Skip to main content

Advertisement

SpringerLink
Log in

Short-term interactive effects of ultraviolet radiation, carbon dioxide and nutrient enrichment on phytoplankton in a shallow coastal lagoon

  • Published:
Aquatic Ecology Aims and scope Submit manuscript

Abstract

The main goal of this study was to evaluate short-term interactions between increased CO2, UVR and inorganic macronutrients (N, P and Si) on summer phytoplankton assemblages in the Ria Formosa coastal lagoon (SW Iberia), subjected to intense anthropogenic pressures and highly vulnerable to climate change. A multifactorial experiment using 20 different nutrient-enriched microcosms exposed to different spectral and CO2 conditions was designed. Before and after a 24-h in situ incubation, phytoplankton abundance and composition were analysed. Impacts and interactive effects of high CO2, UVR and nutrients varied among different functional groups. Increased UVR had negative effects on diatoms and cyanobacteria and positive effects on cryptophytes, whereas increased CO2 inhibited cyanobacteria but increased cryptophyte growth. A positive synergistic interaction between CO2 and UVR was observed for diatoms; high CO2 counteracted the negative effects of UVR under ambient nutrient concentrations. Nutrient enrichments suppressed the negative effects of high CO2 and UVR on cyanobacteria and diatoms, respectively. Beneficial effects of CO2 were observed for diatoms and cryptophytes under combined additions of nitrate and ammonium, suggesting that growth may be limited by DIC availability when the primary limitation by nitrogen is alleviated. Beneficial effects of high CO2 and UVR in diatoms were also induced or intensified by ammonium additions.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Andrade C, Freitas MC, Moreno J, Craveiro SC (2004) Stratigraphical evidence of Late Holocene barrier breaching and extreme storms in lagoonal sediments of Ria Formosa. Mar Geol 210:339–362

    Article  Google Scholar 

  • Badger MR, Price GD, Long BM, Woodger FJ (2006) The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. J Exp Bot 57:249–265. doi:10.1093/jxb/eri286

    Article  CAS  PubMed  Google Scholar 

  • Banaszak AT, Neale PJ (2001) UV sensitivity of photosynthesis in phytoplankton from an estuarine environment. Limnol Oceanogr 46:592–600

    Article  Google Scholar 

  • Barbosa AB (2006) Estrutura e dinâmica da teia alimentar microbiana na Ria Formosa (Structure and dynamics of the microbial food web in the Ria Formosa). Ph.D. Thesis. University of Algarve, 518 p

  • Barbosa AB (2010) Seasonal and interannual variability of planktonic microbes in a mesotidal coastal lagoon (Ria Formosa, SE Portugal). Impact of climatic changes and local human influences. In: Kennish MJ, Paerl HW (eds) Coastal lagoons: critical habitats of environmental change. CRC Press, Boca Raton, pp 334–366

    Google Scholar 

  • Beardall J, Sobrino C, Stojkovic S (2009a) Interactions between the impacts of ultraviolet radiation, elevated CO2, and nutrient limitation on marine primary producers. Photochem Photobiol Sci 8:1257–1265. doi:10.1039/b9pp00034h

    Article  CAS  PubMed  Google Scholar 

  • Beardall J, Stojkovic S, Larsen S (2009b) Living in a high CO2 world: impacts of global climate change on marine phytoplankton. Plant Ecol Divers 2:191–205. doi:10.1080/17550870903271363

    Article  Google Scholar 

  • Berge T, Daugbjerg N, Andersen B, Hansen P (2010) Effect of lowered pH on marine phytoplankton growth rates. Mar Ecol Prog Ser 416:79–91

    Article  Google Scholar 

  • Bouvy M, Bettarel Y, Bouvier C et al (2011) Trophic interactions between viruses, bacteria and nanoflagellates under various nutrient conditions and simulated climate change. Environ Microbiol 13:1842–1857. doi:10.1111/j.1462-2920.2011.02498.x

