Skip to main content

The effects of eutrophication and acidification on the ecophysiology of Ulva pertusa Kjellman

Abstract

In coastal environments, acidification and eutrophication affect the physiology of marine macroalgae. We investigated the responses of Ulva pertusa Kjellman (Ulvales, Chlorophyta) under such conditions. Samples were cultured at two different pH settings (low, 7.5; high, 8.0) and at three different ammonium levels (low, 4; medium, 60; high, 120 μM NH4 +). Our objective was to analyze the influence that elevated CO2 and NH4 + might have on pH, oxygen evolution, rates of nutrient uptake, chlorophyll fluorescence, growth, and C/N ratio of that organism. Variability in pH value was enhanced under low pH/high NH4 + and was significantly different (p < 0.05) from changes measured when the high pH/low NH4 + combination was applied. Rates of NH4 + uptake and relative growth rates by U. pertusa were increased under low pH/high NH4 + conditions and that response was significantly different (p < 0.05) from the other treatments. The rate of photosynthetic oxygen evolution and chlorophyll fluorescence were increased under elevated NH4 + concentrations (p < 0.05). However, the C/N ratio of U. pertusa was not affected by higher concentrations of CO2 and NH4 + (p > 0.05). Our results indicated that the physiological reactions of this alga were heightened when exposed to either the elevated combination of CO2/NH4 + or even when only the level of NH4 + was raised. Although such excessive growth can lead to bloom formations in coastal areas, this species also has greater capacity for taking up nutrients and dissolved inorganic carbon.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Arévalo R, Pinedo S, Ballesteros E (2007) Changes in the composition and structure of Mediterranean rocky-shore communities following a gradient of nutrient enrichment: descriptive study and test of proposed methods to assess water quality regarding macroalgae. Mar Poll Bull 55:104–113

    Article  Google Scholar 

  • Axelsson L, Ryberg H, Beer S (1995) Two modes of bicarbonate utilization in the marine green macroalga Ulva lactuca. Plant Cell Environ 18:439–445

    CAS  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

    CAS  Article  Google Scholar 

  • Beardall J, Beer S, Raven JA (1998) Biodiversity of marine plants in an era of climate change: some predictions based on physiological performance. Bot Mar 41:113–124

    CAS  Article  Google Scholar 

  • Beer S, Israel A (1990) Photosynthesis of Ulva fasciata. IV. pH, carbonic anhydrase and inorganic carbon conversions in the unstirred layer. Plant Cell Environ 13:555–560

    CAS  Article  Google Scholar 

  • Ben-Ari T, Neori A, Ben-Ezra D, Shauli L, Odintsov V, Shpigel M (2014) Management of Ulva lactuca as a biofilter of mariculture effluents in IMTA system. Aquaculture 434:493–498

    Article  Google Scholar 

  • Björk M, Axelsson L, Beer S (2004) Why is Ulva intestinalis the only macroalga inhabiting isolated rockpools along the Swedish Atlantic coast? Mar Ecol Prog Ser 284:109–116

    Article  Google Scholar 

  • Björnsäter BR, Wheeler PA (1990) Effect of nitrogen and phosphorus supply on growth and tissue composition of Ulva fenestrata and Enteromorpha intestinalis (Ulvales, Chlorophyta). J Phycol 26:603–611

    Article  Google Scholar 

  • Bolton JJ, Robertson-Andersson DV, Shuuluka D, Kandjengo L (2009) Growing Ulva (Chlorophyta) in integrated systems as a commercial crop for abalone feed in South Africa: a SWOT analysis. J Appl Phycol 21:575–583

    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

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

    CAS  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

    CAS  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

    CAS  Article  Google Scholar 

  • Cohen RA, Fong P (2006) Using opportunistic green macroalgae as indicators of nitrogen supply and sources to estuaries. Ecol Appl 16:1405–1420

    Article  PubMed  Google Scholar 

  • Cornwall CE, Hurd CL (2015) Experimental design in ocean acidification research: problems and solutions. ICES J Mar Sci 72. doi:10.1093/icesjms/fsv118

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

    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 46:335–344

    Google Scholar 

  • de Faveri C, Schmidt ÉC, Simioni C, Martins CD, Bonomi-Barufi J, Horta PA, Bouzon ZL (2015) Effects of eutrophic seawater and temperature on the physiology and morphology of Hypnea musciformis JV Lamouroux (Gigartinales, Rhodophyta). Ecotoxicology 24:1040–1052

    Article  PubMed  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 sea water from 273.15 to 318.15 K. J Chem Thermodyn 22:113–127

    CAS  Article  Google Scholar 

  • Duke CS, Litaker RW, Ramus J (1987) Seasonal variation in RuBPCase activity and N allocation in the chlorophyte seaweeds Ulva curvata (Kutz.) De Toni and Codium decorticatum (Woodw.) Howe. J Exp Mar Biol Ecol 112:145–164

    CAS  Article  Google Scholar 

  • Falkowski PG, Raven JA (2007) Aquatic photosynthesis. Princeton University Press, Princeton 484 pp

    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 Rios J, Kirke D, Chow F, CAG N, 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 

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

    CAS  Article  PubMed  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

    CAS  Article  PubMed  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 

  • Hiraoka M, Shimada S, Uenosono M, Masuda M (2004) A new green-tide-forming alga, Ulva ohnoi Hiraoka et Shimada sp. nov. (Ulvales, Ulvophyceae) from Japan. Phycol Res 52:17–29

