Skip to main content

Advertisement

Log in

Individual and interactive effects of ocean acidification, global warming, and UV radiation on phytoplankton

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Rising carbon dioxide (CO2) concentrations in the atmosphere result in increasing global temperatures and ocean warming (OW). Concomitantly, dissolution of anthropogenic CO2 declines seawater pH, resulting in ocean acidification (OA) and altering marine chemical environments. The marine biological carbon pump driven by marine photosynthesis plays an important role for oceanic carbon sinks. Therefore, how ocean climate changes affect the amount of carbon fixation by primary producers is closely related to future ocean carbon uptake. OA may upregulate metabolic pathways in phytoplankton, such as upregulating ß-oxidation and the tricarboxylic acid cycle, resulting in increased accumulation of toxic phenolic compounds. Ocean warming decreases global phytoplankton productivity; however, regionally, it may stimulate primary productivity and change phytoplankton community composition, due to different physical and chemical environmental requirements of species. It is still controversial how OA and OW interactively affect marine carbon fixation by photosynthetic organisms. OA impairs the process of calcification in calcifying phytoplankton and aggravate ultraviolet (UV)-induced harms to the cells. Increasing temperatures enhance the activity of cellular repair mechanisms, which mitigates UV-induced damage. The effects of OA, warming, enhanced exposure to UV-B as well as the interactions of these environmental stress factors on phytoplankton productivity and community composition, are discussed in this review.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bach LT, Riebesell U, Gutowska MA, Federwisch L, Schulz KG (2015) A unifying concept of coccolithophore sensitivity to changing carbonate chemistry embedded in an ecological framework. Prog Oceanogr 135:125–138

    Article  Google Scholar 

  • Bais A, McKenzie R, Bernhard G, Aucamp P, Ilyas M, Madronich S, Tourpali K (2015) Ozone depletion and climate change: impacts on UV radiation. Photochem Photobiol Sci 14:19–52

    Article  CAS  PubMed  Google Scholar 

  • Beardall J, Raven JA (2004) The potential effects of global climate change on microalgal photosynthesis, growth and ecology. Phycologia 43:26–40

    Article  Google Scholar 

  • Beardall J, Stojkovic S, Gao K (2014) Interactive effects of nutrient supply and other environmental factors on the sensitivity of marine primary producers to ultraviolet radiation: implications for the impacts of global change. Aquatic Biol 22:5–23

    Article  Google Scholar 

  • Behrenfeld M, O’Malley R, Siegel D, McClain C, Sarmiento J, Feldman G, Milligan A, Falkowski P, Letelier R, Boss E (2006) Climate-driven trends in contemporary ocean productivity. Nature 444:752–755

    Article  CAS  PubMed  Google Scholar 

  • Behrenfeld M, O'Malley R, Boss E, Westberry T, Graff J, Halsey KH, Milligan A, Siegel D, Brown M (2016) Revaluating ocean warming impacts on global phytoplankton. Nat Clim Chang 6:323–330

    Article  Google Scholar 

  • Berthelot H, Moutin T, L'Helguen S, Leblanc K, Hélias S, Grosso O, Leblond N, Charrière B, Bonnet S (2015) Dinitrogen fixation and dissolved organic nitrogen fueled primary production and particulate export during the VAHINE mesocosm experiment (New Caledonia lagoon). Biogeosciences 12:4099–4112

    Article  Google Scholar 

  • Böttjer D, Karl DM, Letelier RM, Viviani DA, Church MJ (2014) Experimental assessment of diazotroph responses to elevated seawater pCO2 in the North Pacific Subtropical Gyre. Glob Biogeochem Cycles 28:601–616

    Article  CAS  Google Scholar 

  • Boyce DG, Lewis MR, Worm B (2010) Global phytoplankton decline over the past century. Nature 466:591–596

    Article  CAS  PubMed  Google Scholar 

  • Boyd PW, Rynearson TA, Armstrong EA, Fu F, Hayashi K, Hu Z, Hutchins DA, Kudela RM, Litchman E, Mulholland MR, Passow U, Strzepek RF, Whittaker KS, Yu E, Thomas MK (2013) Marine phytoplankton temperature versus growth responses from polar to tropical waters—outcome of a scientific community-wide study. PLoS One 8:e63091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyd PW (2011) Beyond ocean acidification. Nat Geosci 4:273–274

    Article  CAS  Google Scholar 

  • Britton D, Cornwall CE, Revill AT, Hurd CL, Johnson CR (2016) Ocean acidification reverses the positive effects of seawater pH fluctuations on growth and photosynthesis of the habitat-forming kelp, Ecklonia radiata. Scient Rep 6:26036

    Article  CAS  Google Scholar 

  • Buitenhuis ET, Pangerc T, Franklin DJ, Le Quéré C, Malin G (2008) Growth rates of six coccolithophorid strains as a function of temperature. Limnol Oceanogr 53:1181–1185

