Skip to main content

Advertisement

Log in

Impact of Temperature, Low pH and NH4+ Enrichment on Ecophysiological Responses of a Green Tide Species Ulva australis Areschoug

  • Article
  • Published:
Ocean Science Journal Aims and scope Submit manuscript

Abstract

Ulva are ubiquitous and opportunistic green algae species that easily adapt to various environmental conditions. These algae are responsible for the green tides that cause many environmental and ecological problems in coastal waters. We investigated the physiological responses of Ulva australis under warming, acidification, and eutrophication conditions. The physiological changes in the algae were observed under various combinations of temperature, pH, and NH4+ levels. Combinations of three temperatures (10°C, 20°C, and 30°C), two pH levels (7.80 and 8.20), and two NH4+ concentrations (4 μM and 120 μM) were considered under laboratory conditions. Temperature, NH4+, and pH had significant impact on the photosynthetic and nutrient uptake rates. However, the 12 h observation could not stimulate the seaweed to change the pH in the cultured media. Changes in relative growth rates, photosynthetic efficiency, and variations in tissue C and N were not affected by the interactions between temperature, pH level, and nutrient concentration. It is probable that, due to global warming, the bloom of Ulva australis may continue in warm, acidic, coastal waters with high nutrient levels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  • Abreu MH, Pereira R, Buschmann AH, Sousa-Pinto I, Yarish C (2011) Nitrogen uptake responses of Gracilaria vermiculophylla (Ohmi) Papenfuss under combined and single addition of nitrate and ammonium. J Exp Mar Biol Ecol 407(2):190–199

    Article  Google Scholar 

  • Axelsson L, Larsson C, Ryberg H (1999) Affinity, capacity and oxygen sensitivity of two different mechanisms for bicarbonate utilization in Ulva lactuca L. (Chlorophyta). Plant Cell Environ 22(8):969–978

    Article  Google Scholar 

  • Bao M, Hu L, Fu Q, Gao G, Li X, Xu L (2019) Different photosynthetic responses of Pyropia yezoensis to ultraviolet radiation under changing temperature and photosynthetic active radiation regimes. Photochem Photobiol 95:1213–1218

    Article  Google Scholar 

  • Bartsch I, Wiencke C, Laepple T (2012) Global seaweed biogeography under a changing climate: The prospected effects of temperature. In: Wiencke C, Bischof K (eds) Seaweed biology. Ecological Studies 219, Springer, Berlin Heidelberg, pp 383–406

  • 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 

  • Brown MB, Edwards MS, Kim KY (2014) Effects of climate change on the physiology of giant kelp, Macrocystis pyrifera, and grazing by purple urchin, Strongylocentrotus purpuratus. Algae 29(3):203–215

    Article  Google Scholar 

  • Boyd PW, Collins S, Dupont S, Fabricius K, Gattuso J-P, Havenhand J, Hutchins DA, Riebesell U, Rintoul MS, Vichi M, Biswas H, Ciotti A, Gao K, Gehlen M, Hurd CL, Kurihara H, McGraw CM, Navarro JM, Nilsson GE, Passow U, Pörtner H-O (2018) Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change—a review. Glob Change Biol 24(6):2239–2261

    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(11):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-Oceans 110:C09S04. doi:https://doi.org/10.1029/2004JC002671

    Article  Google Scholar 

  • Chen F, Johns MR (1991) Effect of C/N ratio and aeration on the fatty acid composition of heterotrophic Chlorella sorokiniana. J Appl Phycol 3(3):203–209

    Article  Google Scholar 

  • Chen L, Lin L, Ma Z, Zhang T, Chen W, Zou D (2019) Carbon and nitrogen accumulation and interspecific competition in two algae species, Pyropia haitanensis and Ulva lactuca, under ocean acidification conditions. Aquacult Int 27(3):721–733

    Article  Google Scholar 

  • Chen B, Zou D, Jiang H (2015) Elevated CO2 exacerbates competition for growth and photosynthesis between Gracilaria lemaneiformis and Ulva lactuca. Aquaculture 443:49–55

