Skip to main content

Advertisement

SpringerLink
Log in

Ecophysiological responses to elevated CO2 and temperature in Cystoseira tamariscifolia (Phaeophyceae)

  • Published:
Climatic Change Aims and scope Submit manuscript

Abstract

Ocean acidification increases the amount of dissolved inorganic carbon (DIC) available in seawater which can benefit photosynthesis in those algae that are currently carbon limited, leading to shifts in the structure and function of seaweed communities. Recent studies have shown that ocean acidification-driven shifts in seaweed community dominance will depend on interactions with other factors such as light and nutrients. The study of interactive effects of ocean acidification and warming can help elucidate the likely effects of climate change on marine primary producers. In this study, we investigated the ecophysiological responses of Cystoseira tamariscifolia (Hudson) Papenfuss. This large brown macroalga plays an important structural role in coastal Mediterranean communities. Algae were collected from both oligotrophic and ultraoligotrophic waters in southern Spain. They were then incubated in tanks at ambient (ca. 400–500 ppm) and high CO2 (ca. 1200–1300 ppm), and at 20 °C (ambient temperature) and 24 °C (ambient temperature +4 °C). Increased CO2 levels benefited the algae from both origins. Biomass increased in elevated CO2 treatments and was similar in algae from both origins. The maximal electron transport rate (ETRmax), used to estimate photosynthetic capacity, increased in ambient temperature/high CO2 treatments. The highest polyphenol content and antioxidant activity were observed in ambient temperature/high CO2 conditions in algae from both origins; phenol content was higher in algae from ultraoligotrophic waters (1.5–3.0%) than that from oligotrophic waters (1.0–2.2%). Our study shows that ongoing ocean acidification can be expected to increase algal productivity (ETRmax), boost antioxidant activity (EC 50 ), and increase production of photoprotective phenols. Cystoseira tamariscifolia collected from oligotrophic and ultraoligotrophic waters were able to benefit from increases in DIC at ambient temperatures. Warming, not acidification, may be the key stressor for this habitat as CO2 levels continue to rise.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

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

    Article  Google Scholar 

  • Arnold TM, Targett NM (2002) Marine tannins: the importance of a mechanistic framework for predicting ecological roles. J Chem Ecol 28(10):1919–1934

    Article  Google Scholar 

  • Arnold T, Mealey LH, 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

    Article  Google Scholar 

  • Baggini C, Salomidi M, Voutsinas E, Bray L, Krasakopoulou E, Hall-Spencer JM (2014) Seasonality affects macroalgal community response to increases in pCO2. PLoS One 9(9):e106520

    Article  Google Scholar 

  • Bender D, Diaz-Pulido G, Dove S (2014) The impact of CO2 emission scenarios and nutrient enrichment on a common coral reef macroalga is modified by temporal effects. J Phycol 50:203–215

    Article  Google Scholar 

  • Betancor S, Tuya F, Gil-Díaz T, Figueroa FL, Hoaroun R (2014) Effects of a submarine eruption on the performance of two brown seaweeds. J Sea Res 87:68–78

    Article  Google Scholar 

  • Blois MS (1958) Antioxidant determinations by the use of a stable free radical. Nature 181:1199–1200

    Article  Google Scholar 

  • Brodie J, Williamson C, Smale DA, Kamenos NA, Mieszkowska N, Santos R, Cunliffe M, Steinke M, Yesson C, Anderson KM, Asnaghi V, Brownlee C, Burdett HL, Burrows MT, Collins S, Donohue PCJ, Harvey B, Foggo A, Noisette F, Nunes J, Ragazzola F, Raven JA, Schmidt DN, Suggett D, Teichberg M, Hall-Spencer JM (2014) The future of the Northeast Atlantic benthic flora in a high CO2 world. Ecol Evol 4(13):2787–2798

    Article  Google Scholar 

  • Celis-Plá PSM, Hall-Spencer JM, Horta PA, Milazzo M, Korbee N, Cornwall CE, Figueroa FL (2015) Macroalgal responses to ocean acidification depend on nutrient and light levels. Front Mar Sci 2:26

    Article  Google Scholar 

  • Celis-Plá PSM, Bouzon ZL, Hall-Spencer JM, Schmidt EC, Korbee N, Figueroa FL (2016) Seasonal changes in photoprotectors and antioxidant capacity of the fucoid macroalga Cystoseira tamariscifolia. Mar Environ Res 115:89–97

    Article  Google Scholar 

  • Coll M, Piroddi C, Steenbeek J, Kaschner K, Ben Rais Lasram F (2010) The biodiversity of the Mediterranean Sea: estimates, Pattterns, and Theats. PLoS One 5(8):e11821371

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Eilers PHC, Peeters JCH (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol Model 42:199–215

    Article  Google Scholar 

  • Figueroa FL, Gómez I (2001) Photoacclimation to solar UV radiation in red macroalgae. J Appl Phycol 13:235–248