    Article  Google Scholar 

  • Caldeira K, Wickett ME (2003) Oceanography: anthropogenic carbon and ocean pH. Nature 425:365–365

    Article  CAS  PubMed  Google Scholar 

  • Chavez FP, Messié M, Pennington JT (2011) Marine primary production in relation to climate variability and change. Annu Rev Mar Sci 3:227–260

    Article  Google Scholar 

  • Chen S, Gao K (2011) Solar ultraviolet radiation and CO2-induced ocean acidification interacts to influence the photosynthetic performance of the red tide alga Phaeocystis globosa (Prymnesiophyceae). Hydrobiologia 675:105–117

    Article  CAS  Google Scholar 

  • Chen SW, Gao KS, Beardall J (2015) Viral attack exacerbates the susceptibility of a bloom-forming alga to ocean acidification. Glob Chang Biol 21:629–636

    Article  PubMed  Google Scholar 

  • Chivers WJ, Walne AW, Hays GC (2017) Mismatch between marine plankton range movements and the velocity of climate change. Nat Commun 8:14434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Claquin P, Probert I, Lefebvre S, Veron B (2008) Effects of temperature on photosynthetic parameters and TEP production in eight species of marine microalgae. Aquat Microb Ecol 51:1–11

    Article  Google Scholar 

  • Coello-Camba A, Agustí S, Holding J, Arrieta JM, Duarte CM (2014) Interactive effect of temperature and CO2 increase in Arctic phytoplankton. Front Mar Sci 1:49

    Article  Google Scholar 

  • Conte MH, Thompson A, Lesley D, Harris RP (1998) Genetic and physiological influences on the alkenone/alkenoate versus growth temperature relationship in Emiliania huxleyi and Gephyrocapsa oceanica. Geochim Cosmochim Acta 62:51–68

    Article  CAS  Google Scholar 

  • Czerny J, Barcelos e Ramos J, Riebesell U (2009) Influence of elevated CO2 concentrations on cell division and nitrogen fixation rates in the bloom-forming cyanobacterium Nodularia spumigena. Biogeosciences 6:1865–1875

    Article  CAS  Google Scholar 

  • De Bodt C, Van Oostende N, Harlay J, Sabbe K, Chou L (2010) Individual and interacting effects of pCO2 and temperature on Emiliania huxleyi calcification: study of the calcite production, the coccolith morphology and the coccosphere size. Biogeosciences 7:1401–1412

    Article  CAS  Google Scholar 

  • Domingues RB, Guerra CC, Galvão HM, Brotas V, Barbosa AB (2017) Short-term interactive effects of ultraviolet radiation, carbon dioxide and nutrient enrichment on phytoplankton in a shallow coastal lagoon. Aquatic Ecol 51:91–105

    Article  Google Scholar 

  • Doyle SA, Saros JE, Williamson CE (2005) Interactive effects of temperature and nutrient limitation on the response of alpine phytoplankton growth to ultraviolet radiation. Limnol Oceanogr 50:1362–1367

    Article  CAS  Google Scholar 

  • Edward M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophie mismatch. Nature 430:881–884

    Article  CAS  Google Scholar 

  • Ehlert D, Zickfeld K, Eby M, Gillett N (2017) The sensitivity of the proportionality between temperature change and cumulative CO2 emissions to ocean mixing. J Clim 30. doi: https://doi.org/10.1175/JCLI-D-16-0247.s1

  • Eichner M, Rost B, Kranz SA (2014) Diversity of ocean acidification effects on marine N2 fixers. J Exp Mar Biol Ecol 457:199–207

    Article  CAS  Google Scholar 

  • Engel A, Piontek J, Grossart H-P, Riebesell U, Schulz KG, Sperling M (2014) Impact of CO2 enrichment on organic matter dynamics during nutrient induced coastal phytoplankton blooms. J Plankton Res 36:641–657

    Article  CAS  Google Scholar 

  • Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240

    Article  CAS  PubMed  Google Scholar 

  • Fu FX, Tatters AO, Hutchins DA (2012) Global change and the future of harmful algal blooms in the ocean. Mar Ecol Prog Ser 470:207–233

    Article  CAS  Google Scholar 

  • Gaitán-Espitia JD, Marshall D, Dupont S, Bacigalupe LD, Bodrossy L, Hobday AJ (2017) Geographical gradients in selection can reveal genetic constraints for evolutionary responses to ocean acidification. Biol Lett 13:20160784

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao K, Campbell D (2014) Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: a review. Funct Plant Biol 41:449–459

    Article  CAS  Google Scholar 

  • Gao K, Helbling EW, Häder D-P, Hutchins DA (2012a) Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Mar Ecol Prog Ser 470:167–189

    Article  CAS  Google Scholar 

  • Gao K, Ruan Z, Villafañe VE, Gattuso JP, Helbling EW (2009) Ocean acidification exacerbates the effect of UV radiation on the calcifying phytoplankter Emiliania huxleyi. Limnol Oceanogr 54:1855–1862