    Article  Google Scholar 

  • Cosgrove J, Borowitzka MA (2011) Chlorophyll fluorescence terminology: An introduction. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: Methods and applications. Springer, Dordrecht, pp 1–17

  • Davison IR (1991) Environmental effects on algal photosynthesis: Temperature. J Phycol 27(1):2–8

    Article  Google Scholar 

  • Dawes CJ, Koch EW (1990) Physiological responses of the red algae Gracilaria verrucosa and G. tikvahiae before and after nutrient enrichment. Bull Mar Sci 46(2):335–344

    Google Scholar 

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

    Article  Google Scholar 

  • Duarte C, López J, Benítez S, Manríquez PH, Navarro JM, Bonta CC, Torres R, Quijón P (2016) Ocean acidification induces changes in algal palatability and herbivore feeding behavior and performance. Oecologia 180(2):453–462

    Article  Google Scholar 

  • Fan X, Xu D, Wang Y, Zhang X, Cao S, Mou S, Ye N (2014) The effect of nutrient concentrations, nutrient ratios and temperature on photosynthesis and nutrient uptake by Ulva prolifera: Implications for the explosion in green tides. J Appl Phycol 26(1):537–544

    Article  Google Scholar 

  • Figueroa FL, Barufi JB, Malta EJ, Conde-Álvarez R, Nitschke U, Arenas F, Mata M, Connan S, Abreu MH, Marquardt R, Vaz-Pinto F, Konotchick T, Celis-Plá PSM, Hermoso M, Ordoñez G, Ruiz E, Flores P, de los Ríos J, Kirke D, Chow F, Nassar CAG, Robledo D, Pérez-Ruzafa Á, Bañares-España E, Altamirano M, Jiménez C, Korbee N, Bischof K, Stengel DB (2014a) Short-term effects of increasing CO2, nitrate and temperature on three Mediterranean macroalgae: Biochemical composition. Aquat Biol 22:177–193

    Article  Google Scholar 

  • Figueroa FL, Conde-Álvarez R, Barufi JB, Celis-Plá PSM, Flores P, Malta EJ, Stengel DB, Meyerhoff O, Pérez-Ruzafa Á (2014b) Continuous monitoring of in vivo chlorophyll a fluorescence in Ulva rigida (Chlorophyta) submitted to different CO2, nutrient and temperature regimes. Aquat Biol 22:195–212

    Article  Google Scholar 

  • Flynn KJ, Clark DR, Mitra A, Fabian H, Hansen PJ, Glibert PM, Wheeler GL, Stoecker DK, Blackford JC, Brownlee C (2015) Ocean acidification with (de) eutrophication will alter future phytoplankton growth and succession. P Roy Soc B-Biol Sci 282(1804):20142604. doi:https://doi.org/10.1098/rspb.2014.2604

    Google Scholar 

  • Gao G, Beardall J, Bao M, Wang C, Ren W, Xu J (2018a) Ocean acidification and nutrient limitation synergistically reduce growth and photosynthetic performances of a green tide alga Ulva linza. Biogeosciences 15(11):3409–3420

    Article  Google Scholar 

  • Gao G, Clare AS, Rose C, Caldwell GS (2017a) Eutrophication and warming-driven green tides (Ulva rigida) are predicted to increase under future climate change scenarios. Mar Pollut Bull 114(1):439–447

    Article  Google Scholar 

  • Gao G, Clare AS, Rose C, Caldwell GS (2018b) Ulva rigida in the future ocean: Potential for carbon capture, bioremediation, and biomethane production. GCB Bioenergy 10(1):39–51

    Article  Google Scholar 

  • Gao K, Beardall J, Donat-P, Häder D-P, Hall-Spencer JM, Gao G, Hutchins DA (2019) Effects of ocean acidification on marine photosynthetic organisms under the concurrent influences of warming, UV radiation and deoxygenation. Front Mar Sci 6:322. doi:https://doi.org/10.3389/fmars.2019.00322

    Article  Google Scholar 

  • Gao X, Endo H, Nagaki M, Agatsuma Y (2016) Growth and survival of juvenile sporophytes of the kelp Ecklonia cava. Fish Sci 82(4):623–629

