen availability influences the biochemical composition and photosynthesis of tank-cultivated Ulva rigida (Chlorophyta). J Appl Phycol 10:383–389

    Article  Google Scholar 

  • Gordillo FJ, Niell FX, Figueroa FL (2001) Non-photosynthetic enhancement of growth by high CO2 level in the nitrophilic seaweed Ulva rigida C. Agardh (Chlorophyta). Planta 213:64–70

    Google Scholar 

  • Gran G (1952) Determination of the equivalence point in potentiometric titrations of seawater with hydrochloric acid. Oceanol Acta 5:209–218

    Google Scholar 

  • Gutow L, Rahman MM, Bartl K, Saborowski R, Bartsch I, Wiencke C (2014) Ocean acidification affects growth but not nutritional quality of the seaweed Fucus vesiculosus (Phaeophyceae, Fucales). J Exp Mar Biol Ecol 453:84–90

    Article  Google Scholar 

  • Hanelt D, Uhrmacher S, Nultsch W (1995) The effect of photoinhibition on photosynthetic oxygen production in the brown alga Dictyota dichotoma. Plant Biol 108:99–105

    Google Scholar 

  • Hernandez-Carmona G, Robledo D, Serviere-Zaragoza E (2001) Effect of nutrient availability on Macrocystis pyrifera recruitment and survival near its southern limit off Baja California. Bot Mar 44:221–229

    Article  Google Scholar 

  • Hill R, Bellgrove A, Macreadie PI, Petrou K, Beardall J, Steven A, Ralph PJ (2015) Can macroalgae contribute to blue carbon? An Australian perspective. Limnol Oceanogr 60:1689–1706

    Article  Google Scholar 

  • Hofmann LC, Straub S, Bischof K (2012) Competition between calcifying and noncalcifying temperate marine macroalgae under elevated CO2 levels. Mar Ecol-Prog Ser 464:89–105

    Article  Google Scholar 

  • IPCC (2014) Climate Change 2014: synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New York, 151 p

    Google Scholar 

  • Israel A, Hophy M (2002) growth, photosynthetic properties and Rubisco activities and amounts of marine macroalgae grown under current and elevated seawater CO2 concentrations. Glob Change Biol 8:831–840

    Article  Google Scholar 

  • Joos F (2015) Global warming: growing feedback from ocean carbon to climate. Nature 522:295–296

    Article  Google Scholar 

  • Kang EJ, Kim KY (2016) Effects of future climate conditions on photosynthesis and biochemical component of Ulva pertusa (Chlorophyta). Algae 31:49–59

    Article  Google Scholar 

  • Kang JW, Chung IK (2017) The effects of eutrophication and acidification on the ecophysiology of Ulva pertusa Kjellman. J Appl Phycol 29:2675–2683

    Article  Google Scholar 

  • Kang JW, Kambey C, Shen Z, Yang Y, Chung IK (2017) The shortterm effects of elevated CO2 and ammonium concentrations on physiological responses in Gracilariopsis lemaneiformis (Rhodophyta). Fish Aquatic Sci 20:18

    Article  Google Scholar 

  • Kim JK, Yarish C, Hwang EK, Park M, Kim Y (2017) Seaweed aquaculture: cultivation technologies, challenges and its ecosystem services. Algae 32:1–13

    Article  Google Scholar 

  • Kram SL, Price NN, Donham EM, Johnson MD, Kelly ELA, Hamilton SL, Smith JE (2016) Variable responses of temperate calcified and fleshy macroalgae to elevated pCO2 and warming. ICES J Mar Sci 73:693–703

    Article  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Metaanalysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434

    Article  Google Scholar 

  • Laurent A, Fennel K, Cai WJ, Huang WJ, Barbero L, Wanninkhof R (2017) Eutrophication-induced acidification of coastal waters in the northern Gulf of Mexico: insights into origin and processes from a coupled physical-biogeochemical model. Geophys Res Lett 44:946–956

    Article  Google Scholar 

  • Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge

    Book  Google Scholar 

  • Li S, Yu K, Huo Y, Zhang J, Wu H, Cai C, Liu Y, Shi D, He P (2016) Effects of nitrogen and phosphorus enrichment on growth and photosynthetic assimilation of carbon in a green tide-forming species (Ulva prolifera) in the Yellow Sea. Hydrobiologia 776: 161–171

    Article  Google Scholar 

  • Liu C, Zou D (2015) Effects of elevated CO2 on the photosynthesis and nitrate reductase activity of Pyropia haitanensis (Bangiales, Rhodophyta) grown at different nutrient levels. Chin J Oceanol Limn 33:419–429

    Article  Google Scholar 

  • Liu D, Keesing JK, Xing Q, Shi P (2009) World’s largest macroalgal bloom caused by expansion of seaweed aquaculture in China. Mar Pollut Bull 58:888–895

    Article  Google Scholar 

  • Luo MB, Liu F, Xu ZL (2012) Growth and nutrient uptake capacity of two co-occurring species, Ulva prolifera and Ulva linza. Aquat Bot 100:18–24