    Article  CAS  Google Scholar 

  • Gao K, Wu Y, Li G, Wu H, Villafañe VE, Helbling EW (2007) Solar UV radiation drives CO2 fixation in marine phytoplankton: a double-edged sword. Plant Physiol 144:54–59

    Article  CAS  PubMed  PubMed Central  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 Chang Biol 16:2388–2398

    Article  Google Scholar 

  • Gao KS, JT X, Gao G, Li YH, Hutchins DA, Huang BQ, Wang L, Zheng Y, Jin P, Cai XN, Häder DP, Li W, Xu K, Liu NN, Riebesell U (2012b) Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nat Clim Chang 2:519–523

    Article  CAS  Google Scholar 

  • Garcia-Corral LS, Martinez-Ayala J, Duarte CM, Agusti S (2015) Experimental assessment of cumulative temperature and UV-B radiation effects on Mediterranean plankton metabolism. Front Mar Sci 2:48

    Article  Google Scholar 

  • Gargett A, Marra J (2002) Effects of upper ocean physical processes (turbulence, advection and air-sea interaction) on oceanic primary production. The Sea 12:19–49

    Google Scholar 

  • Gattuso J-P, Magnan A, Billé R, Cheung W, Howes E, Joos F, Allemand D, Bopp L, Cooley S, Eakin C (2015) Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349(6243):aac4722

    Article  PubMed  CAS  Google Scholar 

  • Geider RJ, MacIntyre HL, Kana TM (1997) A dynamic model of phytoplankton growth and acclimation: responses of the balanced growth rate and chlorophyll a:carbon ratio to light, nutrient-limitation and temperature. Mar Ecol Prog Ser 148:187–200

    Article  Google Scholar 

  • Gradoville MR, White AE, Böttjer D, Church MJ, Letelier RM (2014) Diversity trumps acidification: lack of evidence for carbon dioxide enhancement of Trichodesmium community nitrogen or carbon fixation at Station ALOHA. Limnol Oceanogr 59:645–659

    Article  CAS  Google Scholar 

  • Grear JS, Rynearson TA, Montalbano AL, Govenar B, Menden-Deuer S (2017) pCO2 effects on species composition and growth of an estuarine phytoplankton community. Estuar Coast Shelf Sci 190:40–49

    Article  CAS  Google Scholar 

  • Groetsch PM, Simis SG, Eleveld MA, Peters SW (2016) Spring blooms in the Baltic Sea have weakened but lengthened from 2000 to 2014. Biogeosciences 13(17):4959

    Article  Google Scholar 

  • Guan W, Li P (2017) Dependency of UVR-induced photoinhibition on atomic ratio of N to P in the dinoflagellate Karenia mikimotoi. Mar Biol 164(2):31

    Article  CAS  Google Scholar 

  • Häder D-P, Gao K (2015) Interactions of anthropogenic stress factors on marine phytoplankton. Front Env Sci 3:14

    Google Scholar 

  • Häder D-P, Richter P, Villafañe VE, Helbling EW (2014) Influence of light history on the photosynthetic and motility responses of Gymnodinium chlorophorum exposed to UVR and different temperatures. J Photochem Photobiol B 138:273–281

    Article  PubMed  CAS  Google Scholar 

  • Häder D-P, Williamson CE, Wangberg S-A, Rautio M, Rose KC, Gao K, Helbling EW, Sinha RP, Worrest R (2015) Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors. Photochem Photobiol Sci 14:108–126. https://doi.org/10.1039/C4PP90035A

    Article  PubMed  Google Scholar 

  • Halac S, Villafañe V, Gonçalves R, Helbling E (2014) Photochemical responses of three marine phytoplankton species exposed to ultraviolet radiation and increased temperature: role of photoprotective mechanisms. J Photochem Photobiol B 141:217–227

    Article  CAS  PubMed  Google Scholar 

  • Halac SR, Guendulain-García SD, Villafañe VE, Helbling EW, Banaszak AT (2013) Responses of tropical plankton communities from the Mexican Caribbean to solar ultraviolet radiation exposure and increased temperature. J Exp Mar Biol Ecol 445:99–107

    Article  Google Scholar 

  • Halac SR, Villafañe VE, Helbling EW (2010) Temperature benefits the photosynthetic performance of the diatoms Chaetoceros gracilis and Thalassiosira weissflogii when exposed to UVR. J Photochem Photobiol B 101:196–205

    Article  CAS  PubMed  Google Scholar 

  • Hansell DA, Carlson CA (2014) Biogeochemistry of marine dissolved organic matter. Academic Press

  • Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M (2006) Global temperature change. Proc Nat Acad Sci 103:14288–14293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hattenrath-Lehmann TK, Smith JL, Wallace RB, Merlo LR, Koch F, Mittelsdorf H, Goleski JA, Anderson DM, Gobler CJ (2015) The effects of elevated CO 2 on the growth and toxicity of field populations and cultures of the saxitoxin-producing dinoflagellate, Alexandrium fundyense. Limnol Oceanogr 60:198–214