    Article  Google Scholar 

  • Gao X, Endo H, Nagaki M, Agatsuma Y (2017b) Interactive effects of nutrient availability and temperature on growth and survival of different size classes of Saccharina japonica (Laminariales, Phaeophyceae). Phycologia 56(3):253–260

    Article  Google Scholar 

  • Ge C, Yu X, Kan M, Qu C (2017) Adaption of Ulva pertusa to multiple-contamination of heavy metals and nutrients: Biological mechanism of outbreak of Ulva sp. green tide. Mar Pollut Bull 125:250–253. doi:https://doi.org/10.1016/j.marpolbul.2017.08.025

    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 

  • Gazeau F, Parker LM, Comeau S, Gattuso J-P, O’Connor WA, Martin S, Pörtner HS, Ross PM (2013) Impacts of ocean acidification on marine shelled molluscs. Mar Biol 160(8):2207–2245

    Article  Google Scholar 

  • Gómez-Pinchetti JL, Fernández EdC, 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 FJL, 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

    Article  Google Scholar 

  • Gordillo FJL, Figueroa F, Niell FX (2003) Photon and carbon use efficiency in Ulva rigida at different CO2 and N levels. Planta 218:315–322

    Article  Google Scholar 

  • Graham MH (2004) Effects of local deforestation on the diversity and structure of southern California giant kelp forest food webs. Ecosystems 7(4):341–357

    Article  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 

  • Harley CD, Anderson KM, Demes KW, Jorve JP, Kordas RL, Coyle TA, Graham MH (2012) Effects of climate change on global seaweed communities. J Phycol 48(5):1064–1078

    Article  Google Scholar 

  • Hernández I, Peralta G, Pérez-Lloréns JL, Vergara JJ, Niell FX (1997) Biomass and dynamics of growth of Ulva species in Palmones river estuary. J Phycol 33(5):764–772

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Huppe HC, Turpin DH (1994) Integration of carbon and nitrogen metabolism in plant and algal cells. Annu Rev Plant Biol 45(1):577–607

    Article  Google Scholar 

  • Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology. Cambridge University Press. Cambridge, 562 p

    Book  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 

  • Ji Y, Xu Z, Zou D, Gao K (2016) Ecophysiological responses of marine macroalgae to climate change factors. J Appl Phycol 28(5):2953–2967

    Article  Google Scholar 

  • Kang YH, Park SR, Chung IK (2011) Biofiltration efficiency and biochemical composition of three seaweed species cultivated in a fish-seaweed integrated culture. Algae 26(1):97–108

    Google Scholar 

  • Kang EJ, Kim KY (2016) Effects of future climate conditions on photosynthesis and biochemical component of Ulva pertusa (Chlorophyta). Algae 31(1):49–59

    Article  Google Scholar 

  • Kang EJ, Kim JH, Kim K, Kim KY (2016) Adaptations of a green tide forming Ulva linza (Ulvophyceae, Chlorophyta) to selected salinity and nutrients conditions mimicking representative environments in the Yellow Sea. Phycologia 55(2):210–218

    Article  Google Scholar 

  • Kang JW, Kambey C, Shen Z, Yang Y, Chung IK (2017) The short-term effects of elevated CO2 and ammonium concentrations on physiological responses in Gracilariopsis lemaneiformis (Rhodophyta). Fish Aqua Sci 20(18):1–8

    Google Scholar 

  • Kang JW, Chung IK (2017) The effects of eutrophication and acidification on the ecophysiology of Ulva pertusa Kjellman. J Appl Phycol 29(5):2675–2683

    Article  Google Scholar 

  • Kang YH, Park SR, Chung IK (2011) Biofiltration efficiency and biochemical composition of three seaweed species cultivated in a fish-seaweed integrated culture. Algae 26(1):97–108

    Google Scholar 

  • KHOA (2016) Seawater temperature statistics. Korea Hydrographic and Oceanographic Agency. http://www.khoa.go.kr/koofs/kor/oldobservation/obs_past_search.do Accessed 30 Jun 2016