    Article  CAS  PubMed  Google Scholar 

  • Boyd P, Hutchins D (2012) Understanding the responses of ocean biota to a complex matrix of cumulative anthropogenic change. Mar Ecol Prog Ser 470:125–135. doi:10.3354/meps10121

    Article  Google Scholar 

  • Carrillo P, Delgado-Molina JA, Medina-Sánchez JM et al (2008) Phosphorus inputs unmask negative effects of ultraviolet radiation on algae in a high mountain lake. Glob Chang Biol 14:423–439. doi:10.1111/j.1365-2486.2007.01496.x

    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. doi:10.1007/s10750-011-0807-0

    Article  CAS  Google Scholar 

  • Collins S (2011) Many possible worlds: expanding the ecological scenarios in experimental evolution. Evol Biol 38:3–14. doi:10.1007/s11692-010-9106-3

    Article  Google Scholar 

  • Collins S, Rost B, Rynearson TA (2014) Evolutionary potential of marine phytoplankton under ocean acidification. Evol Appl 7:140–155. doi:10.1111/eva.12120

    Article  CAS  PubMed  Google Scholar 

  • Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315. doi:10.1111/j.1461-0248.2008.01253.x

    Article  PubMed  Google Scholar 

  • Cravo A, Cardeira S, Pereira C et al (2014) Exchanges of nutrients and chlorophyll a through two inlets of Ria Formosa, South of Portugal, during coastal upwelling events. J Sea Res 93:63–74. doi:10.1016/j.seares.2014.04.004

    Article  Google Scholar 

  • Domingues RB, Barbosa A, Galvão H (2008) Constraints on the use of phytoplankton as a biological quality element within the Water Framework Directive in Portuguese waters. Mar Pollut Bull 56:1389–1395. doi:10.1016/j.marpolbul.2008.05.006

    Article  CAS  PubMed  Google Scholar 

  • Domingues RB, Guerra CC, Barbosa AB et al (2014) Effects of ultraviolet radiation and CO2 increase on winter phytoplankton assemblages in a temperate coastal lagoon. J Plankton Res 36:672–684. doi:10.1093/plankt/fbt135

    Article  CAS  Google Scholar 

  • Domingues RB, Guerra CC, Barbosa AB, Galvão HM (2015) Are nutrients and light limiting summer phytoplankton in a temperate coastal lagoon? Aquat Ecol 49:127–146. doi:10.1007/s10452-015-9512-9

    Article  CAS  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. doi:10.4319/lo.2005.50.5.1362

    Article  CAS  Google Scholar 

  • Dytham C (2003) Choosing and using statistics: a biologist’s guide, 2nd edn. Blackwell, Oxford

    Google Scholar 

  • Endo H, Yoshimura T, Kataoka T, Suzuki K (2013) Effects of CO2 and iron availability on phytoplankton and eubacterial community compositions in the northwest subarctic Pacific. J Exp Mar Bio Ecol 439:160–175. doi:10.1016/j.jembe.2012.11.003

    Article  CAS  Google Scholar 

  • Feng Y, Hare CE, Rose JM et al (2010) Interactive effects of iron, irradiance and CO2 on Ross Sea phytoplankton. Deep Res Part I Oceanogr Res Pap 57:368–383. doi:10.1016/j.dsr.2009.10.013

    Article  CAS  Google Scholar 

  • Fu F-X, Warner ME, Zhang Y et al (2007) Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (cyanobacteria). J Phycol 43:485–496. doi:10.1111/j.1529-8817.2007.00355.x

    Article  Google Scholar 

  • Fu F, Mulholland MR, Garcia NS et al (2008) Interactions between changing pCO2, N2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera. Limnol Oceanogr 53:2472–2484