    Article  CAS  PubMed  Google Scholar 

  • Henson SA, Beaulieu C, Lampitt R (2016) Observing climate change trends in ocean biogeochemistry: when and where. Glob Chang Biol 22:1561–1571

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoffmann L, Hoppe CM, Müller R, Dutton GS, Gille JC, Griessbach S, Jones A, Meyer CI, Spang R, Volk CM, Walker KA (2014) Stratospheric lifetime ratio of CFC-11 and CFC-12 from satellite and model climatologies. Atmos Chem Phys 14:12479–12497

    Article  CAS  Google Scholar 

  • Holding JM, Duarte CM, Sanz-Martín M, Mesa E, Arrieta JM, Chierici M, Hendriks I, Garcia-Corral L, Regaudie-de-Gioux A, Delgado A (2015) Temperature dependence of CO2-enhanced primary production in the European Arctic Ocean. Nat Clim Chang 5:1079–1082

    Article  CAS  Google Scholar 

  • Hönisch B, Ridgwell A, Schmidt DN, Thomas E, Gibbs SJ, Sluijs A, Zeebe R, Kump L, Martindale RC, Greene SE (2012) The geological record of ocean acidification. Science 335:1058–1063

    Article  PubMed  CAS  Google Scholar 

  • Honjo S, Eglinton TI, Taylor CD, Ulmer KM, Sievert SM, Bracher A, German CR, Edgcomb V, Francois R, Inglesias-Rodriguez MD (2014) Understanding the role of the biological pump in the global carbon cycle: an imperative for ocean science. Oceanography 27:10–16

    Article  Google Scholar 

  • Huey RB, Stevenson R (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am Zool 19:357–366

    Article  Google Scholar 

  • Hutchins DA, F-X F, Webb EA, Walworth N, Tagliabue A (2013) Taxon-specific response of marine nitrogen fixers to elevated carbon dioxide concentrations. Nat Geosci 6:790–795

    Article  CAS  Google Scholar 

  • Hutchins DA, Walworth NG, Webb EA, Saito MA, Moran D, McIlvin MR, Gale J, F-X F (2015) Irreversibly increased nitrogen fixation in Trichodesmium experimentally adapted to elevated carbon dioxide. Nat Commun 6

  • Hyun B, Choi K-H, Jang P-G, Jang M-C, Lee W-J, Moon C-H, Shin K (2014) Effects of increased CO2 and temperature on the growth of four diatom species (Chaetoceros debilis, Chaetoceros didymus, Skeletonema costatum and Thalassiosira nordenskioeldii) in laboratory experiments. J Env Sci Internat 23:1003–1012

    Article  Google Scholar 

  • IPCC (2014) Climate change 2014: impacts, adaptation, and vulnerability. Part B: Regional Aspects Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change vol 2014

  • Jin P, Ding J, Xing T, Riebesell U, Gao K (2017) High levels of solar radiation offset impacts of ocean acidification on Emiliania huxleyi, with special reference to calcifying and non-calcifying strains. Mar Ecol Prog Ser 568:47–58

    Article  CAS  Google Scholar 

  • Jin P, Gao K, Villafañe V, Campbell D, Helbling W (2013) Ocean acidification alters the photosynthetic responses of a coccolithophorid to fluctuating ultraviolet and visible radiation. Plant Physiol 162:2084–2094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin P, Wang T, Liu N, Dupont S, Beardall J, Boyd PW, Riebesell U, Gao K (2015) Ocean acidification increases the accumulation of toxic phenolic compounds across trophic levels. Nat Commun 6:8714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaeriyama H, Katsuki E, Otsubo M, Yamada M, Ichimi K, Tada K, Harrison PJ (2011) Effects of temperature and irradiance on growth of strains belonging to seven Skeletonema species isolated from Dokai Bay, southern Japan. Eur J Phycol 46:113–124

    Article  Google Scholar 

  • Kim J-H (2006) The effect of seawater CO2 concentration on growth of a natural phytoplankton assemblage in a controlled mesocosm experiment. Limnol Oceanogr 51:1629–1636

    Article  CAS  Google Scholar 

  • Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CL, Robbins LL (2006) Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research. Workshop held 18–20 April 2005, St. Petersburg, FL, sponsored by NSF, NOAA, and the U.S. Geological Survey

  • Kremp A, Godhe A, Egardt J, Dupont S, Suikkanen S, Casabianca S, Penna A (2012) Intraspecific variability in the response of bloom-forming marine microalgae to changed climate conditions. Ecol Evol 2:1195–1207

    Article  PubMed  PubMed Central  Google Scholar 

  • Lammers JM, van Soelen EE, Donders TH, Wagner-Cremer F, Sinninghe Damsté JS, Reichart GJ (2013) Natural environmental changes versus human impact in a Florida Estuary (Rookery Bay, USA). Estuar Coasts 36:149–157