    Google Scholar 

  • Kim JH, Kang EJ, Park MG, Lee BG, Kim KY (2011) Effects of temperature and irradiance on photosynthesis and growth of a green-tide-forming species (Ulva linza) in the Yellow Sea. J Appl Phycol 23(3):421–432

    Article  Google Scholar 

  • Kim JK, Kraemer GP, Neefus CD, Chung IK, Yarish C (2007) Effects of temperature and ammonium on growth, pigment production and nitrogen uptake by four species of Porphyra (Bangiales, Rhodophyta) native to the New England coast. J Appl Phycol 19(5):431–440

    Article  Google Scholar 

  • Kim KY, Choi TS, Kim JH, Han T, Shin HW, Garbary DJ (2004) Physiological ecology and seasonality of Ulva pertusa on a temperate rocky shore. Phycologia 43(4):483–492

    Article  Google Scholar 

  • Kim KY, Lee IK (1996) The germling growth of Enteromorpha intestinalis (Chlorophyta) in laboratory culture under different combinations of irradiance and salinity and temperature and salinity. Phycologia 35(4):327–331

    Article  Google Scholar 

  • Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Change Biol 196(1):103–132

    Article  Google Scholar 

  • Kram SL, Price NN, Donham EM, Johnson MD, Kelly ELA, Hamilton SL, Smith JE (2015) Variable responses of temperate calcified and fleshy macroalgae to elevated pCO2 and warming. ICES J Mar Sci 73(3):693–703

    Article  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso JP (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol 19(6):1884–1896

    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, 21 p

    Google Scholar 

  • Li S, Yu K, Huo Y, Zhang J, Wu H, 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(1):161–171

    Article  Google Scholar 

  • LZhong, J, Zheng M, Zhuo P, Xu N (2018) Photoperiod mediates the effects of elevated CO2 on the growth and physiological performance in the green tide alga Ulva prolifera. Mar Environ Res 141:24–29

  • Littler MM (1980) Morphological form and photosynthetic performances of marine macroalgae: Tests of a functional/form hypothesis. Bot Mar 23(3):161–166

    Article  Google Scholar 

  • Liu DY, Keesing JK, He PM, Wang ZL, Shi YJ, Wang YJ (2013) The world’s largest macroalgal bloom in the Yellow Sea, China: Formation and implications. Estuar Coast Shelf S 129:2–10

    Article  Google Scholar 

  • Liu C, Zou D (2015) Responses of elevated CO2 on photosynthesis and nitrogen metabolism in Ulva lactuca (Chlorophyta) at different temperature levels. Mar Biol Res 11(10):1043–1052

    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 

  • Ma J, Wang W, Qu L, Liu X, Wang Z, Qiao S, Wu H, Gao G, Xu J (2019) Differential photosynthetic eesponse of a green tide alga Ulva linza to ultraviolet radiation, under short-and long-term ocean acidification regimes. Photochem Photobiol 95:990–998

    Article  Google Scholar 

  • Mantri VA, Singh RP, Bijo AJ, Kumari P, Reddy CRK, Jha B (2011) Differential response of varying salinity and temperature on zoospore induction, regeneration and daily growth rate in Ulva fasciata (Chlorophyta, Ulvales). J Appl Phycol 23:243–250

    Article  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence - practical guide. J Exp Bot 51(345):659–668

    Article  Google Scholar 

  • McCoy SJ, Kamenos NA (2015) Coralline algae (Rhodophyta) in a changing world: integrating ecological, physiological, and geochemical responses to global change. J Phycol 51(1):6–24

    Article  Google Scholar 

  • McGlathery KJ, Pedersen MF, Borum J (1996) Changes in intracellular nitrogen pools and feedback controls on nitrogen uptake in Chaetomorpha linum (Chlorophyta). J Phycol 32(3):393–401

    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 

  • Moazami-Goudarzi M, Colman B (2012) Changes in carbon uptake mechanisms in two green marine algae by reduced seawater pH. J Exp Mar Biol Ecol 413:94–99

    Article  Google Scholar 

  • Morand P, Merceron M (2005) Macroalgal population and sustainability. J Coastal Res 21(5):1009–1020

