Abstract
Marine macroalgae are ecologically and economically important primary producers, being adjacent to human living areas and playing key roles in coastal carbon cycles. They are subject to both regional and global environmental changes in coastal waters, where environmental factors fluctuate dramatically due to high biological production and land runoff. Since global ocean changes can influence coastal environments, global warming-induced ocean warming, ocean acidification (OA) caused by atmospheric CO2 rise and increasing ultraviolet B (UVB) irradiance at the earth’s surface are affecting physiology, life cycles, and community structures of macroalgae. Here, we examine recent progress towards understanding the effects of these climate change factors on ecophysiology of macroalgae. Some species tested show enhanced growth and/or photosynthesis under elevated CO2 levels or ocean acidification conditions, possibly due to increased availability of CO2 in seawater with neglected influence of pH drop. Nevertheless, OA can harm some macroalgae due to their high sensitivity to the acidic perturbation to intracellular acid–base stability. Mild ocean warming has been shown to benefit most macroalgae examined. Respiration quotient increased due to combined effects of ocean warming and acidification. UVB almost always harms the physiological functions of macroalgae, which develop protective strategies, such as accumulation of UV-absorbing compounds; UVA can drive photosynthesis under moderate levels of solar radiation or when solely exposed to it. However, little has been documented on the interactions of these multiple stressors. Future work requires further investigations to examine the effects of OA under complex environments or under multiple stressors to advance knowledge on macroalgal global change biology.
Similar content being viewed by others
References
Abdala-Díaz RT, Cabello-Pasini A, Pérez-Rodríguez E, Conde Álvarez RM, Figueroa FL (2006) Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta). Mar Biol 148:459–465
Aguilera J, Karsten U, Lippert H, Vögele B, Philipp E, Hanelt D, Wiencke C (1999) Effects of solar radiation on growth, photosynthesis and respiration of marine macroalgae from the Arctic. Mar Ecol Prog Ser 191:109–119
Aline T, Atkinson MJ, Langdon C (2006) Effects of elevated pCO2 on epilithic and endolithic metabolism of reef carbonates. Glob Chang Biol 12:2200–2208
Altamirano M, Flores-Moya A, Figueroa FL (2000) Long-term effects of natural sunlight under various ultraviolet radiation conditions on growth and photosynthesis of intertidal Ulva rigida (Chlorophyceae) cultivated in situ. Bot Mar 43:119–126
Altamirano M, Flores-Moya A, Figueroa FL (2003) Effects of UV radiation and temperature on growth of germlings of three species of Fucus (Phaeophyceae). Aquat Bot 75:9–20
Andrıá JR, Brun FG, Pérez-Lloréns JL, Vergara JJ (2001) Acclimation responses of Gracilaria sp. (Rhodophyta) and Enteromorpha intestinalis (Chlorophyta) to changes in the external inorganic carbon concentration. Bot Mar 44:361–370
Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci U S A 105:17442–17446
Arnold T, Mealey C, Leahey H, Miller AW, Hall-Spencer JM, Milazzo M, Maers K (2012) Ocean acidification and the loss of phenolic substances in marine plants. PLoS ONE 7(4), e35107
Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351
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
Bates NR, Best MHP, Neely K, Garley R, Dickson AG, Johnson RJ (2012) Detecting anthropogenic carbon dioxide uptake and ocean acidification in the North Atlantic Ocean. Biogeosciences 9:2509–2522
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 41:113–123
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. Aquat Biol 22:5–23