    Article  CAS  Google Scholar 

  • Landschützer P, Gruber N, Bakker D, Schuster U (2014) Recent variability of the global ocean carbon sink. Glob Biogeochem Cycles 28:927–949

    Article  CAS  Google Scholar 

  • Larsen J, Larsen A, Thyrhaug R, Bratbak G, Sandaa R-A (2008) Response of marine viral populations to a nutrient induced phytoplankton bloom at different pCO2 levels. Biogeosciences 5:523–533

    Article  Google Scholar 

  • Leung PT, Yi AX, Ip JC, Mak SS, Leung KM (2017) Photosynthetic and transcriptional responses of the marine diatom Thalassiosira pseudonana to the combined effect of temperature stress and copper exposure. Mar Poll Bull. https://doi.org/10.1016/j.marpolbul.2017.03.038

  • Li G, Gao K (2013) Cell size-dependent effects of solar UV radiation on primary production in coastal waters of the South China Sea. Estuar Coasts 36:728–736

    Article  CAS  Google Scholar 

  • Li G, Gao K, Gao G (2011) Differential impacts of solar UV radiation on photosynthetic carbon fixation from the coastal to offshore surface waters in the South China Sea. Photochem Photobiol 87:329–334

    Article  CAS  PubMed  Google Scholar 

  • Li G, Wu Y, Gao K (2009) Effects of Typhoon Kaemi on coastal phytoplankton assemblages in the South China Sea, with special reference to the effects of solar UV radiation. J Geophys Res Biogeosci 114(G4)

  • Li W, Gao K, Beardall J (2012a) Interactive effects of ocean acidification and nitrogen-limitation on the diatom Phaeodactylum tricornutum. PLoS One 7(12):e51590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Gao KS (2012) A marine secondary producer respires and feeds more in a high CO2 ocean. Mar Poll Bull 64:699–703

    Article  CAS  Google Scholar 

  • Li W, Yang Y, Li Z, Xu J, Gao K (2016) Effects of seawater acidification on the growth rates of the diatom Thalassiosira (Conticribra) weissflogii under different nutrient, light, and UV radiation regimes. J Appl Phycol 29:133–142

    Article  CAS  Google Scholar 

  • Li Y, Gao K, Villafañe V, Helbling E (2012b) Ocean acidification mediates photosynthetic response to UV radiation and temperature increase in the diatom Phaeodactylum tricornutum. Biogeosciences 9:3931–3942

    Article  CAS  Google Scholar 

  • Listmann L, LeRoch M, Schlüter L, Thomas MK, Reusch TB (2016) Swift thermal reaction norm evolution in a key marine phytoplankton species. Evol Appl 9:1156–1164

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu N, Beardall J, Gao K (2017) Elevated CO2 and associated seawater chemistry do not benefit a model diatom grown with increased availability of light. Aquat Microb Ecol 79:137–147

    Article  Google Scholar 

  • Lohbeck K, Riebesell U, Reusch T (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci 5:346–351

    Article  CAS  Google Scholar 

  • Mackey KR, Morris JJ, Morel FM, Kranz SA (2015) Response of photosynthesis to ocean acidification. Oceanography 28:74–91

  • Manney GL, Santee ML, Rex M, Livesey NJ, Pitts MC, Veefkind P, Nash ER, Wohltmann I, Lehmann R, Froidevaux L, Poole LR, Schoeberl MR, Haffner DP, Davies J, Dorokhov V, Gernandt H, Johnson B, Kivi R, Kyrö E, Larsen N, Levelt PF, Makshtas A, McElroy CT, Nakajima H, Parrondo MC, Tarasick DW, von der Gathen P, Walker KA, Zinoviev NS (2011) Unprecedented Arctic ozone loss in 2011. Nature:469–475

  • Marchese C, Albouy C, Tremblay J-É, Dumont D, D’Ortenzio F, Vissault S, Bélanger S (2017) Changes in phytoplankton bloom phenology over the North Water (NOW) polynya: a response to changing environmental conditions. Polar Biol 40:1721–1737

  • Matthiessen B, Eggers SL, Krug S (2012) High nitrate to phosphorus regime attenuates negative effects of rising pCO2 on total population carbon accumulation. Biogeosciences 9:1195–1203

    Article  CAS  Google Scholar 

  • McKenzie RL, Aucamp PJ, Bais AF, Björn LO, Ilyas M, Madronich S (2011) Ozone depletion and climate change: impacts on UV radiation. Photochem Photobiol Sci 10:182–198

    Article  CAS  PubMed  Google Scholar 

  • Meador JA, Baldwin AJ, Catala P, Jeffrey WH, Joux F, Moss JA, Pakulski JD, Stevens R, Mitchell DL (2009) Sunlight-induced DNA damage in marine micro-organisms collected along a latitudinal gradient from 70 oN to 68 oS. Photochem Photobiol 85:412–421