    Article  Google Scholar 

  • Murase N, Maegawa M, Matsui T, Ohgai M, Katayama N, Saitoh M, Yokohama Y (1994) Growth and photosynthesis temperature characteristics of the sterile Ulva pertusa. Nippon Suisan Gakk 65:625–630

    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 

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

    Google Scholar 

  • Pedersen MF, Borum J (1996) Nutrient control of algal growth in estuarine waters. Nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macroalgae. Mar Ecol-Prog Ser 142:261–272

    Article  Google Scholar 

  • Pérez-Mayorga DM, Ladah LB, Zertuche-González JA, Leichter JJ, Filonov AE, Lavin MF (2011) Nitrogen uptake and growth by the opportunistic macroalga Ulva lactuca (Linnaeus) during the internal tide. J Exp Mar Biol Ecol 406(1):108–115

    Article  Google Scholar 

  • Rabalais NN, Turner RE, Diaz RJ, Justic D (2009) Global change and eutrophication of coastal waters. ICES J Mar Sci 66(7): 1528–1537

    Article  Google Scholar 

  • Reidenbach LB, Fernandez PA, Leal PP, Noisette F, McGraw CM, Revill AT, Hurd CL, Kübler JE (2017) Growth, ammonium metabolism, and photosynthetic properties of Ulva australis (Chlorophyta) under decreasing pH and ammonium enrichment. PloS One 12(11):e0188389. doi:https://doi.org/10.1371/journal.pone.0188389

    Article  Google Scholar 

  • Reymond CE, Lloyd A, Kline DI, Dove SG, Pandolfi JM (2013) Decline in growth of foraminifera Marginopora rossi under eutrophication and ocean acidification scenarios. Glob Change Biol 19(1):291–302

    Article  Google Scholar 

  • Runcie JW, Ritchie RJ, Larkum AW (2003) Uptake kinetics and assimilation of inorganic nitrogen by Catenella nipae and Ulva lactuca. Aquat Bot 76(2):155–174

    Article  Google Scholar 

  • Smetacek V, Zingone A (2013) Green and golden seaweed tides on the rise. Nature 504(7478): 84–88

    Article  Google Scholar 

  • Sondak CFA, Ang PO Jr, Beardall J, Bellgrove A, Boo SM, Gerung GS, Hepburn CD, Hong DD, Hu Z, Kawai H, Largo D, Lee JA, Lim PE, Mayakun J, Nelson WA, Oak JH, Pang SM, Sahoo D, Peerapornpis Y, Yang YF, Chung IK (2017) Carbon dioxide mitigation potential of seaweed aquaculture beds (SABs). J Appl Phycol 29:2363–2373

    Article  Google Scholar 

  • Stengel DB, Conde-Álvarez R, Connan S, Nitschke U, Arenas F, Abreu H, Barufi JB, Chow F, Robledo D, Malta EJ, Mata M, Konotchick T, Nassar C, Pérez-Ruzafa Á, López D, Marquardt R, Vaz-Pinto F, Celis-Plá PSM, Hermoso M, Ruiz E, Ordoñez G, Flores P, Zanolla M, Bañares-España E, Altamirano M, Korbee N, Bischof K, Figueroa FL (2014) Short-term effects of CO2, nutrients and temperature on three marine macroalgae under solar radiation. Aquat Biol 22:159–176

    Article  Google Scholar 

  • Suárez-Álvarez S, Gómez-Pinchetti JL, Garcia-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 

  • Taylor R, Fletcher RL, Raven JA (2001) Preliminary studies on the growth of selected ‘green tide’ algae in laboratory culture: Effects of irradiance, temperature, salinity and nutrients on growth rate. Bot Mar 44(4):327–336

    Article  Google Scholar 

  • Teichberg M, Fox SAE, Olsen YS, Valiela I, Martinetto P, Iribarnes O, Muto EY, Petti MA, Corbisier TN, Soto-Jimenez M, Osuna FP, Castro P, Freitas H, Zitelli A, Cardinaletti M, Tagliapitra D (2010) Eutrophication and macroalgal blooms in temperate and tropical coastal waters: Nutrient enrichment experiments with Ulva spp. Glob Change Biol 16:2624–2637