Beer S, Koch E (1996) Photosynthesis of marine macroalgae and seagrasses in globally changing CO2 environments. Mar Ecol Prog Ser 141:199–204
Borowitzka MA (1982) The morphology and cytology of calcium carbonate deposition by algae. Int Rev Cytol 74:127–162
Borowitzka MA (1987) Calcification in algae: mechanisms and the role of metabolism. Crit Rev Plant Sci 6:1–45
Borowitzka MA (1989) Carbonate calcification in algae—initiation and control. In: Mann S, Webb J, Williams RJP (eds) Biomineralization: chemical and biochemical perspectives. VCH Verlag, Weinheim, pp 63–94
Borowitzka MA, Larkum AWD (1976) Calcification in the green alga Halimeda III. The sources of inorganic carbon for photosynthesis and calcification and a model of the mechanism of calcification. J Exp Bot 27:879–893
Breeman AM (1990) Expected effects of changing seawater temperatures on the geographic distribution of seaweed species. In: Beukema JJ, Wolff WJ, Brouns JJWM (eds) Expected effects of climate change on marine coastal ecosystems. Kluwer, Dordrecht, pp 69–76
Büdenbender J, Riebesell U, Form A (2011) Calcification of the Arctic coralline red algae Lithothamnion glaciale in response to elevated CO2. Mar Ecol Prog Ser 441:79–87
Buschmann AH, VaAquez J, Osorio P, Reyes E, Filun L, Hernandez-Gonzalez MC, Vega A (2004) The effect of water movement, temperature and salinity on abundance and reproductive patterns of Macrocystis spp. (Phaeophyta) at different latitudes in Chile. Mar Biol 145:849–862
Caldeira K, Wickett ME (2003) Oceanography: anthropogenic carbon and ocean pH. Nature 425(6956):365
Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, Held I, Jones R, Kolli RK, Kwon WT, Laprise R, Magañarueda V, Mearns L, Menéndez CG, Raïsänen J, Rinke A, Sarr A, Whetton P (2007) Regional climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 847–940
Connell SD, Russell BD (2010) The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc R Soc B 277:1409–1415
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
Cornwall CE, Hepburn CD, McGraw CM, Currie KI, Pilditch CA, Hunter KA, Boyd PW, Hurd CL (2013a) Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc R Soc B 280:20132201
Cornwall CE, Hepburn CD, Pilditch CA, Hurd CL (2013b) Concentration boundary layers around complex assemblages of macroalgae: Implications for the effects of ocean acidification on understory coralline algae. Limnol Oceanogr 58:121–130
Costa H, Gallego SM, Tomaro ML (2002) Effect of UV-B radiation on antioxidant defense system in sunflower cotyledons. Plant Sci 162:939–945
Davison IR (1991) Environmental effects on algal photosynthesis: temperature. J Phycol 27:2–8
Davison IR, Greene RM, Podolak EJ (1991) Temperature acclimation of respiration and photosynthesis in the brown alga Laminaria saccharina. Mar Biol 110:449–454
Deysher LE, Dean TA (1986) In situ recruitment of sporophytes of the giant kelp, Macrocystis pyrifera (L) C.A. Agardh—effects of physical factors. J Exp Mar Biol Ecol 103:41–63
Döhler G (1998) Effect of UV radiation on pigments of the Antartic macroalga Leptosomia simplex L. Photosynthetica 35:473–476
Éder CS, Beatriz P, Rodrigo WS, Claudiane G, Giulia BC, Gabriel SMF, Fernando S, Paulo AH, Roberta PM, Alexandra L, Fernanda R, Marcelo M, Zenilda LB (2012) Responses of the macroalgae Hypnea musciformis after in vitro exposure to UV-B. Aquat Bot 100:8–17
Eggert A, Visser RJW, Van Hassel PR, Breeman AM (2006) Differences in acclimation potential of photosynthesis in seven isolates of the tropical to warm temperate macrophyte Valonia utricularis (Chlorophyta). Phycologia 45:546–556
Eswaran K, Subba-Rao PV, Mairh OP (2001) Impact of ultraviolet-B radiation on Kappaphycus alvarezii (Solieraceae, Rhodophyta). Indian J Mar Sci 30:105–107
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