    Article  Google Scholar 

  • Figueroa FL, Korbee N (2010) Interactive effects of UV radiation and nutrients on ecophysiology: vulnerability and adaptation to climate change. In: Israel A, Einvav R, Seckbach J (eds) Seaweeds and their role in globally changing environments. Springer-Verlag, Berlin Heidelberg, pp 157–182

    Chapter  Google Scholar 

  • Figueroa FL, Domínguez-González B, Korbee N (2014) Vulnerability and acclimation to increased UVB in the three intertidal macroalgae of different morpho-functional groups. Mar Environ Res 101:8–21

    Article  Google Scholar 

  • Gómez-Garreta A, Barceló-Marti M, Gallardo T, Pérez-Ruzafa IM, Ribera MA, Rull J (2001) Flora Phycologica Ibérica. Fucales. Vol. 1. Universidad de Murcia, España

    Google Scholar 

  • Grzymski J, Johnsen G, Sakshug E (1997) The signiwcance of intracellular self-shading on the bio-optical properties of brown, red and green macroalgae. J Phycol 33:408–414

    Article  Google Scholar 

  • Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia MC (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99

    Article  Google Scholar 

  • Hanelt D, Figueroa FL (2012) Physiological and photomorphogenic effects of light of marine macrophytes. In: Wienke C, Bischof K (eds) Seaweed biology ecological studies. Springer-Verlag, Berlin Heidelberg, pp 3–23

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hofmann LC, Bischof K, Baggini C, Johnson A, Koop-Jakobsen K, Teichberg M (2015) CO2 and inorganic nutrient enrichment affect the performance of a calcifying green alga and its noncalcifying epiphyte. Oecologia 177:1157–1169

    Article  Google Scholar 

  • Høiskar BAK, Haugen R, Danielsen T, Kylling A, Edvardsen K, Dahlback A, Johnsen B, Blumthaler M, Schreder J (2003) Multichannel moderate-bandwidth filter instrument for measurement the ozone-column amount, cloud transmittance, and ultraviolet dose rates. Appl Opt 42:18–20

    Article  Google Scholar 

  • IPCC (2014) The physical science basis. Working group I contribution to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  • Johnson VR, Russell BD, Fabricius KE, Brownlee C, Hall-Spencer JM (2012) Temperate and tropical brown macroalgae thrive, despite decalcification, along natural CO2 gradients. Glob Chang Biol 18:2792–2803

    Article  Google Scholar 

  • Ju-Hyoung K, Kang EJ, Edwards MS, Lee K, Jeong HJ, Kim KY (2016) Species-specific responses of temperate macroalgae with different photosynthetic strategies to ocean acidification: a mesocosm study. Algae 31(3):243–256

    Article  Google Scholar 

  • Koroleff F (1983) Determination of phosphorus. In: Grasshoff K, Ehrhardt M, Kremling K (eds) Methods of seawater analysis: second, revised and extended edition. Weinheim, Verlag Chemie, pp 125–139

    Google Scholar 

  • Linares C, Vidal M, Canals M, Kersting DK, Amblas D, Aspillaga E, Cebrián E, Delgado-Huertas A, Díaz D, Garrabou J, Hereu B, Navarro L, Teixidó N, Ballesteros E (2015) Persistent natural acidification drives major distribution shifts in marine benthic ecosystems. Proc R Soc B 282:20150587

    Article  Google Scholar 

  • Martin S, Gattuso P (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Change Biol 15:2089–2100

    Article  Google Scholar 

  • Martínez B, Arenas F, Trilla A, Viejo RM, Carreño F (2015) Combining physiological threshold knowledge to species distribution models is key to improving forecasts of the future niche for macroalgae. Glob Change Biol 21(4):1422–1433

    Article  Google Scholar 

  • Mercado JM, Cortés D, García A, Ramírez T (2007) Seasonal and inter-annual changes in the planktonic communities of the northwest Alboran Sea (Mediterranean Sea). Prog Oceanogr 74:273–293

    Article  Google Scholar 

  • Mercado J, Cortés D, Ramírez T, Gómez F (2012) Decadal weakening of the wind-induced upwelling reduces the impact of nutrient pollution in the bay of Málaga (western Mediterranean Sea). Hydrobiologia 680:91–107

    Article  Google Scholar 

  • Newcomb LA, Milazzo M, Hall-Spencer JM, Carrington E (2015) Ocean acidification bends the mermaid’s wineglass. Biol Lett 11:20141075

    Article  Google Scholar 

  • Organization for Economic Cooperation and Development (1982) Eutrophisation des euax. Métodes de surveillance, d’evaluation et de lutte. Paris

  • Pérez-lloréns JL, Vergara JJ, Olivé I, Mercado JM, Conde-Álvarez R (2014) Autochthonous seagrasses. In: Goffredo S, Dubinsky Z (eds) The Mediterranean Sea: its history and present challenges. Springer Netherlands, Dordrecht, pp 137–158