    Article  Google Scholar 

  • Horta PA, Vieira-Pinto T, Martins CDL, Sissini MN, Ramlov F, Lhullier C, Scherner F, Sanches PF, Farias JN, Bastos E, Bouzon JL, Munoz P, Valduga E, Arantes NP, Batista MB, Riul P, Almeida RS, Paes E, Fonseca A, Schenkel EP, Rorig L, Bouzon Z, Barufi JB, Colepicolo P, Yokoya N, Copertino MS, de Oliveira EC (2012) Evaluation of impacts of climate change and local stressors on the biotechnological potential of marine macroalgae: a brief theoretical discussion of likely scenarios. Rev Bras Farmacogn 22:768–774

    Article  Google Scholar 

  • Hurd CL, Hepburn CD, Currie KI, Raven JA, Hunter KA (2009) Testing the effects of ocean acidification on algal metabolism: consideration for experimental designs. J Phycol 45:1236–1251

    CAS  Article  PubMed  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

    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, Gambi MC, Micheli F (2013) Community dynamics and ecosystem simplification in a high-CO2 ocean. Proc Natl Acad Sci 110:12721–12726

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Larsson C, Axelsson L, Ryberg H, Beer S (1997) Photosynthetic carbon utilization by Enteromorpha intestinalis (Chlorophyta) from a Swedish rockpool. Eur J Phycol 32:49–54

    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, TN, USA

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

    CAS  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 11:1043–1052

    Article  Google Scholar 

  • Liu Y, Xu J, Gao K (2012) CO2-driven seawater acidification increases photochemical stress in a green alga. Phycologia 51:562–566

    CAS  Article  Google Scholar 

  • Lohman K, Priscu JC (1992) Physiological indicator of nutrient deficiency in Cladophora (Chlorophyta) in the Clark Fork of the Columbia River, Montana. J Phycol 28:443–448

    CAS  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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Mercado JM, Javier F, Gordillo L, Niell FX, Figueroa FL (1999) Effects of different levels of CO2 on photosynthesis and cell components of the red alga Porphyra leucosticta. J Appl Phycol 11:455–461

    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

    CAS  Article  Google Scholar 

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

    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

    CAS  Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Raven JA (1997) Inorganic carbon acquisition by marine autotrophs. Adv Bot Res 27:85–209

    CAS  Article  Google Scholar 

  • Raven JA, Giordano M, Beardall J, Maberly SC (2011) Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynth Res 109:281–296

    CAS  Article  PubMed  Google Scholar 

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

    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 76:155–174

    CAS  Article  Google Scholar 

  • Sarker MY, Bartsch I, Olischläger M, Gutow L, Wiencke C (2013) Combined effects of CO2, temperature, irradiance and time on the physiological performance of Chondrus crispus (Rhodophyta). Bot Mar 56:63–74

    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, 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 

  • Sunda WG, Cai WJ (2012) Eutrophication induced CO2-acidification of subsurface coastal waters: interactive effects of temperature, salinity, and atmospheric pCO2. Environ Sci Technol 46:10651–10659

    CAS  Article  PubMed  Google Scholar 

  • Valiela I, McClelland J, Hauxwell J, Behr PJ, Hersh D, Foreman K (1997) Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnol Oceanogr 42:1105–1118

    Article  Google Scholar 

  • Wang Y, Zhou B, Tang X (2009) Effects of two species of macroalgae—Ulva pertusa and Gracilaria lemaneiformis—on growth of Heterosigma akashiwo (Raphidophyceae). J Appl Phycol 21:375–385

    Article  Google Scholar 

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

    Article  PubMed  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

    CAS  Article  PubMed  PubMed Central  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

    CAS  Article  Google Scholar 

  • Ye NH, Zhang XW, Mao YZ, Liang CW, Xu D, Zou J, Zhuang ZM, Wang QY (2011) ‘Green tides’ are overwhelming the coastline of our blue planet: taking the world’s largest example. Ecol Res 26:477–485

    Article  Google Scholar 

  • Yong YS, Yong WTL, Anton A (2013) Analysis of formulae for determination of seaweed growth rate. J Appl Phycol 25:1831–1834

    Article  Google Scholar 

  • Young CS, Gobler CJ (2016) Ocean acidification accelerates the growth of two bloom-forming macroalgae. PLoS One 11:e0155152

    Article  PubMed  PubMed Central  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 Sinica 31:73–82

    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 250:726–735

    CAS  Article  Google Scholar 

  • Zou D (2014) The effects of severe carbon limitation on the green seaweed, Ulva conglobata (Chlorophyta). J Appl Phycol 26:2417–2424

    CAS  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

    CAS  Article  Google Scholar 

Download references

Acknowledgement

This work was supported by a 2-Year Research Grant of Pusan National University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ik Kyo Chung.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kang, J.W., Chung, I.K. The effects of eutrophication and acidification on the ecophysiology of Ulva pertusa Kjellman. J Appl Phycol 29, 2675–2683 (2017). https://doi.org/10.1007/s10811-017-1087-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1087-5

Keywords

  • Ammonium (NH4 +)
  • Carbon dioxide (CO2)
  • Eutrophication
  • Ocean acidification (OA)
  • Ulva pertusa
  • Chlorophyceae