Figueroa FL, Gómez I (2001) Photosynthetic acclimation to solar UV radiation of marine red algae from the warm-temperate coast of southern Spain: a review. J Appl Phycol 13:233–245
Gao K, Campbell DA (2014) Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: a review. Funct Plant Biol 41:449–459
Gao K, McKinley KR (1994) Use of macroalgae for marine biomass production and CO2 remediation: a review. J Appl Phycol 6:45–60
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
Gao K, Aruga Y, Asada K, Ishihara T, Akano T, Kiyohara M (1991) Enhanced growth of the red alga Porphyra yezoensis Ueda in high CO2 concentrations. J Appl Phycol 3:355–362
Gao K, Aruga Y, Asada K, Ishihara T, Akano T, Kiyohara M (1993a) Calcification in the articulated coralline alga Corallina pilulifera, with special reference to the effect of elevated CO2 concentration. Mar Biol 117:129–132
Gao K, Aruga Y, Asada K, Kiyohara M (1993b) Infuence of enhanced CO2 on growth and photosynthesis of the red algae Gracilaria sp. and G. chilensis. J Appl Phycol 5:563–571
Gao K, Ji Y, Aruga Y (1999) Relationship of CO2 concentrations to photosynthesis of intertidal macroalgae during emersion. Hydrobiologia 398/399:355–359
Gao K, Xu J, Gao G, Li Y, Hutchins DA, Huang B, Wang L, Zheng Y, Jin P, Cai X, Häder DP, Li W, Xu K, Liu N, Riebesell U (2012) Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nat Clim Chang 2:519–523
Garcıá-Sánchez MJ, Fernández JA, Niell X (1994) Effect of inorganic carbon supply on the photosynthetic physiology of Gracilaria tenuistipitata. Planta 194:55–61
Gómez I, Figueroa FL, Sousa-Pinto I, Viñegla B, Pérez-Rodríguez P, Maestre Z, Coelho S, Felga A, Pereira R (2001) Effects of UV radiation and temperature on photosynthesis as measured by PAM fluorescence in the red alga Gelidium pulchellum (Turner) Kützing. Bot Mar 44:9–16
Goncalves RJ, Souza MS, Aigo J, Modenutti B, Balseiro E, Villafañe VE, Cussac V, Helbling EW (2010) Responses of plankton and fish and temperate zones to UVR and temperature in a context of global change. Ecología Austral 20:129–153
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
Grobe CW, Murphy TM (1994) Inhibition of growth of Ulva expansa (Chlorophyta) by ultraviolet-B radiation. J Phycol 30:783–790
Guinotte JM, Fabry VJ (2008) Ocean acidification and its potential effects on marine ecosystems. Ann N Y Acad Sci 1134:320–342
Häder DP, Figueroa FL (1997) Photoecophysiology of marine macroalgae. Photochem Photobiol 66:1–14
Häder DP, Kumar HD, Smith RC, Worrest RC (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 6:267–285
Han YS, Han T (2005) UV-B induction of UV-B protection in Ulva pertusa (Chlorophyta). J Phycol 41:523–530
Harley CDG, Anderson KM, Demes KW, Jorve JP, Kordas RL, Coyle TA (2012) Effects of climate change on global seaweed communities. J Phycol 48:1064–1078
Helbling EW, Buma AGJ, Boelen P, Van der Strate HJ, Giordanino MVF, Villafañe VE (2011) Increase in Rubisco activity and gene expression due to elevated temperature partially counteracts ultraviolet radiation-induced photoinhibition in the marine diatom Thalassiossira weissflogii. Limnol Oceanogr 56:1330–1342
Henley WJ, Lindley ST, Levavasseur G, Osmond CB, Ramus J (1992) Photosynthetic response of Ulva rotundata to light and temperature during emersion on an intertidal sand flat. Oecologia 89:516–523
Hepburn CD, Pritchard DW, Cornwall CE, McLeod RJ, Beardall J, Raven JA, Hurd CL (2011) Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 ocean. Glob Chang Biol 17:2488–2497
Hoffman JR, Hansen LJ, Klinger T (2003) Interactions between UV radiation and temperature limit inferences from single-factor experiments. J Phycol 39:268–272
Hofmann LC, Yildiz G, Hanelt D, Bischof K (2012) Physiological responses of the calcifying rhodophyte, Corallina officinalis (L.), to future CO2 levels. Mar Biol 159:783–792