    Article  CAS  PubMed  Google Scholar 

  • Michaels AF, Karl DM, Capone DG (2001) Element stoichiometry, new production and nitrogen fixation. Oceanography 14:68–77

    Article  Google Scholar 

  • Millero FJ (2007) The marine inorganic carbon cycle. Chem Rev 107:308–341

    Article  CAS  PubMed  Google Scholar 

  • Milner S, Langer G, Grelaud M, Ziveri P (2016) Ocean warming modulates the effects of acidification on Emiliania huxleyi calcification and sinking. Limnol Oceanogr 61:1322–1336

    Article  CAS  Google Scholar 

  • Miyairi S (1995) CO2 assimilation in a thermophilic cyanobacterium. Energy Convers Manag 36:763–766

    Article  CAS  Google Scholar 

  • Moisan TA, Goes J, Neale PJ (2009) Mycosporine-like amino acids in phytoplankton: biochemistry, physiology and optics. In: Kersey WT, Munger SP (eds) Marine phytoplankton. Nova Science Publishers, New York, pp 119–143

    Google Scholar 

  • Montagnes DJ, Franklin M (2001) Effect of temperature on diatom volume, growth rate, and carbon and nitrogen content: reconsidering some paradigms. Limnol Oceanogr 46:2008–2018

    Article  CAS  Google Scholar 

  • Monteiro FM, Bach LT, Brownlee C, Bown P, Rickaby RE, Poulton AJ, Tyrrell T, Beaufort L, Dutkiewicz S, Gibbs S (2016) Why marine phytoplankton calcify. Sci Adv 2(7):e1501822

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Neale PJ, Helbling EW, Zagarese HE (2003) Modulation of UVR exposure and effects by vertical mixing and advection. In: Helbling EW, Zagarese H (eds) UV Effects in aquatic organisms and ecosystems, vol 1. The royal society of chemistry, London pp 107–134

  • Newman PA, McKenzie RL (2011) UV impacts avoided by the Montreal Protocol. Photochem Photobiol Sci 10:1152–1160.

  • Nick FM, Vieli A, Andersen ML, Joughin I, Payne A, Edwards TL, Pattyn F, van de Wal RS (2013) Future sea-level rise from Greenland’s main outlet glaciers in a warming climate. Nature 497:235–238

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Paul C, Sommer U, Garzke J, Moustaka-Gouni M, Paul A, Matthiessen B (2016) Effects of increased CO2 concentration on nutrient limited coastal summer plankton depend on temperature. Limnol Oceanogr 61:853–868

    Article  CAS  Google Scholar 

  • Piazena H, Perez-Rodrigues E, Häder D-P, Lopez-Figueroa F (2002) Penetration of solar radiation into the water column of the central subtropical Atlantic Ocean—optical properties and possible biological consequences. Deep-Sea Res II 49:3513–3528

    Article  CAS  Google Scholar 

  • Rastogi R, Singh S, Incharoensakdi A, Häder D-P, Sinha R (2014) Ultraviolet radiation-induced generation of reactive oxygen species, DNA damage and induction of UV-absorbing compounds in the cyanobacterium Rivularia sp. HKAR-4. S Afr J Bot 90:163–169

    Article  CAS  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. Policy Document 12/05. The Royal Society, London, p 57

  • Raymont JE (2014) Plankton & productivity in the oceans: Volume 1: Phytoplankton. Elsevier

  • Richa, Sinha RP, Häder D-P (2016) Effects of global change, including UV and UV screening compounds. In: Borowitzka MA, Beardall J, Raven J (eds) The physiology of microalgae. Springer, Cham, pp 373–409

    Chapter  Google Scholar 

  • Riebesell U, Gattuso J-P (2015) Lessons learned from ocean acidification research. Nat Clim Chang 5(1):12–14

    Article  CAS  Google Scholar 

  • Riebesell U, Schulz KG, Bellerby RGJ, Botros M, Fritsche P, Meyerhöfer M, Neill C, Nondal G, Oschlies A, Wohlers J, Zöllner E (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450:545–548

    Article  CAS  PubMed  Google Scholar 

  • Riebesell U, Tortell PD (2011) Effects of ocean acidification on pelagic organisms and ecosystems. In: Gattuso JP, Hansson L (eds) Ocean acidification. Oxford University Press, Oxford, pp 99–116

    Google Scholar 

  • Rind D, Suozzo R, Balachandran N, Prather M (1990) Climate change and the middle atmosphere. Part I: the doubled CO2 climate. J Atmos Sci 47:475–494

    Article  Google Scholar 

  • Rosas-Navarro A, Langer G, Ziveri P (2016) Temperature affects the morphology and calcification of Emiliania huxleyi strains. Biogeosciences 13:2913–2926

    Article  Google Scholar 

  • Rose JM, Feng Y, DiTullio GR, Dunbar RB, Hare CE, Lee PA, Lohan M, Long M, Smith WO Jr, Sohst B, Tozzi S, Zhang Y, Hutchins DA (2009) Synergistic effects of iron and temperature on Antarctic phytoplankton and microzooplankton assemblages. Biogeosciences 6:3131–3147