    Article  Google Scholar 

  • Maberly SC (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J Phycol 26:439–449

    Article  Google Scholar 

  • Marinho GS, Holdt SL, Birkeland MJ, Angelidaki I (2015) Commercial cultivation and bioremediation potential of sugar kelp, Saccharina latissima, in Danish waters. J Appl Phycol 27:1963–1973

    Article  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  Google Scholar 

  • Millero FJ, Graham TB, Huang F, Bustos-Serrano H, Pierrot D (2006) Dissociation constants of carbonic acid in seawater as a function of salinity and temperature. Mar Chem 100:80–94

    Article  Google Scholar 

  • Murru M, Sandgren CD (2004) Habitat matters for inorganic carbon acquisition in 38 species of red macroalgae (Rhodophyta) from Puget Sound, Washington, USA. J Phycol 40:837–845

    Article  Google Scholar 

  • Nunes J, McCoy SJ, Findlay HS, Hopkins FE, Kitidis V, Queirós AM, Rayner L, Widdicombe S (2016) Two intertidal, noncalcifying macroalgae (Palmaria palmata and Saccharina latissima) show complex and variable responses to short-term CO2 acidification. ICES J Mar Sci 73:887–896

    Article  Google Scholar 

  • Ober GT, Thornber CS (2017) Divergent responses in growth and nutritional quality of coastal macroalgae to the combination of increased pCO2 and nutrients. Mar Environ Res 131:69–79

    Article  Google Scholar 

  • Oh JC, Yu OH, Choi HG (2015) Interactive effects of increased temperature and pCO2 concentration on the growth of a brown algae Ecklonia cava in the sporophyte and gametophyte stages. Ocean Polar Res 37:201–209

    Article  Google Scholar 

  • Olischläger M, Bartsch I, Gutow L, Wiencke C (2012) Effects of ocean acidification on different life-cycle stages of the kelp Laminaria hyperborea (Phaeophyceae). Bot Mar 55:511–525

    Article  Google Scholar 

  • Olischläger M, Iñiguez C, Gordillo FJL, Wiencke C (2014) Biochemical composition of temperate and Arctic populations of Saccharina latissima after exposure to increased pCO2 and temperature reveals ecotypic variation. Planta 240:1213–1224

    Article  Google Scholar 

  • Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686

    Article  Google Scholar 

  • Pang SJ, Jin ZH, Sun JZ, Gao SQ (2007) Temperature tolerance of young sporophytes from two populations of Laminaria japonica revealed by chlorophyll fluorescence measurements and short-term growth and survival performances in tank culture. Aquaculture 262:493–503

    Article  Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon press, NewYork, 173 p

    Google Scholar 

  • Raven J, Caldeira K, Elderfield H, Hoegh-Guldberg O, Liss P, Riebesell U, Shepherd J, Turley C, Watson A (2005) Ocean acidification due to increasing atmospheric carbon dioxide. The Royal Society, London, 60 p

    Google Scholar 

  • Raven JA, Giordano M, Beardall J, Maberly SC (2012) Algal evolution in relation to atmospheric CO2: carboxylases, carbonconcentrating mechanisms and carbon oxidation cycles. Philos T Roy Soc B 367:493–507

    Article  Google Scholar 

  • Raven JA, Hurd CL (2012) Ecophysiology of photosynthesis in macroalgae. Photosynth Res 113:105–125

    Article  Google Scholar 

  • Schmid R, Mills JA, Dring MJ (1996) Influence of carbon supply on the stimulation of light-saturated photosynthesis by blue light in Laminaria saccharina: implications for the mechanism of carbon acquisition in higher brown algae. Plant Cell Environ 19:383–391

    Article  Google Scholar 

  • Smetacek V, Zingone A (2013) Green and golden seaweed tides on the rise. Nature 504:84–88

    Article  Google Scholar 

  • Smith VH, Tilman GD, Nekola JC (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Pollut 100:179–196

    Article  Google Scholar 

  • Snoeijs P, Klenell M, Choo K, Comhaire I, Ray S, Pedersén M (2002) Strategies for carbon acquisition in the red marine macroalga Coccotylus truncatus from the Baltic Sea. Mar Biol 140:435–444

    Article  Google Scholar 

  • Suárez-Álvarez S, Gómez-Pinchetti JL, García-Reina G (2012) Effects of increased CO2 levels on growth, photosynthesis, ammonium uptake and cell composition in the macroalga Hypnea spinella (Gigartinales, Rhodophyta). J Appl Phycol 24:815–823

    Article  Google Scholar 

  • Surif MB, Raven JA (1989) Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and the Laminariales (Phaeophyta): ecological and taxonomic implications. Oecologia 78:97–105

    Article  Google Scholar 

  • Van de Waal DB, Verschoor AM, Verspagen JM, van Donk E, Huisman J (2010) Climate-driven changes in the ecological stoichiometry of aquatic ecosystems. Front Ecol Environ 8: 145–152