    Article  CAS  Google Scholar 

  • Fu FX, Place AR, Garcia NS, Hutchins DA (2010) CO2 and phosphate availability control the toxicity of the harmful bloom dinoflagellate Karlodinium veneficum. Aquat Microb Ecol 59:55–65. doi:10.3354/ame01396

    Article  Google Scholar 

  • Gao K, Campbell DA (2014) Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: a review. Funct Plant Biol 41:449–459. doi:10.1071/FP13247

    Article  CAS  Google Scholar 

  • Gao K, Wu Y, Li G et al (2007) Solar UV radiation drives CO2 fixation in marine phytoplankton: a double-edged sword. Plant Physiol 144:54–59. doi:10.1104/pp.107.098491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao K, Ruan Z, Villafañe VE et al (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, Helbling E, Häder D-P, Hutchins D (2012a) Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Mar Ecol Prog Ser 470:167–189. doi:10.3354/meps10043

    Article  CAS  Google Scholar 

  • Gao K, Xu J, Gao G et al (2012b) Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nat Clim Chang 2:1–5. doi:10.1038/nclimate1507

    Article  Google Scholar 

  • García-Gómez C, Gordillo FJL, Palma A et al (2014) Elevated CO2 alleviates high PAR and UV stress in the unicellular chlorophyte Dunaliella tertiolecta. Photochem Photobiol Sci 13:1347. doi:10.1039/C4PP00044G

    Article  PubMed  Google Scholar 

  • Garcia-Pichel F (1994) A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnol Oceanogr 39:1704–1717. doi:10.4319/lo.1994.39.7.1704

    Article  Google Scholar 

  • Gattuso J-P, Gao K, Lee K, et al (2010) Approaches and tools to manipulate the carbonate chemistry. In: Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (eds) Guide to best practices ocean acidification research. Data Report. Publications Office of the European Union, pp 41–52

  • Gerber S, Häder DP (1995) Effects of enhanced solar irradiation on chlorophyll fluorescence and photosynthetic oxygen production of 5 species of phytoplankton. FEMS Microbiol Ecol 16:33–41

    Article  CAS  Google Scholar 

  • Grasshoff K, Ehrhardt M, Kremling K (1983) Methods of seawater analysis. Verlag Chemie, Weinheim

    Google Scholar 

  • Haas LW (1982) Improved epifluorescence microscopy for observing planktonic micro-organisms. Ann l’Institut Oceanogr 58:261–266

    Google Scholar 

  • Heraud P, Roberts S, Shelly K, Beardall J (2005) Interactions between UV-B exposure and phosphorus nutrition. II. Effects on rates of damage and repair. J Phycol 41:1212–1218. doi:10.1111/j.1529-8817.2005.00149.x

    Article  CAS  Google Scholar 

  • Hutchins DA, Fu F-X, Zhang Y et al (2007) CO2 control of trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: implications for past, present, and future ocean biogeochemistry. Limnol Oceanogr 52:1293–1304. doi:10.4319/lo.2007.52.4.1293

    Article  CAS  Google Scholar 

  • Ingalls AE, Whitehead K, Bridoux MC (2010) Tinted windows: the presence of the UV absorbing compounds called mycosporine-like amino acids embedded in the frustules of marine diatoms. Geochem Cosmochim Acta 74:104–115

    Article  CAS  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. IPCC, Geneva

    Google Scholar 

  • Li G, Campbell DA (2013) Rising CO2 interacts with growth light and growth rate to alter photosystem II photoinactivation of the coastal diatom Thalassiosira pseudonana. PLoS ONE 8:e55562. doi:10.1371/journal.pone.0055562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li G, Gao K (2014) Effects of solar UV radiation on photosynthetic performance of the diatom Skeletonema costatum grown under nitrate limited condition. Algae 29:27–34

    Article  Google Scholar 

  • Li Y, Gao K, Villafañe VE, Helbling EW (2012) Ocean acidification mediates photosynthetic response to UV radiation and temperature increase in the diatom Phaeodactylum tricornutum. Biogeosci Discuss 9:7197–7226. doi:10.5194/bgd-9-7197-2012