    Article  CAS  Google Scholar 

  • Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Won CS, Wallace DWR, Tilbrook B, Millero FJ, Peng T-H, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371

    Article  CAS  PubMed  Google Scholar 

  • Schädel C, Bader MK-F, Schuur EA, Biasi C, Bracho R, Čapek P, De Baets S, Diáková K, Ernakovich J, Estop-Aragones C (2016) Potential carbon emissions dominated by carbon dioxide from thawed permafrost soils. Nat Clim Chang 6:950–953

    Article  CAS  Google Scholar 

  • Schlüter L, Lohbeck KT, Gutowska MA, Gröger JP, Riebesell U, Reusch TB (2014) Adaptation of a globally important coccolithophore to ocean warming and acidification. Nat Clim Chang 4:1024–1030

    Article  CAS  Google Scholar 

  • Sett S, Bach LT, Schulz KG, Koch-Klavsen S, Lebrato M, Riebesell U (2014) Temperature modulates coccolithophorid sensitivity of growth, photosynthesis and calcification to increasing seawater pCO2. PLoS One 9(2):e88308

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shi D, Kranz SA, Kim J-M, Morel FM (2012) Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions. Proc Nat Acad Sci 109:E3094–E3100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siegel DA, Behrenfeld MJ, Maritorena S, McClain CR, Antoine D, Bailey SW, Bontempi PS, Boss ES, Dierssen HM, Doney SC (2013) Regional to global assessments of phytoplankton dynamics from the SeaWiFS mission. Remote Sens Environ 135:77–91

    Article  Google Scholar 

  • Solomon S, Ivy DJ, Kinnison D, Mills MJ, Neely RR, Schmidt A (2016) Emergence of healing in the Antarctic ozone layer. Science 353:269–274

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Steinacher M, Joos F, Froelicher TL, Bopp L, Cadule P, Cocco V, Doney SC, Gehlen M, Lindsay K, Moore JK, Schneider B, Segschneider J (2010) Projected 21st century decrease in marine productivity: a multi-model analysis. Biogeosciences 7:979–1005

    Article  CAS  Google Scholar 

  • Steinberg DK, Nelson NB, Craig AC, Prusak A (2004) Production of chromophoric dissolved organic matter (CDOM) in the open ocean by zooplankton and the colonial cyanobacterium Trichodesmium spp. Mar Ecol Prog Ser 267:45–56

    Article  CAS  Google Scholar 

  • Stolarski RS (1988) The Antarctic ozone hole. Sci Am 258:20–26

    Article  Google Scholar 

  • Sun J, Hutchins DA, Feng Y, Seubert EL, Caron DA, F-X F (2011) Effects of changing pCO2 and phosphate availability on domoic acid production and physiology of the marine harmful bloom diatom Pseudo-nitzschia multiseries. Limnol Oceanogr 56:829–840

    Article  CAS  Google Scholar 

  • Suzuki Y, Takahashi M (1995) Growth responses of several diatom species isolated from various environments to temperature. J Phycol 31:880–888

    Article  Google Scholar 

  • Thomas MK, Kremer CT, Klausmeier CA, Litchman E (2012) A global pattern of thermal adaptation in marine phytoplankton. Science 338:1085–1088

    Article  CAS  PubMed  Google Scholar 

  • Tilstone G, Šedivá B, Tarran G, Kaňa R, Prášil O (2016) Effect of CO2 enrichment on phytoplankton photosynthesis in the North Atlantic sub-tropical gyre. Progr Oceanogr. https://doi.org/10.1016/j.pocean.2016.12.005

  • Tong S, Hutchins D, Gao K (2017) Physiological and biochemical responses of Emiliania huxleyi to ocean acidification and warming are modulated by UV radiation. Biogeosci Discuss. https://doi.org/10.5194/bg-2017-269

  • Tortell PD, DiTullio GR, Sigman DM, Morel FM (2002) CO2 effects on taxonomic composition and nutrient utilization in an equatorial Pacific phytoplankton assemblage. Mar Ecol Prog Ser 236:37–43

    Article  Google Scholar 

  • Tortell PD, Rau GH, Morel FM (2000) Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnol Oceanogr 45:1485–1500

    Article  CAS  Google Scholar 

  • United Nations Environment Programme Environmental Effects Assessment Panel (2017) Environmental effects of ozone depletion and its interactions with climate change: progress report, 2016. Photochem Photobiol Sci 16:107–145

    Article  Google Scholar 

  • Van de Waal DB, Verspagen JMH, Finke JF, Vournazou V, Immers AK, Kardinaal WEA, Tonk L, Becker S, Van Donk E, Visser PM, Huisman J (2011) Reversal in competitive dominance of a toxic versus non-toxic cyanobacterium in response to rising CO2. ISME J 5:1438–1450