Hofmann LC, Straub S, Bischof K (2013) Elevated CO2 levels affect the activity of nitrate reductase and carbonic anhydrase in the calcifying rhodophyte Corallina officinalis. J Exp Bot 64:899–908
Holzinger A, Lütz C, Karsten U, Wiencke C (2004) The effect of ultraviolet radiation on ultrastructure and photosynthesis in the red macroalgae Palmaria palmata and Odonthalia dentata from Arctic waters. Plant Biol 6:568–577
Houghton RA (2008) Carbon flux to the atmosphere from land-use changes: 1850–2005, In: TRENDS: A Compendium of Data on Global Change. Carbon Dioxide Information Analysis Center, OakRidge National Laboratory, U.S. Department of Energy, Oak Ridge, Tennessee, USA, 2008
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 Chang Biol 8:831–840
Ji Y, Tanaka J (2002) Effect of desiccation on the photosynthesis of seaweeds from the intertidal zone in Honshu, Japan. Phycol Res 50:145–153
Jiang HX, Gao KS (2008) Effects of UV radiation on the photosynthesis of conchocelis of Porphyra haitanensis (Bangiales, Rhodophyta). Phycologia 47:241–248
Jiang HX, Gao KS, Helbling E (2007) Effects of solar UV radiation on germination of conchospores and morphogenesis of sporelings in Porphyra haitanensis (Rhodophyta). Mar Biol 151:1751–1759
Jiang HX, Gao KS, Helbling W (2009) The conchocelis of Porphyra haitanensis (Rhodophyta) is protected from harmful UV radiation by the covering calcareous matrix. J Phycol 45:1270–1277
Johnston AM, Raven JA (1990) Effects of culture in high CO2 on the photosynthetic physiology of Fucus serratus. Br Phycol J 25:75–82
Jueterbock A, Tyberghein L, Verbruggen H, Coyer JA, Olsen JL, Hoarau G (2013) Climate change impact on seaweed meadow distribution in the North Atlantic rocky intertidal. Ecol Evol 3:1356–1373
Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Chang Biol 13:103–132
Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434
Kübler JE, Davison IR (1993) High-temperature tolerance of photosynthesis in the red alga Chondrus crispus. Mar Biol 117:327–335
Kübler JE, Davison IR (1995) Thermal acclimation of light use characteristics of Chondrus crispus (Rhodophyta). Eur J Phycol 30:189–195
Kübler JE, Raven JA (1994) Consequences of light limitation for carbon acquisition in three rhodophytes. Mar Ecol Prog Ser 110:203–209
Kübler JE, Davison IR, Yarish C (1991) Photosynthetic adaptation to temperature in the red algae Lomentaria baileyana and Lomentaria orcadensis. Br Phycol J 26:9–19
Kübler JE, Johnston AM, Raven JA (1999) The effects of reduced and elevated CO2 and O2 on the seaweed Lomentaria articulata. Plant Cell Environ 22:1303–1310
Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117
Ladah LB, Zertuche-González JA (2007) Survival of microscopic stages of a perennial kelp (Macrocystis pyrifera) from the center and the southern extreme of its range in the Northern Hemisphere after exposure to simulated El Nino stress. Mar Biol 152:677–686
Li W, Gao KS, Beardall J (2012) Interactive effects of ocean acidification and nitrogen-limitation on the diatom Phaeodactylum tricornutum. PLoS ONE 7, e51590
Lotze HK, Worm B (2002) Complex interactions of climatic and ecological controls on macroalgal recruitment. Limnol Oceanogr 47:1734–1741
Machalek KM, Davison IR, Falkowski PG (1996) Thermal acclimation and photoacclimation of photosynthesis in the brown alga Laminaria saccharina. Plant Cell Environ 19:1005–1016
Madronich S (1992) Implications of recent total atmospheric ozone measurements for biological active ultraviolet radiation reaching the Earth’s surface. Geophys Res Lett 19:37–40
Martin S, Gattuso J-P (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Chang Biol 15:2089–2100
Martínez B, Arenas F, Rubal M, Burgués S, Esteban R, García-Plazaola I, Figueroa FL, Pereira R, Saldaña L, Sousa-Pinto I, Trilla A, Viejo RM (2012) Physical factors driving intertidal macroalgae distribution: physiological stress of a dominant fucoid at its southern limit. Oecologia 170:341–353