    Article  Google Scholar 

  • Litchman E, Neale PJ, Banaszak AT (2002) Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: photoprotection and repair. Limnol Oceanogr 47:86–94. doi:10.4319/lo.2002.47.1.0086

    Article  CAS  Google Scholar 

  • Litchman E, Edwards K, Klausmeier C, Thomas M (2012) Phytoplankton niches, traits and eco-evolutionary responses to global environmental change. Mar Ecol Prog Ser 470:235–248. doi:10.3354/meps09912

    Article  Google Scholar 

  • Llabrés M, Agustí S, Alonso-Laita P, Herndl G (2010) Synechococcus and Prochlorococcus cell death induced by UV radiation and the penetration of lethal UVR in the Mediterranean Sea. Mar Ecol Prog Ser 399:27–37. doi:10.3354/meps08332

    Article  Google Scholar 

  • Lohbeck KT, Riebesell U, Reusch TBH (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci 5:346–351. doi:10.1038/ngeo1441

    Article  CAS  Google Scholar 

  • Loureiro S, Newton A, Icely J (2005) Effects of nutrient enrichments on primary production in the Ria Formosa coastal lagoon (Southern Portugal). Hydrobiologia 550:29–45. doi:10.1007/s10750-005-4357-1

    Article  CAS  Google Scholar 

  • Machado LM (2010) A radiação UV-B na Ria Formosa: incidência e impactes biológicos. University of Algarve, Faro

    Google Scholar 

  • Medina-Sánchez JM, Villar-Argaiz M, Carrillo P (2006) Solar radiation-nutrient interaction enhances the resource and predation algal control on bacterioplankton: a short-term experimental study. Limnol Oceanogr 51:913–924. doi:10.4319/lo.2006.51.2.0913

    Article  Google Scholar 

  • Neale PJ, Cullen JJ, Davis RF (1998) Inhibition of marine photosynthesis by ultraviolet radiation: variable sensitivity of phytoplankton in the Wedell-Scotia Confluence during the austral spring. Limnol Oceanogr 43:433–448

    Article  CAS  Google Scholar 

  • Neale P, Sobrino C, Segovia M et al (2014) Effect of CO2, nutrients and light on coastal plankton. I. Abiotic conditions and biological responses. Aquat Biol 22:25–41. doi:10.3354/ab00587

    Article  Google Scholar 

  • Newton A, Mudge SM (2003) Temperature and salinity regimes in a shallow, mesotidal lagoon, the Ria Formosa, Portugal. Estuar Coast Shelf Sci 57:73–85. doi:10.1016/S0272-7714(02)00332-3

    Article  CAS  Google Scholar 

  • Newton A, Icely JD, Falcao M et al (2003) Evaluation of eutrophication in the Ria Formosa coastal lagoon, Portugal. Cont Shelf Res 23:1945–1961. doi:10.1016/j.csr.2003.06.008

    Article  Google Scholar 

  • Nielsen LT, Jakobsen HH, Hansen PJ (2010) High resilience of two coastal plankton communities to twenty-first century seawater acidification: evidence from microcosm studies. Mar Biol Res 6:542–555. doi:10.1080/17451000903476941

    Article  Google Scholar 

  • Nielsen L, Hallegraeff G, Wright S, Hansen P (2012) Effects of experimental seawater acidification on an estuarine plankton community. Aquat Microb Ecol 65:271–286. doi:10.3354/ame01554

    Article  Google Scholar 

  • Nogueira P, Domingues RB, Barbosa AB (2014) Are microcosm volume and sample pre-filtration relevant to evaluate phytoplankton growth? J Exp Mar Bio Ecol 461:323–330. doi:10.1016/j.jembe.2014.09.006