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Verspagen JM, Van de Waal DB, Finke JF, Visser PM, Huisman J (2014) Contrasting effects of rising CO2 on primary production and ecological stoichiometry at different nutrient levels. Ecol Lett 17:951–960

    Article  PubMed  Google Scholar 

  • Villafañe VE, Gao K, Li P, Helbling EW (2007) Vertical mixing within the epilimnion modulates UVR-induced photoinhibition in tropical freshwater phytoplankton from southern China. Freshw Biol 52:1260–1270

    Article  CAS  Google Scholar 

  • Villar-Argaiz M, Balseiro E, Modenutti B, Souza M, Bullejos F, Medina-Sánchez J, Carrillo P (2017) Resource versus consumer regulation of phytoplankton: testing the role of UVR in a Southern and Northern hemisphere lake. Hydrobiologia https://doi.org/10.1007/s10750-017-3251-y

  • Wallington TJ, Schneider WF, Worsnop DR, Nielsen OJ, Sehested J, Debruyn WJ, Shorter JA (1994) The environmental impact of CFC replacements HFCs and HCFCs. Envi Sci Technol 28:320A–326A

  • Wang G, Xie S-P, Huang RX, Chen C (2015) Robust warming pattern of global subtropical oceans and its mechanism. J Clim 28:8574–8584

    Article  Google Scholar 

  • Wannicke N, Endres S, Engel A, Grossart H-P, Nausch M, Unger J, Voss M (2012) Response of Nodularia spumigena to pCO2—part 1: growth, production and nitrogen cycling. Biogeosciences 9:2973–2988

    Article  CAS  Google Scholar 

  • van Wells ML, Trainer VL, Smayda TJ, Karlson BS, Trick CG, Kudela RM, Ishikawa A, Bernard S, Wulff A, Anderson DM (2015) Harmful algal blooms and climate change: learning from the past and present to forecast the future. Harmful Algae 49:68–93

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu X, Gao G, Giordano M, Gao K (2012) Growth and photosynthesis of a diatom grown under elevated CO2 in the presence of solar UV radiation. Fund Appl Limnol 180:279–290

    Article  CAS  Google Scholar 

  • Wu Y, Gao K, Riebesell U (2010) CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7:2915–2923

    Article  CAS  Google Scholar 

  • Xing T, Gao K, Beardall J (2015) Response of growth and photosynthesis of Emiliania huxleyi to visible and UV irradiances under different light regimes. Photochem Photobiol 91:343–349

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Gao K, Li Y, Hutchins DA (2014) Multiple future ocean changes interactively alter physiological and biochemical processes of diatoms. Mar Ecol Progr Ser 515:73–81

    Article  Google Scholar 

  • Xu K, Gao K (2015) Solar UV irradiances modulate effects of ocean acidification on the Coccolithophorid Emiliania huxleyi. Photochem Photobiol 91:92–101

    Article  CAS  PubMed  Google Scholar 

  • Xu K, Gao K, Villafañe V, Helbling E (2011) Photosynthetic responses of Emiliania huxleyi to UV radiation and elevated temperature: roles of calcified coccoliths. Biogeosciences 8:1441–1452

    Article  CAS  Google Scholar 

  • Zeebe RE (2012) History of seawater carbonate chemistry, atmospheric CO2, and ocean acidification. Annu Rev Earth Planet Sci 40:141–165

    Article  CAS  Google Scholar 

  • Zeebe RE, Wolf-Gladrow DA (2001) CO2 in seawater: equilibrium, kinetics, isotopes. Elsevier, Amsterdam

    Google Scholar 

  • Zhang Y, Bach LT, Schulz KG, Riebesell U (2015) The modulating effect of light intensity on the response of the coccolithophore Gephyrocapsa oceanica to ocean acidification. Limnol Oceanogr 60:2145–2157

    Article  CAS  Google Scholar 

  • Zhang Y, Jiang HB, Qiu BS (2013) Effects of UVB radiation on competition between the bloom-forming cyanobacterium Microcystis aeruginosa and the Chlorophyceae Chlamydomonas microsphaera. J Phycol 49:318–328

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Klapper R, Lohbeck KT, Bach LT, Schulz KG, Reusch TB, Riebesell U (2014) Between-and within-population variations in thermal reaction norms of the coccolithophore Emiliania huxleyi. Limnol Oceanogr 59:1570–1580

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation (41430967, 41720104005, 41721005), Joint project of NSFC and Shandong province for marine ecology and environmental sciences (Grant No. U1406404), China Postdoctoral Science Foundation (2017 M612129), and the outstanding postdoctoral program of State Key Laboratory of Marine Environmental Science (Xiamen University).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kunshan Gao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, K., Zhang, Y. & Häder, DP. Individual and interactive effects of ocean acidification, global warming, and UV radiation on phytoplankton. J Appl Phycol 30, 743–759 (2018). https://doi.org/10.1007/s10811-017-1329-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1329-6

Keywords

Navigation