McKenzie RL, Björn LO, Bais A, Ilyasd M (2003) Changes in biologically active ultraviolet radiation reaching the Earth’s surface. Photochem Photobiol Sci 2:5–15
Michler T, Aguilera J, Hanelt D, Bischof K, Wiencke C (2002) Long term effects of ultraviolet radiation on growth and photosynthetic performance of polar and cold-temperate macroalgae. Mar Biol 140:1117–1127
Molis M, Wahl M (2009) Comparison of the impacts of consumers, ambient UV, and future UVB irradiance on mid-latitudinal macroepibenthic assemblages. Glob Chang Biol 15:1833–1845
Molis M, Lenz M, Wahl M (2003) Radiation effects along a UV-B gradient on species composition and diversity of a shallow-water macrobenthic community in the western Baltic. Mar Ecol Prog Ser 263:113–125
Müller R, Wiencke C, Bischof K (2008) Interactive effects of UV radiation and temperature on microstages of Laminariales (Phaeophyceae) from the Arctic and North Sea. Clim Res 37:203–213
Pakker H, Breeman AM (1996) Temperature responses of tropical to warm-temperate Atlantic seaweeds. II. Evidence for ecotypic differentiation in amphi-Atlantic tropical-Mediterranean species. Eur J Phycol 31:133–141
Pakker H, Klerk H, Campen JH, Olsen JL, Breeman AM (1996) Evolutionary and ecological differentiation in the pantropical to warm-temperate seaweed Digenea simplex (Rhodophyta). J Phycol 32:250–257
Pearson GA, Lago-Leston A, Mota C (2009) Frayed at the edges: selective pressure and adaptive response to abiotic stressors are mismatched in low diversity edge populations. J Ecol 97:450–462
Poppe F, Hanelt D, Wiencke C (2002) Changes in ultrastructure, photosynthetic activity and pigments in the Antarctic red alga Palmaria decipiens during acclimation to UV radiation. Bot Mar 45:253–261
Poppe F, Schmidt RAM, Hanelt D, Wiencke C (2003) Effects of UV radiation on the ultrastructure of several red algae. Physiol Res 51:11–19
Price NN, Hamilton SL, Tootell JS, Smith JE (2011) Species-specific consequences of ocean acidification for the calcareous tropical green algae Halimeda. Mar Ecol Prog Ser 440:67–78
Raven JA (1997) Putting the C in phycology. Eur J Phycol 32:319–333
Raven JA, Giordano M, Beardall J, Maberly SC (2012) Algal evolution in relation to atmospheric CO2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles. Phil Trans R Soc B: Biol Sci 367:493–507
Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134
Rodolfo-Metalpa R, Houlbrèque F, Tambutté É, Boisson F, Baggini C, Patti FP, Jeffree R, Foggo A, Gattuso J-P, Hall-Spencer JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat Clim Chang 1:308–312
Roleda MY, van de Poll WH, Wiencke C, Hanelt D (2004) PAR and UVBR effects on photosynthesis, viability, growth and DNA in different life stages of two coexisting Gigartinales: implications for recruitment and zonation pattern. Mar Ecol Prog Ser 281:37–50
Roleda MY, Lütz-Meindl U, Wiencke C, Lütz C (2010) Physiological, biochemical, and ultrastructural responses of the green macroalga Urospora penicilliformis from Arctic Spitsbergen to UV radiation. Protoplasma 243:105–116
Roleda MY, Boyd PW, Hurd CL (2012a) Before ocean acidification: calcifier chemistry lessons. J Phycol 48:840–843
Roleda MY, Morris JN, McGraw CM, Hurd CL (2012b) Ocean acidification and seaweed reproduction: increased CO2 ameliorates the negative effect of lowered pH on meiospore germination in the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae). Glob Chang Biol 18:854–864
Rönnbäck P, Kautsky N, Pihl L, Troell M, Söderqvist T, Wennhage H (2007) Ecosystem goods and services from Swedish coastal habitats: identification, valuation, and implications of ecosystem shifts. Ambio 36:534–544