    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(4):405–415

    Article  Google Scholar 

  • Wallace RB, Baumann H, Grear JS, Aller RC, Gobler CJ (2014) Invited feature coastal ocean acidification: The other eutrophication problem. Estuar Coast Shelf S 148:1–13

    Article  Google Scholar 

  • Wallentinus I (1984) Comparisons of nutrient uptake rates for Baltic macroalgae with different thallus morphologies. Mar Biol 80(2):215–225

    Article  Google Scholar 

  • Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: Procedures, patterns and problems. Glob Change Biol 18(5):1491–1498

    Article  Google Scholar 

  • Widdicombe S, Dupont S, Thorndyke M (2010) Laboratory experiments and benthic mesocosm studies. In: Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (eds) Guide to best practices for ocean acidification research and data reporting. Luxembourg Publications Office of the European Union, Luxembourg, pp 113–122

    Google Scholar 

  • Xu J, Gao K (2012) Future CO2-induced ocean acidification mediates the physiological performance of a green tide alga. Plant Physiol 160(4):1762–1769

    Article  Google Scholar 

  • Xu Z, Wu H, Zhan D, Sun F, Sun J, Wang G (2014) Combined effects of light intensity and NH4+-enrichment on growth, pigmentation, and photosynthetic performance of Ulva prolifera (Chlorophyta). Chin J Oceanol Limn 32(5):1016–1023

    Article  Google Scholar 

  • Xu Z, Gao G, Xu J, Wu H (2017) 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 

  • Young EB, Beardall J (2005) Modulation of photosynthesis and inorganic carbon acquisition in a marine microalga by nitrogen, iron, and light availability. Can J Bot 83(7):917–928

    Article  Google Scholar 

  • Young CS, Gobler CJ (2017) The organizing effects of elevated CO2 on competition among estuarine primary producers. Sci Rep 7:7667. doi:https://doi.org/10.1038/s41598-017-08178-5

    Article  Google Scholar 

  • Yue F, Gao G, Ma J, Wu H, Li X, Xu J (2019) Future CO2-induced seawater acidification mediates the physiological performance of a green alga Ulva linza in different photoperiods. Peer J 7:e7048. doi:https://doi.org/10.7717/peerj.7048

    Article  Google Scholar 

  • Zhang N, Song J, Cao C, Ren R, Wu F, Zhang S, Sun X (2012) The influence of macro nitrogen (NO3 and NH4+) addition with Ulva pertusa on dissolved inorganic carbon system. Acta Oceanol Sin 1(1):73–82

    Article  Google Scholar 

  • Zheng M, Lin J, Zhou S, Zhong J, Li Y, Xu N (2019) Salinity mediates the effects of nitrogen enrichment on the growth, photosynthesis, and biochemical composition of Ulva prolifera. Environ Sci Pollut R 26:19982–19990. doi:https://doi.org/10.1007/s11356-019-05364-y

    Article  Google Scholar 

  • Zou D (2005) Effects of elevated atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiforme (Sargassaceae, Phaeophyta). Aquaculture 250(3):726–735

    Article  Google Scholar 

  • Zou D, Gao K (2014a) Temperature response of photosynthetic light-and carbon-use characteristics in the red seaweed Gracilariopsis lemaneiformis (Gracilariales, Rhodophyta). J Phycol 50(2):366–375

    Article  Google Scholar 

  • Zou D, Gao K (2014b) The photosynthetic and respiratory responses to temperature and nitrogen supply in the marine green macroalga Ulva conglobata (Chlorophyta). Phycologia 53(1):86–94

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Editage (http://www.editage.co.kr) for the English language editing.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ik Kyo Chung.

Additional information

Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kambey, C.S.B., Kang, J.W. & Chung, I.K. Impact of Temperature, Low pH and NH4+ Enrichment on Ecophysiological Responses of a Green Tide Species Ulva australis Areschoug. Ocean Sci. J. 55, 115–127 (2020). https://doi.org/10.1007/s12601-020-0005-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12601-020-0005-y

Keywords

Navigation