    Chapter  Google Scholar 

  • Pérez-Rodríguez E (2000) Bióptica de aguas oceánicas y costeras. Fotosíntesis, fotoinhibición y fotoprotección en algas a la radiación solar. Doctoral Thesis. Málaga University

  • Ramírez T, Cortés D, Mercado JM, Vargas-Yáñez M, Sebastián M, Liger E (2005) Seasonal dynamics of inorganic nutrients and phytoplankton biomass in the NW Alboran Sea. Estuar Coast Shelf S 65:654–670

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Roleda MY, Morris JN, McGraw CM, Hurd CL (2012) 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 Change Biol 18:854–864

    Article  Google Scholar 

  • Russell BD, Pasasrelli CA, Connell SD (2011) Forecasted CO2 modifies the influence of light in shaping subtidal habitat. J Phycol 47:744–752

    Article  Google Scholar 

  • Schoenwaelder MEA (2008) The biology of phenolic containing vesicles. Algae 23:163–175

    Article  Google Scholar 

  • Schreiber U, Endo T, Mi H, Asada K (1995) Quenching analysis of chlorophyll fluorescence by saturation pulse method: particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant Cell Physiol 36:873–882

    Article  Google Scholar 

  • Stengel D, Conde-Álvarez R, Connan S, Nitschke U, Arenas F, Abreu H, Bonomi Barufi J, Chow F, Robledo D, Malta EJ, Mata M, Konotchick T, Nassar C, Pérez-Ruzafa A, 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, nutrient and temperature impacts on three marine macroalgae under solar radiation. Aquat Biol 22:159–176

    Article  Google Scholar 

  • Strain EMA, Thomson RJ, Micheli F, Mancuso FP, Airoldi L (2014) Identifying the interacting roles of stressors in driving the global loss of canopy-forming to mat- forming algae in marine ecosystems. Glob Change Biol 20(11):3300–3312

    Article  Google Scholar 

  • Swanson AK, Fox CH (2007) Altered kelp (Laminariales) phlorotannins and growth under elevated carbon dioxide and ultraviolet-B treatments can influence associated intertidal food webs. Glob Change Biol 13:1696–1709

    Article  Google Scholar 

  • Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge, New York, 509 pp

  • Wernberg T, Bennett S, Babcock RC, de Bettignies T, Cure K, Depczynski M, Dufois F, Fromont J, Fulton CJ, Hovey RK, Harvey ES, Holmes TH, Kendrick GA, Radford B, Santana-Garcon J, Saunders BJ, Smale DA, Thomsen MS, Tuckett CA, Tuya F, Vanderklift MA, Wilson S (2016) Climate-driven regime shift of a temperate marine ecosystem. Science 353(6295):169–172

    Article  Google Scholar 

  • Zou D, Gao K (2009) Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) grown at different irradiance levels. Phycologia 48(6):510–517

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Junta de Andalucía (Project RNM-5750), by the research group RNM-295, and by the University of Málaga: Programa de Fortalecimiento de Las capacidades de I + D + I en Las universidades 2014-2015, Consejería de Economía, Innovación, Ciencia y Empleo, cofinanciado por el FEDER (Project FC-14CGL-09). Paula S. M. Celis-Plá gratefully acknowledges financial support from “Becas-Chile” (CONICYT) of the Ministry of Education, Republic of Chile, and technical support of David Lopez (University of Malaga).

Author information

Authors and Affiliations

  1. Laboratory of Coastal Environmental Research, Centre of Advanced Studies, University of Playa Ancha, Traslaviña 450, 2581782, Viña del Mar, Chile

    Paula S. M. Celis-Plá

  2. Department of Ecology, Faculty of Sciences, University of Malaga, 29071, Malaga, Spain

    Paula S. M. Celis-Plá, Nathalie Korbee & Félix L. Figueroa

  3. Biodiversity and Conservation Unit, Rey Juan Carlos University, 28933, Mostoles, Spain

    Brezo Martínez

  4. Marine Biology and Ecology Research Centre, University of Plymouth, Plymouth, PL4 8AA, UK

    Jason M. Hall-Spencer

  5. Shimoda Marine Research Centre, Tsukuba University, Tsukuba, Japan

    Jason M. Hall-Spencer

Authors
  1. Paula S. M. Celis-Plá
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brezo Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nathalie Korbee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jason M. Hall-Spencer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Félix L. Figueroa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paula S. M. Celis-Plá.

Electronic supplementary material

Table S1

(DOCX 13 kb)

Table S2

(DOCX 11 kb)

Table S3

(DOCX 15 kb)

Table S4

(DOCX 14 kb)

Table S5

(DOCX 12 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Celis-Plá, P.S.M., Martínez, B., Korbee, N. et al. Ecophysiological responses to elevated CO2 and temperature in Cystoseira tamariscifolia (Phaeophyceae). Climatic Change 142, 67–81 (2017). https://doi.org/10.1007/s10584-017-1943-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10584-017-1943-y

Keywords

Search

Navigation