    Article  Google Scholar 

  • Vergara JJ, Niell FX, Torres M (1993) Culture of Gelidium sesquipedale (Clem.) Born. et Thur. in a chemostat system. Biomass production and metabolic responses affected by N flow. J Appl Phycol 5:405–415

    Article  Google Scholar 

  • Wang J, Jin W, Zhang W, Hou Y, Zhang H, Zhang Q (2013) Hypoglycemic property of acidic polysaccharide extracted from Saccharina japonica and its potential mechanism. Carbohyd Polym 95:143–147

    Article  Google Scholar 

  • Wu H, Huo Y, Hu M, Wei Z, He P (2015) Eutrophication assessment and bioremediation strategy using seaweeds co-cultured with aquatic animals in an enclosed bay in China. Mar Pollut Bull 95:342–349

    Article  Google Scholar 

  • Wu H, Zou D, Gao K (2008) Impacts of increased atmospheric CO2 concentration on photosynthesis and growth of microand macro-algae. Sci China Ser C 51:1144–1150

    Article  Google Scholar 

  • Xiao X, Agusti S, Lin F, Li K, Pan Y, Yu Y, Zheng Y, Wu J, Duarte CM (2017) Nutrient removal from Chinese coastal waters by large-scale seaweed aquaculture. Sci Rep 7:46613

    Article  Google Scholar 

  • Xu D, Gao Z, Zhang X, Qi Z, Meng C, Zhuang Z, Ye N (2011) Evaluation of the potential role of the macroalga Laminaria japonica for alleviating coastal eutrophication. Bioresource Technol 102:9912–9918

    Article  Google Scholar 

  • Xu D, Schaum CE, Lin F, Sun K, Munroe JR, Zhang XW, Fan X, Teng LH, Wang YT, Zhuang ZM, Ye N (2017a) Acclimation of bloom-forming and perennial seaweeds to elevated pCO2 conserved across levels of environmental complexity. Glob Change Biol 23:4828–4839

    Article  Google Scholar 

  • Xu D, Wang D, Li B, Fan X, Zhang XW, Ye NH, Wang Y, Mou S, Zhuang Z (2015) Effects of CO2 and seawater acidification on the early stages of Saccharina japonica development. Environ Sci Technol 49:3548–3556

    Article  Google Scholar 

  • Xu J, Gao K (2012) Future CO2-induced ocean acidification mediates the physiological performance of a green tide alga. Plant Physiol 160:1762–1769

    Article  Google Scholar 

  • Xu Z, Gao G, Xu J, Wu H (2017b) Physiological response of a golden tide alga (Sargassum muticum) to the interaction of ocean acidification and phosphorus enrichment. Biogeosciences 14: 671–681

    Article  Google Scholar 

  • Xu Z, Zou D, Gao K (2010) Effects of elevated CO2 and phosphorus supply on growth, photosynthesis and nutrient uptake in the marine macroalga Gracilaria lemaneiformis (Rhodophyta). Bot Mar 53:123–129

    Article  Google Scholar 

  • Yang H, Zhou Y, Mao Y, Li X, Liu Y, Zhang F (2005) Growth characters and photosynthetic capacity of Gracilaria lemaneiformis as a biofilter in a shellfish farming area in Sanggou Bay, China. J Appl Phycol 17:199–206

    Article  Google Scholar 

  • Yang YF, Fei XG, Song JM, Hu HY, Wang GC, Chung IK (2006) Growth of Gracilaria lemaneiformis under different cultivation conditions and its effects on nutrient removal in Chinese coastal waters. Aquaculture 254:248–255

    Article  Google Scholar 

  • Zer H, Ohad I (2003) Light, redox state, thylakoid-protein phosphorylation and signaling gene expression. Trends Biochem Sci 28:467–470

    Article  Google Scholar 

  • Zhang N, Song J, Cao C, Ren R, Wu F, Zhang S, Sun X (2012) The influence of macronitrogen (NO3 - and NH4 +) addition with Ulva pertusa on dissolved inorganic carbon system. Acta Oceanol Sin 31:73–82

    Article  Google Scholar 

  • Zhang X, Hu H, Tan T (2006) Photosynthetic inorganic carbon utilization of gametophytes and sporophytes of Undaria pinnatifida (Phaeophyceae). Phycologia 45:642–647

    Article  Google Scholar 

  • Zou D, Gao K (2014) The photosynthetic and respiratory responses to temperature and nitrogen supply in the marine green macroalga Ulva conglobata (Chlorophyta). Phycologia 53:86–94

    Article  Google Scholar 

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Kang, J.W., Chung, I.K. The Interactive Effects of Elevated CO2 and Ammonium Enrichment on the Physiological Performances of Saccharina japonica (Laminariales, Phaeophyta). Ocean Sci. J. 53, 487–497 (2018). https://doi.org/10.1007/s12601-018-0014-2

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