Rothaüsler E, Gomez I, Karsten U, Tala F, Thiel M (2011) Physiological acclimation of floating Macrocystis pyrifera to temperature and irradiance ensures long-term persistence at the sea surface at mid-latitudes. J Exp Mar Biol Ecol 405:33–41
Ruhland CT, Fogal MJ, Buyarski CR, Krna MA (2007) Solar ultraviolet-B radiation increases phenolic content and ferric reducing antioxidant power in Avena sativa. Molecules 12:1220–1232
Russell BD, Thompson JI, Falkenberg LJ, Connell SD (2009) Synergistic effects of climate change and local stressors: CO2 and nutrient-driven change in subtidal rocky habitats. Glob Chang Biol 15:2153–2162
Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DWR, Tilbrook B, Millero FJ, Peng TH, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371
Schmidt EC, Nunes BG, Maraschin M, Bouzon ZL (2010) Effect of ultraviolet-B radiation on growth, photosynthetic pigments, and cell biology of Kappaphycus alvarezii (Rhodophyta, Gigartinales) macroalgae brown strain. Photosynthetica 48:161–172
Schmidt EC, Pereira B, dos Santos RW, Gouveia C, Costa GB, Faria GSM, Scherner F, Horta PA, Martins RDP, Latini A, Ramlov F, Maraschin M, Bouzon ZL (2012) Responses of the macroalgae Hypnea musciformis after in vitro exposure to UV-B. Aquat Bot 100:8–17
Staehr PA, Wernberg T (2009) Physiological responses of Ecklonia radiata (Laminariales) to a latitudinal gradient in ocean temperature. J Phycol 45:91–99
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 24:840–823
Van de Poll WH, Eggert A, Buma AGJ, Breeman AM (2001) Effects of UV-B induced DNA damage and photoinhibition on growth of temperate marine red macrophytes: habitat-related differences in UV-B tolerance. J Phycol 37:30–38
van de Poll WH, Eggert A, Buma AGJ, Breeman AM (2002) Temperature dependence of UV radiation effects in Arctic and temperate isolates of three red macrophytes. Eur J Phycol 37:59–68
Van den Hoek C, Breeman AM, Stam WT (1990) The geographic distribution of seaweeds species in relation to temperature: present and past. In: Beukema JJ (ed) Expected effects of climatic change on marine coastal ecosystems. Kluwer, Dordrecht, pp 55–67
Vass I (1997) Adverse effects of UV-B light on the structure and function of the photosynthetic apparatus. In: Handbook of photosynthesis. Marcel Dekker Inc., New York, pp 931–949
Wahl M, Molis M, Davis A, Dobretsov S, Dürr S, Johansson J, Kinley J, Kirugara D, Langer M, Lotze HK, Thiel M, Thomason JC, Worm B, Ben-Yosef DZ (2004) UV effects that come and go: a global comparison of marine benthic community level impacts. Glob Chang Biol 10:1962–1972
Weatherhead EC, Andersen SB (2006) The search for signs of recovery of the ozone layer. Nature 441:39–45
Wernberg T, Kendrick GA, Phillips JC (2003) Regional differences in kelp-associated algal assemblages on temperate limestone reefs in south-western Australia. Divers Distrib 9:427–441
Wernberg T, Thomsen MS, Tuya F, Kendrick GA, Staehr PA, Toohey BD (2010) Decreasing resilience of kelp beds along a latitudinal temperature gradient: potential implications for a warmer future. Ecol Lett 13:685–694
Wernberg T, Russell BD, Thomsen MS, Gurgel CF, Bradshaw CJ, Poloczanska ES, Connell SD (2011) Seaweed communities in retreat from ocean warming. Curr Biol 21:1828–1832
Williams SL, Dethier MN (2005) High and dry: variation in net photosynthesis of the intertidal seaweed Fucus gardneri. Ecology 86:2373–2379
Wood WF (1989) Photoadaptive responses of the tropical red alga Eucheuma striatum Schmitz (Gigartinales) to ultra-violet radiation. Aquat Bot 33:41–51
Xia JR, Gao KS (2005) Impacts of elevated CO2 concentration on biochemical composition, carbonic anhydrase, and nitrate reductase activity of freshwater green algae. J Integr Plant Biol 47:668–675
Xu JT, Gao KS (2010a) Use of UV-A energy for photosynthesis in the red macroalga Gracilaria lemaneiformis. Photochem Photobiol 86:580–585