    Article  Google Scholar 

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

    Google Scholar 

  • Paulino AI, Egge JK, Larsen A (2008) Effects of increased atmospheric CO2 on small and intermediate sized osmotrophs during a nutrient induced phytoplankton bloom. Biogeosciences 5:739–748. doi:10.5194/bg-5-739-2008

    Article  CAS  Google Scholar 

  • Piggott JJ, Townsend CR, Matthaei CD (2015) Reconceptualizing synergism and antagonism among multiple stressors. Ecol Evol 5:1538–1547. doi:10.1002/ece3.1465

    Article  PubMed  PubMed Central  Google Scholar 

  • Rastogi RP, Sinha RP, Moh SH et al (2014) Ultraviolet radiation and cyanobacteria. J Photochem Photobiol B Biol 141:154–169. doi:10.1016/j.jphotobiol.2014.09.020

    Article  CAS  Google Scholar 

  • Reul A, Muñoz M, Bautista B et al (2014) Effect of CO2, nutrients and light on coastal plankton. III. Trophic cascade, size structure and composition. Aquat Biol 22:59–76. doi:10.3354/ab00585

    Article  Google Scholar 

  • Reusch TBH, Boyd PW (2013) Experimental evolution meets marine phytoplankton. Evolution (NY) 67:1849–1859. doi:10.1111/evo.12035

    Article  Google Scholar 

  • Sala MM, Aparicio FL, Balagué V et al (2015) Contrasting effects of ocean acidification on the microbial food web under different trophic conditions. ICES J. Mar, Sci

    Google Scholar 

  • Schlüter L, Lohbeck KT, Gutowska MA et al (2014) Adaptation of a globally important coccolithophore to ocean warming and acidification. Nat Clim Chang 4:1024–1030. doi:10.1038/nclimate2379

    Article  Google Scholar 

  • Shelly K, Heraud P, Beardall J (2002) Nitrogen limitation in Dunaliella tertiolecta Butcher (Chlorophyceae) leads to increased susceptibility to damage by ultraviolet-B radiation but also increased repair capacity. J Phycol 38:1–8

    Article  Google Scholar 

  • Sobrino C, Montero O, Lubián L (2005) Effect of UV-A and UV-B on diel patterns of growth and metabolic activity in Nannochloris atomus cultures assessed by flow cytometry. Mar Ecol Prog Ser 293:29–35. doi:10.3354/meps293029

    Article  CAS  Google Scholar 

  • Sobrino C, Ward ML, Neale PJ (2008) Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnol Oceanogr 53:494–505

    Article  CAS  Google Scholar 

  • Sobrino C, Neale PJ, Phillips-Kress JD et al (2009) Elevated CO2 increases sensitivity to ultraviolet radiation in lacustrine phytoplankton assemblages. Limnol Oceanogr 54:2448–2459

    Article  CAS  Google Scholar 

  • Sobrino C, Segovia M, Neale P et al (2014) Effect of CO2, nutrients and light on coastal plankton. IV. Physiological responses. Aquat Biol 22:77–93. doi:10.3354/ab00590

    Article  Google Scholar 

  • Stramma L, Cornillon P, Weller RA et al (1986) Large diurnal sea surface temperature variability: satellite and in situ measurements. J Phys Oceanogr 56:345–358. doi:10.1175/1520-0485(1986)016<0827:LDSSTV>2.0.CO;2

    Google Scholar 

  • Stuart-Menteth AC, Robinson IS, Challenor PG (2003) A global study of diurnal warming using satellite-derived sea surface temperature. J Geophys Res 108:3155. doi:10.1029/2002JC001534

    Article  Google Scholar 

  • Sun J, Hutchins DA, Feng Y et al (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. doi:10.4319/lo.2011.56.3.0829