Xu JT, Gao KS (2010b) UV-A enhanced growth and UV-B induced positive effects in the recovery of photochemical yield in Gracilaria lemaneiformis (Rhodophyta). J Photochem Photobiol B 100:117–122
Xu JT, Gao KS (2012) Future CO2-induced ocean acidification mediates the physiological performance of a green tide alga. Plant Physiol 160:1762–1769
Xu ZG, Gao KS (2009) Impacts of UV radiation on growth and photosynthetic carbon acquisition in Gracilaria lemaneiformis (Rhodophyta) under phosphorus-limited and replete conditions. Funct Plant Biol 36:1057–1064
Zheng YQ, Gao KS (2009) Impacts of solar UV radiation on the photosynthesis, growth and UV-absorbing compounds in Gracilaria lemaneiformis (Rhodophyta) grown at different nitrate concentrations. J Phycol 45:314–323
Zou DH, Gao KS (2002a) Effects of desiccation and CO2 concentrations on emersed photosynthesis in Porphyra haitanensis (Bangiales, Rhodophyta), a species farmed in China. Eur J Phycol 37:587–592
Zou DH, Gao KS (2002b) Photosynthetic bicarbonate utilization in Porphyra haitanensis (Bangiales, Rhodophyta). Chin Sci Bull 47:1629–1633
Zou DH, Gao KS (2002c) Photosynthetic responses to inorganic carbon in Ulva lactuca under aquatic and aerial states. Acta Bot Sinica 44:1291–1296
Zou DH, Gao KS (2005) Ecophysiological characteristics of four intertidal marine macroalgae during emersion along Shantou coast of China, with a special reference to the relationship of photosynthesis and CO2. Acta Oceanol Sinica 24:105–113
Zou DH, Gao KS (2009) Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) grown at different irradiance levels. Phycologia 48:510–517
Zou DH, Gao KS (2010) Acquisition of inorganic carbon by Endarachne binghamiae (Scytosiphonales, Phaeophyceae). Eur J Phycol 45:119–128
Zou DH, Gao KS (2013) Thermal acclimation of respiration and photosynthesis in the marine macroalga Gracilaria lemaneiformia (Gracilariales, Rhodophyta). J Phycol 49:61–68
Zou DH, Gao KS (2014a) Temperature response of the photosynthetic light- and carbon-use characteristics in the red seaweed Gracilaria lemaneiformis (Gracilariales, Rhodophyta). J Phycol 50:366–375
Zou DH, Gao KS (2014b) The photosynthetic and respiratory responses to temperature and nitrogen supply in the marine green macroalga Ulva conglobata (Chlorophyta). Phycologia 53:86–94
Zou DH, Gao KS, Xia JR (2003) Photosynthetic utilization of inorganic carbon in the economic brown alga, Hizikia fusiforme (Sargassaceae) from the South China Sea. J Phycol 39:1095–1100
Zou DH, Gao KS, Ruan ZX (2007) Daily timing of emersion and elevated atmospheric CO2 concentration affect photosynthetic performance of the intertidal macroalga Ulva lactuca (Chorophyta) in sunlight. Bot Mar 50:275–279
Zou DH, Gao KS, Luo HJ (2011a) Short- and long-term effects of elevated CO2 on photosynthesis and respiration in the marine macroalga Hizikia fusiformis (Sargassaceae, Phaeophyta) grown at low and high N supplies. J Phycol 47:87–97
Zou DH, Gao KS, Xia JR (2011b) Dark respiration in the light and in darkness of three marine macroalgal species grown under ambient and elevated CO2 concentrations. Acta Oceanol Sinica 30:1–7
Acknowledgments
This study was supported by National Natural Science Foundation (NSFC, no. 41430967, 41120164007, and 41376129), State Oceanic Administration (National Programme on Global Change and Air-Sea Interaction, GASI-03-01-02-04), joint project of the National Natural Science Foundation of China and Shandong province (no. U1406403), and Strategic Priority Research Program of Chinese Academy of Sciences (no. XDA1102030204).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ji, Y., Xu, Z., Zou, D. et al. Ecophysiological responses of marine macroalgae to climate change factors. J Appl Phycol 28, 2953–2967 (2016). https://doi.org/10.1007/s10811-016-0840-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-016-0840-5