    Article  CAS  Google Scholar 

  • Tatters AO, Fu FX, Hutchins DA (2012) High CO2 and silicate limitation synergistically increase the toxicity of Pseudo-nitzschia fraudulenta. PLoS ONE 7:e32116. doi:10.1371/journal.pone.0032116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Timmermans KR, van der Wagt B, Veldhuis MJW et al (2005) Physiological responses of three species of marine pico-phytoplankton to ammonium, phosphate, iron and light limitation. J Sea Res 53:109–120. doi:10.1016/j.seares.2004.05.003

    Article  CAS  Google Scholar 

  • Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt Int Ver Theor und Angew Limnol 9:1–38

    Google Scholar 

  • van de Poll WH, van Leewe MA, Roggeveld J, Buma AGJ (2005) Nutrient limitation and high irradiance acclimation reduce PAR and UV-induced viability loss in the Antarctic diatom Chaetoceros brevis (Bacillariophyceae). J Phycol 41:840–850

    Article  Google Scholar 

  • Varona-Cordero F, Gutiérrez-Mendieta FJ, Rivera-Monroy VH (2014) in situ response of phytoplankton to nutrient additions in a Tropical Coastal Lagoon, (La Mancha, Veracruz, Mexico). Estuar Coasts 37:1353–1375. doi:10.1007/s12237-014-9806-5

    Article  CAS  Google Scholar 

  • Venrick EL (1978) How many cells to count? In: Sournia A (ed) Phytoplankt. Man. UNESCO, Paris, pp 167–180

    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. doi:10.5194/bg-7-2915-2010

    Article  CAS  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. Fundam Appl Limnol/Arch für Hydrobiol 180:279–290. doi:10.1127/1863-9135/2012/0299

    Article  CAS  Google Scholar 

  • Wu Y, Campbell DA, Gao K (2014) Faster recovery of a diatom from UV damage under ocean acidification. J Photochem Photobiol B Biol 140:249–254. doi:10.1016/j.jphotobiol.2014.08.006

    Article  CAS  Google Scholar 

  • Xenopoulos MA, Frost PC (2003) UV radiation, phosphorus, and their combined effects on the taxonomic composition of phytoplankton in a Boreal Lake 1. J Phycol 302:291–302

    Article  Google Scholar 

  • Xu Z, Gao K (2012) NH4+ enrichment and UV radiation interact to affect the photosynthesis and nitrogen uptake of Gracilaria lemaneiformis (Rhodophyta). Mar Pollut Bull 64:99–105. doi:10.1016/j.marpolbul.2011.10.016

    Article  CAS  PubMed  Google Scholar 

  • Zudaire L, Roy S (2001) Photoprotection and long-term acclimation to UV radiation in the marine diatom Thalassiosira weisflogii. J Photochem Photobiol B Biol 62:26–34

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Portuguese Foundation for Science and Technology (FCT) through project PHYTORIA (PTDC/MAR/114380/2009). FCT provided funding for RBD through a postdoctoral fellowship (SFRH/BPD/68688/2010).

Author information

Authors and Affiliations

  1. CIMA - Centre for Marine and Environmental Research, Universidade do Algarve, Campus de Gambelas, 8005-139, Faro, Portugal

    Rita B. Domingues, Cátia C. Guerra, Helena M. Galvão & Ana B. Barbosa

  2. MARE - Marine and Environmental Sciences Centre, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, 1749-016, Lisbon, Portugal

    Rita B. Domingues & Vanda Brotas

Authors
  1. Rita B. Domingues
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cátia C. Guerra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Helena M. Galvão
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vanda Brotas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ana B. Barbosa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rita B. Domingues.

Additional information

Handling Editor: Bas W. Ibelings.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Domingues, R.B., Guerra, C.C., Galvão, H.M. et al. Short-term interactive effects of ultraviolet radiation, carbon dioxide and nutrient enrichment on phytoplankton in a shallow coastal lagoon. Aquat Ecol 51, 91–105 (2017). https://doi.org/10.1007/s10452-016-9601-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10452-016-9601-4

Keywords

Search

Navigation